Bacterial Associations with Legumes

Critical Reviews in Plant Sciences

ISSN: 0735-2689 (Print) 1549-7836 (Online) Journal homepage: http://www.tandfonline.com/loi/bpts20

Bacterial Associations with Legumes Alvaro Peix, Martha H. Ramírez-Bahena, Encarna Velázquez & Eulogio J. Bedmar To cite this article: Alvaro Peix, Martha H. Ramírez-Bahena, Encarna Velázquez & Eulogio J. Bedmar (2015) Bacterial Associations with Legumes, Critical Reviews in Plant Sciences, 34:1-3, 17-42, DOI: 10.1080/07352689.2014.897899 To link to this article: http://dx.doi.org/10.1080/07352689.2014.897899

Published online: 24 Oct 2014.

Submit your article to this journal

Article views: 983

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=bpts20 Download by: [Shanghai Institutes for Biological Sciences]

Date: 21 July 2016, At: 00:54

Critical Reviews in Plant Sciences, 34:17–42, 2015 C Taylor & Francis Group, LLC Copyright ISSN: 0735-2689 print / 1549-7836 online DOI: 10.1080/07352689.2014.897899

Bacterial Associations with Legumes Alvaro Peix,1,2 Martha H. Ram´ırez-Bahena,1,2 Encarna Velázquez,2,3 and Eulogio J. Bedmar4

Downloaded by [Shanghai Institutes for Biological Sciences] at 00:54 21 July 2016

1

Departamento de Desarrollo Sostenible de Sistemas Agroforestales y Ganaderos, Instituto de Recursos Naturales y Agrobiolog´ıa (IRNASA), CSIC, Salamanca, Spain 2 Unidad Asociada Universidad de Salamanca-CSIC “Interacción Planta-Microorganismo,” Salamanca, Spain 3 Departamento de Microbiolog´ıa y Genética, Universidad de Salamanca, Salamanca, Spain 4 Departamento de Microbiolog´ıa del Suelo y Sistemas Simbióticos, Estación Experimental del Zaid´ın (EEZ), CSIC, Granada, Spain

Table of Contents I.

INTRODUCTION

II.

RHIZOBIA: THE LEGUME ENDOSYMBIONTS ................................................................................................................................ 18 A. The Species Concept in Rhizobia ................................................................................................................................................................ 19 1. “Classical” species of rhizobia ................................................................................................................................................................ 20 2. The new rhizobial species ......................................................................................................................................................................... 20 B. The Symbiovar Concept in Rhizobia .......................................................................................................................................................... 27 1. Former biovars based on the cross inoculation groups ................................................................................................................... 27 2. New symbiovars based on the analysis of symbiotic genes .......................................................................................................... 29 C. The Concept of Promiscuity in the Rhizobia-Legume Symbiosis ................................................................................................... 29 1. Host range of rhizobia and legume promiscuity ............................................................................................................................... 30 D. Bacterial Endophytes of Legume Nodules ............................................................................................................................................... 30 1. Gram-negative endophytes ....................................................................................................................................................................... 30 2. Gram-positive endophytes ........................................................................................................................................................................ 31 3. Beneficial interactions between nodule endophytes and legumes .............................................................................................. 32

................................................................................................................................................................................................... 18

ACKNOWLEDGMENTS FUNDING

................................................................................................................................................................................................. 32

................................................................................................................................................................................................................................ 32

REFERENCES

...................................................................................................................................................................................................................... 32

with diazotrophic bacteria, collectively known as rhizobia, which induce root nodules where biological nitrogen fixation takes place, conferring legumes a relevant ecological advantage. This group of bacteria that for many years was thought to be formed by a scarce number of genera and species within alpha proteobacteria, shows nowadays an important genetic diversity including species phylogenetically divergent both in core and symbiotic genes sequences. Together with rhizobia, other endophytic bacteria are present in legume nodules coexisting with rhizobial strains and their

Legumes form a large group of plants that constitute the third largest family of angiosperms, including near 20,000 species and 750 genera. Most of them have the ability to establish symbioses Address correspondence to Eulogio J. Bedmar, Department of Microbiology and Symbiotic systems, Estación Experimental del Zaid´ın, CSIC, P. O. Box 419. 18080-Granada, Spain. E-mail: eulogio.bedmar@ eez.csic.es

17

18

A. PEIX ET AL.

ecological role remains unknown in most cases, but they likely have an effect in plant health, plant growth or even in the rhizobialegume symbiosis. In this review we present an overview of the associations of bacteria with legumes, the current available knowledge on the phylogenetic diversity of both rhizobia and endophytic bacteria inhabiting root nodules, and the symbiotic features used to define symbiovars in rhizobia. Keywords


I.

rhizobia, legumes, endophytic bacteria, PGPR, nodC gene, symbiovar, rrs gene, symbiosis

INTRODUCTION Legumes are a large group of angiospermal plants found in all continents capable of growing in very diverse aquatic and terrestrial environments, under different edaphic and climatic conditions. They form a wide family named Fabaceae or Leguminosae that contain three subfamilies Faboideae (or Papillionoideae), Mimosoideae and Caesalpinioideae. Fabaceae is the third largest family of angiosperms that comprises some 20,000 species and 750 genera, where only a reduced number of species are used in human and animal feeding, some are medicinal species and a few are toxic (reviewed by Velázquez et al., 2010a). The legumes constitute the second most important food for the man and a combination of legumes and cereals may contain all the necessary amino acids for a healthy human nutrition (Ejigui et al., 2007; Paul et al., 2008). These combinations have been used empirically in different cultures both in crop rotation in agriculture and in human feeding. Chickpea, faba bean, lentil and pea together with cereals like wheat are used in Mediterranean diet since the Roman Age (Prowse et al., 2003). Common bean in combination with maize has been eaten in America since the Pre-columbian Age (Finucane et al., 2006; Boyd et al., 2008). In Asia, the combination of soybean with rice has been used for centuries (Paul et al., 2008). In Africa, cereals were the basic food since ancient times together with legumes such as lentils and cowpea (Fuller, 2007). The benefits of using legumes in rotation with cereals is derived from their ability to establish symbiosis with some bacteria, rhizobia, that induce the formation of new organs in roots and stems called nodules where the rhizobia converted into bacteroids carry out the fixation of atmospheric nitrogen. The rhizobia comprise two groups of bacteria, one formed by the genera that were initially described as legume endosymbionts (classical rhizobia), although currently contains also saprophytic or even plant pathogenic species, and a second group formed by different genera that for many years were not described as legume endosymbionts, but contains some species able to form legume nodules (new rhizobia). In addition to rhizobia, the bacteria responsible for nodulation, other endophytic bacteria are also found in legume nodules that can enter the inner of nodules together with the rhizobia as has been recently observed in Vigna nodules by confocal microscopy (Pandya et al., 2013). These bacteria were discarded for decades during screening for isolation of rhizobia, losing

important information on the diversity of endophytes coexisting in the nodules with rhizobial strains and their possible essential role in plant growth. Also, it was a common fact that a failure in the rhizobial isolation from nodules made many researchers wrongly think that the non-rhizobial strains isolated in the plates were the responsible of the nodules formation. This occurred with strains of gamma-Proteobacteria that were suggested as nodule-inducing bacteria in Hedysarum species because the authors were not able to isolate rhizobia from nodules of those legumes (Benhizia et al., 2004). Recently the same authors detected the presence of unculturable rhizobia in nodules from which only the endophytes were isolated (Muresu et al., 2008). Taking into account these results and the high diversity of endophytic bacteria inhabiting legume nodules together with rhizobia, it is necessary to be very cautious before concluding that a “non-rhizobia” strain is the responsible of legume nodulation. For example, it has been reported the nodulation of Robinia pseudoacacia by a strain of the gamma-Proteobacteria Pseudomonas (Shiraishi et al., 2010) and that of legumes from Tribe Trifoliae by a strain of the sporulating Gram-positive Paenibacillus sepulcri (Latif et al., 2013). The authors stated that these strains reinfected their legume hosts inducing nodules, but the only testing performed was the amplification of nod genes without sequencing them. The amplification of a band even of the expected size is not enough to assume that it correspond to the expected gene. Therefore, the results of Shiraishi et al. (2010) and Latif et al. (2013) should be taken with extreme prudence and further confirmed by using adequate techniques in order to unequivocally affirm, as do the authors, that Pseudomonas and Paenibacillus are able to nodulate legumes, especially when dealing with legumes as restrictive for nodulation as those of the Tribe Trifoliae (Pueppke and Broughton, 1999). In order to improve the isolation of rhizobia from legume nodules, it has been proposed that nodule treatments with different antioxidants or enzymes tested either as modified squashing buffers or added in plates yielded dramatic increases of culturability of both rhizobia and endophytes. It seems that reactive oxygen species (ROS) generation during isolation is a major factor limiting microbiota isolation that can be significantly improved with these treatments (Muresu et al., 2013). In any case, when the isolation is not possible there are currently available metagenomic approaches to detect the presence of rhizobia in nodules that avoid mistakes in assigning to endophytic bacteria a role in the nodulation process.

II.

RHIZOBIA: THE LEGUME ENDOSYMBIONTS The beneficial association between rhizobia and legumes has been known for more than a century when, in 1888, Beijerink obtained the first pure bacterial culture from a legume nodule responsible for nitrogen fixation. A year later, Frank named this bacteria Rhizobium leguminosarum (Frank, 1889) and from this date the legume nodule forming bacteria were named “rhizobia.” These bacteria are Gram-negative aerobic rods having


BACTERIAL ASSOCIATIONS WITH LEGUMES

the ability to induce nodules and fix atmospheric nitrogen after their transformation into bacteroids. Depending on the legume, the nodules induced by rhizobia are indeterminate with apical meristematic growth as occurs in temperate legumes such as clover or determinate with growth by expansion of infected cells in the central nodule zone as occurs in tropical legumes such as soybean (Sprent, 2007). From the discovery of nitrogen-fixing rhizobia-legume symbiosis, many of these symbiotic relationships have been analysed showing that nodulation is common in Papilionoideae, less abundant in Mimosoideae and seldom in Cesalpinoideae (Sprent, 2007). The symbiosis rhizobia-legume depends of the specificity, infectivity and effectiveness of rhizobia and follows a series of steps, which are the result of the expression of different molecules by the bacterium, the host plant, or both. Specific flavonoids released by legume roots serve as chemoattractants for the rhizobial symbiont (Gulash, 1984) and they also activate the expression of rhizobial nod genes, responsible for the synthesis of nod factors (lipochitin-oligosaccharides) that are receptors for the plant flavonoid signal (Denarié et al., 1996; Broughton and Perret, 1999; Downie and Walker, 1999; Gough and Cullimore, 2011; Oldroyd, 2013). Nevertheless, in some photosynthetic Bradyrhizobium strains that form nitrogenfixing nodules on the roots and stems of an aquatic host, Aeschynomene sensitiva, the common nod genes were not detected after complete sequencing of their genomes (Giraud et al., 2007). After mutational analysis the authors proposed that these strains use an alternative pathway to induce nodules, where a purine derivative could be involved in triggering nodule formation. After the recognition of rhizobia by the plant, several molecules are involved in the attachment of bacteria to the roots such as the lectins produced by legumes, proteins that reversibly and nonenzymatically bind specific carbohydrates and are classified into different families according to their carbohydrate recognition domains (Arason, 1996; van Damme et al., 2004). Therefore, the importance of bacterial polysaccharides are critical in the infection, so that mutants defective in their biosynthesis are characterized by low infectivity, a low capacity for nodulation, and in some cases, changes in the host range (Gray and Rolfe, 1990; Dazzo, 1991; Gibson, 2008). Once bacteria enter plant roots, they are transformed into bacteroids that carry out the nitrogen fixation, a nitrogenasemediated process that is the primary function of the symbiosis (Rees et al., 2005). The nitrogenase produced by the bacteroids is oxygen-sensitive and therefore need a microaerophilic environment to be active. This is possible because of leghaemoglobin, a protein produced by the legumes whose function is to remove oxygen from the symbiosomes (Ott et al., 2005). When nitrogen fixation is carried out within the nodules they have a pink colour due to the expression of leghaemoglobin, indicating an efficient symbiosis. A white colour of nodules completely developed are indicative of an inefficient symbiosis as occurs in some of non “clasical” rhizobial species such

19

as Phyllobacterium trifolii that formed typical, but ineffective nodules in Trifolium repens (Valverde et al., 2005). Effective and ineffective legume symbiosis have been widely studied in the last decades increasing the number of rhizobia isolated from legume nodules that belong to different Classes of Proteobacteria and have different host range. Nevertheless, there are many legumes and ecosystems that have not been analysed yet and then the number of rhizobial species and symbiovars will certainly increase in future years. A.

The Species Concept in Rhizobia The bacterial species concept has changed over time and whereas “symptoms” induced were essential to define species at the begining of Bacteriology, currently the core genes are the basis of the species differentiation. Between these times, many other criteria have been applied to the species definition, and they have been conserved in more or less extension. In the case of rhizobia, the symptoms considered were nodule induction in legume plants, which originated the so-called cross-inoculation groups (Baldwin and Fred, 1929) whose differentiation was based on their ability to nodulate the same host. This criterion was central in the description of the first rhizobial species and only a few phenotypic characteristics were recorded in Bergey’s Manuals in contrast with other genera of Family Rhizobiaceae, such as Agrobacterium, whose species were distinguishable by phenotypic characteristics in addition to the symptoms originated in plants (Jordan and Allen 1974; Jordan 1984). From the 1970s decade, it was known that the ability to induce nodules are codified by genes harboured in autoconjugative plasmids in fast-growing rhizobia (Zurkowski and Lorkiewic, 1979) and in 2000s decade it was discovered that these genes are harboured in symbiotic islands in the case of most intermediate and slow-growing rhizobia (Kaneko et al., 2002; Sullivan et al., 2002). In all cases, nodulation genes are subjected to lateral transfer in rhizosphere. Although mobile genetic elements are inadequate taxonomic tools for bacterial species delineation, the symbiotic characteristics have been used in rhizobial taxonomy for decades and they are still considered in rhizobial species descriptions. The first change in the rhizobial species concept was the application of a physiological characteristic to the reclassification of R. japonicum into a new genus, Bradyrhizobium, created to include the slow-growing rhizobia with a single species nodulating soybean (Jordan, 1982). Although from this date numerical taxonomy was introduced increasing the number of characteristics used for species definition (Chen et al., 1988), phenotypic characteristics have never been useful in rhizobial species identification. In spite of that, currently extended tables of phenotypic differences are mandatory for species description, and some of them were included in the last edition of Bergey’s Manual (Kuykendall, 2005). The most important change in the bacterial species concept was linked to the advent of genomic techniques analysing nucleic acids as occurred in all groups of bacteria. After the


20

A. PEIX ET AL.

proposal for using the ribosomal 16S (rrs) gene as universal tool for classification and identification of bacteria (Woese et al., 1984), rhizobia were included in the phylum Proteobacteria and the complete sequence of rrs gene has been obtained in all rhizobial species that have been classified in different genera and families within this Phylum. The reliability of rrs gene to differentiate rhizobial species and genera enforced this criterion over other ones on species concept also in rhizobia. Moreover, the ease of gene sequencing and the advances in the knowledge of genes involved in different cell functions have allowed the selection of core genes for species differentiation and auxilliary ones (those transmisible among bacteria) for diagnostic and infraspecific classifications. In this way, in the case of rhizobia, in addition to rrs gene, several housekeeping genes have been proposed for species differentiation (Gaunt et al., 2001). The species concept in rhizobia is currently linked to core genes which have even allowed the description of several new species of fast and slow growing rhizobia whose ability to produce plant symptoms is unknown (see Table 1). Conversely, sequencing of these core genes allowed the identification of other bacteria in legume nodules such as Burkholderia that was the first beta-Proteobacteria described as endosymbiont of a legume (Moulin et al., 2001).

1.

“Classical” species of rhizobia At the beginning of rhizobiology, all rhizobial species regardless their growth rate were included in a single genus, Rhizobium (Frank, 1889) and later included in the Rhizobiaceae (Conn, 1938). As mentioned above, the different species were named according to the legume host they were able to nodulate. This way, the fast growing species were named R. leguminosarum nodulating Vicia, Pisum and Lens (Frank, 1889), R. phaseoli nodulating Phaseolus, R. trifolii nodulating Trifolium and R. meliloti nodulating Medicago (Dangeard, 1926), and the slow growing species R. japonicum nodulating Glycine (Buchanan, 1926) and R. lupini nodulating Lupinus (Eckhardt et al., 1931). The slow growing species were later reclassified into a new genus named Bradyrhizobium (Jordan, 1982) reducing the number of Rhizobium species not only for this reason, but also for internal reclassifications (Jordan, 1984). One of the most relevant changes coinciding with this reclassification was the description of R. fredii, a new fast growing species nodulating soja (G. max), commonly nodulated by slow-growing species of genus Bradyrhizobium. This fact questioned the use of crossinoculation groups as taxonomic criterion since it revealed the nodulation of the same legume by very different rhizobial species. Moreover, the description of this species constituted a turning point in rhizobial taxonomy since it was the first officially described species in the Rhizobiaceae (Scholla and Elkan 1984) introducing the numerical taxonomy in rhizobia. Later this species was separated in a second fast growing genus within family Rhizobiaceae named Sinorhizobium (Chen et al., 1988).

Nevertheless, the most important change was the use of rrs gene to classify rhizobial species that represented a definitive breaking point with the cross-inoculation groups allowing the affiliation of rhizobia within the alpha subdivision of Proteobacteria (Woese et al., 1984). After this date, several species and genera were described within rhizobia, two genera, Allorhizobium and Agrobacterium, were reclassified into genus Rhizobium (Young et al., 2001) and Sinorhizobium was reclassified into Ensifer. This latter was due to the closeness of the rrs gene of Sinorhizobium type species to that of Ensifer adhaerens (Casida, 1982), a species described prior to that of Sinorhizobium (Judicial Commission of the International Committee on Systematic of Prokaryotes, 2008). Then, genus Rhizobium includes currently both symbiotic and plant pathogenic strains and the Rhizobiaceae only comprises two of the “classical” genera of rhizobia, Rhizobium and Ensifer. Based on the rrs gene analysis, the remaining genera were distributed into several families (Kuykendall, 2005), which gave rise to a significant increase in the number of rhizobial species (Table 1). Because of its high degree of evolutive conservation, the rrs gene may not be discriminative enough to differentiate closely related rhizobial species (Valverde et al., 2006; Ram´ırez-Bahena et al., 2008; Sa¨ıdi et al., 2013). This was overcome by the analysis of housekeeping genes such as recA, atpD, glnII among others that are particularly useful for species identification. Mulitlocus sequence analysis produced a significant increase in the number of rhizobial species and also made possible the finding of species from typical rhizobial genera that have not been isolated from legume nodules (Table 1). Today, the isolation of species from classical rhizobial genera from the rhizosphere, bioreactors, etc. is common. The first described species of ‘rhizobia’ unable to nodulate legumes was E. morelense (Wang et al., 2002). Nevertheless, given that it was isolated from nodules of Leucaena leucocephala, the non-nodulating feature could be confusing. The first species isolated from a completely different source that a nodule was B. betae (Rivas et al., 2004), which was isolated from roots of Beta vulgaris. Later, many other species were isolated from different sources, such as plant tissues or sawdust, rhizosphere and roots of diverse plants, water, soil, sand, activated sludge, bioreactors, etc. (Table 1). These results show that diversity of rhizobia is higher than ever expected and that these microorganisms are widespread in very diverse ecosystems. 2.

The new rhizobial species In spite of the important discoveries within the “classical” rhizobia, the most relevant fact from 2000 year was the finding of non-rhizobial genera able to induce legume nodules, which we call here ‘new rhizobia’ (Table 2). For more than a century, rhizobia were thought to be the unique bacteria capable of originating nodules in legumes and this fact made researchers to discard all those colonies obtained from nodules that had not the appearance of rhizobia on yeast mannitol agar (YMA) plates.

21


TABLE 1 Species of “classical” rhizobia isolated from different sources


Species

R. alamii∗ R. alkalisoli R. azibense R. calliandrae R. cauense R. etli R. fabae R. freirei R. galegae R. gallicum R. giardinii R. grahamii R. helanshanense R. jaguaris R. hainanense

R. herbae R. huautlense R. indigoferae R. laguerreae R. leguminosarum R. leucaenae R. loessense R. lupini R. lusitanum R. mayense R. mesoamericanum

Original source Genus Rhizobium Species isolated from legume nodules Medicago ruthenica Caragana intermedia Phaseolus vulgaris Calliandra grandiflora Kummerowia stipulacea Phaseolus vulgaris Vicia faba Phaseolus vulgaris Galega officinalis Phaseolus vulgaris Phaseolus vulgaris Dalea leporina, Leucaena leucocephala, Clitoria ternatea Spaherophysa salsula Calliandra grandiflora Desmodium spp., Stylosanthes guyanansis, Centrosema pubescens, Tephrosia candida, Acacia sinuata, Arachis hypogaea, Zornia diphylla, Uraria crinita, Macroptilium lathyroides Astragalus membranaceus, Oxytropis cashemiriana Sesbania herbacea Indigofera spp., Vicia spp. Pisum sativum

R. oryzae R. phaseoli

Leucaena leucocephala, Phaseolus vulgaris Astragalus spp. Lupinus spp. Phaseolus vulgaris Calliandra grandiflora Phaseolus vulgaris, Macroptilium atropurpureum, Vigna unguiculata, Mimosa pudica Albizia julibrissin, Kummerowia spp., Dalbergia spp. Lespedeza chinensis Medicago ruthenica Lotus spp., Alhagi toum, Astragalus spp., Halimodendron halodendron, Oxytropis spp., Robinia pseudoacacia, Sophora alopecuriodes, Caragana jubata, Lathyrus odoratus, Vicia hirsuta Oryza sativa Phaseolus vulgaris

R. pisi

Pisum sativum

R. mesosinicum R. miluonense R. mongolense R. multihospitium

Reference

Berge et al., 2009 Lu et al., 2009a Mnasri et al., 2014 Rincón-Rosales et al., 2013 Liu et al., 2012a Segovia et al., 1993 Tian et al., 2008 Dall’agnol et al., 2013 Lindstrom, 1989 Amarger et al., 1997 Amarger et al., 1997 López-López et al., 2012 Qin et al., 2012 Rincón-Rosales et al., 2013 Chen et al., 1997

Ren da et al., 2011b Wang et al., 1998 Wei et al., 2002 Sa¨ıdi et al., 2014 Frank, 1879, 1889; Ram´ırez-Bahena et al., 2008 Ribeiro et al., 2012 Wei et al., 2003 Eckhardt et al., 1931 Valverde et al., 2006 Rincón-Rosales et al., 2013 López-López et al., 2012

Lin et al., 2009 Gu et al., 2008 van Berkum et al., 1998 Han et al., 2008b

Peng et al., 2008 Dangeard et al., 1926; Ram´ırez-Bahena et al., 2008 Ram´ırez-Bahena et al., 2008 (Continued on next page)

22

A. PEIX ET AL.

TABLE 1 Species of “classical” rhizobia isolated from different sources (Continued)


Species

R. pongamiae R. sullae R. sphaerophysae R. taibaishanense R. tibeticum R. tropici R. tubonense R. undicola R. vallis R. vignae R. yanglingense

R. larrymoorei R. nepotum

Original source Genus Rhizobium Species isolated from legume nodules Pongamia pinnata Hedysarum coronarium Sphaerophysa salsula Kummerowia striata Trigonella archiducis-nicolai Phaseolus vulgaris, Leucaena leucocephala Oxytropis glabra Neptunia natans Phaseolus vulgaris, Mimosa pudica, Indigofera spicata Vigna radiata, Desmodium microphyllum, Astragalus spp. Coronilla varia, Gueldenstaedtia multiflora, Amphicarpaea trisperma Species isolated from plant deformations aerial galls on Ficus benjamina

R. rhizogenes

galls on Prunus cerasifera, Rubus idaeus, Vitis vinifera, Prunus avium hairy roots of Prunus malus

R. rubi

galls on Rubus

R. skierniewicense R. vitis

tumours on Chrysanthemum spp., Prunus cerasifera tumours on Vitis vinifera

R. aggregatum R. borbori R. cellulosilyticum R. daejeonense R. endolithicum R. endophyticum R. flavum R. halophytocola R. halotolerans R. lemnae R. naphtalenivorans R. oryzae R. paknamense

Species isolated from other sources surface lake water activated sludge sawdust of Populus alba cyanide treatment bioreactor beach sand seeds of Phaseolus vulgaris soil roots of Rosa rugosa chloroethylenes contaminated soil Lemna aequinoctialis tissues sediment of a polychlorinated-dioxin-transforming microcosm Oryza sativa Lemna aequinoctialis tissues

R. petrolearium R. phenanthrenilyticum R. pseudoryzae R. pusense R. qilianshanense R. radiobacter§

oil-contaminated soil petroleum residue treatment system rhizosphere of Oryza sativa rhizosphere of Cicer arietinum Oxytropis ochrocephala soil

Reference

Kesari et al., 2013 Squartini et al., 2002 Xu et al., 2011 Yao et al., 2012 Hou et al., 2009 Mart´ınez-Romero et al., 1991 Zhang et al., 2011b de Lajudie et al., 1998a; Young et al., 2001 Wang et al., 2011 Ren da et al., 2011a Tan et al., 2001

Bouzar and Jones, 2001; Young, 2004 Puławska et al., 2012a Riker et al., 1930; Young et al., 2001 Hildebrand, 1940; Young et al., 2001 Puławska et al., 2012b Ophel and Kerr, 1990; Young et al., 2001 Kaur et al., 2011 Zhang et al., 2011a Garc´ıa-Fraile et al., 2007 Quan et al., 2005 Parag et al., 2013 López-López et al., 2010 Gu et al., 2014 Bibi et al., 2012 Diange and Lee, 2013 Kittiwongwattana Thawai, 2014 Kaiya et al., 2012 Peng et al., 2008 Kittiwongwattana and Thawai, 2013 Zhang et al., 2012b Wen et al., 2011 Zhang et al., 2011c Panday et al., 2011 Xu et al., 2013 Beijerinck and van Delden, 1902; Sawada et al., 1993; Young et al. 2001

23


TABLE 1 Species of “classical” rhizobia isolated from different sources (Continued) Species

Original source

Reference


Genus Rhizobium Species isolated from other sources R. rhizoryzae R. rosettiformans R. selenitireducens R. soli R. straminoryzae R. subbaraonis R. tarimense

rice roots hexachlorocyclohexane dump site bioreactor soil rice straw beach sand soil Genus Ensifer (formerly Sinorhizobium)

E. americanum

Acacia spp.

E. arboris E. fredii

Acacia senegal, Prosopis chilensis Glycine max

E. garamanticus E. kostiensis E. kummerowiae E. medicae E. meliloti

Argyrolobium uniflorum, Medicago sativa Acacia senegal, Prosopis chilensis Kummerowia stipulacea Medicago truncatula Medicago sativa

E. mexicanus E. numidicus E. psoraleae E. saheli

Acacia angustissima Argyrolobium uniflorum, Lotus creticus Psoralea corylifolia, Sesbania cannabina Sesbania spp.

E. sesbaniae E. sojae E. terangae

Sesbania cannabina, Medicago lupulina Glycine max Acacia spp., Sesbania spp.

Zhang et al., 2014 Kaur et al., 2011 Hunter et al., 2007 Yoon et al., 2010 Lin et al., 2014 Ramana et al., 2013 Turdahon et al., 2013

Species isolated from legume nodules

Species isolated from other sources E. adhaerens soil E. morelense associated to nodules Leucaena leucocephala

Toledo et al., 2003; Wang et al., 2013c Nick et al., 1999; Young, 2003 Scholla and Elkan, 1984; Jarvis et al., 1992; Young, 2003 Merabet et al., 2010 Nick et al., 1999; Young, 2003 Wei et al., 2002; Young, 2003 Rome et al., 1996; Young, 2003 Dangeard, 1926; de Lajudie et al., 1994; Young, 2003 Lloret et al., 2007 Merabet et al., 2010 Wang et al., 2013c de Lajudie et al., 1994; Young, 2003 Wang et al., 2013c Li et al., 2011 de Lajudie et al., 1994; Young, 2003 Casida, 1982 Wang et al., 2002; Wang et al., 2013c

Genus Mesorhizobium M. abyssinicae M. albiziae M. alhagi M. amorphae M. australicum M. camelthorni M. caraganae M. chacoense M. ciceri

Acacia abyssinica Albizia kalkora Alhagi sparsifolia Amorpha fruticosa Biserrula pelecinus Alhagi sparsifolia Caragana spp. Prosopis alba Cicer arietinum

M. gobiense M. hawassense M. huakuii

Astragalus filicaulis, Lotus spp., Oxytropis glabra, Sesbania sesban Astragalus sinicus

Degefu et al., 2013 Wang et al., 2007 Chen et al., 2010 Wang et al., 1999b Nandasena et al. 2009 Chen et al., 2011 Guan et al., 2008 Velázquez et al., 2001 Nour et al., 1994; Jarvis et al., 1997 Han et al., 2008a Degefu et al., 2013 Chen et al., 1991; Jarvis et al. 1997

24

A. PEIX ET AL.

TABLE 1 Species of “classical” rhizobia isolated from different sources (Continued) Species

Original source

Reference


Genus Mesorhizobium M. loti

Lotus spp.

M. mediterraneum

Cicer arietinum

M. metallidurans M. muleiense M. opportunistum M. plurifarium

Anthyllis vulneraria Cicer arietinum Biserrula pelecinus Acacia spp., Prosopis juliflora, Chamaecrista ensiformis, Leucaena spp. Astragalus sinicus Robinia pseudoacacia Astragalus spp. Astragalus adsurgens Caragana spp. Acacia abyssinica Astragalus spp. Anagyris latifolia, Lotus berthelotii Lotus frondosus Astragalus adsurgens Glycyrrhiza sp., Sophora alopecuroides, Halimodendron holodendron, Caragana polourensis, Swainsonia salsula, Glycine spp.

M. qingshengii M. robiniae M. sangaii M. septentrionale M. shangrilense M. shonense M. silamurunense M. tamadayense M. tarimense M. temperatum M. tianshanense

Jarvis et al.,1982; Jarvis et al., 1997 Nour et al., 1995; Jarvis et al., 1997 Vidal et al., 2009 Zhang et al., 2012a Nandasena et al., 2009 de Lajudie et al., 1998b Zheng et al., 2013 Zhou et al., 2010 Zhou et al., 2013 Gao et al., 2004 Lu et al., 2009b Degefu et al., 2013 Zhao et al., 2012 Ram´ırez-Bahena et al., 2012 Han et al., 2008a Gao et al., 2004 Chen et al., 1995; Jarvis et al., 1997

M. thiogangeticum

Species isolated from other sources rhizosphere of Clitoria ternatea

Ghosh and Roy 2006

B. arachidis B. canariense B. cytisi B. daqingense B. diazoefficiens B. elkanii B. ganzhouense B. huanghuaihaiense B. icense B. japonicum B. jicamae B. lablabi B. liaoningense B. manausense B. pachyrhizi B. paxllaeri B. retamae B. rifense B. valentinum B. yuanmingense

Genus Bradyrhizobium Species isolated from legume nodules Arachis hypogaea Chamaecytisus proliferus Cytisus villosus Glycine max Glycine max Glycine max Acacia melanoxylon Glycine max Phaseolus lunatus Glycine max Pachyrhizus erosus Lablab purpureus, Arachis hypogaea Glycine max Vigna unguiculata Pachyrhizus erosus Phaseolus lunatus Retama spp. Cytisus villosus Lupinus mariae-josephae Lespedeza cuneata

Wang et al., 2013b Vinuesa et al., 2005 Chahboune et al., 2011 Wang et al., 2013a Delamuta et al., 2013 Kuykendall et al., 1992 Lu et al., 2014 Zhang et al., 2012c Durán et al., 2014a Kirchner, 1896; Jordan, 1982 Ram´ırez-Bahena et al., 2009 Chang et al., 2011 Xu et al., 1995 Venancio Silva et al., 2014 Ram´ırez-Bahena et al., 2009 Durán et al., 2014a Guerrouj et al., 2013 Chahboune et al., 2012 Durán et al., 2014b Yao et al., 2002

B. betae B. iriomotense

Species isolated from plant deformations root tumours on Beta vulgaris root tumours on Entada koshunensis

Rivas et al., 2004 Islam et al., 2008

25


TABLE 1 Species of “classical” rhizobia isolated from different sources


Species

Original source

Reference

Species isolated from other sources

B. denitrificans‡

Water

B. oligotrophicum

Rice paddy soil

A. dobereinereae A. caulinodans

Genus Azorhizobium Species isolated from legume nodules Sesbania virgata Sesbania rostrata Species isolated from other sources macerated petioles of Rumex sp.

A. oxalatiphilum

Hirsch and Müller, 1985; van Berkum et al. 2006 Ohta and Hattori, 1983; Ram´ırez-Bahena et al., 2013a

Souza-Moreira et al., 2006 Dreyfus et al., 1988 Lang et al., 2013

∗

The type strain of this species was isolated from rhizosphere of Arabidopsis thaliana. §This species contains the type strain of the former species Agrobacterium tumefaciens. These species are synonyms since they have identical core gene sequences. ‡This species is able to fix nitrogen in Aeschynomene nodules according to van Berkum and Eardly (2002).

However, in 2001, the reports of two atypical bacteria belonging to the genera Methylobacterium and Burkholderia able to nodulate legumes open a new research path of ‘non-rhizobial’ bacteria inducing legume nodules (Moulin et al., 2001; Sy et al., 2001). The most surprising of these findings was the Burkholderia case, since it was the first report of a beta-Proteobacteria nodulating a legume. Confirmation of nodule formation and effective nitrogen fixation by Burkholderia was obtained after inoculation of green fluorescent protein (GFP)-marked strains of B. nodosa and B. mimosarum on Mimosa (Chen et al., 2005a; b). The presence of the common nodulation nodABC genes phylogenetically related to those found in “classic” rhizobia in Burkholderia, supported the hypothesis of lateral gene transfer in the rhizosphere crossing the boundary between classes alpha and beta Proteobacteria (Moulin et al., 2001; Bontemps et al., 2010). Recently, the analysis of the complete genome of strain Burkholderia sp. CCGE1002 isolated in Mexico from Mimosa occidentalis showed that this strain carries a symbiotic plasmid (pSym) harbouring nodulation and nitrogen-fixation genes (Ormeño-Orrillo et al., 2012b). From the first report of legume nodulation by Burkholderia, different species of this genus have been found to be legume endosymbionts, mainly of Mimosa species (reviewed by Angus and Hirsch, 2010; Gyaneshwar et al., 2011). Nevertheless, several other members of the Mimosoideae are also nodulated by Burkholderia such as Piptadenia spp., Parapiptadenia spp., Pseudopiptadenia spp., Anadenanthera spp. and Microlobius foetidus (Table 2). Also, Burkholderia can nodulate some Papilionoideae legumes such as Cyclopia spp., P. vulgaris, Macroptilium atropurpureum, Podalyria canescens, Dalbergia spp. and Lebeckia ambigua (Table 2). Mimosa species are also nodulated by other betaProteobacteria initially named Ralstonia taiwanensis (Chen

et al., 2003a) and later reclassified as Cupriavidus taiwanensis (Vandamme and Coenye 2004) that carries functioning nodulation and nitrogen fixation genes (Amadou et al., 2008). Moreover, as was reported for Burkholderia, the nodule formation was confirmed after inoculation of green fluorescent protein (GFP)marked strains of C. taiwanensis in Mimosa plants (Chen et al., 2003a). Burkholderia and Cupriavidus have been reported to nodulate primarily mimosoid legumes and the coexistence of species of these two genera in nodules of Mimosa species has been reported being the main endosymbionts of Mimosa on several continents (Barrett and Parker, 2006; Chen et al., 2003b; Liu et al., 2012b). Nevertheless, in situ immunolocalization on the nodules of Mimosa species using antibodies against Burkholderia and Cupriavidus showed that Burkholderia was the predominant endosymbiont of Mimosa spp. (Elliott et al., 2009, Bontemps et al., 2010, dos Reis et al., 2010, Mishra et al., 2012) even being more competitive than R. tropici for nodulation of this legume (Elliott et al., 2009). According to Bontemps et al. (2010) data, based on symbiotic gene phylogenies, Burkholderia-legume symbiosis history is both ancient and stable with an increasing number of species from this beta-Proteobacteria genus isolated from legume nodules in recent years (Table 2). Most of the non-rhizobial species able to nodulate legumes belong to the class alpha-Proteobacteria from which the previously mentioned Methylobacterium nodulans was the first one reported. Afterwards, the ability to nodulate legumes was also demonstrated in several species from genera Devosia, Ochrobactrum, Phyllobacterium, Shinella, Aminobacter and Microvirga (Table 2). From them, only Shinella belongs to the Rhizobiaceae and it is difficult to establish whether it is a rhizobial or ‘non-rhizobial’ genus, since it contains non-nodulating species and one, Shinella kummerowiae,

26

A. PEIX ET AL.

TABLE 2 New rhizobia able to nodulate legumes


Species

Host

Reference

Alpha-Proteobacteria Aminobacter anthyllidis Devosia neptuniae Methylobacterium nodulans Microvirga lotononidis Microvirga lupini Microvirga vignae Microvirga zambiensis Ochrobactrum lupini Ochrobactrum cytisi Phyllobacterium trifolii Shinella kummerowiae

Anthyllis vulneraria Neptunia natans Crotalaria spp. Listia angolensis Lupinus texensis Vigna unguiculata Listia angolensis Lupinus albus Cytisus scoparius Trifolium pratense Kummerowia stipulacea

Maynaud et al., 2012 Rivas et al., 2003 Jourand et al., 2004 Ardley et al., 2011 Ardley et al., 2011 Radl et al., 2014 Ardley et al., 2011 Trujillo et al., 2005 Zurdo-Piñeiro et al., 2007 Valverde et al., 2005 Lin et al., 2008

Beta-Proteobacteria Burkholderia caballeronis Burkholderia caribensis Burkholderia cepacia

Phaseolus vulgaris Mimosa spp., Parapiptadenia rigida Dalbergia spp.

Mart´ınez-Aguilar et al., 2013 Liu et al., 2011; Bournaud et al., 2013 Rasolomampianina et al., 2005; Lu et al., 2012 Sheu et al., 2013; Bournaud et al., 2013

Burkholderia diazotrophica

Burkholderia dilworthii Burkholderia mimosarum Burkholderia nodosa

Burkholderia phenoliruptrix

Burkholderia phymatum

Burkholderia sabiae

Burkholderia rhynchosiae Burkholderia sprentiae Burkholderia symbiotica Burkholderia tuberum

Burkholderia sp.

Cupriavidus necator

Cupriavidus taiwanensis

Mimosa spp., Anadenanthera peregrina, Anadenanthera colubrina, Parapiptadenia blanchetti Lebeckia ambigua Mimosa spp. Mimosa spp., Piptadenia gonoacantha, Piptadenia trisperma, Parapiptadenia pterosperma, Parapiptadenia rigida, Pseudopiptadenia contorta Piptadenia gonoacantha, Piptadenia paniculata, Piptadenia monoliformis, Anadenanthera peregrina, Anadenanthera colubrina Machaerium, Mimosa spp., Parapiptadenia pterosperma, Phaseolus vulgaris Mimosa caesalpiniifolia, Piptadenia trisperma, Anadenanthera peregrina, Parapiptadenia pterosperma, Parapiptadenia rigida, Pseudopiptadenia bahiana Rhynchosia ferulifolia Lebeckia ambigua Mimosa spp. Aspalathus carnosa, Cyclopia spp., Mimosa spp., Macroptilium atropurpureum, Podalyria ssp., Virgilia spp., Phaseolus vulgaris Parapiptadenia rigida, Lebeckia ambigua, Piptadenia viridiflora, Piptadenia stipulacea, Microlobius foetidus Phaseolus vulgaris, Leucaena leucocephala, Mimosa caesalpiniaefolia, Macroptilium atropurpureum, Vigna unguiculata Mimosa spp.

de Meyer et al., 2014 Chen et al., 2006 Chen et al., 2007; Bournaud et al., 2013

Bournaud et al., 2013

Vandamme et al., 2002; Elliott et al.,2007b; Bournaud et al., 2013; Talbi et al., 2010 Chen et al., 2008, Bournaud et al., 2013

de Meyer et al., 2013b de Meyer et al., 2013a Sheu et al., 2012 Vandamme et al., 2002; Elliott et al., 2007a; Barrett and Parker, 2006; Gyaneshwar et al., 2011 Taulé et al., 2012; Howieson et al., 2013; Bournaud et al., 2013 da Silva et al., 2012

Chen et al., 2003a; Vandamme and Coenye, 2004; Barrett and Parker, 2006, Verma et al., 2004; Andam et al., 2007; Liu et al., 2011



which nodulates the legume Kummerowia stipulata (Lin et al., 2008). In some species, the nodulation genes have been detected as occurred in the case D. neptuniae that carry nodD and nifH genes closely related to those of R. tropici CIAT899T (Rivas et al., 2002). The high identity of these genes suggested that they were transferred to D. neptuniae from R. tropici, an American species nodulating Leucaena (Mart´ınez-Romero et al., 1991) and Neptunia in America (Zurdo-Piñeiro et al., 2004). Also the nifH and nodD genes were detected in plasmids using nifH and nodD probes in Ochrobactrum lupini (Trujillo et al., 2005) and P. trifolii (Valverde et al. 2005). Collectivelly, the findings about new rhizobia nodulating legumes showed that their diversity is yet underestimated and further analyses are necessary in order to expand our knowledge about this symbiosis in different legumes. B.

The Symbiovar Concept in Rhizobia The term symbiovar, proposed by Rogel et al. (2011), is equivalent to the classic term “biovar,” and the concept aims to group the strains within a species that are able to establish symbiosis with a specific legume. At the begining of the rhizobiology, the line between species and biovar was diffuse since the ability to nodulate one or other legume was used to delimite the first species within rhizobia (Jordan and Allen, 1974). The limit was not defined until the discovery that symbiotic genes are harbored in autoconjugative plasmids in Rhizobium (Zurkowski and Lorkiewic, 1979) and it was Jordan (1984) that used the possibility of transferring nodulation plasmids among rhizobial strains to define biovars (Jordan, 1984). Nevertheless, at that time the rrs gene sequencing was not yet applied to the Rhizobium taxonomy and then the biovar concept was defined before having a correct definition of rhizobial species, which has caused many problems in the taxonomy of this genus. Laguerre et al. (2001) were the first authors that used the nodC gene to delineate biovars in Rhizobium within species clearly defined by rrs gene analysis. After this date, several biovars have been defined based on the analysis of other genes such as nodA (Bailly et al., 2007) and nifH (Rincón-Rosales et al., 2013) and on the ability to fix nitrogen in symbiosis with specific legumes (Gubry-Rangin et al., 2013). The biovar definition was much clearer in Mesorhizobium and Bradyrhizobium because the first biovars defined within these genera were already based on the phylogenetic analysis of nodulation genes, after these genes had been found to be harboured in symbiotic islands in the chromosome in the intermediate and slow growing rhizobia (Barnett et al., 2001; Sullivan et al., 2002; Uchiumi et al., 2004; Flores et al., 2005; Young et al., 2006; Nandasena et al., 2007; Crossman et al., 2008). Sequencing the nodC gene was used to define the first biovars in genus Bradyrhizobium, bv. genistearum and bv. glycinearum, within the species B. japonicum (Vinuesa et al., 2005) and in genus Mesorhizobium, the bv. ciceri, within M. amorphae and M. tianshanense (Rivas et al., 2007).

27

Considering all rhizobial genera, most symbiovars are currently defined based on the range of legumes they can nodulate, and mainly on the basis of the nodC gene analysis, whose phylogenies make possible the correct differentiation of these categories within species of all rhizobial genera. Therefore, the analysis of this gene will allow the definition of additional symbiovars some of them already found in legume nodules but not yet officially defined (Ram´ırez-Bahena et al., 2013b). 1.

Former biovars based on the cross inoculation groups The discovery that symbiotic abilities are codified in transmisible plasmids led Jordan (1984) to reclassify the former species R. phaseoli and R. trifolii as biovars of R. leguminosarum. It was Jordan who applied by the first time the concept of “biovar” in rhizobia to design a group of strains belonging to a species that is able to nodulate a legume but not others. Nevertheless, because the Jordan’s classification did not distinguish clearly between chromosomal and plasmidic features, the reclassification was erroneous. After Jordan’s proposal, some other biovars were also proposed on the basis of symbiotic traits. This was the case for R. etli, where two biovars were defined, phaseoli and mimosae, which differ in the ability of biovar mimosae to nodulate Leucaena (Wang et al., 1999a). Different symbiotic traits also allowed the definition of two biovars named officinalis and orientalis in R. galegae (Radeva et al., 2001). Therefore, the biovar concept was directly linked to the cross-inoculation group. Because the latter is related to symbiotic genes which are not useful in taxonmy due to their transferability in nature (Finan, 2002), the biovar concept is not adequate to define rhizobial species. This horizontal transfer can occur from plasmids to genomic islands (Nakatsukasa et al., 2008), from bacteria to plants (Broothaerts et al., 2005) and among bacteria (Rogel et al., 2001). Applying the new taxonomic criteria based on the analysis of core genes, today we know that R. phaseoli was a valid species, that R. trifolii was a synonym of R. leguminosarum (Ram´ırez-Bahena et al., 2008), and that R. leguminosarum has the three biovars initially proposed by Jordan (1984), which are bona fide according to the analysis of the symbiotic nodC gene (Garc´ıa-Fraile et al., 2010). Moreover, we currently know that the ‘biovar’ and the ‘crossinoculation group’ concepts are not completely equivalent, and only coincided in the cases of legumes restrictive for nodulation (see below). For example, Vicia and Trifolium are restrictive hosts and there are no cross-nodulation abilities between biovars viciae and trifolii; however, strains of these two biovars can nodulate the legume host of the biovar phaseoli because Phaseolus is a promiscuous legume. For this reason the suitability of the definition of biovars affecting this type of legumes has been discussed (Zurdo-Piñeiro et al., 2009). This point can be solved by using a phylogenetic criterion based on the nodC gene analysis which makes it possible to clearly distinguish the biovars viciae, trifolii and phaseoli (Garc´ıa-Fraile et al., 2010). In fact, most of the described biovars (Table 3) were defined on the basis of the nodC gene analysis, which support the results

28

A. PEIX ET AL.

TABLE 3 Symbiovars (formerly biovars) of rhizobial species Species R. calliandrae, R. jaguaris, R. mayense R. etli R. galegae


R. gallicum R. giardinii R. laguerreae R. leguminosarum

R. pisi

E. americanum E. chiapanecum, E. mexicanum E. fredii E. meliloti

E. saheli, E. terangae

M. amorphae, M. mediterraneum, M. tianshanense M. ciceri M. tamadayense B. canariense B. cytisi B. japonicum B. retamae

B. rifense Bradyrhizobium sp. Bradyrhizobium sp.

Symbiovar calliandrae

Isolation legume Genus Rhizobium Calliandra grandiflora

References Rincón-Rosales et al., 2013

mimosae phaseoli officinalis orientalis gallicum phaseoli gallicum phaseoli viciae phaseoli trifolii viciae trifolii viciae

Mimosa affinis Phaseolus vulgaris Galega officinalis Galega orientalis Phaseolus vulgaris Phaseolus vulgaris Phaseolus vulgaris Phaseolus vulgaris Vicia spp. Phaseolus vulgaris Trifolium spp. Pisum sativum, Vicia spp. Trifolium spp. Pisum sativum, Vicia spp.

Wang et al., 1999a Segovia et al., 1993 Radeva et al., 2001 Radeva et al., 2001 Amarger et al., 1997 Amarger et al., 1997 Amarger et al., 1997 Amarger et al., 1997 Sa¨ıdi et al., 2013 Jordan, 1984; Garc´ıa-Fraile 2010 Jordan 1984; Garc´ıa-Fraile, 2010 Jordan, 1984; Garc´ıa-Fraile, 2010 Marek-Kozaczuk et al., 2013 Robledo et al., 2011

mediterranense acaciellae

Genus Ensifer Phaseolus vulgaris Acaciella angustissima

Mnasri et al., 2012 Rogel et al., 2011

fredii mediterranense lancerottense medicaginis mediterranense meliloti rigiduloides acacieae sesbaniae

Glycine max Phaseolus vulgaris Lotus spp. Medicago laciniata Phaseolus vulgaris Medicago sativa Medicago rigiduloides Acacia Sesbania

Mnasri et al., 2007 Mnasri et al., 2007 León-Barrios et al., 2009 Villegas et al., 2006 Mnasri et al., 2007 Villegas et al., 2006 Gubry-Rangin et al., 2013 Lortet et al., 1996 Lortet et al., 1996

ciceri

biserrulae ciceri loti

Genus Mesorhizobium Cicer arietinum

Biserrula pelecinus Cicer arietinum Lotus berthelotii Genus Bradyrhizobium genistearum Genisteae legumes genistearum Cytisus villosus genistearum Genisteae legumes glycinearum Glycine max retamae Retama spp., Lablab purpureus genistearum Retama spp. and other Genisteae legumes genistearum Cytisus villosus sierranevadense Genista versicolor vignae Vigna unguiculata

Rivas et al., 2007

Nandasena et al., 2007 Rivas et al., 2007 Ram´ırez-Bahena et al., 2012 Vinuesa et al., 2005 Chahboune et al., 2011b Vinuesa et al., 2005 Vinuesa et al., 2005 Guerrouj et al., 2013 Guerrouj et al., 2012 Chahboune et al., 2012 Cobo-D´ıaz et al., 2014 Bejarano et al., 2014



of other genes such as nodA. Thus, in the biovar medicaginis of E. meliloti, nodC gene sequence analysis supported the existence of this biovar defined on the basis of nodA gene analysis (Bailly et al., 2007). The nodC gene was used, for instance, to define the biovar mediterranense that include strains of E. fredii and E. meliloti able to nodulate Phaseolus, but not Medicago (Mnasri et al., 2007), or the new biovar lancerottense that was recently described within E. meliloti to include the strains able to nodulate Lotus endemic of Canary Islands (León-Barrios et al., 2009). These strains harbour a nodC gene phylogenetically unrelated to those carried by other E. meliloti biovars and by M. loti. In addition to M. ciceri bv. ciceri (Rivas et al., 2007), another biovar named biserrulae was described based on nodA gene to include rhizobia nodulating Biserrula pelecinus (Nandasena et al., 2007). These two biovars can be also differentiated through nodC gene analysis (Armas-Capote et al., 2014). In the slow-growing genus Bradyhizobium, two biovars named glycinearum and genistearum with phylogenetically divergent nodC were defined in B. japonicum to differentiate strains nodulating soybean or Genisteae legumes, respectively (Vinuesa et al., 2005). The biovar genistearum was also defined in B. canariense due to the high similarities of its nodC genes, although for the moment all strains of B. canariense belong to the same biovar (Vinuesa et al., 2005). Therefore, considering all biovars described until year 2011 we can observe both an increase in the trend of using nodC gene to define biovars within rhizobial species, and also its doubtless usefulness as biogeography phylogenetic marker for all rhizobial genera (Laranjo et al., 2008; Han et al., 2009; Lu et al., 2009c; Velázquez et al., 2010b; Garc´ıa-Fraile et al., 2010; Zhang et al., 2011d; D´ıaz-Alcántara et al., 2013; Ram´ırezBahena et al., 2013b). 2.

New symbiovars based on the analysis of symbiotic genes Rogel et al. (2011) proposed the term “symbiovar” to replace “biovar” based on the fact that this term designs the groups within a species able to establish symbiosis with a specific legume. From this date, the new biovars defined within rhizobial species are called symbiovars, although they are completely equivalent as occurred in the case of the old biovar mediterranense that is now called symbiovar mediterranense (Mnasri et al., 2012). Rogel et al. (2011) included in their proposal the description of the first new symbiovar acaciellae within E. chiapanecum and E. mexicanum from the nodC and nifH gene analysis. Although the nifH gene was initially proposed to identify the biovar phaseoli (Mart´ınez et al., 1985; Aguilar et al., 1998), it has been used to show that the novel species R. calliandrae, R. jaguaris and R. mayense share the biovar calliandrae (Rincón-Rosales et al., 2013). The ability of a strain to fix nitrogen has also been used to define the symbiovar rigiduloides within E. meliloti as the symbiovar is able to fix nitrogen in M. rigiduloides but not in M. truncatula (Gubry-Rangin et al., 2013).

29

Nevertheless, in genus Bradyrhizobium, the recently described symbiovar retamae within B. retamae was defined based on nodC genes, which were phylogenetically divergent to those of the remaining symbiovars from the genus, including the symbiovar genistearum able to nodulate the same host, Retama (Guerrouj et al., 2013). After the last symbiovars descriptions, it is clear that there is not a general consense yet in the symbiovar concept, because different features have been used to define the distinct symbiovars reported up to date. In our opinion, it is essential to gain a consense and establish a common feature on which symbiovars are defined that makes it possible to analyse together all symbiovars of rhizobia for evolutionary and biogeography studies. Considering that nifH gene phylogenies are not completely congruent with those of nodulation genes (Laguerre et al., 2001), and that nod genes are the ones involved in nodulation, which is a unique characteristic of nodulating bacteria, they are the most suitable for phylogenetic analysis of symbiovars. The nodC gene has a single copy in most rhizobial genomes sequenced up to date and all nodC genes have the same function, which facilitates to predict the host range of a strain. For all these reasons, we propose to include the nodC gene as a minimal standard for rhizobial symbiovars definition. Due to its relatively high conservation degree, the nodC gene may even allow to phylogenetically analyze those of all rhizobial species, which is very useful for biogeography studies. C.

The Concept of Promiscuity in the Rhizobia-Legume Symbiosis The concept of promiscuity is directly linked to the concept of symbiovars and host range of rhizobia. It has been known for many years that legumes have different promiscuity degrees. Whereas some of them can be nodulated by several species of rhizobia such as Macroptilium or Phaseolus (Perret et al., 2000; Michiels et al., 1998; Zurdo-Piñeiro et al., 2009; Garc´ıa-Fraile et al., 2010), others are restrictive hosts for nodulation such as Cicer, Trifolium or Vicia (Broughton and Perret 1999). In the same way, rhizobial strains can have a broad or a narrow host range. For instance, some R. leguminosarum bv. trifolii strains can only nodulate plants of genus Trifolium whereas Ensifer sp. NGR234 nodulates over 100 legumes as well as the non-legume Parasponia (Pueppke and Broughton 1999). Utilization of the promiscuity concept requires caution because this feature in a legume should not be based on the number of taxonomic (chromosomal) rhizobial species able to nodulate it, but on the different symbiotic genes able to induce the nodulation process (Rivas et al., 2007). The nod genes are responsible for the synthesis of Nod factors (lipochitin-oligosaccharides) that are receptors for the plant flavonoid signal (Denarié et al., 1996; Broughton and Perret, 1999; Downie and Walker, 1999; Gough and Cullimore, 2011; Oldroyd, 2013). The nod genes of the operon nodABC are determinants of the host range (Winsor 1989; Györgypal et al., 1991; Relic et al., 1994; Roche et al., 1996; Perret et al., 2000). Within these genes, the nodC has been widely analyzed in

30

A. PEIX ET AL.

rhizobial strains and found to be related not only with the host range of rhizobia but also with the promiscuity degree of the hosts (Roche et al., 1996; Perret et al., 2000; Laguerre et al., 2001; Rivas et al., 2007; Iglesias et al., 2007; Zurdo-Piñeiro et al., 2009, Ru´ız-D´ıez et al., 2012a, b). The analysis of this gene allowed confirmation that P. vulgaris is a very promiscuous host as it can be nodulated by several divergent nodC symbiovars such as phaseoli, gallicum, giardinii and mediterranense, and that C. arietinum is a very resctrictive host as it can be nodulated only by the symbiovar ciceri (Table 3).


1.

Host range of rhizobia and legume promiscuity Some strains of rhizobia are able to nodulate a high number of legumes whereas other strains can only nodulate a few hosts. The ability to nodulate more than one host may rely on the promiscuity either of the rhizobia, or the legumes, or both. The existence of several copies of the nodD gene in many strains of rhizobia permits them to respond to different types of flavonoids, which enables the infection of very different legumes (Perret et al., 2000). Strains of genus Ensifer such as NGR234 and USDA257 share a broad similar host range (Pueppke and Broughton, 1999) and have two different nodD genes (Schuldes et al., 2012). Moreover, R. tropici type strain CIAT 899 can nodulate several legumes including P. vulgaris, Leucaena leucocephala and Macroptilium atropurpureum because it harbours several nodD copies (van Rhijn et al., 1993). The broad host range of CIAT 899 has also been related to the existence of different nodA genes (Ormeño-Orrillo et al., 2012a). Summarizing, the ability of a strain to nodulate several legumes is linked to the presence in its genome of different nodulation genes, but also with the legume promiscuity. The legume tribes Cicereae, Trifoliae and Viciae are very restrictive for nodulation (Perret et al., 2000). C. arietinum can be nodulated by strains of several species of Mesorhizobium, but all of them carry nearly identical nodC genes and belong to the symbiovar ciceri (Rivas et al., 2007; Laranjo et al., 2008). In contrast, P. vulgaris is very promiscuous, and can be nodulated by different symbiovars that carry very divergent symbiotic genes (Michiels et al., 1998; Zurdo-Piñeiro et al., 2009). The study of the promiscuity degree of legumes deserves more investigations to fill the the lack of knowledge about all the endosymbionts able to nodulate each legume. Accordingly, more diversity studies are necessary before establishing conclusions at this respect. D.

Bacterial Endophytes of Legume Nodules Together with rhizobia, legume nodules are occupied by a variable microbiome where very phylogenetically diverse bacteria co-inhabit and play a usually unknown ecological role with respect to the plant. In the last decades, research on the genetic diversity of nodule legume endophytes has increased and currently it is an attractive field of research complementary to that of rhizobial diversity. The analysis of rrs gene allowed the classification of bacterial endophytes known up to

date into several species, genera, families and classes within the phyla Proteobacteria, Firmicutes and Actinobacteria (reviewed in Velázquez et al., 2013). In the last years several new genera and species of bacteria have been isolated from legume nodules (Table 4). Nevertheless, the number of legumes analysed up to date represent a minimal part of those able to nodulate and, therefore, the number of endophytic species isolated from nodules will increase in the future. Moreover, there is still a lack of information on the role of the legume nodular endophytes in the infection process by rhizobia as well as about their possible contribution to nitrogen fixation and plant growth. The development of more research about the nodular endophytic diversity will highlight their importance in the legume symbiosis enabling likely their use in agriculture.

1.

Gram-negative endophytes Gram-negative nodular endophytes have been reported in the last years, mainly within alpha, beta and gamma-Proteobacteria. Since the “classical” rhizobia are classified within alphaProteobacteria, it was considered for many years that rhizobial strains should always nodulate legumes. Currently, we know that rhizobia can also be endophytic in legume nodules. In fact, it is common the isolation of rhizobial strains from nodules that, despite their inability to reinfect the legume from which they were isolated, can even promote its growth. In this way, R. leguminosarum bv. phaseoli and M. loti isolated from nodules of T. pratense (Sturtz et al., 1997) and strains of genera Rhizobium, Ensifer and Shinella isolated from nodules of Vicia were unable to reinfect the plants from which they were isolated (Lei et al., 2008). Not surprisingly, genus Agrobacterium (currently classified as Rhizobium) is one of the most reported endophytes of legume nodules (see Velázquez et al., 2013). Genetic diversity of endophytic alpha-Proteobacteria that can be found in legume nodules has been revealed by studies of Zakhia et al. (2006), Muresu et al. (2008), Deng et al. (2011a), Hoque et al. (2011) and Li et al. (2008). Although many of the isolated strains did not form nodules, some of them have nifH genes close to those of E. meliloti (Zakhia et al., 2006). Isolated from alfalfa nodules, a novel endophytic genus Endobacter (family Acetobacteraceae) has been described (Ram´ırezBahena et al., 2013c). The genus Burkholderia from beta-Proteobacteria contains species able to induce effective nodules in different legumes, but also can live as an endophyte in several legume nodules. Endophytic Burkholderia strains were found in nodules of Mimosa pudica (Pandey et al., 2005), G. max (Li et al., 2008) and Acacia seyal (Diouf et al., 2007). The beta-Proteobacteria Herbaspirillum lusitanum is endophytic of common bean nodules (Valverde et al., 2003) and its genome has been completely sequenced (Weiss et al., 2012). Genus Herbaspirillum and other beta Proteobacteria have been found in Acacia nodules (Hoque et al., 2011).

31


TABLE 4 New genera and species of bacteria isolated from the first time from legume nodules and unable to nodulate legumes (endophytic bacteria)


Species Bosea lathyrus Bosea lupini Bosea robiniae Devosia yakushimensis Endobacter medicaginis Herbaspirillum lusitanum Ochrobactrum ciceri Labrys neptuniae Phyllobacterium endophyticum Phyllobacterium loti Tardiphaga robiniae Cohnella lupini Cohnella phaseoli Fontibacillus phaseoli Kribbella lupini Micromonospora lupini Micromonospora pisi Micromonospora saelisecensis Paenibacillus endophyticus Paenibacillus lupini Paenibacillus prosopidis Paracoccus sphaerophysae

Legume host Gram negative Lathyrus latifolius Lupinus polyphyllus Robinia pseudoacacia Pueraria lobata Medicago sativa Phaseolus vulgaris Cicer arietinum Neptunia natans Phaseolus vulgaris Lotus corniculatus Robinia pseudoacacia Gram positive Lupinus albus Phaseolus vulgaris Phaseolus vulgaris Lupinus angustifolius Lupinus angustifolius Pisum sativum Lupinus angustifolius Cicer arietinum Lupinus albus Prosopis farcta Sphaerophysa salsula

Within gamma-Proteobacteria, the presence of Pseudomonas strains in legume nodules was first described by Benhizia et al. (2004), and later reported by other authors (Zakhia et al., 2006; Ibán˜ ez et al., 2009; Deng et al., 2011a). In addition to Pseudomonas, the most abundant endophytes of legume nodules from gamma-Proteobacteria belong to the Enterobacteraceae, which have been found together with other endophytic species from the same class (Zakhia et al., 2006; Ibán˜ ez et al., 2009; Deng et al., 2011a; Hoque et al., 2011; Li et al., 2008). In conclussion, results obtained up to date in different studies carried out in diverse legumes show that Gram-negative bacteria are the most widely extended in legume nodules. They include not only endosymbionts able to induce the nodulation process, but also endophytic strains, many of them able to fix atmospheric nitrogen, that can contribute significantly to the efficience of the rhizobia-legume symbiosis (Velázquez et al., 2013). 2.

Gram-positive endophytes Although the best studied mutualistic interactions between plants and microorganisms involve Gram-negative bacteria, the presence of Gram-positive bacteria in legume nodules is more frequent than was initially thought. In this way, several en-

Reference de Meyer and Willems, 2012 de Meyer and Willems, 2012 de Meyer and Willems, 2012 Bautista et al., 2010 Ram´ırez-Bahena et al., 2013c Valverde et al., 2003 Imran et al., 2010 Chou et al., 2007 Flores-Félix et al., 2013 Sánchez et al., 2014 de Meyer et al., 2012 Flores-Félix et al., 2014 Garc´ıa-Fraile et al., 2008 Flores-Félix et al., 2014 Trujillo et al., 2006 Trujillo et al., 2007 Garc´ıa et al., 2010 Trujillo et al., 2007 Carro et al., 2013 Carro et al., 2014 Valverde et al., 2010 Deng et al., 2011b

dophytic new species of legume nodules belong to the phyla Firmicutes and Actinobacteria which comprises Gram-positive bacteria with low and high G+C content, respectively. Although some non-sporulating strains from the Firmicutes have been isolated from legume nodules (Deng et al., 2011a), the most abundant endophytes are sporulating bacilli from genera Bacillus and Paenibacillus (Zakhia et al., 2006; Shiraishi et al., 2010; Deng et al., 2011a; Li et al., 2008; Rajendran et al., 2012). More than 20% of the strains isolated from nodules of Glycyrrhiza plants were Gram-positive bacteria, with 30 strains belonging to genus Paenibacillus (Li et al., 2008). Also, about 30% of the strains isolated from nodules of Trigonella foenumgraecum were Gram-positive bacilli (Rajendran et al., 2012). The importance of sporulating bacilli as nodule endophytes is pointed out by the increasing number of new species being described, among them P. endophyticus and Cohnella phaseoli isolated from nodules of Cicer and Phaseolus, respectively (Carro et al., 2013; Flores-Félix et al., 2013a). The phylum Actinobacteria is also widely represented in legume nodules, from which several species and and genera, among them Microbacterium, Mycobacterium, Agromyces, Ornithinicoccus, Nocardia, Streptomyces and Micromonospora

32

A. PEIX ET AL.

have been isolated (Zakhia et al., 2006; Trujillo et al., 2010; Deng et al., 2011a).


3.

Beneficial interactions between nodule endophytes and legumes Plant endophytes, including those living in legume nodules, have a great potential as plant growth-promoting rhizobacteria for use in agriculture. The presence of in vitro plant growth promotion mechanisms has been analysed in several endophytes, including those of the Agrobacterium/Rhizobium group considered as pathogenic bacteria. For example, strains close to A. tumefaciens (currently R. radiobacter) recently isolated from nodules of the medicinal legume Glycyrrhiza in China showed ability to solubilize phosphate, to produce indole acetic acid and siderophores and to express ACC deaminase acivity (Li et al., 2012). Similarly, a strain of this species isolated from nodules of Lespedeza showed different in vitro plant growth promotion mechanisms such as phosphate solubilization, ACC deaminase activity and siderophore and indole acetic acid production (Palaniappan et al., 2010). The study of plant growth promotion mechanisms in Rhizobium sensu stricto strains have revealed that R. leguminosarum bv. phaesoli and trifolii produce indole acetic acid and siderophores, and promote plant growth even of non legume plants (Garc´ıa-Fraile et al., 2012; Flores-Félix et al., in press). Within beta-Proteobacteria, Burkholderia strains presented in vitro plant growth mechanisms such as phytohormone secretion, ACC deaminase, phosphate solubilization and biocontrol activity (Pandey et al., 2005). Nevertheless, these mechanisms have been mostly studied in sporulating bacilli because sporulation represents a technologic advantage over other bacteria for biofertilizers formulation. Li et al. (2012) studied Paenibacillus strains isolated from legume nodules and found that a high percentage of them had protease and cellulose activity, siderophores and also small amounts of IAA production. The presence of in vitro mechanisms of plant growth promotion, however, do not guarantee a plant growth promotion activity in vivo, and viceversa, strains where the studied plant growth promotion mechanisms were absent or not detected could be an active PGPR in vivo. In fact, a strain of P. fluorescens able to promote plant growth that have not the commonly analysed in vitro plant growth promotion mechanisms have been reported (Smyth et al., 2011). Therefore, the ability of plant growth promotion should be analysed in vivo in order to select nodule endophytic strains for inoculation of legumes and non legumes. This way, a strain of the former species A. radiobacter promoted plant growth of Lespedeza (Palaniappan et al., 2010) and B. megaterium isolated from T. pratense nodules was able to promote its growth in absence of Rhizobium (Sturz et al., 1997). Moreover, a strain of Streptomyces lydicus isolated from P. sativum nodules promoted growth of this plant by increasing the nodule size and enhancing assimilation of iron and possibly other soil nutrients (Tokala et al., 2002). Also, inoculations with non-rhizobial strains isolated from nodules of M. sativa

caused significant increase in shoot and root parameters compared to those of the uninoculated control plants (Stajkovi et al., 2009). In some cases, the effect of coinoculations with endophytic bacteria and Rhizobium has also been explored. Combinations of endophytic R. leguminosarum bv. phaseoli strains and R. leguminosarum bv. trifolii resulted in the promotion of clover growth (Sturtz et al., 1997). Moreover, B. insolitus and B. brevis isolated from T. pratense nodules were able to promote the nodulation by R. leguminosarum bv. trifolii (Sturz et al., 1997). B. subtilis, B. thuringiensis and B. pumilus isolated from G. max promoted plant growth when they were coinoculated with Bradyrhizobium strains nodulating this host (Bai et al., 2002; Li et al., 2008). Single, dual and triple inoculations of P. vulgaris with Rhizobium, N2 -fixing B. subtilis and P-solubilizing B. megaterium resulted in an increase in growth, nodulation and seed yield under field conditions (Elkoca et al., 2010). In summary, diversity and ecology of bacterial associations with legumes is a broad research field that, in spite of the advances gained over the years, remains poorly studied and deserves more investigations specially from now, the ‘green age,’ in which plant production must necessarily be obtained under environmentally friendly schemes in order to preserve ecosystems balance and conservation of biodiversity. ACKNOWLEDGMENTS We thank M. Fernández-Pascual for her critical review of this manuscript. The authors would also like to thank our numerous collaborators and students involved in this research over the years. FUNDING Funding was provided by Ministerio de Ciencia e Innovación (MICINN), Junta de Castilla y León and Junta de Andaluc´ıa from Spain. REFERENCES Amarger, N., Macheret, V., and Laguerre, G. 1997. Rhizobium gallicum sp. nov., and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int. J. Syst. Bacteriol. 47: 996–1006. Aguilar, O. M., Grasso, D. H., Riccillo, P. M., López, M. V., and Szafer, E. 1998. Rapid identification of bean Rhizobium isolates by a nifH gene-pcr assay. Soil Biol. Biochem. 30: 1655–1661. Amadou, C., Pascal, G., Mangenot, S., Glew, M., Bontemps, C., Capela, D., Carrere, S., Cruveiller, S., Dossat, C., Lajus, A., Marchetti, M., Poinsot, V., Rouy, Z., Servin, B., Saad, M., Schenowitz, C., Barbe, V., Batut, J., Medigue, C. and Masson-Boivin, C. 2008. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 18: 1472–1483. Andam, C. P., Mondo, S. J., and Parker, M. A. 2007. Monophyly of nodA and nifH Genes across Texan and Costa Rican Populations of Cupriavidus Nodule Symbionts. Appl. Environ. Microbiol. 73: 4686–4690. Angus, A. A., and Hirsch, A. M. 2010. Insights into the history of the legumebetaproteobacterial symbiosis. Mol. Ecol. 19: 28–30. Arason, G. J. 1996. Lectins as molecules in vertebrates and invertebrates. Fish Shellfish Immunol. 6: 277–289.


BACTERIAL ASSOCIATIONS WITH LEGUMES Ardley, J. K., Parker, M. A., de Meyer, S. E., Trengove, R. D., O’Hara, G. W., Reeve, W. G., Yates, R. J., Dilworth, M. J., Willems, A., and Howieson, J. G. 2012. Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are alphaproteobacterial root-nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int. J. Syst. Evol. Microbiol. 62: 2579–2588. Armas-Capote, N., Pérez-Yepez, J., Mart´ınez-Hidalgo, P., Garzón-Machado, V., del Arco-Aguilar, M., Velázquez, E. and León-Barrios, M. 2014. Core and symbiotic genes reveal nine Mesorhizobium genospecies and three symbiotic lineages among the rhizobia nodulating Cicer canariense in its natural habitat (La Palma, Canary Is.) Syst. Appl. Microbiol.. 37: 140–148. Bai, Y., D’Aoust, F., Smith, D. L., and Driscoll, B. T. 2002. Isolation of plantgrowth-promoting Bacillus strains from soybean root. Can. J. Microbiol. 48: 230–238. Bailly, X., Olivieri, I., Brunel, B., Cleyet-Marel, J. C., and Béna, G. 2007. Horizontal gene transfer and homologous recombination drive the evolution of the nitrogen-fixing symbionts of Medicago species. J. Bacteriol. 189: 5223–5236. Baldwin, I. L., and Fred, E. B. 1929. Nomenclature of the root-nodule bacteria of Leguminosae. J. Bacteriol. 17: 141–150. Barnett, M. J., Fisher, R. F., Jones, T., Komp, C., Abola, A. P., Barloy-Hubler, F., Bowser, L., Capela, D., Galibert, F., Gouzy, J., Gurjal, M., Hong, A., Huizar, L., Hyman, R. W., Kahn, D., Kahn, M. L., Kalman, S., Keating, D. H., Palm, C., Peck, M. C., Surzycki, R., Wells, D. H., Yeh, K. C., Davis, R. W., Federspiel, N. A., and Long, S. R. 2001. Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc. Natl. Acad. Sci. USA. 98: 9883–9888. Barrett, C. F., and Parker, M. A. 2006. Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl. Environ. Microbiol. 72: 1198–1206. Bautista, V. V., Monsalud, R. G., and Yokota, A. 2010. Devosia yakushimensis sp. nov., isolated from root nodules of Pueraria lobata (Willd.) Ohwi. Int. J. Syst. Evol. Microbiol. 60: 627–632. Beijerinck, M. W. 1888. Cultur des Bacillus radicicola aus den Knöllchen. Bot. Ztg. 46: 740–750. Beijerinck, M. W., and van Delden, A. 1902. Ueber die Assimilation des freien Stickstoffs durch Bakterien. Zentbl. Bakt. Parasitenk. Infekt. Abt II 9: 3–43. Bejarano, A., Ram´ırez-Bahena, M. H., Velázquez, E., and Peix, A. 2014. Vigna unguiculata is nodulated in Spain by endosymbionts of Genisteae legumes and by a new symbiovar (vignae) of the genus Bradyrhizobium. Syst Appl Microbiol. In press. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A., and Squartini, A. 2004. Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst. Appl. Microbiol. 27: 462–468. Berge, O., Lodhi, A., Brandelet, G., Santaella, C., Roncato, M. A., Christen, R., Heulin, T., and Achouak, W. 2009. Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int. J. Syst. Evol. Microbiol. 59: 367–372. Bibi, F., Chung, E. J., Khan, A., Jeon, C. O., and Chung, Y. R. 2012. Rhizobium halophytocola sp. nov., isolated from the root of a coastal dune plant. Int. J. Syst. Evol. Microbiol. 62: 1997–2003. Bontemps, C., Elliott, G. N., Simon, M. F., Dos Reis Júnior, F. B., Gross, E., Lawton, R. C., Neto, N. E., Loureiro, M. F, de Faria, S. M., Sprent, J. I., James, E. K., and Young, J. P. 2010. Burkholderia species are ancient symbionts of legumes. Mol. Ecol. 19: 44–52. Bournaud, C., de Faria, S. M., dos Santos, J. M., Tisseyre, P., Silva, M., Chaintreuil, C., Gross, E., James, E. K., Prin, Y., and Moulin, L. 2013. Burkholderia species are the most common and preferred nodulating symbionts of the Piptadenia group (tribe Mimoseae). PLoS One. 8: e63478. Bouzar, H., and Jones, J. B. 2001. Agrobacterium larrymoorei sp. nov., a pathogen isolated from aerial tumours of Ficus benjamina. Int. J. Syst. Evol. Microbiol. 51: 1023–1026. Boyd, M., Varney, T., Surette, C., and Surette, J. 2008. Reassessing the northern limit of maize consumption in North America: stable isotope, plant micro-

33

fossil, and trace element content of carbonized food residue. J. Archaeol. Sci. 35: 2545–2556. Broothaerts, W., Mitchell, H. J., Weir, B., Kaines, S., Smith, L. M., Yang, W., Mayer, J. E., Roa-Rodr´ıguez, C., and Jefferson, R. A. 2005. Gene transfer to plants by diverse species of bacteria. Nature 433: 629–633. Broughton, W. J., Jabbouri, S., and Perret, X. 2000. Keys to symbiotic harmony. J. Bacteriol. 182: 5641–5652. Broughton, W. J., and Perret, X. 1999. Genealogy of legume-Rhizobium symbioses. Curr. Opin. Plant. Biol. 2: 305–311. Buchanan, R. E. 1926. What names should be used for the organisms producing nodules on the roots of leguminous plants? Proc. Iowa Acad. Sci. 33: 81–90. Carro, L., Flores-Felix, J. D., Cerda-Castillo, E., Ram´ırez-Bahena, M. H., Igual, J. M., Tejedor, C., Velázquez, E., and Peix, A. 2013. Paenibacillus endophyticus sp. nov., isolated from nodules of Cicer arietinum in Spain. Int. J. Syst. Evol. Microbiol. 63: 4433–4438. Carro, L., Flores-Felix, J. D., Ram´ırez-Bahena, M. H., Garc´ıa-Fraile, P., Mart´ınez-Hidalgo, P., Igual, J. M., Tejedor, C., Peix, A., and Velápzquez, E. 2014. Paenibacillus lupini sp. nov., isolated from nodules of Lupinus albus. Int. J. Syst. Evol. Microbiol. 64: 3028–3033. Casida, Jr. L. E. 1982. Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in soil. Int. J. Syst. Bacteriol. 32: 339–345. Chahboune, R., Barrijal, S., Moreno, S., and Bedmar, E. J. 2011. Characterization of Bradyrhizobium species isolated from root nodules of Cytisus villosus grown in Morocco. Syst. Appl. Microbiol. 34: 440–445. Chahboune, R., Carro, L., Peix, A., Barrijal, S., Velázquez, E., and Bedmar, E. J. 2011. Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisus villosus. Int. J. Syst. Evol. Microbiol. 61: 2922–2927. Chahboune, R., Carro, L., Peix, A., Ram´ırez-Bahena, M. H., Barrijal, S., Velázquez, E., and Bedmar, E. J. 2012. Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst. Appl. Microbiol. 35: 302–305. Chang, Y. L., Wang, J. Y., Wang, E. T., Liu, H. C., Sui, X. H., and Chen, W. X. 2011. Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea. Int. J. Syst. Evol. Microbiol. 61: 2496–2502. Chen, W. M., de Faria, S. M., Chou, J. H., James, E. K., Elliott, G. N., Sprent, J. I., Bontemps, C., Young, J. P., and Vandamme, P. 2008. Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int. J. Syst. Evol. Microbiol. 58: 2174–2179. Chen, W. M., de Faria, S. M., James, E. K., Elliott, G. N., Lin, K. Y., Chou, J. H., Sheu, S. Y., Cnockaert, M., Sprent, J. I., and Vandamme, P. 2007. Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int. J. Syst. Evol. Microbiol. 57: 1055–1059. Chen, W. M., de Faria, S. M., Straliotto, R., Pitard, R. M., Simões-Araùjo, J. L., Chou, J. H., Chou, Y. J., Barrios, E., Prescott, A. R., Elliott, G. N., Sprent, J. I., Young, J. P., and James, E. K. 2005a. Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl. Environ. Microbiol. 71: 7461–7471. Chen, W. M., James, E. K., Chou, J. H., Sheu, S. Y., Yang, S. Z., and Sprent, J. I. 2005b. Beta-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol. 168: 661–675. Chen, W. M., James, E. K., Coenye, T., Chou, J. H., Barrios, E., de Faria, S. M., Elliott, G. N., Sheu, S. Y., Sprent, J. I., and Vandamme, P. 2006. Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int. J. Syst. Evol. Microbiol. 56: 1847–1851. Chen, W. M., James, E. K., Prescott, A. R., Kierans, M., and Sprent, J. I. 2003a. Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Mol. Plant Microbe Interact. 16: 1051–1061. Chen, W. M., Moulin, L., Bontemps, C., Vandamme, P., Béna, G., and Boivin-Masson, C. 2003b. Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J. Bacteriol. 185: 7266– 7272.


34

A. PEIX ET AL.

Chen, W. M., Zhu, W. F., Bontemps, C., Young, J. P., and Wei, G. H. 2010. Mesorhizobium alhagi sp. nov., isolated from wild Alhagi sparsifolia in North-western China. Int. J. Syst. Evol. Microbiol. 60: 958–962. Chen, W. M., Zhu, W. F., Bontemps, C., Young, J. P., and Wei, G. H. 2011. Mesorhizobium camelthorni sp. nov., isolated from Alhagi sparsifolia. Int. J. Syst. Evol. Microbiol. 61: 574–579. Chen, W. X., Li, G. S., Qi, Y. L., Wang, E. T., Yuan, H. L., and Li, J. L. 1991. Rhizobium huakuii sp. nov., isolated from the root nodules of Astragalus sinicus. Int. J. Syst. Bacteriol. 41: 275–280. Chen, W. X., Tan, Z. Y., Gao, J. L., Li, Y., and Wang, E. T. 1997. Rhizobium hainanense sp. nov., isolated from tropical legumes. Int. J. Syst. Bacteriol. 47: 870–873. Chen, W. X., Wang, E., Wang, S., Li, Y., Chen, X., and Li, Y. 1995. Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China. Int. J. Syst. Bacteriol. 45: 153–159. Chen, W. X., Yan, G. H., and Li, J. L. 1988. Numerical taxonomy study of fastgrowing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int. J. Syst. Bacteriol. 38: 392–397. Chou, Y. J., Elliott, G. N., James, E. K., Lin, K. Y., Chou, J. H., Sheu, S. Y., Sheu, D. S., Sprent, J. I., and Chen, W. M. 2007. Labrys neptuniae sp. nov., isolated from root nodules of the aquatic legume Neptunia oleracea. Int. J. Syst. Evol. Microbiol. 57: 577–581. Cobo-Diaz, J. F., Martinez-Hidalgo, P., Fernandez-Gonzalez, A. J., MartinezMolina, E., Toro, N., Velazquez, E., and Fernandez-Lopez, M. 2014. The endemic Genista versicolor from Sierra Nevada National Park in Spain is nodulated by putative new Bradyrhizobium species and a novel symbiovar (sierranevadense). Syst. Appl. Microbiol. 37: 177–185. Conn, H. J. 1938. Taxonomic relationships of certain non-sporeforming rods in soil. J. Bacteriol. 36: 320–321. Crossman, L. C., Castillo-Ram´ırez, S., McAnnula, C., Lozano, L., Vernikos, G. S., Acosta, J. L., Ghazoui, Z. F., Hernández-González, I., Meakin, G., Walker, A. W., Hynes, M. F., Young, J. P. W., Downie, J. A., Romero, D., Johnston, A. W. B., Dávila, G., Parkhill, J., and González, V. 2008. A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen fixing bacteria. PLoS One. 2–3: e2567. da Silva, K., Florentino, L. A., Barroso da Silva, K. B., de Brandt, E., Vandamme, P., and de Souza Moreira, F. M. 2012. Cupriavidus necator isolates are able to fix nitrogen in symbiosis with different legume species. Syst. Appl. Microbiol. 35(3): 175–182. Dall’agnol, R. F., Ribeiro, R. A., Ormeno-Orrillo, E., Rogel, M. A., Delamuta, J. R., Andrade, D. S., Mart´ınez-Romero, E., and Hungria, M. 2013. Rhizobium freirei, a symbiont of Phaseolus vulgaris very effective in fixing nitrogen. Int. J. Syst. Evol. Microbiol. 63: 4167–4173. Dangeard, P. A. C. 1926. Recherches sur les tubercles radicaux des Légumineuses. 1st ed., Du Botaniste, Paris, France. Dazzo, F. B., Truchet, G. L., Hollingsworth, R. I., Hrabak, E. M., Pankratz, H. S., Philip-Hollingsworth, S., Salzwedel, J. L., Chapman, K., Appenzeller, L. and Squartini, A. 1991. Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs. J. Bacteriol. 173: 5371–5384. de Lajudie, P., Laurent-Fulele, E., Willems, A., Torck, U., Coopman, R., Collins, M. D., Kersters, K., Dreyfus, B., and Gillis, M. 1998a. Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int. J. Syst. Bacteriol. 42: 93–96. de Lajudie, P., Willems, A., Nick, G., Moreira, F., Molouba, F., Hoste, B., Torck, U., Neyra, M., Collins, M. D., Lindström, K., Dreyfus, B., and Gillis, M. 1998b. Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int. J. Syst. Bacteriol. 48: 369–382. de Lajudie, P., Willems, A., Pot, B., Dewettinck, D., Maestrojuan, G., Neyra, M., Collins, M. D., Dreyfus, B., Kersters, K., and Gillis, M. 1994. Polyphasic taxonomy of Rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int. J. Syst. Bacteriol. 44: 715–733. de Meyer, S. E., and Willems, A. 2012. Multilocus sequence analysis of Bosea species and description of Bosea lupini sp. nov., Bosea lathyri sp. nov. and

Bosea robiniae sp. nov., isolated from legumes. Int. J. Syst. Evol. Microbiol. 62: 2505–2510. de Meyer, S. E., Cnockaert, M., Ardley, J. K., Maker, G., Yates, R., Howieson, J. G., and Vandamme, P. 2013a. Burkholderia sprentiae sp. nov. isolated from Lebeckia ambigua root nodules from South Africa. Int. J. Syst. Evol. Microbiol. 63: 2505–2510. de Meyer, S. E., Cnockaert, M., Ardley, J. K., Trengove, R. D., Garau, G., Howieson, J. G., and Vandamme, P. 2013b. Burkholderia rhynchosiae sp. nov. isolated from Rhynchosia ferulifolia root nodules from South Africa. Int. J. Syst. Evol. Microbiol. 63: 3944–3949. de Meyer, S. E., Coorevits, A., and Willems, A. 2012. Tardiphaga robiniae gen. nov., sp. nov., a new genus in the family Bradyrhizobiaceae isolated from Robinia pseudoacacia in Flanders (Belgium). Syst. Appl. Microbiol. 35: 205–214. de Meyer, S. E., Cnockaert, M., Ardley, J. K., Van Wyk, B. E., Vandamme, P. A., and Howieson, J. G. 2014. Burkholderia dilworthii sp. nov., isolated from Lebeckia ambigua root nodules. Int. J. Syst. Evol. Microbiol. 64: 1090–1095. Degefu, T., Wolde-Meskel, E., Liu, B., Cleenwerck, I., Willems, A., and Frosteg˚ard, Å. 2013. Mesorhizobium shonense sp. nov., Mesorhizobium hawassense sp. nov. and Mesorhizobium abyssinicae sp. nov., isolated from root nodules of different agroforestry legume trees. Int. J. Syst. Evol. Microbiol. 63: 1746–1753. Delamuta, J. R., Ribeiro, R. A., Ormeño-Orrillo, E., Melo, I. S., Mart´ınezRomero, E., and Hungria, M. 2013. Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int. J. Syst. Evol. Microbiol. 63: 3342–3351. Denarié, J., Debbelle, F., and Promé, J.C. 1996. Rhizobium lipo-chitinoligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Ann. Rev. Biochem. 65: 503–535. Deng, Z. S., Zhao, L. F., Kong, Z. Y., Yang, W. Q., Lindström, K., Wang, E. T., and Wei, G. H. 2011a. Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol. Ecol. 76: 463–475. Deng, Z. S., Zhao, L. F., Xu, L., Kong, Z. Y., Zhao, P., Qin, W., Chang, J. L., and Wei, G. H. 2011b. Paracoccus sphaerophysae sp. nov., a siderophoreproducing, endophytic bacterium isolated from root nodules of Sphaerophysa salsula. Int. J. Syst. Evol. Microbiol. 61: 665–669. Diange, E. A., and Lee, S. S. 2013. Rhizobium halotolerans sp. nov., Isolated from chloroethylenes contaminated soil. Curr. Microbiol. 66: 599–605. D´ıaz-Alcántara, C. A., Ram´ırez-Bahena, M. H., Mulas, D., Garc´ıa-Fraile, P., Gómez-Moriano, A., Peix, A., Velázquez, E., and González-Andres, F. 2013. Analysis of rhizobial strains nodulating Phaseolus vulgaris in the Hispaniola Island, a geographic bridge between Meso and South America and the first historical link with Europe. Int. J. Syst. Evol. Microbiol. 37: 149–156. Diouf, D., Samba-Mbaye, R., Lesueur, D., Ba, A. T., Dreyfus, B., de Lajudie, P., and Neyra, M. 2007. Genetic diversity of Acacia seyal Del. rhizobial populations indigenous to Senegalese soils in relation to salinity and pH of the sampling sites. Microbial Ecol. 54: 553–566. dos Reis, F. B. Jr., Simon, M. F., Gross, E., Boddey, R. M., Elliott, G. N., Neto, N. E., Loureiro, M. F., de Queiroz, L.P., Scotti, M. R., Chen, W. M., Norén, A., Rubio, M. C., de Faria, S. M., Bontemps, C., Goi1, S. R., Young, J. P. W., Sprent, J. I., and James, E. K. 2010. Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol. 186: 934–946. Downie, J. A., and Walker, S. A. 1999. Plant responses to nodulation factors. Curr. Opin. Plant Biol. 2: 483–489. Dreyfus, B., Garcia, J. L., and Gillis, M. 1988. Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a Stem-Nodulating Nitrogen-Fixing Bacterium Isolated from Sesbania rostrata. Int. J. Syst. Bacteriol. 38: 89–98. Durán, D., Rey, L., Mayo, J., Zún˜ iga-Davila, D., Imperial, J., Ruiz-Argüeso, T., Mart´ınez-Romero, E., and Ormeño-Orrillo, E. 2014a. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int. J. Syst. Evol. Microbiol. 64: 2072–2078.


BACTERIAL ASSOCIATIONS WITH LEGUMES Durán, D., Rey, L., Navarro, A., Busquets, A., Imperial, J., and Ruiz-Argüeso, T. 2014b. Bradyrhizobium valentinum sp. nov., isolated from effective nodules of Lupinus mariae-josephae, a lupine endemic of basic-lime soils in Eastern Spain. Syst Appl Microbiol. 37: 336–341. Eckhardt, M. M., Baldwin, I. R., and Fred, E. B. 1931. Studies on the root-nodule bacteria of Lupinus. J. Bacteriol. 21: 273–285. Ejigui, J., Savoie, L., Marin, J., and Desrosiers, T. 2007. Improvement of the nutritional quality of a traditional complementary porridge made of fermented yellow maize (Zea mays): effect of maize-legume combinations and traditional processing methods. Food. Nutr. Bull. 28: 23–34. Elkoca, E., Turan, M., and Donmez, M. F. 2010. Effects of single, dual and triple inoculations with Bacillus subtilis, Bacillus megaterium and Rhizobium leguminosarum bv. phaseoli on nodulation, nutrient uptake, yield and yield parameters of common bean (Phaseolus vulgaris L). J. Plant Nutr. 33: 2104–2119. Elliott, G. N., Chen, W. M., Bontemps, C., Chou, J. H., Young, J. P., Sprent, J. I., and James, E. K. 2007a. Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann. Bot. 100: 1403–1411. Elliott, G. N., Chen, W. M., Chou, J. H., Wang, H. C., Sheu, S. Y., Perin, L., Reis, V. M., Moulin, L., Simon, M. F., Bontemps, C., Sutherland, J. M., Bessi, R., de Faria, S. M., Trinick, M. J., Prescott, A. R., Sprent, J. I., and James, E. K. 2007b. Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol. 173: 168–180. Elliott, G. N., Chou, J. H., Chen, W. M., Bloemberg, G. V., Bontemps, C., Mart´ınez-Romero, E., Velázquez, E., Young, J. P., Sprent, J. I., and James, E. K. 2009. Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ. Microbiol. 11: 762–778. Finan, T. M. 2002. Evolving insights: symbiosis islands and horizontal gene transfer. J. Bacteriol. 184: 2855–2856. Finucane, B., Agurto, P. M., and Isbell, W. H. 2006. Human and animal diet at Conchopata, Peru: stable isotope evidence for maize agriculture and animal management practices during the Middle Horizon. J. Archaeol. Sci. 33: 1766–1776. Flores, M., Morales, L., Avila, A., González, V., Bustos, P., Garc´ıa, D., Mora, Y., Guo, X., Collado-Vides, J., Piñero, D., Dávila, G., Mora, J., and Palacios, R. 2005. Diversification of DNA sequences in the symbiotic genome of Rhizobium etli. J. Bacteriol. 187: 7185–7192. Flores-Félix, J. D., Carro, L., Ram´ırez-Bahena, M. H., Tejedor, C., Igual, J. M., Peix, A., and Velázquez, E. 2014. Cohnella lupini sp. nov., an endophytic bacterium isolated from root nodules of Lupinus albus. Int. J. Syst. Evol. Microbiol. 64: 83–87. Flores-Félix, J. D., Menéndez, E., Rivera, L. P., Marcos-Garc´ıa, M., Mart´ınezHidalgo, P., Mateos, P. F., Mart´ınez-Molina, E., Velázquez, E., Garc´ıa-Fraile, P., and Rivas, R. 2013. Use of Rhizobium leguminosarum as a potential biofertilizer for Lactuca sativa and Daucus carota crops. J. Plant Nutr. Soil Sci. 166: 876–882. Flores-Felix, J. D., Mulas, R., Ram´ırez-Bahena, M. H., Cuesta, M. J., Rivas, R., Brañas, J., Mulas, D., González-Andrés, F., Peix, A., and Velázquez, E. 2014. Fontibacillus phaseoli sp. nov. isolated from Phaseolus vulgaris nodules. Antonie Van Leeuwenhoek. 105: 23–28. ¨ Frank, B. 1879. Uber die Parasiten in den Wurzelanschwillungen der Papilionaceen. Bet. Dtsch. Bot. Ges. 37: 394–399. Frank, B. 1889. Ueber die Pilzsymbiose der Leguminosen. Bet. Dtsch. Bot. Ges. 7: 332–346. Fuller, D. Q. 2007. Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Ann. Bot. 100: 903–924. Gao, J. L, Turner, S. L., Kan, F. L., Wang, E. T., Tan, Z. Y., Qiu, Y. H., Gu, J., Terefework, Z., Young, J. P., Lindström, K., and Chen, W. X. 2004. Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the Northern regions of China. Int. J. Syst. Evol. Microbiol. 54: 2003–2012. Garc´ıa, L. C., Martinez-Molina, E., and Trujillo, M. E. 2010. Micromonospora pisi sp. nov., isolated from root nodules of Pisum sativum. Int. J. Syst. Evol. Microbiol. 60: 331–337.

35

Garc´ıa-Fraile, P., Mulas-Garc´ıa, D., Peix, A., Rivas, R., González-Andrés, F., and Velázquez, E. 2010. Phaseolus vulgaris is nodulated in northern Spain by Rhizobium leguminosarum strains harboring two nodC alleles present in American Rhizobium etli strains: biogeographical and evolutionary implications. Can. J. Microbiol. 56: 657–666. Garc´ıa-Fraile, P., Rivas, R., Willems, A., Peix, A., Martens, M., Mart´ınezMolina, E., Mateos, P. F., and Velázquez, E. 2007. Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int. J. Syst. Evol. Microbiol. 57: 844–848. Garc´ıa-Fraile, P., Velázquez, E., Mateos, P. F., Mart´ınez-Molina, E., and Rivas, R. 2008. Cohnella phaseoli sp. nov., isolated from root nodules of Phaseolus coccineus in Spain, and emended description of the genus Cohnella. Int. J. Syst. Evol. Microbiol. 58: 1855–1859. Garc´ıa-Fraile, P., Carro, L., Robledo, M., Ram´ırez-Bahena, M. H., Flores-Félix, J. D., Fernández, M. T., Mateos, P. F., Rivas, R., Igual, J. M., Mart´ınez-Molina, E., Peix, A., and Velázquez, E. 2012. Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One. 7: e38122. Gaunt, M. W., Turner, S. L-, Rigottier-Gois, L., Lloyd-Macgilp, S. A., and Young, J. P. W. 2001. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 51: 2037–2048. Ghosh, W., and Roy, P. 2006. Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int. J. Syst. Evol. Microbiol. 56: 91–97. Gibson, K. E, Kobayashi, H., and Walker, G. C. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42: 413–441. Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J. C., Jaubert, M., Simon, D., Cartieaux, F., Prin, Y., Bena, G., Hannibal, L., Fardoux, J., Kojadinovic, M., Vuillet, L., Lajus, A., Cruveiller, S., Rouy, Z., Mangenot, S., Segurens, B., Dossat, C., Franck, W. L., Chang, W. S., Saunders, E., Bruce, D., Richardson, P., Normand, P., Dreyfus, B., Pignol, D., Stacey, G., Emerich, D., Verméglio, A., Médigue, C. and Sadowsky, M. 2007. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science. 316: 1307–1312. Gough, C., and Cullimore, J. 2011. Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant Microbe Interact. 24: 867–878. Gray, J. X., and Rolfe, B. G. 1990. Exopolysaccharide production in Rhizobium and its role in invasion. Mol. Microbiol. 4: 1425–1431. Gu, C. T., Wang, E. T., Tian, C. F., Han, T. X., Chen, W. F., Sui, X. H., and Chen, W. X. 2008. Rhizobium miluonense sp. nov., a symbiotic bacterium isolated from Lespedeza root nodules. Int. J. Syst. Evol. Microbiol. 58: 1364– 1368. Gu, T., Sun, L. N., Zhang, J., Sui, X., and Li, S. P. 2014. Rhizobium flavum sp. nov., a triazophos-degrading bacterium isolated from soil under the long-term application of triazophos. Int. J. Syst. Evol. Microbiol. 64: 2017–2022. Guan, S. H., Chen, W. F., Wang, E. T., Lu, Y. L., Yan, X. R., Zhang, X. X., and Chen, W. X. 2008. Mesorhizobium caraganae sp. nov., a novel rhizobial species nodulated with Caragana spp. in China. Int. J. Syst. Evol. Microbiol. 58: 2646–2653. Gubry-Rangin, C., Béna, G., Cleyet-Marel, J. C., and Brunel, B. 2013. Definition and evolution of a new symbiovar, sv. rigiduloides, among Ensifer meliloti efficiently nodulating Medicago species. Syst. Appl. Microbiol. 36: 490–496. Guerrouj, K., Ru´ız-D´ıez, B., Chahboune, R., Ram´ırez-Bahena, M. H., Abdelmoumen, H., Quiñones, M. A., El Idrissi, M. M., Velázquez, E., FernándezPascual, M., Bedmar, E. J., and Peix, A. 2013. Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst. Appl. Microbiol. 36: 218–223. Gulash, M., Ames, P., Larosiliere, R. C., and Bergman, K. 1984. Rhizobia are attracted to localized sites on legume roots. Appl. Environ. Microbiol. 48: 149–152. Gyaneshwar, P., Hirsch, A. M., Moulin, L., Chen, W. M., Elliott, G. N., Bontemps, C., Estrada-de Los Santos, P., Gross, E., Dos Reis, F. B., Sprent, J. I., Young, J. P., and James, E. K. 2011. Legume-nodulating betaproteobacteria:


36

A. PEIX ET AL.

diversity, host range, and future prospects. Mol. Plant Microbe Interact. 24: 1276–1288. Györgypal, Z., Kondorosi, E., and Kondorosi, A. 1991. Diverse signal sensitivity of NodD protein homologs from narrow and broad host range rhizobia. Mol. Plant Microbe Interact. 4: 356–364. Han, L. L., Wang, E. T., Han, T. X., Liu, J., Sui, X. H., Chen, W. F., and Chen, W. X. 2009. Unique community structure and biogeography of soybean rhizobia in the saline-alkaline soils of Xinjiang, China. Plant Soil. 324: 291– 305. Han, T. X., Han, L. L., Wu, L. J., Chen, W. F., Sui, X. H., Gu, J. G., Wang, E. T., and Chen, W. X. 2008a. Mesorhizobium gobiense sp. nov. and Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China. Int. J. Syst. Evol. Microbiol. 58: 2610–2618. Han, T. X., Wang, E. T., Wu, L. J., Chen, W. F., Gu, J. G., Gu, C. T., Tian, C. F., and Chen, W. X. 2008b. Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China. Int. J. Syst. Evol. Microbiol. 58: 1693–1699. Hildebrand, E. M. 1940. Cane gall of brambles caused by Phytomonas rubi N. sp. J. Agric. Res. 61: 685–696. Hirsch, P., and Müller, M. 1985. Blastobacter aggregatus sp. nov., Blastobacter capsulatus sp. nov., and Blastobacter denitrificans sp. nov., new budding bacteria from freshwater habitats. Syst. Appl. Microbiol. 6: 281–286. Hoque, M. S., Broadhurst, L. M., and Thrall, P. H. 2011. Genetic characterization of root-nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across South-Eastern Australia. Int. J. Syst. Evol. Microbiol. 61: 299–309. Hou, B. C., Wang, E. T., Li, Y., Jia, R. Z., Chen, W. F., Gao, Y., Dong, R. J., and Chen, W. X. 2009. Rhizobium tibeticum sp. nov., a symbiotic bacterium isolated from Trigonella archiducis-nicolai (Sirj.) Vassilcz. Int. J. Syst. Evol. Microbiol. 59: 3051–3057. Howieson, J. G., De Meyer, S. E., Vivas-Marfisi, A., Ratnayake, S., Ardley, J. K., and Yates, R. J. 2013. Novel Burkholderia bacteria isolated from Lebeckia ambigua – A perennial suffrutescent legume of the fynbos. Soil Biol. Biochem. 60: 55–64. Hunter, W. J., Kuykendall, L. D., and Manter, D. K. 2007. Rhizobium selenireducens sp. nov.: A Selenite-Reducing alpha-Proteobacteria Isolated From a Bioreactor. Curr. Microbiol. 55: 455–460. Ibán˜ ez, F., Angelini, J., Taurian, T., Tonelli, M. L., and Fabra, A. 2009. Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. System. Appl. Microbiol. 32: 49–55. Iglesias, O., Rivas, R., Garc´ıa-Fraile, P., Abril, A., Mateos, P. F., MartinezMolina, E., and Velázquez, E. 2007. Genetic characterization of fast-growing rhizobia able to nodulate Prosopis alba in North Spain. FEMS Microbiol. Lett. 277: 210–216. Imran, A., Hafeez, F. Y., Frühling, A., Schumann, P., Malik, K. A., and Stackebrandt, E. 2010. Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. Int. J. Syst. Evol. Microbiol. 60: 1548–1553. Islam, M. S., Kawasaki, H., Muramatsu, Y., Nakagawa, Y., and Seki, T. 2008. Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci. Biotechnol. Biochem. 72: 1416–1429. Jarvis, B. D. W., Downer, H. L., and Young, J. P. W. 1992. Phylogeny of fastgrowing soybean-nodulating rhizobia supports synonymy of Sinorhizobium and Rhizobium and assignment to Rhizobium fredii. Int. J. Syst. Bacteriol. 42: 93–96. Jarvis, B. D. W., Pankhurst, C. E., and Patel, J. J. 1982. Rhizobium loti, a new species of legume root nodule bacteria. Int. J. Syst. Bacteriol. 32: 378–380. Jarvis, B. D. W., van Berkum, P., Chen, W. X., Nour, S. M., Fernandez, M. P., Cleyet-Marel, J. C., and Gillis, M. 1997. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int. J. Syst. Evol. Microbiol. 47: 895–898. Jordan D. C. 1982. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int. J. Syst. Bacteriol. 32: 136–139.

Jordan, D. C. 1984 Family III. Rhizobiaceae. In: Bergey’s Manual of Systematic Bacteriology Vol. I. pp. 234–242. Krieg, N. R., and Holt, J. G. Eds., Williams and Wilkins Co, Baltimore, USA. Jordan, D. C., and Allen, O. N. 1974. Family 111. Rhizobiaceae Conn, 1938. In: Bergey’s Manual of Determinative Bacteriology, 8th edition. pp. 261–264. Buchanan, R. E., and Gibbons, N. E., Eds., The Williams & Wilkins Co., Baltimore, USA. Jourand, P., Giraud, E., Béna, G., Sy, A., Willems, A., Gillis, M., Dreyfus, B., and de Lajudie, P. 2004. Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int. J. Syst. Evol. Microbiol. 54: 2269–2273. Judicial Commission of the International Committee on Systematics of Prokaryotes 2008. The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘Sinorhizobium adhaerens’ is not validly published. Opinion 84. Int. J. Syst. Evol. Microbiol. 58: 1973. Kaiya, S., Rubaba, O., Yoshida, N., Yamada, T., and Hiraishi, A. 2012. Characterization of Rhizobium naphthalenivorans sp. nov. with special emphasis on aromatic compound degradation and multilocus sequence analysis of housekeeping genes. J. Gen. Appl. Microbiol. 58: 211–224. Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Watanabe, A., Idesawa, K., Iriguchi, M., Kawashima, K., Kohara, M., Matsumoto, M., Shimpo, S., Tsuruoka, H., Wada, T., Yamada, M., and Tabata, S. 2002. Complete genomic sequence of nitrogen- fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9: 189–197. Kaur, J., Verma, M., and Lal, R. 2011. Rhizobium rosettiformans sp. nov., isolated from hexachlorocyclohexane (HCH) dump site in India, and reclassification of Blastobacter aggregatus Hirsch and Müller (1985) as Rhizobium aggregatum comb. nov. Int. J. Syst. Evol. Microbiol. 61: 1218–1225. Kesari, V., Ramesh, A. M., and Rangan, L. 2013. Rhizobium pongamiae sp. nov. from Root Nodules of Pongamia pinnata. Biomed. Res Int. 2013: 165198. Kirchner, O. 1896. Die Wurzelknöllchen der Sojabohne. Beitr. Biol. Pflanz. 7: 213–224. Kittiwongwattana, C., and Thawai, C. 2013. Rhizobium paknamense sp. nov., isolated from lesser duckweeds (Lemna aequinoctialis). Int. J. Syst. Evol. Microbiol. 63: 3823–3828. Kittiwongwattana, C., and Thawai, C. 2014. Rhizobium lemnae sp. nov., a bacterial endophyte of Lemna aequinoctialis. Int. J. Syst. Evol. Microbiol. 64: 2455–2460. Kuykendall, L. D. 2005. Order VI. Rhizobiales ord. nov. In: Bergey’s Manual of Systematic Bacteriology, 2nd edn, vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria). p. 324. Brenner, D. J., Krieg, N. R., Staley, J. T., and Garrity, G. M. Eds., Springer, New York, USA. Kuykendall, L. D., Saxena, B., Devine, T. E., and Udell, S. E. 1992. Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can. J. Microbiol. 38: 501–505. Laguerre, G., Nour, S. M., Macheret, V., Sanjuan, J., Drouin, P., and Amarger, N. 2001. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology. 147: 981–993. Lang, E., Schumann, P., Adler, S., Spröer, C., and Sahin, N. 2013. Azorhizobium oxalatiphilum sp. nov., and emended description of the genus Azorhizobium. Int. J. Syst. Evol. Microbiol. 63: 1505–1511. Laranjo, M., Alexandre, A., Rivas, R., Velázquez, E., Young, J. P., and Oliveira, S. 2008. Chickpea rhizobia symbiosis genes are highly conserved across multiple Mesorhizobium species. FEMS Microbiol. Ecol. 66: 391–400. Latif, S., Khan, S., Naveed, M., Mustafa, G., Bashir, T., and Mumtaz, A. S. 2013. The diversity of Rhizobia, Sinorhizobia and novel non-Rhizobial Paenibacillus nodulating wild herbaceous legumes. Arch. Microbiol. 195: 647–653. Lei, X., Wang, E. T., Chen, W. F., Sui, X. H., and Chen, W. X. 2008. Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate region of China. Arch. Microbiol. 190: 657–671. Leon-Barrios, M., Lorite, M. J., Donate-Correa, J., and Sanjuan, J. 2009. Ensifer meliloti bv. lancerottense establishes nitrogen-fixing symbiosis with Lotus


BACTERIAL ASSOCIATIONS WITH LEGUMES endemic to the Canary Islands and shows distinctive symbiotic genotypes and host range. Syst. Appl. Microbiol. 32: 413–420. Li, J. H., Wang, E. T., Chea, W. F., and Chen, W. X. 2008. Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biol. Biochem. 40: 238–246. Li, Q. Q., Wang, E. T., Chang, Y. L., Zhang, Y. Z., Zhang, Y. M., Sui, X. H., Chen, W. F., and Chen, W. X. 2011. Ensifer sojae sp. nov., isolated from root nodules of Glycine max grown in saline-alkaline soils. Int. J. Syst. Evol. Microbiol. 61: 1981–1988. Li, L., Sinkko, H., Montonen, L., Wei, G., Lindström, K., and Räsänen, L. A. 2011. Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol. Ecol. 79: 46–68. Lin, D. X., Chen, W. F., Wang, F. Q., Hu, D., Wang, E. T., Sui, X. H., and Chen, W. X. 2009. Rhizobium mesosinicum sp. nov., isolated from root nodules of three different legumes. Int. J. Syst. Evol. Microbiol. 59: 1919–1923. Lin, D. X., Wang, E. T., Tang, H., Han, T. X., He, Y. R., Guan, S. H., and Chen, W. X. 2008. Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int. J. Syst. Evol. Microbiol. 58: 1409–1413. Lin, S. Y., Hsu, Y. H., Liu Y. C., Hung, M. H., Hameed, A., Lai, W. A., Yen, W. S., and Young, C. C. 2014. Rhizobium straminoryzae sp. nov., a novel species isolated from surface of rice-straw in Taiwan. Int. J. Syst. Evol. Microbiol. 64: 2962–2968. Lindström, K. 1989. Rhizobium galegae, a new species of legume root nodule bacteria. Int. J. Syst. Bacteriol. 39: 365–367. Liu, T. Y., Li, Y. Jr., Liu, X. X., Sui, X. H., Zhang, X. X., Wang, E. T., Chen, W. X., Chen, W. F., Puławska, J. 2012a. Rhizobium cauense sp. nov., isolated from root nodules of the herbaceous legume Kummerowia stipulacea grown in campus lawn soil. Syst Appl Microbiol. 35: 415–420. Liu, X. Y., Wu, W., Wang, E. T., Zhang, B., Macdermott, J., and Chen, W. X. 2011. Phylogenetic relationships and diversity of β-rhizobia associated with Mimosa species grown in Sishuangbanna, China. Int. J. Syst. Evol. Microbiol. 61: 334–342. Liu, X., Wei, S., Wang, F., James, E. K., Guo, X., Zagar, C., Xia, L. G., Dong, X., and Wang, Y. P. 2012b. Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in Southern China. FEMS Microbiol. Ecol. 80: 417–426. Lloret, L., Ormeño-Orrillo, E., Rincón, R., Mart´ınez-Romero, J., RogelHernández, M. A., and Mart´ınez-Romero, E. 2007. Ensifer mexicanus sp. nov. a new species nodulating Acacia angustissima (Mill.) Kuntze in Mexico. Syst. Appl. Microbiol. 30: 280–290. López-López, A., Rogel, M. A., Ormeño-Orrillo, E., Mart´ınez-Romero, J., and Mart´ınez-Romero, E. 2010. Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst. Appl. Microbiol. 33: 322–327. López-López, A., Rogel-Hernández, M. A., Barois, I., Ortiz Ceballos, A. I., Mart´ınez, J., Ormeño-Orrillo, E., and Mart´ınez-Romero, E. 2012. Rhizobium grahamii sp. nov., from nodules of Dalea leporina, Leucaena leucocephala and Clitoria ternatea, and Rhizobium mesoamericanum sp. nov., from nodules of Phaseolus vulgaris, siratro, cowpea and Mimosa pudica. Int. J. Syst. Evol. Microbiol. 62: 2264–2271. Lortet, G., Mear, N., Lorquin, J., Dreyfus, B., de Lajudie, P., Rosenberg, C., and Boivin, C. 1996. Nod factor thin-layer chromatography profiling as a tool to characterize symbiotic specificity of rhizobial strains: Application to Sinorhizobium saheli, S. teranga, and Rhizobium sp. strains isolated from Acacia and Sesbania. Mol. Plant Microbe Interact. 9: 736–747. Lu, J. K., He, X. H., Huang, L. B., Kang, L. H., and Xu D. P. 2012. Two Burkholderia strains from nodules of Dalbergia odorifera T. Chen in Hainan Island, Southern China. New Forests. 43: 397–409. Lu, Y. L., Chen, W. F., Han, L. L., Wang, E. T., and Chen, W. X. 2009a. Rhizobium alkalisoli sp. nov., isolated from Caragana intermedia growing in saline-alkaline soils in the North of China. Int. J. Syst. Evol. Microbiol. 59: 3006–3011.

37

Lu, Y. L., Chen, W. F., Han, L. L., Wang, E. T., Zhang, X. X., Chen, W. X., and Han, S. Z. 2009b. Mesorhizobium shangrilense sp. nov., isolated from root nodules of Caragana spp. Int. J. Syst. Evol. Microbiol. 59: 3012–3018. Lu, Y. L., Chen, W. F., Wang, E. T., Guan, S. H., Yan, X. R., Chen, W. X. 2009c. Genetic diversity and biogeography of rhizobia associated with Caragana species in three ecological regions of China. Syst. Appl. Microbiol. 32: 351–361. Lu, J. K., Dou, Y. J., Zhu, Y. J., Wang, S. K., Sui, X. H., and Kang, L. H. 2014. Bradyrhizobium ganzhouense sp. nov., effective symbiotic bacterium isolated from Acacia melanoxylon R. Br. nodules. Int. J. Syst. Evol. Microbiol. 64: 1900–1905. Marek-Kozaczuk, M., Leszcz, A., Wielbo, J., Wdowiak-Wróbel, S., and Skorupsk, A. 2013. Rhizobium pisi sv. trifolii K3.22 harboring nod genes of the Rhizobium leguminosarum sv. trifolii cluster. Syst. Appl. Microbiol. 36: 252–258. Mart´ınez, E., Pardo, M. A., Palacios, R., and Cevallos, M. A. 1985. Reiteration of nitrogen fixation gene sequences and specificity of Rhizobium in nodulation and nitrogen fixation in Phaseolus vulgaris. J. Gen. Microbiol. 131: 1779–1786. Mart´ınez-Aguilar, L., Salazar-Salazar, C., Méndez, R. D., Caballero-Mellado, J., Hirsch, A. M., Vásquez-Murrieta, M. S., and Estrada de los Santos, P. 2013. Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris. Antonie Van Leeuwenhoek. 104: 1063–1071. Mart´ınez-Romero, E., Segovia, L., Mercante, F. M., Franco, A. A., Graham, P., and Pardo, M. A. 1991. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 41: 417–426. Maynaud, G., Willems, A., Soussou, S., Vidal, C., Mauré, L., Moulin, L., CleyetMarel, J. C., and Brunel, B. 2012. Molecular and phenotypic characterization of strains nodulating Anthyllis vulneraria in mine tailings, and proposal of Aminobacter anthyllidis sp. nov., the first definition of Aminobacter as legume-nodulating bacteria. Syst. Appl. Microbiol. 35: 65–72. Merabet, C., Martens, M., Mahdhi, M., Zakhia, F., Sy, A., Le Roux, C., Domergue, O., Coopman, R., Bekki, A., Mars, M., Willems, A., and de Lajudie, P. 2010. Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov. Int. J. Syst. Evol. Microbiol. 60: 664– 674. Michiels, J., Dombrecht, B., Vermeiren, N., Xi, C., Luyten, E., and Vanderleyden, J. 1998. Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol. Ecol. 26: 193–205. Mishra, R. P., Tisseyre, P., Melkonian, R., Chaintreuil, C., Miché, L., Klonowska, A., Gonzalez, S., Bena, G., Laguerre, G., and Moulin, L. 2012. Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol. Ecol. 79: 487–503. Mnasri, B., Mrabet, M., Laguerre, G., Aouani, M. E., and Mhamdi, R. 2007. Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2 -fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 187: 79–85. Mnasri, B., Sa¨ıdi, S., Chihaoui, S. A., and Mhamdi, R. 2012. Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Syst. Appl. Microbiol. 35: 263–269. Mnasri, B., Liu, T. Y., Saidi, S., Chen, W. F., Chen, W. X., Zhang, X. X., and Mhamdi, R. 2014. Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. Int. J. Syst. Evol. Microbiol. 64: 1501–1506. Moulin, L., Munive, A., Dreyfus, B., and Boivin-Masson, C. 2001. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411: 948–950. Erratum in: Nature 412:926.


38

A. PEIX ET AL.

Muresu, R., Polone, E., Sulas, L., Baldan, B., Tondello, A., Delogu, G., Cappuccinelli, P., Alberghini, S., Benhizia, Y., Benhizia, H., Benguedouar, A., Mori, B., Calamassi, R., Dazzo, F. B., and Squartini, A. 2008. Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol. Ecol. 63: 383– 400. Muresu, R., Tondello, A., Polone, E., Sulas, L., Baldan, B., and Squartini, A. 2013. Antioxidant treatments counteract the non-culturability of bacterial endophytes isolated from legume nodules. Arch. Microbiol. 195: 385–391. Nakatsukasa, H., Uchiumi, T., Kucho, K., Suzuki, A., Higashi, S., and Abe, M. 2008. Transposon mediation allows a symbiotic plasmid of Rhizobium leguminosarum bv. trifolii to become a symbiosis island in Agrobacterium and Rhizobium. J. Gen. Appl. Microbiol. 54: 107–118. Nandasena, K. G., O’Hara, G. W., Tiwari, R. P., Willems, A., and Howieson, J. G. 2007. Mesorhizobium ciceri biovar biserrulae, a novel biovar nodulating the pasture legume Biserrula pelecinus L. Int. J. Syst. Evol. Microbiol. 57: 1041–1045. Nandasena, K. G., O’Hara, G. W., Tiwari, R. P., Willems, A., and Howieson, J. G. 2009. Mesorhizobium australicum sp. nov. and Mesorhizobium opportunistum sp. nov., isolated from Biserrula pelecinus L. in Australia. Int. J. Syst. Evol. Microbiol. 59: 2140–2147. Nick, G., de Lajudie, P., Eardly, B. D., Suomalainen, S., Paulin, L., Zhang, X., Gillis, M., and Lindström, K. 1999. Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int. J. Syst. Bacteriol. 49: 1359–1368. Nour, S. M., Cleyet-Marel, J. C., Normand, P., and Fernandez, M. P. 1995. Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int. J. Syst. Bacteriol. 45: 640–648. Nour, S. M., Fernandez, M. P., Normand, P., and Cleyet-Marel, J. C. 1994. Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.). Int. J. Syst. Bacteriol. 44: 511–522. Ohta, H., and Hattori, T. 1983. Agromonas oligotrophica gen. nov., sp. nov., a nitrogen-fixing oligotrophic bacterium. Antonie van Leeuwenhoek 49: 429–446. Oldroyd, G. E. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11: 252–263. Ophel, K., and Kerr, A. 1990. Agrobacterium vitis sp. nov. for Strains of Agrobacterium biovar 3 from Grapevines. Int. J. Syst. Bacteriol. 40: 236–241. Ormeño-Orrillo, E., Menna, P., Almeida, L. G., Ollero, F. J., Nicolás, M. F., Pains Rodrigues, E., Shigueyoshi Nakatani, A., Silva Batista, J. S., Oliveira Chueire, L. M., Souza, R. C., Ribeiro Vasconcelos, A. T., Meg´ıas, M., Hungria, M., and Mart´ınez-Romero, E. 2012a. Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 which are used in inoculants for common bean (Phaseolus vulgaris L.). BMC Genomics. 13: 735. Ormeño-Orrillo, E., Rogel, M. A., Chueire, L. M., Tiedje, J. M., Mart´ınezRomero, E., and Hungria, M. 2012b. Genome sequences of Burkholderia sp. strains CCGE1002 and H160, isolated from legume nodules in Mexico and Brazil. J. Bacteriol. 194: 6927–6927. Ott, T., van Dongen, J. T., Günther, C., Krusell, L., Desbrosses, G., Vigeolas, H., Bock, V., Czechowski, T., Geigenberger, P., and Udvardi, M. K. 2005. Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr. Biol. 15: 531–535. Palaniappan, P., Chauhan, P. S., Saravanan, V. S., Anandham, R. and Sa, T. 2010. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol. Fertil. Soils. 46: 807–816. Panday, D., Schumann, P. and Das, S. K. 2011. Rhizobium pusense sp. nov., isolated from the rhizosphere of chickpea (Cicer arietinum L.). Int. J. Syst. Evol. Microbiol. 61: 2632–2639. Pandey, A., Kang, S. C., and Maheshwari, D. K. 2005. Isolation of endophytic plant growth promoting Burkholderia sp. MSSP from root nodules of Mimosa pudica. Curr. Sci. 89: 177–180.

Pandya M., Naresh Kumar, G., and Rajkumar, S. 2013. Invasion of rhizobial infection thread by non rhizobia for colonization of Vigna radiata root nodules. FEMS Microbiol. Lett. 348: 58–65. Parag, B., Sasikala, C., and Ramana, C. V. 2013. Molecular and culture dependent characterization of endolithic bacteria in two beach sand samples and description of Rhizobium endolithicum sp. nov. Antonie Van Leeuwenhoek. 104: 1235–1244. Paul, K. H., Dickin, K. L., Ali, N. S., Monterrosa, E. C., and Stoltzfus, R. J. 2008. Soy and rice-based processed complementary food increases nutrient intakes in infants and is equally acceptable with or without added milk powder. J. Nutr. 138: 1963–1968. Peng, G., Yuan, Q., Li, H., Zhang, W., and Tan, Z. 2008. Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Int. J. Syst. Evol. Microbiol. 58: 2158–2163. Perret, X., Staehelin, C., and Broughton, W. J. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64: 180–201. Prowse, T., Schwarcz, H.P., Saunders, S., Macchiarelli, R., and Bondioli, L. 2003. Isotopic paleodiet studies of skeletons from the Imperial Roman-age cemetery of Isola Sacra, Rome, Italy. J. Archaeol. Sci. 31: 259–272. Pueppke, S. G., and Broughton, W. J. 1999. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant Microbe Interact. 12: 293–318. Puławska, J., Willems, A., and Sobiczewski, P. 2012b. Rhizobium skierniewicense sp. nov., isolated from tumours on chrysanthemum and cherry plum. Int. J. Syst. Evol. Microbiol. 62: 895–899. Puławska, J., Willems, A., de Meyer, S. E., and Süle, S. 2012a. Rhizobium nepotum sp. nov. isolated from tumors on different plant species. Syst. Appl. Microbiol. 35: 215–220. Qin, W., Deng, Z. S., Xu, L., Wang, N. N., and Wei, G. H. 2012. Rhizobium helanshanense sp. nov., a bacterium that nodulates Sphaerophysa salsula (Pall.) DC. in China. Arch. Microbiol. 194: 371–378. Quan, Z. X., Bae, H. S., Baek, J. H., Chen, W. F., Im, W. T., and Lee, S. T. 2005. Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor. Int. J. Syst. Evol. Microbiol. 55: 2543– 2549. Radeva, G., Jurgens, G., Niemi, M., Nick, G., Suominen, L., and Lindström, K. 2001. Description of two biovars in the Rhizobium galegae species: Biovar orientalis and biovar officinalis. Syst. Appl. Microbiol. 24: 192–205. Radl, V., Simões-Araújo, J. L., Leite, J., Passos, S. R., Martins, L. M., Xavier, G. R., Rumjanek, N. G., Baldani, J. I., and Zilli, J. E. 2014. Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int. J. Syst. Evol. Microbiol. 64: 725–730. Rajendran, G., Patel, M. H., and Joshi, S. J. 2012. Isolation and characterization of nodule-associated exiguobacterium sp. from the root nodules of fenugreek (Trigonella foenum-graecum) and their possible role in plant growth promotion. Int J. Microbiol. 2012: 693982. Ramana, C. V., Parag, B., Girija, K. R., Ram, B. R., Ramana, V. V., and Sasikala, C. 2013. Rhizobium subbaraonis sp. nov., an endolithic bacterium isolated from beach sand. Int. J. Syst. Evol. Microbiol. 63: 581–585. Ram´ırez-Bahena, M. H., Chahboune, R., Peix, A., and Velázquez, E. 2013a. Reclassification of Agromonas oligotrophica into the genus Bradyrhizobium as Bradyrhizobium oligotrophicum comb. nov. Int. J. Syst. Evol. Microbiol. 63: 1013–1016. Ram´ırez-Bahena, M. H., Chahboune, R., Velázquez, E., Gómez-Moriano, A., Mora, E., Peix, A., and Toro, M. 2013b. Centrosema is a promiscuous legume nodulated by several new putative species and symbiovars of Bradyrhizobium in various American countries. Syst. Appl. Microbiol. 36: 392–400. Ram´ırez-Bahena, M. H., Garc´ıa-Fraile, P., Peix, A., Valverde, A., Rivas, R., Igual, J. M., Mateos, P. F., Mart´ınez-Molina, E., and Velázquez, E. 2008. Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889 AL, Rhizobium phaseoli Dangeard 1926 AL and Rhizobium trifolii Dangeard 1926 AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. Int. J. Syst. Evol. Microbiol. 58: 2484–2490.


BACTERIAL ASSOCIATIONS WITH LEGUMES Ram´ırez-Bahena, M. H., Hernández, M., Peix, A., Velázquez, E., and LeónBarrios, M. 2012. Mesorhizobial strains nodulating Anagyris latifolia and Lotus berthelotii in Tamadaya ravine (Tenerife, Canary Islands) are two symbiovars of the same species, Mesorhizobium tamadayense sp. nov. Syst. Appl. Microbiol. 35: 334–341. Ram´ırez-Bahena, M. H., Peix, A., Rivas, R., Camacho, M., Rodr´ıguez-Navarro, D. N., Mateos, P. F., Mart´ınez-Molina, E., Willems, A., and Velázquez, E. 2009. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int. J. Syst. Evol. Microbiol. 59: 1929–1934. Ram´ırez-Bahena, M. H., Tejedor, C., Mart´ın, I., Velázquez, E., and Peix, A. 2013c. Endobacter medicaginis gen. nov., sp. nov., isolated from alfalfa nodules in an acidic soil. Int. J. Syst. Evol. Microbiol. 63: 1760–1765. Rasolomampianina, R., Bailly, X., Fetiarison, R., Rabevohitra, R., Béna, G., Ramaroson, L., Raherimandimby, M., Moulin, L., De Lajudie, P., Dreyfus, B., and Avarre, J. C. 2005. Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to alpha- and beta-Proteobacteria. Mol. Ecol. 14: 4135–4146. Rees, D. C., Akif Tezcan, F., Haynes, C.A., Walton, M. Y., Andrade, S., Einsle, O., and Howard, J. B. 2005. Structural basis of biological nitrogen fixation. Philos. Trans. A Math. Phys. Eng. Sci. 363: 971–984. Relic, B., Perret, X., Estrada-Garc´ıa, M. T., Kopcinska, J., Golinowski, W., Krishnan, H. B., Pueppke, S. G., and Broughton, W. J. 1994. Nod factors of Rhizobium are a key to the legume door. Mol. Microbiol. 13: 171–178. Ren da, W., Chen, W. F., Sui, X. H., Wang, E. T., and Chen, W. X. 2011a. Rhizobium vignae sp. nov., a symbiotic bacterium isolated from multiple legume species. Int. J. Syst. Evol. Microbiol. 61: 580–586. Ren da, W., Wang, E. T., Chen, W. F., Sui, X. H., Zhang, X. X., Liu, H. C., and Chen, W. X. 2011b. Rhizobium herbae sp. nov. and Rhizobium giardiniirelated bacteria, minor microsymbionts of various wild legumes in China. Int. J. Syst. Evol. Microbiol. 61: 1912–1920. Ribeiro, R. A., Rogel, M. A., López-López, A., Ormeño-Orrillo, E., Barcellos, F. G., Mart´ınez, J., Thompson, F. L., Mart´ınez-Romero, E., and Hungria, M. 2012. Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int. J. Syst. Evol. Microbiol. 62: 1179–1184. Riker, A. J., Banfield, W. M., Wright, W. H., Keitt, G. W., and Sagen, H.E. 1930. Studies on infectious hairy root of nursery apple trees. Jour. Agr. Research (U. S.) 41: 507–540. Rincón-Rosales, R., Villalobos-Escobedo, J. M., Rogel, M. A., Martinez, J., Ormeño-Orrillo, E., and Mart´ınez-Romero, E. 2013. Rhizobium calliandrae sp. nov., Rhizobium mayense sp. nov. and Rhizobium jaguaris sp. nov., rhizobial species nodulating the medicinal legume Calliandra grandiflora. Int. J. Syst. Evol. Microbiol. 63: 3423–3429. Rivas, R., Laranjo, M., Mateos, P. F., Oliveira, S., Mart´ınez-Molina, E., and Velázquez, E. 2007. Strains of Mesorhizobium amorphae and Mesorhizobium tianshanense, carrying symbiotic genes of common chickpea endosymbiotic species, constitute a novel biovar (ciceri) capable of nodulating Cicer arietinum. Lett. Appl. Microbiol. 44: 412–418. Rivas, R., Velázquez, E., Willems, A., Vizca´ıno, N., Subba-Rao, N. S., Mateos, P. F., Gillis, M., Dazzo, F. B., and Mart´ınez-Molina, E. 2002. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl. Environ. Microbiol. 68: 5217–5222. Rivas, R., Willems, A., Palomo, J. L., Garc´ıa-Benavides, P., Mateos, P. F., Mart´ınez-Molina, E., Gillis, M., and Velázquez, E. 2004. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int. J. Syst. Evol. Microbiol. 54: 1271–1275. Rivas, R., Willems, A., Subba-Rao, N. S., Mateos, P. F., Dazzo, F. B., Kroppenstedt, R. M., Mart´ınez-Molina, E., Gillis, M., and Velázquez, E. 2003. Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst. Appl. Microbiol. 26: 47–53. Robledo, M., Velázquez, E., Ram´ırez-Bahena, M. H., Garcia-Fraile, P., PerezAlonso, A., Rivas, R., Martinez-Molina, E., and Mateos, P. F. 2011. The celC

39

gene, a new phylogenetic marker useful for taxonomic studies in Rhizobium. Syst. Appl. Microbiol. 34: 393–399. Roche, P., Maillet, F., Plazanet, C., Debelle, F., Ferro, M., Truchet, G., Promé, J. C., and Denarié, J. 1996. The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc. Natl. Acad. Sci. USA. 93: 15305–15310. Rogel, M. A., Hernández-Lucas, I., Kuykendall, L. D., Balkwill, D. L., and Mart´ınez-Romero, E. 2001. Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl. Environ. Microbiol. 67: 3264–3268. Rogel, M. A., Ormeño-Orrillo, E., and Martinez Romero, E. 2011. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst. App. Microbiol. 34: 96–104. Rome, S., Fernandez, M. P., Brunel, B., Normand, P., and Cleyet-Marel, J. C. 1996. Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int. J. Syst. Bacteriol. 46: 972–980. Ruiz-D´ıez, B., Quiñones, M. A., Fajardo, S., López-Berdonces, M. A., Higueras, P., and Fernández-Pascual, M. 2012a. Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl. Microbiol. Biotechnol. 96: 543–554. Ruiz-D´ıez, B., Fajardo, S. and Fernández-Pascual, M. 2012b. Selection of rhizobia from agronomic legumes grown in semiarid soils to be employed as bioinoculants. Agron. J. 104: 550–559. Sa¨ıdi, S., Ram´ırez-Bahena, M. H., Santillana, N., Zún˜ iga, D., Alvarez-Mart´ınez, E., Peix, A., Mhamdi, R., and Velázquez, E. 2014. Rhizobium laguerreae sp. nov. nodulates Vicia faba in several continents. Int. J. Syst. Evol. Microbiol. 64: 242–247. Sánchez, M., Ram´ırez-Bahena, M. H., Peix, A., Lorite, M. J., Sanjuán, J., Velázquez, E., and Monza, J. 2014. Phyllobacterium loti sp. nov. isolated from nodules of Lotus corniculatus. Int. J. Syst. Evol. Microbiol. 64: 781–786. Sawada, H., Ieki, H., Oyaizu, H., and Matsumoto, S. 1993. Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes. Int. J. Syst. Bacteriol. 43: 694–702. Scholla, M. H., and Elkan, G. H. 1984. Rhizobium fredii sp. nov., a fastgrowing species that effectively nodulates soybeans. Int. J. Syst .Bacteriol. 34: 484–486. Schuldes, J., Rodriguez Orbegoso, M., Schmeisser, C., Krishnan, H. B., Daniel, R., and Streit, W. R. 2012. Complete genome sequence of the broad-hostrange strain Sinorhizobium fredii USDA257. J. Bacteriol. 194: 4483. Segovia, L., Young, J. P., and Mart´ınez-Romero, E. 1993. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 43: 374–377. Sheu, S. Y., Chou, J. H., Bontemps, C., Elliott, G. N., Gross, E., dos Reis Junior, F. B., Melkonian, R., Moulin, L., James, E. K., Sprent, J. I., Young, J. P., and Chen, W. M. 2013. Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp. Int. J. Syst. Evol. Microbiol. 63: 435–441. Sheu, S. Y., Chou, J. H., Bontemps, C., Elliott, G. N., Gross, E., James, E. K., Sprent, J. I., Young, J. P., and Chen, W. M. 2012. Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int. J. Syst. Evol. Microbiol. 62: 2272–2878. Shiraishi, A., Matsushita, N., and Hougetsu, T. 2010. Nodulation in black locust by the Gammaproteobacteria Pseudomonas sp. and the Betaproteobacteria Burkholderia sp. Syst. Appl. Microbiol. 33: 269–274. Smyth, E. M., McCarthy, J., Nevin, R., Khan, M. R., Dow, J. M., O’Gara, F., and Doohan, F. M. 2011. In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J. Appl. Microbiol. 111: 683–692. Souza Moreira, M. F., Cruz, L., Miana de Faria, S., Marsh, T., Mart´ınez-Romero, E., de Oliveira Pedrosa, F., Maria Pitard, R., and Young, J. P. W. 2006. Azorhizobium doebereinerae sp. nov. microsymbiont of Sesbania virgata (Caz.) Pers. Syst. Appl. Microbiol. 29: 197–206. Sprent, J. I. 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol. 174: 11–25.


40

A. PEIX ET AL.

Squartini, A., Struffi, P., Döring, H., Selenska-Pobell, S., Tola, E., Giacomini, A., Vendramin, E., Velázquez, E., Mateos, P. F., Mart´ınez-Molina, E., Dazzo, F. B., Casella, S., and Nuti, M. P. 2002. Rhizobium sullae sp. nov. (formerly ‘Rhizobium hedysari’), the root-nodule microsymbiont of Hedysarum coronarium L. Int. J. Syst. Evol. Microbiol. 52: 1267–1276. Stajković, O., de Meyer, S., Mili, B., Willems, A., and Deli, D. 2009. Isolation and characterization of endophytic non-rhizobial bacteria from root nodules of alfalfa (Medicago sativa L.). Botanica Serbica. 33: 107– 114. Sturz, A. V., Christie, B. R., Matheson B. G., and Nowak, J. 1997. Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol. Fertil. Soils. 25: 13–19. Sullivan, J. T., Trzebiatowski, J. R., Cruickshank, R. W., Gouzy, J., Brown, S. D., Elliot, R. M., Fleetwood, D. J., McCallum, N. G., Rossbach, U., Stuart, G.S., Weaver, J. E., Webby, R.J., De Bruijn, F. J., and Ronson, C. W. 2002. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 184: 3086–3095. Sy, A., Giraud, E., Jourand, P., Garcia, N., Willems, A., de Lajudie, P., Prin, Y., Neyra, M., Gillis, M., Boivin-Masson, C., and Dreyfus, B. 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183: 214–220. Talbi, C., Delgado, M. J., Girard, L., Ram´ırez-Trujillo, A., Caballero-Mellado, J., and Bedmar, E. J. 2010. Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl. Environ. Microbiol. 76: 4587–4591. Tan, Z. Y., Kan, F., Peng, G. X., Wang, E. T., Reinhold-Hurek, B., and Chen, W. X. 2001. Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China. Int. J. Syst. Evol. Microbiol. 51: 909–914. Taulé, C., Zabaleta, M., Mareque, C., Platero, R., Sanjurjo, L., Sicardi, M., Frioni, L., Battistoni, F., and Fabiano, E. 2012 New betaproteobacterial Rhizobium strains able to efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl Environ Microbiol. 78: 1692–1700. Tian, C.F., Wang, E.T., Wu, L.J., Han, T.X., Chen, WF, Gu, C.T., Gu, J.G., and Chen, W.X. 2009. Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int. J. Syst. Evol. Microbiol. 58: 2871–2875. Tokala, R. K., Strap, J. L., Jung, C. M., Crawford, D. L., Salove, M. H., Deobald, L. A., Bailey, J. F., and Morra, M. J. 2002. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl. Environ. Microbiol. 68: 2161–2171. Toledo, I., Lloret, L., and Martinez-Romero, E. 2003. Sinorhizobium americanus sp.nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst. Appl. Microbiol. 26: 54–64. Trujillo, M. E., Alonso-Vega, P., Rodr´ıguez, R., Carro, L., Cerda, E., Alonso, P., and Mart´ınez-Molina, E. 2010. The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J. 4: 1265–1281. Trujillo, M. E., Kroppenstedt, R. M., Fernández-Molinero, C., Schumann, P., and Mart´ınez-Molina, E. 2007. Micromonospora lupini sp. nov. and Micromonospora saelicesensis sp. nov., isolated from root nodules of Lupinus angustifolius. Int. J. Syst. Evol. Microbiol. 57: 2799–2804. Trujillo, M. E., Kroppenstedt, R. M., Schumann, P., and Mart´ınez-Molina, E. 2006. Kribbella lupini sp. nov., isolated from the roots of Lupinus angustifolius. Int. J. Syst. Evol. Microbiol. 56: 407–411. Trujillo, M. E., Willems, A., Abril, A., Planchuelo, A. M., Rivas, R., Ludeña, D., Mateos, P. F., Mart´ınez-Molina, E., and Velázquez, E. 2005. Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl. Environ. Microbiol. 71: 1318–1327. Turdahon, M., Osman, G., Hamdun, M., Yusuf, K., Abdurehim, Z., Abaydulla, G., Abdukerim, M., Fang, C., and Rahman, E. 2013. Rhizobium tarimense sp. nov., isolated from soil in the ancient Khiyik River. Int. J. Syst. Evol. Microbiol. 63: 2424–2429. Uchiumi, T., Ohwada, T., Itakura, M., Mitsui, H., Nukui, N., Dawadi, P., Kaneko, T., Tabata, S., Yokoyama, T., Tejima, K., Saeki, K., Omori, H., Hayashi, M., Maekawa, T., Sriprang, R., Murooka, Y., Tajima, S., Simomura, K., Nomura,

M., Suzuki, A., Shimoda, Y., Sioya, K., Abe, M., and Minamisawa, K. 2004. Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J. Bacteriol. 186: 2439–2448. Valverde, A., Fterich, A., Mahdhi, M., Ram´ırez-Bahena, M. H., Caviedes, M. A., Mars, M., Velázquez, E., and Rodriguez-Llorente, I. D. 2010. Paenibacillus prosopidis sp. nov., isolated from the nodules of Prosopis farcta. Int. J. Syst. Evol. Microbiol. 60: 2182–2186. Valverde, A., Igual, J. M., Peix, A., Cervantes, E., and Velázquez, E. 2006. Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int. J. Syst. Evol. Microbiol. 56: 2631–2637. Valverde, A., Velázquez, E., Fernández-Santos, F., Vizca´ıno, N., Rivas, R., Mateos, P. F., Mart´ınez-Molina, E., Igual, J. M., and Willems, A. 2005. Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int. J. Syst. Evol. Microbiol. 55: 1985–1989. Valverde, A., Velázquez, E., Gutiérrez, C., Cervantes, E., Ventosa, A., and Igual, J. M. 2003. Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int. J. Syst. Evol. Microbiol. 53: 1979–1983. van Berkum, P., and Eardly, B.D. 2002. The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl. Environ. Microbiol. 68: 1132–1136. van Berkum, P., Beyene, D., Bao, G., Campbell, T. A., and Eardly, B. D. 1998. Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int. J. Syst. Bacteriol. 48: 13–22. van Berkum, P., Leibold, J. M., and Eardly, B. D. 2006. Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst. Appl. Microbiol. 29: 207–215. Van Damme, E. J. M., Barre, A., Rougé, P., and Peumans, W. J. 2004. Cytoplasmic/ nuclear plant lectins: a new story. Trends Plant Sci. 9: 484–489. van Rhijn, P. J., Feys, B., Verreth, C., and Vanderleyden, J. 1993. Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J. Bacteriol. 175: 438–447. Vandamme, P., and Coenye, T. 2004. Taxonomy of the genus Cupriavidus: a tale of lost and found. Int. J. Syst. Evol. Microbiol. 54: 2285–2289. Vandamme, P., Goris, J., Chen, W. M., de Vos, P., and Willems, A. 2002. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst. Appl. Microbiol. 25: 507–512. Velázquez, E., Igual, J. M., Willems, A., Fernández, M. P., Muñoz, E., Mateos, P. F., Abril, A., Toro, N., Normand, P., Cervantes, E., Gillis, M., and Mart´ınezMolina, E. 2001. Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina). Int. J. Syst. Evol. Microbiol. 51: 1011–1021. Velázquez, E., Mart´ınez-Hidalgo, P., Carro, L., Alonso, P., Peix, A., Trujillo, M. E., and Mart´ınez-Molina, E. 2013. Nodular endophytes: an untapped diversity. In: Beneficial Plant-Microbial Interactions: Ecology and Applications. pp. 214–235. Rodelas-González, M. B., González-López, J. Eds., CRC Press, Boca Raton, FL. Velázquez, E., Silva, L., and Peix, A. 2010a. Legumes: A healthy and ecological source of flavonoids. Current Nutrition & Food Science. 6: 109–144. Velázquez, E., Valverde, A., Rivas, R., Gomis, V., Peix, A., Gantois, I., Igual, J. M., León-Barrios, M., Willems, A., Mateos, P. F., and Mart´ınez-Molina, E. 2010b. Strains nodulating Lupinus albus on different continents belong to several new chromosomal and symbiotic lineages within Bradyrhizobium. Antonie Van Leeuwenhoek. 97: 363–376. Venancio Silva, F., De Meyer, S. E., Simões de Araujo, J. L., da Costa Barbé, T., Xavier, G. R., O’Hara, G., Ardley, J., Rumjanek, N. G., Willems, A., and Zilli, J. E. 2014. Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazon rainforest soils. Int. J. Syst. Evol. Microbiol. 64: 2358–2363. Verma, S. H., Chowdhury, S. P., and Tripathi, A. K. 2004. Phylogeny based on 16S rDNA and nifH sequences of Ralstonia taiwanensis strains isolated from


BACTERIAL ASSOCIATIONS WITH LEGUMES nitrogen-fixing nodules of Mimosa pudica, in India. Can. J. Microbiol. 50: 313–322. Vidal, C., Chantreuil, C., Berge, O., Maure, L., Escarre, J., Bena, G., Brunel, B., Cleyet-Marel, J. C. 2009. Mesorhizobium metallidurans sp. nov., a metalresistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc, France. Int J Syst Evol Microbiol. 59: 850–855. Villegas, M. C., Rome, S., Maure, L., Domergue, O., Gardan, L., Bailly, X., Cleyet-Marel, J. C., and Brunel, B. 2006. Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti. Syst. Appl. Microbiol. 29: 526–538. Vinuesa, P., León-Barrios, M., Silva, C., Willems, A., Jarabo-Lorenzo, A., Pérez-Galdona, R., Werner, D., and Mart´ınez-Romero, E. 2005. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int. J. Syst. Evol. Microbiol. 55: 569–575. Wang, E. T., Rogel, M. A., Garc´ıa-de los Santos, A., Mart´ınez-Romero, J., Cevallos, M. A., and Mart´ınez-Romero, E. 1999a. Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int. J. Syst. Bacteriol. 49: 1479–1491. Wang, E. T., Tan, Z. Y., Willems, A., Fernández-López, M., Reinhold-Hurek, B., and Mart´ınez-Romero, E. 2002. Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int. J. Syst. Evol. Microbiol. 52: 1687–1693. Wang, E. T., van Berkum, P., Beyene, D., Sui, X. H., Dorado, O., Chen, W. X., and Mart´ınez-Romero, E. 1998. Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int. J. Syst. Bacteriol. 48: 687–699. Wang, E. T., van Berkum, P., Sui, X. H., Beyene, D., Chen, W. X., and Mart´ınezRomero, E. 1999b. Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int. J. Syst. Bacteriol. 49: 51–65. Wang, F., Wang, E. T., Wu, L. J., Sui, X. H., Li, Y. Jr., and Chen, W. X. 2011. Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int. J. Syst. Evol. Microbiol. 61: 2582–2588. Wang, F. Q., Wang, E. T., Liu, J., Chen, Q., Sui, X. H., Chen, W. F., and Chen, W. X. 2007. Mesorhizobium albiziae sp. nov., a novel bacterium that nodulates Albizia kalkora in a subtropical region of China. Int. J. Syst. Evol. Microbiol. 57: 1192–1199. Wang, J. Y., Wang, R., Zhang, Y. M., Liu, H. C., Chen, W. F., Wang, E. T., Sui, X. H., and Chen, W. X. 2013a. Bradyrhizobium daqingense sp. nov., isolated from soybean nodules. Int. J. Syst. Evol. Microbiol. 63: 616– 624. Wang, R., Chang, Y. L., Zheng, W. T., Zhang, D., Zhang, X. X., Sui, X. H., Wang, E. T., Hu, J. Q., Zhang, L.Y., and Chen, W.X. 2013b. Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst Appl Microbiol. 36: 101–105. Wang, Y. C., Wang, F., Hou, B. C., Wang, E. T., Chen, W. F., Sui, X. H., Chen, W. X., Li, Y., and Zhang, Y. B. 2013c. Proposal of Ensifer psoraleae sp. nov., Ensifer sesbaniae sp. nov., Ensifer morelense comb. nov. and Ensifer americanum comb. nov. Syst. Appl. Microbiol. 36: 467–473. Wei, G. H., Tan, Z. Y., Zhu, M. E., Wang, E. T., Han, S. Z., and Chen, W. X. 2003. Characterization of rhizobia isolated from legume species within the genera Astragalus and Lespedeza grown in the Loess Plateau of China and description of Rhizobium loessense sp. nov. Int. J. Syst. Evol. Microbiol. 53: 1575–1583. Wei, G. H., Wang, E. T., Tan, Z. Y., Zhu, M. E., and Chen, W. X. 2002. Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int. J. Syst. Evol. Microbiol. 52: 2231–2239. Weiss, V. A., Faoro, H., Tadra-Sfeir, M. Z., Raittz, R. T., de Souza, E. M., Monteiro, R. A., Cardoso, R. L., Wassem, R., Chubatsu, L. S., Huergo, L. F., Müller-Santos, M., Steffens, M. B., Rigo, L. U., Pedrosa, F. O., and Cruz,

41

L. M. 2012. Draft genome sequence of Herbaspirillum lusitanum P6-12, an endophyte isolated from root nodules of Phaseolus vulgaris. J. Bacteriol. 194: 4136–4137. Wen, Y., Zhang, J., Yan, Q., Li, S., and Hong, Q. 2011. Rhizobium phenanthrenilyticum sp. nov., a novel phenanthrene-degrading bacterium isolated from a petroleum residue treatment system. J. Gen. Appl. Microbiol. 57: 319– 329. Winsor, B. A. 1989. A nod at differentiation: the nodD gene product and initiation of Rhizobium nodulation. Trends Genet. 5: 199–201. Woese, C. R., Stackebrandt, E., Weisburg, W. G., Paster, B, J., Madigan, M. T., Fowler, V. J., Hahn, C. M., Blanz, P., Gupta, R., Nealson, K. H., and Fox, G. E. 1984. The phylogeny of purple bacteria: the alpha subdivision. Syst. Appl. Microbiol. 5: 315–326. Xu, L. M., Ge, C., Cui, Z., Li, J., and Fan, H. 1995. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int. J. Syst. Bacteriol. 45: 706–711. Xu, L., Shi, J. F., Zhao, P., Chen, W. M., Qin, W., Tang, M., and Wei, G. H. 2011. Rhizobium sphaerophysae sp. nov., a novel species isolated from root nodules of Sphaerophysa salsula in China. Antonie Van Leeuwenhoek. 99: 845–854. Xu, L., Zhang, Y., Deng, Z. S., Zhao, L., Wei, X. L., and Wei, G. H. 2013. Rhizobium qilianshanense sp. nov., a novel species isolated from root nodule of Oxytropis ochrocephala Bunge in China. Antonie Van Leeuwenhoek. 103: 559–565. Yao, L. J., Shen, Y. Y., Zhan, J. P., Xu, W., Cui, G. L., and Wei, G. H. 2012. Rhizobium taibaishanense sp. nov., isolated from a root nodule of Kummerowia striata. Int. J. Syst. Evol. Microbiol. 62: 335–341. Yao, Z. Y., Kan, F. L., Wang, E. T., Wei, G. H., and Chen, W. X. 2002. Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int. J. Syst. Evol. Microbiol. 52: 2219–2230. Yoon, J. H., Kang, S. J., Yi, H. S., Oh, T. K., and Ryu, C. M. 2010. Rhizobium soli sp. nov., isolated from soil. Int. J. Syst. Evol. Microbiol. 60: 1387– 1393. Young, J. M. 2003. The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination “Sinorhizobium adhaerens” Casida 1982 Willems et al. 2003 legitimate? Request for an Opinion. Int. J. Syst. Evol. Microbiol. 53: 2107–2110. Young, J. M. 2004. Renaming of Agrobacterium larrymoorei Bouzar and Jones 2001 as Rhizobium larrymoorei (Bouzar and Jones 2001) comb. nov. Int. J. Syst. Evol. Microbiol. 54: 149. Young, J. M., Kuykendall, L. D., Mart´ınez-Romero, E., Kerr, A., and Sawada, H. 2001. A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int. J. Syst. Evol. Microbiol. 51: 89–103. Young, J. P., Crossman, L. C., Johnston, A. W., Thomson, N. R., Ghazoui, Z. F., Hull, K. H., Wexler, M., Curson, A. R., Todd, J. D., Poole, P. S., Mauchline, T. H., East, A. K., Quail, M. A., Churcher, C., Arrowsmith, C., Cherevach, I., Chillingworth, T., Clarke, K., Cronin, A., Davis, P., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Mungall, K., Norbertczak, H., Rabbinowitsch, E., Sanders, M., Simmonds, M., Whitehead, S., and Parkhill, J. 2006. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7: R34. Zakhia F., Jeder, H. Willems, A. Gillis, M., Dreyfus, B., and de Lajudie, P. 2006. Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb. Ecol. 51: 375–393. Zhang, G. X., Ren, S. Z., Xu, M. Y., Zeng, G. Q., Luo, H. D.,Chen, J. L., Tan, Z. Y., and Sun, G. P. 2011a. Rhizobium borbori sp. nov., an aniline-degrading bacterium isolated from activated sludge. Int. J. Syst. Evol. Microbiol. 61: 816–822.


42

A. PEIX ET AL.

Zhang, J. J., Liu, T. Y., Chen, W. F., Wang, E. T., Sui, X. H., Zhang, X. X., Li, Y., Li, Y., and Chen, W. X. 2012a. Mesorhizobium muleiense sp. nov., nodulating with Cicer arietinum L. Int. J. Syst. Evol. Microbiol. 62: 2737–2742. Zhang, R. J., Hou, B. C., Wang, E. T., Li,Y. Jr., Zhang, X. X., and Chen, W. X. 2011b. Rhizobium tubonense sp. nov., isolated from root nodules of Oxytropis glabra. Int. J. Syst. Evol. Microbiol. 61: 512–517. Zhang, X., Li, B., Wang, H., Sui, X., Ma, X., Hong, Q., and Jiang, R. 2012b. Rhizobium petrolearium sp. nov., isolated from oil-contaminated soil. Int. J. Syst. Evol. Microbiol. 62: 1871–1876. Zhang, X., Sun, L., Ma, X., Sui, X. H., and Jiang, R. 2011c. Rhizobium pseudoryzae sp. nov., isolated from the rhizosphere of rice. Int. J. Syst. Evol. Microbiol. 61: 2425–2429. Zhang, Y. M., Li, Y. Jr, Chen, W. F., Wang, E. T., Tian, C. F., Li, Q. Q., Zhang, Y. Z., Sui, X. H., Chen, W. X. 2011d. Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl. Environ. Microbiol. 77: 6331–6342. Zhang, X. X., Tang, X., Sheirdil, R. A., Sun, L., and Ma, X. T. 2014. Rhizobium rhizoryzae sp. nov., isolated from rice roots. Int. J. Syst. Evol. Microbiol. 64: 1373–1377. Zhang, Y. M., Li, Y. Jr., Chen, W. F., Wang, E. T., Sui, X. H., Li, Q. Q., Zhang, Y. Z., Zhou, Y. G., and Chen, W. X. 2012c. Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules. Int. J. Syst. Evol. Microbiol. 62: 1951–1957. Zhao, C. T., Wang, E. T., Zhang, Y. M., Chen, W. F., Sui, X. H., Chen, W. X., Liu, H. C., and Zhang, X. X. 2012. Mesorhizobium silamurunense sp. nov., isolated from root nodules of Astragalus species. Int. J. Syst. Evol. Microbiol. 62: 2180–2186.

Zheng, W. T., Li, Y. Jr., Wang, R., Sui, X. H., Zhang, X. X., Zhang, J. J., Wang, E. T., and Chen, W. X. 2013. Mesorhizobium qingshengii sp. nov., isolated from effective nodules of Astragalus sinicus. Int. J. Syst. Evol. Microbiol. 63: 2002–2007. Zhou, P. F., Chen, W. M., and Wei, G. H. 2010. Mesorhizobium robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia. Int. J. Syst. Evol. Microbiol. 60: 2552–2556. Zhou, S., Li, Q., Jiang, H., Lindström, K., and Zhang, X. 2013. Mesorhizobium sangaii sp. nov., isolated from the root nodules of Astragalus luteolus and Astragalus ernestii. Int. J. Syst. Evol. Microbiol. 63: 2794–2799. Zurdo-Piñeiro, J. L., Rivas, R., Trujillo, M. E., Vizca´ıno, N., Carrasco, J. A., Chamber, M., Palomares, A., Mateos, P. F., Mart´ınez-Molina, E., and Velázquez, E. 2007. Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int. J. Syst. Evol. Microbiol. 57: 784–788. Zurdo-Piñeiro, J. L., Velázquez, E., Lorite, M. J., Brelles-Mariño, G., Schröder, E. C., Bedmar, E. J., Mateos, P. F., and Mart´ınez-Molina, E. 2004. Identification of fast-growing rhizobia nodulating tropical legumes from Puerto Rico as Rhizobium gallicum and Rhizobium tropici. Syst. Appl. Microbiol. 27: 469–477. Zurdo-Piñeiro, J. L., Garc´ıa-Fraile, P., Rivas, R., Peix, A., León-Barrios, M., Willems, A., Mateos, P.F., Mart´ınez-Molina, E., Velázquez, E., and van Berkum, P. 2009. Rhizobia from Lanzarote, the Canary Islands, that nodulate Phaseolus vulgaris have characteristics in common with Sinorhizobium meliloti from mainland Spain. Appl. Environ. Microbiol. 75: 2354– 2359. Zurkowski, W., and Lorkiewicz, Z. 1979. Plasmid-mediated control of nodulation in Rhizobium trifolii. Arch. Microbiol. 123: 195–201.