Legume nodulation - CiteSeerX

CSIRO PUBLISHING

Functional Plant Biology, 2006, 33, 707–721

www.publish.csiro.au/journals/fpb

Review: Legume nodulation: successful symbiosis through short- and long-distance signalling Mark KinkemaA , Paul T. ScottA and Peter M. Gresshoff A,B A ARC

Centre of Excellence for Integrative Legume Research, The University of Queensland, St Lucia, Brisbane, Qld 4072, Australia. B Corresponding author. Email: [email protected]

Abstract. Nodulation in legumes provides a major conduit of available nitrogen into the biosphere. The development of nitrogen-fixing nodules results from a symbiotic interaction between soil bacteria, commonly called rhizobia, and legume plants. Molecular genetic analysis in both model and agriculturally important legume species has resulted in the identification of a variety of genes that are essential for the establishment, maintenance and regulation of this symbiosis. Autoregulation of nodulation (AON) is a major internal process by which nodule numbers are controlled through prior nodulation events. Characterisation of AON-deficient mutants has revealed a novel systemic signal transduction pathway controlled by a receptor-like kinase. This review reports our present level of understanding on the short- and long-distance signalling networks controlling early nodulation events and AON.

Introduction With a few exceptions, the formation and development of nitrogen-fixing root nodules (Fig. 1) is the result of a symbiotic relationship between leguminous plants and soil bacteria collectively called rhizobia, but including more specifically the genera Azorhizobium, Allorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium. Exceptions to the rhizobia–legume symbiosis include the actinomycete Frankia spp., which are well-known partners in the formation of symbiotic nitrogen-fixing nodules on non-legumes such as Casuariana and Alnus species (Soltis et al. 1995; Vessey et al. 2005), Burkholderia spp., which have recently been shown to produce nodules on the legume Mimosa spp. (Chen et al. 2005), and the Parasponia–Rhizobium symbiosis (Price et al. 1984). The importance of nodulation and nitrogen fixation to agriculture, natural ecosystems and the global nitrogen cycle are indisputable (Graham and Vance 2003). Legumes are cultivated on 12–15% of available arable land and constitute more than 25% of the world’s primary crop production. They provide roughly 200 million tons of nitrogen per year. Second only in importance to the Graminiae with respect to agricultural production and human and animal consumption, some of the more dominant crop and pasture legumes include soybean [Glycine max (L.) Merr.], common bean (Phaseolus vulgaris L.), pea (Pisum sativum L.),

chickpea (Cicer arietinum L.), peanut (Arachis hypogaea L.), pigeon pea [Cajanus cajan (L.) Millsp.], broad bean (Vicia faba L.), alfalfa (Medicago sativa L.) and the clovers (Trifolium spp.). Apart from the obvious potential for increased agricultural productivity, a more comprehensive understanding of nodulation will enhance our knowledge of plant development and plant–microorganism interactions. For example, the development of root nodules has parallels with lateral root formation (Krusell et al. 2002; Mathesius 2003; Bright et al. 2005; Olah et al. 2005). Therefore, nodulation research will help provide insight on this general developmental process in plants. In addition, some of the steps in nodule formation are common to, and likely derived from, the pathway leading to symbiosis between mycorrhiza and their respective plant hosts (Endre et al. 2002; Stracke et al. 2002; Lévy et al. 2004; Kistner et al. 2005). Similarly, the plant parasitic rootknot nematode, Meloidogyne incognita, is proposed to infect susceptible plants via a process that shares similarities with Rhizobium infection (Weerasinghe et al. 2005). The shared pathways of these symbiotic and pathogenic organisms and their respective plant hosts are suggestive of a common evolutionary development, probably arising from the more ancestral mycorrhiza–plant interaction. Nodulation research has made great strides over the past few years because of the production and characterisation of an extensive collection of legume mutants with defects in nodule

Abbreviations used: AMF, arbuscular mycorrhizal fungi; AON, autoregulation of nodulation; ISR, induced systemic resistance; NF, Nod factor; ROS, reactive oxygen species; SAR, systemic acquired resistance. © CSIRO 2006

10.1071/FP06056

1445-4408/06/080707

708

M. Kinkema et al.

Functional Plant Biology

Rhizobium

Root meristem

Infection thread

Nodule

Nodule Primordium

ID: infection droplet; BE: endocytosed bacteria; B: non-differentiated bacteria

Fig. 1. Schematic diagram of nodule development. Following the reception of flavonoid signals from root exudate the rhizobia (blue) attach to the surface of root hairs. Production of Nod factor by the rhizobia initiates a cascade of events (left to right), which at the morphological level include swelling, deformation and curling of the root hair, formation of the infection thread (blue) arising from the encapsulated bacterial cells, growth of the infection thread towards the nodule primordium with the release of the bacteria via infection droplets (diagram by Dong Xue Li, CILR, Brisbane).

development or the regulation of nodule number. This work has illustrated how nodulation is controlled by networks of short- and long-distance signals between the site of bacterial infection in the root, and additional cells in both the root and shoot of the host plant. This review describes some of the important research in the field of legume nodulation with a particular emphasis on the latest findings dealing with the short- and long-distance signalling pathways controlling the development, regulation and maintenance of nodules. Nodule initiation and development Nodulation mutants with well-defined phenotypes have been identified in a variety of legumes, particularly Lotus japonicus L., Medicago truncatula Gaertn., soybean and pea (Caetano-Anollés and Gresshoff 1991; Gresshoff 1993; Stacey et al. 2006). These phenotypes, many of which are associated with the early events of nodule formation, include alterations and defects in root hair swelling, branching and curling, infection thread formation, failure to exhibit Ca2+ spiking, inhibition of cortical cell division, and ultimately failure to form functional nodules, and these are described in detail below. Characterisation of these nodulation mutants has enabled researchers to construct an ordered network of early physiological events (Fig. 2). Cloning of the genes responsible for these mutant phenotypes has revealed a molecular network that can be best described as a series of three distinct but linked processes (Fig. 2). Initially, there is the perception of the rhizobia-derived signal(s) by membrane receptors, principally Nod factor perception by LysM-type protein receptor kinases (Limpens et al. 2003; Madsen et al. 2003; Radutoiu et al. 2003; A Indrasumunar, I Searle, A Kereszt, A Men, PM Gresshoff, BJ Carroll

unpubl. data), followed by a NBS-LRR-receptor kinase called LjNORK, MsSYMRK, MtDMI2 or PsSYM19 (Endre et al. 2002; Stracke et al. 2002; Mitra et al. 2004a; Capoen et al. 2005). Next, the reception of the rhizobia-derived signal is processed via the action of channels in the nuclear, cytoplasmic and plastid membranes (Ané et al. 2004; Imaizumi-Anraku et al. 2005; Kanamori et al. 2006), which is seen most readily by depolarisation of the host cell membrane and through an initial influx (Shaw and Long 2003a) and subsequent spiking in cytosolic Ca2+ concentration (Felle et al. 1998; Wais et al. 2000; Walker et al. 2000; Oldroyd 2001; Lévy et al. 2004; Mitra et al. 2004a). Finally, there is execution of the response to rhizobia infection, primarily through the action of transcription factors, which are proposed to activate as yet uncharacterised target genes (Schauser et al. 1999; Borisov et al. 2003; Kalo et al. 2005; Smit et al. 2005). An understanding of the overall ontogeny of legume nodulation (Fig. 1) may help shed light on the interaction between early events in nodulation and the AON regulatory network that systemically controls nodule development. It is now well established that rhizobia receive flavonoid signals through the rhizosphere of the appropriate legume host to induce a cascade of nodulation genes that govern the synthesis of a lipo-chito-oligosaccharide, commonly called the nodulation or Nod factor (NF; Spaink 2000). These NFs differ in their chemical decorations and modifications and appear to be a major constituent determining Rhizobium host range. NFs appear to be perceived by LysM-type receptor kinases in the plasma membrane. For both L. japonicus and G. max, non-nodulation mutants have been characterised to reveal NFR1 and NFR5 as the genes encoding NF receptors

Legume nodulation signalling


709

LRR receptor kinase GmNARK LjHAR1 PsSYM29 MtSUNN

Shoot-derived Inhibitor

LjKLAVIER Ethylene Transcription factor MtSICKLE

Rhizobia

AM fungi

LysM NF receptors

LRR Receptor kinase

LjNFR5 PsSYM10 LjNFR1

LjSYMRK MsNORK MtDMI2 PsSYM19

Ca2+ flux Root-hair swelling

LjASTRAY

Root-derived AON signal

Plasma membrane Calcium– Transcription factors cation channel calmodulin– MtNSP1 Cell divisions MtDMI1 dependent kinase MtNSP2 Infection thread LjCASTOR PsSYM7 MtDMI3 LjPOLLUX PsSYM9 LjSYM3 LjNIN PsSYM8 PsSYM35 Ca2+ spiking

Root-hair branching and curling

MtSICKLE

Fig. 2. Model depicting the physiological events and genes associated with the early stages of nodulation and AON. The yellow boxes indicate the genes that encode for proteins common to both the nodulation and mycorrhiza signalling pathways.

(Madsen et al. 2003; Radutoiu et al. 2003; A Indrasumunar, I Searle, A Kereszt, A Men, PM Gresshoff, BJ Carroll unpublished data). Related receptors were detected in pea and M. truncatula (Limpens et al. 2003; Madsen et al. 2003). NF perception and processing also requires a downstream leucine-rich repeat receptor kinase, namely LjSYMRK, MsNORK, MtDMI2, PsSYM19 and SrSYMRK from L. japonicus, M. sativa, M. truncatula, P. sativum and Sesbania rostrata, respectively (Endre et al. 2002; Stracke et al. 2002; Mitra et al. 2004a; Capoen et al. 2005). Interestingly, this receptor also controls arbuscular mycorrhization, a common plant–fungal symbiosis. The NF signal is processed through a signal transduction cascade involving proteins that are predicted to encode membrane ion channels (MtDMI1, LjCASTOR, LjPOLLUX; Ané et al. 2004; Imaizumi-Anraku et al. 2005), a nucleoporin (NUP133; Kanamori et al. 2006), calcium–calmodulindependent protein kinases (MtDMI3) (Lévy et al. 2004) and eventually transcription factors of the GRAS (MtNSP1, MtNSP2) and NIN type (LjNIN, PsSYM35) (Schauser et al. 1999; Borisov et al. 2003; Kalo et al. 2005; Smit et al. 2005).

The membrane ion channels, nucleoporin and calcium– calmodulin-dependent protein kinases are also utilised by the signal transduction pathway controlling mycorrhization. NF, being similar in structure and function to some fungal elicitors, may result in a cellular redistribution of calcium, which in turn causes transcriptional changes (Gabriel and Rolfe 1990). Nod factor is sufficient to induce many of the early physiological, molecular, and developmental responses leading to nodule formation (Truchet et al. 1991; Mitra et al. 2004b). NF perception has two developmental outcomes, namely root-hair deformation and the initiation of cortical as well as pericycle cell divisions. Additionally one presumes that exposed tissues comprising perhaps several cell types enter an ‘activated state’, related in response to perception of pathogenic elicitors (Gresshoff et al. 2005). Indeed the ‘activated state’ may be a precursor for the events leading to root hair deformation / curling and induction of cortical / pericycle cell divisions. Interestingly, pathogenic fungi do not induce such responses suggesting additional signals for specific responses.

710

M. Kinkema et al.


Root-hair curling creates a microenvironment for the bacteria, enriching NF levels and facilitating subsequent bacterial invasion. The cell types that divide in response to NF to form the nodule primordia vary depending on whether the legume develops determinate nodules (spherical in shape due to early meristem termination) or indeterminate nodules (cylindrical in shape due to later meristem termination). Determinate nodules in plants such as soybean initially form from cell divisions in the outer cortex. In contrast, indeterminate nodules in legumes such as Medicago, clover and pea develop initially from inner cortical cells with both determinate and indeterminate nodulators subsequently accompanied by a limited number of cell divisions in the pericycle (Timmers et al. 1999; Morris and Djordjevic 2006). Additionally, as a prelude to infection thread growth towards the nodule primordium, cortical cells are involved in the formation of pre-infection threads, which are cytoplasmic bridges across the central vacuole of radially aligned cells (van Brussel et al. 1992; Timmers et al. 1999). Studies on Vicia sativa, a model for pre-infection thread formation, suggest that during this process cells of the inner cortex enter into cell division, while cells of the outer cortex do not divide but form the cytoplasmic bridges (van Brussel et al. 1992). van Brussel et al. (1992) also found that if V. sativa was exposed to NF in the absence of rhizobia, then root hairs would form instead of infection threads, supporting the proposal that nodule formation and root formation may share some common pathway(s). Further, in both V. sativa and M. sativa pre-infection thread formation failed to take place with rhizobia that either failed to produce the relevant NF or produced NF with modifications of the substituent groups (van Brussel et al. 1992; Timmers et al. 1999). One should note that root-hair cells and epidermal cells, although targets of the NF signalling, are not induced to divide. In addition, the physical and chemical properties of NF make it an unlikely candidate to directly initiate the division of cortical and pericycle cells within the root. Thus, NF perception likely triggers a signalling cascade that regulates processes such as bacterial infection thread formation and cell division. Bacteria within the infection thread provide a continuous source of NF for signalling and subsequent development of the mature nitrogen-fixing nodules. However, it has been shown that the expression of NF is population dependent, being repressed at high population densities, and that bacteria in the mature nodules do not produce NF (Schlaman et al. 1991; Loh et al. 2001). Although symbiotic nitrogen fixation is an important attribute that provides legumes with a distinct advantage in nitrogen-poor environments, the process of nodulation is regulated by the plant to ensure that nodule formation is balanced for optimal growth and development. This is especially so during seedling establishment. Because NF is the key signalling molecule involved in nodule formation,

it would not be surprising if mechanisms involved in the regulation of nodulation targeted the NF signal transduction pathway. Ethylene has been shown to play a role in regulating the radial positioning of nodule formation in the root (Penmetsa and Cook 1997), and appears to function, at least in part, by inhibiting NF signalling (Oldroyd et al. 2001). The major systemic pathway regulating nodulation is AON. Ethylene regulation of nodulation functions independently of AON as ethylene insensitive legume mutants still possess AON and AON mutants are still ethylene sensitive (Penmetsa and Cook 1997; Wopereis et al. 2000). Although the mechanism by which AON regulates nodule formation is not known, it may also operate by interfering with NF perception and / or signalling. Autoregulation of nodulation Autoregulation of nodulation, or feedback inhibition of nodulation, involves long distance signalling between the root and shoot whereby early nodulation events act to inhibit subsequent nodule development (Bauer 1981; Kosslak and Bohlool 1984; Caetano-Anollés and Gresshoff 1991). Such a regulatory circuit, operating in seedlings, presumably allows the plant to monitor the level of nodulation and balance nodule formation with overall growth and development. Most AON mutants are characterised by a supernodulation or hypernodulation phenotype as well as nitrate-tolerant nodulation (Carroll et al. 1985a, b; Park and Buttery 1988; Duc and Messager 1989; Wopereis et al. 2000; Schnabel et al. 2005), suggesting that fixed nitrogen and AON may operate, at least transiently, through a similar control point of nodule development. In this context the results of experiments involving the use of split-root systems (where the root of a plant is physically separated into two compartments so each root part can be independently treated) in soybean are relevant (Hinson 1975). It was found that root portions exposed to inhibitory nitrate concentrations showed a reduction in nodule number and specific nitrogenase activity (nitrogen fixation per mg nodule mass), while the attached root portion not exposed to nitrate displayed a reduction in nitrogen fixation but wild-type numbers of nodules. This suggests that nitrate inhibition of nodule initiation relies on a local effect, while inhibition of nitrogen fixation is systemic. This result from a determinate-nodulator (i.e. soybean) was confirmed in the indeterminate nodulation type, white clover (Carroll and Gresshoff 1983). The phenomenon of host-mediated regulation of nodule number was first observed in red clover by Nutman (1952). These experiments revealed that removal of nodules or root tips resulted in the formation of new nodules. This discovery suggested that nodule and root meristems negatively regulate further nodule formation. Identical results were obtained in soybean (Caetano-Anollés et al. 1991), indicating that feedback inhibition of nodule formation was similar in plants forming either indeterminate or determinate nodules. In


addition, these results suggested that AON might involve the recognition of signals elicited by cell division. Importantly, the work of Caetano-Anollés et al. (1991) also showed that the newly formed nodules in soybean were not the result of new bacterial infections, but developed from preexisting ‘dormant’ infections. Anatomical studies on infected roots of soybean support these results as many infections appear to be arrested at early stages of development (Calvert et al. 1984; Mathews et al. 1989). Characterisation of the zone of nodulation has shown that successful infections occur around the root tip at the time of inoculation, in the region of newly developing root hairs (Bhuvaneswari et al. 1980). This ‘susceptible zone’ or ‘window’ of nodulation is transient and moves along with the growth of the root. Early nodulation events act to suppress nodule development in younger portions of the root through AON (Pierce and Bauer 1983). Autoregulation of nodulation appears to target nodule ontogeny at different stages depending on whether the legume forms determinate or indeterminate nodules. In soybean (determinate nodules), autoregulation inhibits nodulation through a major control point after initiation of cortical cell division clusters (Mathews et al. 1989). In contrast, autoregulation in the legumes pea and M. sativa (indeterminate nodules) acts at an earlier stage such that nodulation-inhibited root zones are void of cortical cell divisions (Caetano-Anollés and Gresshoff 1991; Sagan and Gresshoff 1996). Since determinate and indeterminate nodules develop from distinct cell types (outer v. inner cortical cells, respectively), the timing of AON inhibition may reflect differences in NF signalling that lead to cell divisions in the inner and outer cortical cells. The distinct target stages for AON arrest could be explained by the apparent need for NF stimulation of the early symbiotic stages, as illustrated by continued NF biosynthetic gene expression in invading bacteria (Loh and Stacey 2003) and continued expression of symbiotic genes such as DMI2 (Bersoult et al. 2005). Elegant experiments involving the use of split roots provided the first evidence that AON is regulated systemically (Kosslak and Bohlool 1984) and active in a variety of different plant species (Sargent et al. 1987; Caetano-Anollés and Bauer 1988). Physical separation of a plant’s root system allowed the inoculation of one part of the root followed by a delayed inoculation of the second half of the root. Inoculation of the first root-half was found to suppress nodulation on the opposite side in a time-dependent fashion such that nodulation was reduced after a 24-h delay and essentially 100% suppressed after ∼7–10 d. The rapid AON response indicated that neither nitrogen fixation nor mature nodules were necessary to elicit the feedback control of nodulation. To help identify the signal that triggers AON, researchers utilised both split-roots and grafted plants in combination with various bacterial or plant nodulation mutants.


711

Caetano-Anollés and Gresshoff (1990) used approachgrafts of wild-type plants with two different non-nodulation mutants (nod139 and nod49) to show that only a limited number of cell divisions (characteristic of nod49 in response to inoculation) were necessary to activate AON in soybean. In contrast, mutant nod139, which lacks all symbiotic responses, failed to activate AON. In alfalfa, the formation of empty, non-functional nodules by a Sinorhizobium meliloti exopolysaccharide-deficient mutant was sufficient to induce AON, further demonstrating that mature, nitrogen-fixing nodules are not necessary to elicit the AON signal (CaetanoAnollés et al. 1990). These results are consistent with the theory that cell divisions, or signalling events closely associated with them, may trigger the root-derived signal that activates AON. Split-root experiments have shown that arbuscular mycorrhizal fungi (AMF) infection is sufficient to trigger AON (Catford et al. 2003; Meixner et al. 2005). This result suggests that specific signals, and not cell division per se, may be the trigger because mycorrhizae do not induce cells to divide, yet utilise some of the early signalling components involved in nodulation. Interestingly, in the common bean P. vulgaris the initiation of nodule formation was not sufficient for the induction of AON, but required the presence of nodules containing bacteria (George and Robert 1991). This apparent requirement for developed nodules with bacteria may be due to a reduced response of bean to NF signalling. Induction of the ‘activated state’ needed to trigger AON in bean may therefore require a continued source of NF, which is supplied by the bacteria within the developing nodule. Consistent with this theory is the fact that activation of AON in P. vulgaris is significantly slower relative to other legume species (George and Robert 1991). The theory that AON involves long-distance signalling between the root and shoot was clearly demonstrated by root–shoot grafts of wild-type plants and supernodulating mutants (Delves et al. 1986). Grafting of shoots from supernodulating soybean mutants to the roots of wild-type plants resulted in a supernodulating phenotype, while the reciprocal graft allowed normal regulation of nodule number. Clearly the supernodulation mutation affected the perception of a root-derived signal in the shoot and / or the ability to generate the shoot-derived inhibitor. These experiments also demonstrated that the mutated gene was not required for production of the root-derived signal as roots from the supernodulation mutant grafted to wild-type shoots resulted in normal levels of root nodulation. The identity of the root signal and how it acts to induce the production of a leaf-derived inhibitor of nodulation is currently unknown. Cloning the genes responsible for a supernodulating phenotype in soybean (GmNARK, G. max Nodule Autoregulation Receptor Kinase; Searle et al. 2003), L. japonicus (HAR1, Hypernodulation and Aberrant Root; Krusell et al. 2002; Nishimura et al. 2002a), pea (SYM29,

712

M. Kinkema et al.


SYMbiosis; Krusell et al. 2002), and M. truncatula (SUNN, SUper Numeric Nodules; Schnabel et al. 2005), however, has shown that a putative transmembrane, leucine-rich repeat (LRR) receptor-like kinase (GmNARK, HAR1, SYM29, and SUNN are collectively referred to henceforth as the ‘AON receptor-like kinases’) is a key regulator of the AON signalling pathway, and has shed some light on other potential players. The predicted proteins for the AON receptor-like kinases are most similar to the Arabidopsis thaliana receptor kinase, clavata1 (CLV1), which regulates shoot and floral meristem proliferation by relatively short distance cell-tocell signalling (Clark et al. 1997). Since all these proteins function in meristem regulation, it is thought that the legume counterparts probably evolved from CLV1 to function in the long distance regulation of nodule meristem development. The functional and sequence conservation between CLV1 and the AON receptor-like kinases make it tempting to speculate that they may also share additional similarities in their signal transduction pathways. Various evidence suggests that AtCLV1 functions in a protein complex with a LRR receptorlike protein (CLV2), a kinase associated protein phosphatase (KAPP), a Rho-like GTPase (Rop) and a small, extracellular polypeptide (CLV3). CLV3 is believed to be the ligand that activates the complex, resulting in a signal transduction cascade that regulates the nuclear-localised transcription factor WUSCHEL (DeYoung and Clark 2001; Sharma et al. 2003). Potential orthologues of CLV2 and KAPP (M Kinkema, A Miyahara, PM Gresshoff unpubl. data) have been cloned from soybean, and their possible role in AON is currently under investigation. The identification of proteins that interact with the AON receptor-like kinases will help advance our understanding of the signal transduction pathway controlling AON and establish if symbiotic root meristems are regulated in a manner similar to meristematic cells in the shoot. Interestingly, although grafting experiments have clearly demonstrated that GmNARK, LjHar1, and SUNN function in the shoot, transcripts for these genes are abundant in both the shoot and root (Yamamoto et al. 2000; Krusell et al. 2002; Nishimura et al. 2002a; Schnabel et al. 2005). This finding begs the question of why root expression does not restore wild-type nodulation when grafted to a supernodulating shoot. One possible explanation is that the receptors interact with a shoot-specific ligand in response to the root-derived signal. Alternatively, essential components of the signalling pathway, such as the substrate acted upon by the receptor kinase, may not be present in the root. The soybean genome contains a gene, GmCLV1A, which shares 92% sequence identity with GmNARK and is expressed at a comparable level in leaves (Yamamoto et al. 2000). Despite this relatedness, GmCLV1A does not appear to complement the AON phenotype of the GmNARK mutant as GmNARK behaves as a single, recessive, loss of function mutant. GmCLV1A is more closely related to AtCLV1 than is

GmNARK, suggesting that GmCLV1A may be the functional orthologue of AtCLV1. Preliminary results on the analysis of GmCLV1A TILLING (Targeting Induced Local Lesions IN Genomes; McCallum et al. 2000) mutants suggest that GmCLV1A may control an activity similar to AtCLV1, namely the maintenance of apical meristem integrity in juvenile nodes as GmCLV1A mutants have cotyledonary node basal branching (T Mellouki, PM Gresshoff, K Meksem unpubl. data). Another mutant showing the AON phenotype of increased nodulation and an expanded nodulation zone is astray in L. japonicus (Nishimura et al. 2002c). Although it is not known if astray functions in the shoot or root, this mutant clearly differs from the GmNARK, har1, sym29, and sunn supernodulating mutants because it possesses less nodules and is not nitrate-tolerant. The astray gene encodes a basic leucine zipper (bZIP) protein with a RING-finger motif, and is similar to the Arabidopsis photomorphogenesis transcriptional activator HY5 (Nishimura et al. 2002b). It is possible that ASTRAY functions by transducing the shoot signal and directly regulating a portion of the genes involved in AON signalling. Full activation of AON may require additional transcription factors that serve to activate other pathways associated with the regulation of nodule number. The cloning of additional novel genes involved in AON, such as L. japonicus KLAVIER (Oka-Kira et al. 2005), will help dissect the signal transduction pathway involved in long distance regulation of nodulation. Additional supernodulating mutants exist in several legumes. In pea, nod3 increases nodule number in a nitrate-insensitive manner (Jacobsen and Feenstra 1984), and grafting experiments have clearly shown that this gene functions in the root (Postma et al. 1988). Sagan and Duc (1996) described another locus in pea that displays shootcontrolled supernodulation (Pssym28). This mutant may be altered in a homologue of LjKLAVIER. Following a wide screen of M. truncatula, Julia Frugoli and co-workers (Clemson University) isolated several supernodulation mutants affected in novel genes. One mutant, rdn, exhibits a phenotype indicating root control of nodulation via a gene that may be a homologue of PsNOD3. Another gene, lss (Like SUNN Supernodulator; formerly sn-1), which fails to rescue the sunn mutation, may be a homologue of LjKLAVIER and PsSYM28 (Stacey et al. 2006) as these mutants display common phenotypes of shoot-controlled supernodulation, nitrate tolerance, stem fasciation and altered photoperiodism. Nitrate inhibition The primary environmental condition that controls nodulation in legumes is the availability of fixed nitrogen (ammonia or nitrate) in the soil. This type of environmental control prevents the plant from investing in nodule development under conditions where nitrogen is not limiting.


Fixed nitrogen appears to function by directly or indirectly blocking some of the early events in nodulation, such as root-hair curling, cortical-cell division, and infection-thread formation (Malik et al. 1987; Carroll and Mathews 1990; Heidstra et al. 1994). The timing of nitrate inhibition was carefully examined by Malik et al. (1987) by exposing plants to inhibitory concentrations of nitrate at different times after Rhizobium inoculation. This work illustrated that nitrate inhibition of nodule formation was significantly reduced when plants were inoculated 18–24 h before treatment with 15 mM KNO3 , suggesting that the nitrate sensitive steps may occur within 18 h of inoculation. As plants are continuously sensing their environment, it is not surprising that nitrate inhibition is reversible (Malik et al. 1987) so that nodule formation can be controlled as nitrogen availability in the soil changes. Although fixed nitrogen clearly plays an integral part in controlling nodulation, the mechanism of this regulation is not yet clear. However, as mentioned above, nitrate appears to suppress nodulation locally while limiting nitrogen fixation systemically (Hinson 1975). As discussed earlier, NFs play a key role in early events such as root-hair curling and cortical-cell divisions. However, it is not likely that nitrate inhibition is due to a complete loss of Nod factor perception because not all aspects of Nod factor signalling are blocked by nitrate (Heidstra et al. 1997a). Clearly there are early responses that are sensitive to nitrate and are also essential for nodule formation. As nitrate is known to have a variety of physiological effects on plants, it may indirectly regulate nodulation through multiple signalling pathways. Nitrate inhibition of nodulation in soybean is known to be affected by the titre of inoculating Bradyrhizobium cells (Lawson et al. 1988), and this effect is independent of the inoculum’s ability to metabolise nitrate. When wild type soybean plants were inoculated with low bacterial titres, nitrate inhibition was severe. Increasing the inoculum titre, however, significantly reduced the level of inhibition. A modern interpretation of this result may be that NF perception is limited in soybean and that nitrate directly affects the strength of the NF perception cascade. Ethylene and nodulation In addition to AON, which acts to restrict the zone of nodulation in the root, nodule formation is controlled within the susceptible zone by an independent process involving the hormone ethylene. Ethylene treatment has been shown to reduce nodule formation in a variety of plants (Grobbelaar et al. 1971; Goodlass and Smith 1979; Lee and LaRue 1992; Nukui et al. 2000; Goormachtig et al. 2004), while inhibitors of ethylene perception and synthesis lead to an increase in nodulation (Peters and Crist-Estes 1989; Fearn and LaRue 1991; Guinel and LaRue 1992; Goormachtig et al. 2004). However, the generalisation that ethylene insensitivity leads to increased nodulation is not warranted as a strong


713

triple response mutant (the triple response is characterised by three specific morphological changes in dark grown seedlings exposed to ethylene; shortened and thickened hypocotyl, inhibition of root growth, and exaggerated apical hook) of L. japonicus MG20 was isolated that fails to show increased nodulation (PK Chan, PM Gresshoff unpubl. data). In addition, conflicting results have been obtained regarding the role of ethylene in the regulation of nodulation in soybean (Lee and LaRue 1992; Hunter 1993; Suganuma et al. 1995; Xie et al. 1996; Caba et al. 1999; Ligero et al. 1999; Schmidt et al. 1999), and these findings may be due to differing ethylene sensitivities among cultivars. The exact mechanism by which ethylene inhibits nodulation is not clear, but evidence indicates that it is capable of inhibiting many of the early steps in NF signalling (Oldroyd et al. 2001). In addition to regulating nodule formation, ethylene has also been shown to play a role in the regulation of nodule type (indeterminate and determinate) in the semiaquatic legume S. rostrata, which is capable of forming both types of nodules (Fernández-López et al. 1998). Ethylene appears to provide positional information within the root and, thereby, regulate the spatial formation of nodules. Nodule formation normally occurs opposite xylem poles in the root. Heidstra et al. (1997b) found that the application of inhibitors for ethylene perception and synthesis to pea roots led to an increase in nodule formation across from phloem poles, where nodule formation is normally suppressed. In addition, expression of the ethylene biosynthetic enzyme ACC oxidase was localised specifically in cells opposite phloem poles (Heidstra et al. 1997b). These results suggest that localised ethylene synthesis in the root may play a role in the spatial distribution of nodules by inhibiting nodule formation around phloem poles. Further support for this theory came from the identification of the M. truncatula sickle mutant that displays hypernodulation in the susceptible zone and is insensitive to ethylene (Penmetsa and Cook 1997). Spatial distribution of nodule formation is abolished in sickle as nodulation occurs randomly in the cortical region of the root. Transgenic L. japonicus plants showing an ethylene insensitive phenotype due to expression of a mutant ethylene receptor display a similar phenotype to sickle (Nukui et al. 2004; D Lohar, J Stiller, S Hababunga, JW Kam, J Dunlap, G Stacey, PM Gresshoff unpubl. data). Importantly, the increased nodulation present in sickle, transgenic L. japonicus expressing a mutant ethylene receptor, and in plants treated with ethylene inhibitors (Peters and Crist-Estes 1989) is due to more nodules in the susceptible zone and not an increase in the zone of nodulation as found in AON mutants. Mutants showing a correlation between nitrate-tolerant symbiosis and supernodulation indicate that AON and nitrate may share overlapping signals to control nodule number. There is also evidence that nitrate inhibition of nodulation involves an ethylene-dependent mechanism. In alfalfa, both

714


nitrate and Rhizobium treatment cause an increase in ethylene production, and inhibitors of ethylene biosynthesis and perception have resulted in increased nodulation in the presence of high nitrate (Ligero et al. 1986, 1987, 1991, 1999; Caba et al. 1998). Thus, nodule formation is regulated by at least two distinct pathways: ethylene-dependent signalling to control the distribution of nodules in the susceptible zone, and long-distance signalling to limit the extent of nodulation along the root. Nitrate may utilise both of these pathways to ensure that nodulation is suppressed under environmental conditions where nodulation is not needed. Although the exact mechanism involved in nodule regulation is not known, it is likely that these different pathways operate in part by interfering with NF signalling and / or perception. Reactive oxygen species and nodulation The interaction between avirulent plant pathogens and their respective hosts is characterised by the production of reactive oxygen species (ROS) in the early stages of the plant defence . response. These ROS, including the superoxide anion (O2 − ) and hydrogen peroxide (H2 O2 ), play an integral role in plant defence, particularly as part of the hypersensitive response (HR). While it has been suggested that ROS may be involved in the direct killing of pathogens, more substantive support has been for the role of ROS in HR through participation as a component in signalling and in the cross-linking of plant cell-wall proteins that delimit the pathogen (Lamb and Dixon 1997; Apel and Hirt 2004). Just as the invasion of a host plant by a pathogen involves a network of recognition, signalling and response, so too the symbiosis between rhizobia and legumes is composed of a similarly intricate signalling network. Moreover, as nodulation entails the invasion of host legumes by rhizobia it has been considered likely that the recognition and response by the host plant shares, at least in part, mechanisms common to invasion by pathogens and defence by the host plants (Vasse et al. 1993; Gage 2004). To this, there have been several studies examining the production and fate of ROS during nodule development (Santos et al. 2001; Ramu et al. 2002; D’Haeze et al. 2003; Jamet et al. 2003; Shaw and Long 2003b). In response to S. meliloti infection of M. sativa Santos . et al. (2001) detected O2 − in infection threads and nodules by histochemical staining with nitroblue tetrazolium and H2 O2 in nodules by transmission electron microscopy following staining with cerium chloride. Ramu et al. (2002) demonstrated that ROS production in M. truncatula was induced by S. meliloti in a Nod-factor-specific manner. Superoxide accumulation in roots, which could occur with purified Nod factor in the absence of bacterial cells, was abolished with S. meliloti mutants that either failed to produce Nod factor or produced Nod factor without the reducing end sulfate. ROS production in M. truncatula was able to

M. Kinkema et al.

induce the expression of rip1, which is an early nodulin gene and encodes a putative peroxidase. In support of the role for ROS in nodule formation, the symbiotic mutant dmi1-1 of M. truncatula, which does not exhibit early Nod factor responses, failed to produce superoxide and induce rip1 expression. In contrast, Shaw and Long (2003b) observed a reduction in H2 O2 efflux in the roots of M. truncatula upon exposure to Nod factor, a response that could be suppressed in mutants unable to form nodules. Shaw and Long (2003b) propose that the differences in ROS production seen between their study and that of Ramu et al. (2002) may be due to the times at which ROS production was determined. Shaw and Long (2003b) determined H2 O2 efflux during the first 90 min of exposure to Nod factor, while Ramu et al. (2002) detected ROS accumulation some 12 h following inoculation with S. meliloti. Clarification of ROS production throughout the entirety of nodule ontogeny remains a continuing challenge. To attenuate a defence response and accumulation of ROS Jamet et al. (2003) have shown that S. meliloti possess three genes (katA, katB and katC ) encoding catalase, which can be expressed during nodule formation. Two of these genes, katB and katC, are essential for nodulation. The obvious question remains as to whether or not the expression of these catalase genes may suppress the effects of oxidative stress from ROS. Common signals in symbiosis and development It is likely that legume nodulation and the regulation of nodulation evolved by utilising pre-existing pathways functioning in other symbiotic interactions, and involved in aspects of plant development. Arbuscular mycorrhizal fungi (AMF) form a symbiotic relationship with most land plants and enhance nutrient uptake by the roots while parasitic nematodes can be a devastating pest for a variety of crops. Nevertheless, both of these interactions (mutualistic and parasitic, respectively) share a variety of similarities with the processes involved in nodulation and the formation of lateral roots (Mathesius 2003). Nutman (1948) first noted a strong correlation between lateral root and nodule formation and suggested that rhizobia may induce nodulation by acting on the dividing cells of lateral root primordia. This hypothesis is supported by the work of Mathesius et al. (2000), who showed that rhizobia could induce nodules in the mature region of the root (normally not responsive to nodulation) in cells associated with lateral root formation. This finding suggests that some of the early responses in nodule development may be activated in lateral root primordia. Grafts between wild type L. japonicus and the supernodulating har1 mutant show that the shoot genotype can control both the supernodulation and increased lateral root phenotypes of har1 (Krusell et al. 2002; Buzas and Gresshoff 2006). Buzas and Gresshoff (2006) have also shown that the root genotype influences the non-symbiotic root phenotype. It


will be interesting to determine if the signalling components upstream and downstream of this receptor kinase are also shared in the long-distance control of nodulation and lateral root development. The fact that several different nodulation mutants display defects in root development (Wopereis et al. 2000; Nishimura et al. 2002a; Penmetsa et al. 2003; Searle et al. 2003) further supports the theory that nodulation utilises programs functioning in other aspects of plant development. Non-nodulation and supernodulation mutants have also shown that rhizobia, AMF, and nematodes may have more in common than meets the eye. Plant mutants defective for both rhizobia (nod− ) and mycorrhizae (myc− ) associations clearly indicate that some common steps are involved in the initial infection process (Duc et al. 1989; Bradbury et al. 1991; Catoira et al. 2000; Shrihari et al. 2000; Kistner et al. 2005). Like the regulation of nodulation by AON, systemic feedback control also exists for AMF colonisation (Vierheilig et al. 2000a, b), and mutants with increased nodulation have been shown to exhibit enhanced AMF colonisation (Shrihari et al. 2000; Solaiman et al. 2000). Catford et al. (2003) used split roots in alfalfa and showed that rhizobia inoculation of one root could suppress AMF colonisation of the second root, and vice versa. Thus, nodulation and AMF colonisation may involve similar mechanisms for early infection and the subsequent control of infection via a feedback autoregulatory response. Lohar and Bird (2003) have shown that the har1 supernodulating mutant is more susceptible to infection by root knot nematode suggesting that AON may also be involved in the control of this plant parasite. Moreover, root-knot nematodes invoke a similar cytoskeletal rearrangement in L. japonicus to that exhibited in response to rhizobia, and this response was attenuated or abolished in the nfr1, nfr5 and symRK nodulation mutants (Weerasinghe et al. 2005). What are the common signals that regulate the interactions with these diverse organisms and control specific aspects of root development? It is believed that one of the key players is the plant hormone auxin. The importance of auxin in lateral root development is well established (Casimiro et al. 2003), and its role in nodulation was first reported by Thimann (1936). Rhizobium inoculation (Mathesius et al. 1998b; Pacios-Bras et al. 2003), nematode infection (Hutangura et al. 1999), and lateral root formation (Mathesius et al. 1998b) all appear to result in a similar auxin distribution pattern as inferred by using transgenic plants containing an auxin-responsive promoter (GH3) fused with GUS or GFP. These experiments imply that during the initiation of cell division auxin levels are high, specifically in the dividing cells, while expression is subsequently reduced as the organs begin to differentiate. This pattern of auxin accumulation may be established by an inhibition in polar auxin transport. Such a mechanism would be consistent with the observations that inhibitors of auxin transport have been shown to induce


715

nodule-like structures in alfalfa (Hirsch et al. 1989) and clover (Wu et al. 1996). Flavonoids are known inhibitors of polar auxin transport (Jacobs and Rubery 1988) and are good candidates for regulating auxin accumulation in the cells of the root. The application of flavonoids mimics the effect of nodulating rhizobia, resulting in the accumulation of auxin at the site of nodule formation (Mathesius et al. 1998a). In addition, the timing and localisation of flavonoid expression in the root following RKN infection (Hutangura et al. 1999), lateral root development, and rhizobia inoculation (Mathesius et al. 1998a) suggest that flavonoids may be a common signal involved in the establishment of these different organs. Expression of flavonoids preceded and overlapped with auxin accumulation and was detected specifically in the primordia destined to form galls, lateral roots, and nodules. The control of cell division through a flavonoid-mediated regulation of auxin accumulation may therefore play an important role in these various processes. Although AMF colonisation does not usually involve cell division, auxin and flavonoids may be important signals mediating this association as well (Xie et al. 1995, 1998). The fact that both Rhizobium and NFs were able to enhance AMF infection (Xie et al. 1995, 1998) further suggests that the establishment of these symbiotic associations may involve similar regulatory processes. Lastly, the conservation of downstream signalling events was shown by Koltai et al. (2001), who found that two transcription factors involved in meristem development were expressed in a similar spatial and temporal pattern in lateral roots, nodules, and RNK galls of M. truncatula. In addition to shared signals and pathways with lateral root formation, mycorrhizal associations and the infection by nematodes, nodulation is also thought to have parallels with the processes of systemic acquired resistance (SAR; Durrant and Dong 2004) and induced systemic resistance (ISR; van Loon et al. 1998). SAR is a plant immune response that is often triggered after a local pathogen infection, and can provide long-term resistance throughout the plant to subsequent infections by a broad range of pathogens. It is characterised by the accumulation of salicylic acid and the increased expression of pathogenesis-related proteins (PRs) both at the infection site and in uninfected tissue. ISR also invokes resistance to a broad range of pathogens, but can be distinguished from SAR by the ability of non-pathogenic bacteria to induce resistance. Further, ISR is characterised by signalling involving jasmonic acid and / or ethylene. The early work of Kosslak and Bohlool (1984) demonstrating the systemic nature of AON via their split-root system supports the idea that nodulation shares, at least in part, signalling pathways from SAR and / or ISR. More recently, Nakagawa and Kawaguchi (2006) demonstrated that the application of methyl jasmonate to the shoots of L. japonicus strongly suppressed nodulation. van Spronsen et al. (2003) also demonstrated that salicylic acid (SA) at a concentration

716

M. Kinkema et al.


of 10−4 M inhibited nodulation and blocked the mitogenic effect of 18 : 4 acyl containing NF in Vicia sativa. Thus, a variety of evidence from genetic, molecular, phenotypic, and physiological studies suggest that overlapping regulatory pathways may function in development and the interaction with parasitic and mutualistic symbionts.

Acknowledgments We thank the Australian Research Council, the University of Queensland Strategic Research Fund and the Queensland State Government Smart State Initiative for funding under the Centre of Excellence Scheme. Special thanks are given to CILR members, especially Dr Attila Kereszt, for providing unpublished data and valued criticism.

Future directions Our current understanding of the early events in nodulation is based on the identification and characterisation of a substantial collection of host plant and bacterial symbiont genes. A sophisticated genetic network controlling the perception and early response to rhizobial NFs is now well established. Approaches targeting events downstream of the early nodulation events will help to provide a more comprehensive view of the relationship between nodule development and systemic regulation of nodulation in legumes. For example, identification of the genes that are regulated by the transcription factors NIN (Schauser et al. 1999), NSP1 (Smit et al. 2005), and NSP2 (Kalo et al. 2005) may provide clues on the nature of the root-derived signal implicated in AON. Characterisation of the upstream and downstream components functioning with the AON receptor-like kinases will also help in the identification of this root-derived systemic signal as well as the nature of the shoot-derived inhibitor. The yeast two-hybrid system has previously been utilised to identify proteins that interact with other receptor kinases (Nam and Li 2002, 2004; Tang et al. 2002; Hattan et al. 2004; Kaothien et al. 2005; Rienties et al. 2005), and similar studies may also help to characterise additional components involved in the AON signal transduction pathway. Further, protein–protein interaction methodologies, such as the co-immunoprecipitation of receptor complexes, fluorescence resonance energy transfer (FRET) and bimolecular fluorescence complementation, have already been extensively utilised in the characterisation of other receptor-like kinases and protein complexes (Shah et al. 2001; Li et al. 2002; Walter et al. 2004; Ehsan et al. 2005; Karlova et al. 2006). Hormones such as auxin and cytokinin are clearly important signals involved in the initiation of nodulation, but their roles in long-distance control of nodule formation is less clear. It is possible that these hormones are also involved in AON via direct or indirect effects on NF signalling. Recent studies by van Noorden et al. (2006) indicate that AON in M. truncatula may involve the regulation of polar auxin transport from the shoot to the root. Work by Ferguson et al. (2005) indicates that another class of plant hormones, the brassinosteroids, may also be involved in AON, and this regulation appears to be independent of auxin. Future studies will help determine the relationships between these various hormones, the AON receptor-like kinases, and the long-distance control of nodulation.

References Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367. doi: 10.1126/science.1092986 Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399. doi: 10.1146/annurev.arplant.55.031903.141701 Bauer WD (1981) Infection of legumes by rhizobia. Annual Review of Plant Physiology 32, 407–449. doi: 10.1146/annurev. pp.32.060181.002203 Bersoult A, Camut S, Perhald A, Kereszt A, Kiss GB, Cullimore J (2005) Expression of the Medicago truncatula DMI2 gene suggests roles of the symbiotic nodulation receptor kinase in nodules and during early nodule development. Molecular Plant–Microbe Interactions 18, 869–876. Bhuvaneswari TV, Turgeon BG, Bauer WD (1980) Early stages in the infection of soybean (Glycine max (L.) Merr.) by Rhizobium japonicum. I. Localization of infectible root cells. Plant Physiology 66, 1027–1031. Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, et al. (2003) The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiology 131, 1009–1017. doi: 10.1104/pp.102.016071 Bradbury SM, Peterson RL, Bowley SR (1991) Interaction between three alfalfa nodulation genotypes and two Glomus species. New Phytologist 119, 115–120. doi: 10.1111/j.1469-8137. 1991.tb01014.x Bright LJ, Liang Y, Mitchell DM, Harris JM (2005) The LATD gene of Medicago truncatula is required for both nodule and root development. Molecular Plant–Microbe Interactions 18, 521–532. Buzas DM, Gresshoff PM (2006) Short and long distance control of root development by LjHAR1 during the juvenile stage of Lotus japonicus. Journal of Plant Physiology (in press). Caba JM, Recalde L, Ligero F (1998) Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa. Plant, Cell & Environment 21, 87–93. doi: 10.1046/j.1365-3040.1998.00242.x Caba JM, Poveda JL, Gresshoff PM, Ligero F (1999) Differential sensitivity of nodulation to ethylene in soybean cv. Bragg and a supernodulating mutant. New Phytologist 142, 233–242. doi: 10.1046/j.1469-8137.1999.00386.x Caetano-Anollés G, Bauer WD (1988) Feedback regulation of nodule formation in alfalfa. Planta 175, 546–557. doi: 10.1007/ BF00393078 Caetano-Anollés G, Gresshoff PM (1990) Early induction of feedback regulatory responses governing nodulation in soybean. Plant Science 71, 69–81. doi: 10.1016/0168-9452(90)90069-Z Caetano-Anollés G, Gresshoff PM (1991) Plant genetic control of nodulation. Annual Review of Microbiology 45, 345–382. doi: 10.1146/annurev.mi.45.100191.002021 Caetano-Anollés G, Lagares A, Bauer WD (1990) Rhizobium meliloti exopolysaccharide mutants elicit feedback regulation of nodule formation in alfalfa. Plant Physiology 91, 368–374.


Caetano-Anollés G, Paparozzi ET, Gresshoff PM (1991) Mature nodules and root tips control nodulation in soybean. Journal of Plant Physiology 137, 389–396. Calvert HE, Pence MK, Pierce M, Malik NSA, Bauer WD (1984) Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots. Canadian Journal of Botany 62, 2375–2384. Capoen W, Goormachtig S, De Rycke R, Schroeyers K, Holsters M (2005) SrSymRK, a plant receptor essential for symbiosome formation. Proceedings of the National Academy of Sciences USA 102, 10 369–10 374. doi: 10.1073/pnas.0504250102 Carroll BJ, Gresshoff PM (1983) Nitrate inhibition of nodulation and nitrogen fixation in white clover. Zeitschrift fur Pflanzenphysiologie 110, 77–88. Carroll BJ, Mathews A (1990) Nitrate inhibition of nodulation in legumes. In ‘Molecular biology of symbiotic nitrogen fixation’. (Ed. PM Gresshoff) pp. 159–180. (CRC Press: Boca Raton) Carroll BJ, McNeil DL, Gresshoff PM (1985a) Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proceedings of the National Academy of Sciences USA 82, 4162–4166. Carroll BJ, McNeil DL, Gresshoff PM (1985b) A supernodulation and nitrate tolerant symbiotic (nts) soybean mutant. Plant Physiology 78, 34–40. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165–171. doi: 10.1016/S1360-1385(03)00051-7 Catford J-G, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with nod factors. Journal of Experimental Botany 54, 1481–1487. doi: 10.1093/jxb/erg156 Catoira R, Galera C, De Billy F, Penmetsa RV, Journet E-P, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. The Plant Cell 12, 1647–1666. doi: 10.1105/tpc.12.9.1647 Chen W-M, de Faria SM, Straliotto R, Pitard RM, Simões Araùjo JL, Chou J-H, Chou Y-J, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JPW, James EK (2005) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosanodulating strains from South America. Applied and Environmental Microbiology 71, 7461–7471. doi: 10.1128/AEM.71.11.74617471.2005 Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575–585. doi: 10.1016/S0092-8674(00)80239-1 Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM (1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiology 82, 588–590. DeYoung BJ, Clark SE (2001) Signaling through the CLV1 receptor complex. Plant Molecular Biology 46, 505–513. doi: 10.1023/A:1010672910703 D’Haeze W, De Rycke R, Mathis R, Goormachtig S, Pagnotta S, Verplancke C, Capoen W, Holsters M (2003) Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proceedings of the National Academy of Sciences USA 100, 11 789–11 794. doi: 10.1073/ pnas.1333899100 Duc G, Messager A (1989) Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Science 60, 207–213. doi: 10.1016/0168-9452(89)90168-4


717

Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal plant mutants (Myc− ) obtained in pea (Pisum sativum L.) and faba bean (Vicia faba L.). Plant Science 60, 215–222. doi: 10.1016/0168-9452(89)90169-6 Durrant WE, Dong X (2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185–209. doi: 10.1146/annurev. phyto.42.040803.140421 Ehsan H, Ray WK, Phinney B, Wang X, Huber SC, Clouse SD (2005) Interaction of Arabidopsis BRASSINOSTEROIDINSENSITIVE 1 receptor kinase with a homolog of mammalian TGF-β receptor interacting protein. The Plant Journal 43, 251–261. doi: 10.1111/j.1365-313X.2005.02448.x Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966. doi: 10.1038/nature00842 Fearn JC, LaRue TA (1991) Ethylene inhibitors restore nodulation to sym5 mutants of Pisum sativum L. cv sparkle. Plant Physiology 96, 239–244. ´ Schultze M (1998) The role of ´ Kondorosi A, Felle HH, Kondorosi E, ion fluxes in Nod factor signalling in Medicago sativa. The Plant Journal 13, 455–463. doi: 10.1046/j.1365-313X.1998.00041.x Ferguson BJ, Ross JJ, Reid JB (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiology 138, 2396–2405. doi: 10.1104/pp.105.062414 Fernández-López M, Goormachtig S, Gao M, D’Haeze W, Van Montagu M, Holsters M (1998) Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrata. Proceedings of the National Academy of Sciences USA 95, 12 724–12 728. Gabriel DW, Rolfe BG (1990) Working models of specific recognition in plant–microbe interactions. Annual Review of Phytopathology 28, 365–391. doi: 10.1146/annurev.py.28.090190.002053 Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews 68, 280–300. doi: 10.1128/MMBR.68.2.280-300.2004 George MLC, Robert FM (1991) Autoregulatory response of Phaseolus vulgaris L. to symbiotic mutants of Rhizobium leguminosarum bv. phaseoli. Applied and Environmental Microbiology 57, 2687–2692. Goodlass G, Smith KA (1979) Effects of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.). Plant and Soil 51, 387–395. doi: 10.1007/BF02197785 Goormachtig S, Capoen W, James EK, Holsters M (2004) Switch from intracellular to intercellular invasion during water stresstolerant legume nodulation. Proceedings of the National Academy of Sciences USA 101, 6303–6308. doi: 10.1073/pnas.0401540101 Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiology 131, 872–877. doi: 10.1104/ pp.017004 Gresshoff PM (1993) Molecular genetic analysis of nodulation genes in soybean. Plant Breeding Reviews 11, 275–318. Gresshoff PM, Gualtieri G, Laniya T, Indrasumunar A, Miyahara A, et al. (2005) Functional genomics of the regulation of nodule number in legumes. In ‘Biological nitrogen fixation, sustainable agriculture and the environment: proceedings of the 14th international nitrogen fixation congress’. (Eds Y-P Wang, M Lin, Z-X Tian, C Elmerich, WE Newton) pp. 173–178. (Springer: Dordrecht) Grobbelaar N, Clarke B, Hough MC (1971) The nodulation and nitrogen fixation of isolated roots of Phaseolus vulgaris L. Plant and Soil Special Vol., 215–223. Guinel FC, LaRue TA (1992) Ethylene inhibitors partly restore nodulation to pea mutant E107 (brz). Plant Physiology 99, 515–518.

718


Hattan J, Kanamoto H, Takemura M, Yokota A, Kohchi T (2004) Molecular characterization of the cytoplasmic interacting protein of the receptor kinase IRK expressed in the inflorescence and root apices of Arabidopsis. Bioscience, Biotechnology, and Biochemistry 68, 2598–2606. doi: 10.1271/bbb.68.2598 Heidstra R, Geurts R, Franssen H, Spaink HP, van Kammen A, Bisseling T (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiology 105, 787–797. Heidstra R, Nilsen G, Martinez-Abarca F, van Kammen A, Bisseling T (1997a) Nod factor-induced expression of leghemoglobin to study the mechanism of NH4 NO3 inhibition on root hair deformation. Molecular Plant–Microbe Interactions 10, 215–220. Heidstra R, Yang WC, Yalcin Y, Peck S, Emons A, Van Kammen A, Bisseling T (1997b) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124, 1781–1787. Hinson K (1975) Nodulation responses from nitrogen applied to soybean half-root systems. Agronomy Journal 67, 799–804. Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proceedings of the National Academy of Sciences of the United States of America 86, 1244–1248. Hunter WJ (1993) Ethylene production by root nodules and effect of ethylene on nodulation in Glycine max. Applied and Environmental Microbiology 59, 1947–1950. Hutangura P, Mathesius U, Jones MGK, Rolfe BG (1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Australian Journal of Plant Physiology 26, 221–231. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, et al. (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527–531. doi: 10.1038/ nature03237 Jacobs M, Rubery PH (1988) Naturally occuring auxin transport regulators. Science 241, 346–349. Jacobsen E, Feenstra WJ (1984) A new pea mutant with efficient nodulation in the presence of nitrate. Plant Science Letters 33, 337–344. doi: 10.1016/0304-4211(84)90025-7 Jamet A, Sigaud S, Van de Sype G, Puppo A, Hérouart D (2003) Expression of the bacterial catalase genes during Sinorhizobium meliloti–Medicago sativa symbiosis and their crucial role during the infection process. Molecular Plant–Microbe Interactions 16, 217–225. Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786–1789. doi: 10.1126/science.1110951 Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EMH, et al. (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proceedings of the National Academy of Sciences USA 103, 359–364. doi: 10.1073/pnas.0508883103 Kaothien P, Ok SH, Shuai B, Wengier D, Cotter R, Kelley D, Kiriakopolos S, Muschietti J, McCormick S (2005) Kinase partner protein interacts with LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. The Plant Journal 42, 492–503. doi: 10.1111/j.1365-313X.2005.02388.x Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S (2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTORLIKE KINASE1 protein complex includes BRASSINOSTEROIDINSENSITIVE1. The Plant Cell 18, 626–638.

M. Kinkema et al.

Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. The Plant Cell 17, 2217–2229. doi: 10.1105/tpc.105.032714 Koltai H, Dhandaydham M, Oppermann CH, Thomas J, Bird D (2001) Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Molecular Plant– Microbe Interactions 14, 1168–1177. Kosslak RM, Bohlool BB (1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiology 75, 125–130. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, et al. (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420, 422–426. doi: 10.1038/ nature01207 Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275. doi: 10.1146/annurev.arplant.48.1.251 Lawson CGR, Carroll BJ, Gresshoff PM (1988) Alleviation of nitrate inhibition of soybean nodulation by high inoculum does not involve bacterial nitrate metabolism. Plant and Soil 110, 123–127. doi: 10.1007/BF02143547 Lee KH, La Rue T (1992) Exogenous ethylene inhibits nodulation of Pisum sativum L. cv sparkle. Plant Physiology 100, 1759–1763. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364. doi: 10.1126/science.1093038 Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213–222. doi: 10.1016/S0092-8674(02)00812-7 Ligero F, Lluch C, Olivares J (1986) Evolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti. Journal of Plant Physiology 125, 361–365. Ligero F, Lluch C, Olivares J (1987) Evolution of ethylene from roots and nodulation rate of alfalfa (Medicago sativa L.) plants inoculated with Rhizobium meliloti as affected by the presence of nitrate. Journal of Plant Physiology 129, 461–467. Ligero F, Caba JM, Lluch C, Olivares J (1991) Nitrate inhibition of nodulation can be overcome by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiology 97, 1221–1225. Ligero F, Poveda JL, Gresshoff PM, Caba JM (1999) Nitrate-and inoculation-enhanced ethylene biosynthesis in soybean roots as a possible mediator of nodulation control. Journal of Plant Physiology 154, 482–488. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630–633. doi: 10.1126/ science.1090074 Loh J, Stacey G (2003) Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Applied and Environmental Microbiology 69, 10–17. doi: 10.1128/ AEM.69.1.10-17.2003 Loh JT, Yuen-Tsai JPY, Stacey MG, Lohar D, Welborn A, Stacey G (2001) Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes. Molecular Microbiology 42, 37–46. doi: 10.1046/j.1365-2958.2001.02625.x Lohar DP, Bird DMcK (2003) Lotus japonicus: A new model to study root-parasitic nematodes. Plant & Cell Physiology 44, 1176–1184. doi: 10.1093/pcp/pcg146 Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640. doi: 10.1038/nature02045


Malik NSA, Calvert HE, Bauer WD (1987) Nitrate induced regulation of nodule formation in soybean. Plant Physiology 84, 266–271. Mathesius U (2003) Conservation and divergence of signalling pathways between roots and soil microbes — the Rhizobium–legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls. Plant and Soil 255, 105–119. doi: 10.1023/A:1026139026780 Mathesius U, Bayliss C, Weinman JJ, Schlaman HRM, Spaink HP, Rolfe BG, McCully ME, Djordjevic MA (1998a) Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover. Molecular Plant–Microbe Interactions 11, 1223–1232. Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998b) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. The Plant Journal 14, 23–34. doi: 10.1046/j.1365-313X.1998.00090.x Mathesius U, Weinman JJ, Rolfe BG, Djordjevic MA (2000) Rhizobia can induce nodules in white clover by ‘hijacking’ mature cortical cells activated during lateral root development. Molecular Plant– Microbe Interactions 13, 170–182. Mathews A, Carroll BJ, Gresshoff PM (1989) Development of Bradyrhizobium infections in a supernodulating and non-nodulating mutant of soybean (Glycine max (L.) Merr). Protoplasma 150, 40–47. doi: 10.1007/BF01352919 McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nature Biotechnology 18, 455–457. doi: 10.1038/74542 Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222, 709–715. doi: 10.1007/s00425-005-0003-4 Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004a) A Ca2+ / calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences USA 101, 4701–4705. doi: 10.1073/pnas.0400595101 Mitra RM, Shaw SL, Long SR (2004b) Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume–rhizobia symbiosis. Proceedings of the National Academy of Sciences USA 101, 10 217–10 222. doi: 10.1073/pnas.0402186101 Morris AC, Djordjevic MA (2006) The Rhizobium leguminosarum biovar trifolii ANU794 induces novel developmental responses on the subterranean clover cultivar Woogenellup. Molecular Plant– Microbe Interactions 19, 471–479. Nakagawa T, Kawaguchi M (2006) Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant & Cell Physiology 47, 176–180. doi: 10.1093/pcp/pci222 Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203–212. doi: 10.1016/S00928674(02)00814-0 Nam KH, Li J (2004) The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROID-INSENSITIVE 1. The Plant Cell 16, 2406–2417. doi: 10.1105/tpc.104.023903 Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, et al. (2002a) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420, 426–429. doi: 10.1038/nature01231 Nishimura R, Ohmori M, Fujita H, Kawaguchi M (2002b) A lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proceedings of the National Academy of Sciences USA 99, 15 206–15 210. doi: 10.1073/pnas.222302699


719

Nishimura R, Ohmori M, Kawaguchi M (2002c) The novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant & Cell Physiology 43, 853–859. doi: 10.1093/ pcp/pcf098 Nukui N, Ezura H, Yuhashi K-I, Yasuta T, Minamisawa K (2000) Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant & Cell Physiology 41, 893–897. doi: 10.1093/pcp/pcd011 Nukui N, Ezura H, Minamisawa K (2004) Transgenic Lotus japonicus with an ethylene receptor gene Cm-ERS1/H70A enhances formation of infection threads and nodule primordia. Plant & Cell Physiology 45, 427–435. doi: 10.1093/pcp/pch046 Nutman PS (1948) Physiological studies on nodule formation I. The relation between nodulation and lateral root formation in red clover. Annals of Botany 12, 81–96. Nutman PS (1952) Studies on the physiology of nodule formation. III. Experiments on the excision of root-tips and nodules. Annals of Botany 16, 80–102. Oka-Kira E, Tateno K, Miura K, Haga T, Hayashi M, et al. (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. The Plant Journal 44, 505–515. doi: 10.1111/j.1365-313X.2005.02543.x Olah B, Brière C, Bécaud G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1 / DMI2 signalling pathway. The Plant Journal 44, 195–207. doi: 10.1111/j.1365-313X.2005.02522.x Oldroyd GED (2001) Dissecting symbiosis: developments in Nod factor signal transduction. Annals of Botany 87, 709–718. doi: 10.1006/anbo.2001.1410 Oldroyd GED, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. The Plant Cell 13, 1835–1849. doi: 10.1105/tpc.13.8.1835 Pacios-Bras C, Schlaman HRM, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Molecular Biology 52, 1169–1180. doi: 10.1023/B:PLAN.0000004308.78057.f5 Park SJ, Buttery BR (1988) Nodulation mutants of white bean (Phaseolus vulgaris L.) induced by ethyl-methane sulfonate. Canadian Journal of Plant Science 68, 199–202. Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530. doi: 10.1126/science.275.5299.527 Penmetsa RV, Frugoli JA, Smith LS, Long SR, Cook DR (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiology 131, 998–1008. doi: 10.1104/ pp.015677 Peters NK, Crist-Estes DK (1989) Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiology 91, 690–693. Pierce M, Bauer WD (1983) A rapid regulatory response governing nodulation in soybean. Plant Physiology 73, 286–290. Postma JG, Jacobsen E, Feenstra WJ (1988) Three pea mutants with an altered nodulation studied by genetic analysis and grafting. Journal of Plant Physiology 132, 424–430. Price GD, Mohapatra SS, Gresshoff PM (1984) Structure of nodules formed by Rhizobium strain ANU289 in the non-legume Parasponia and legume siratro (Macroptilium atropurpureum). Botanical Gazette (Chicago, Ill.) 145, 444–451. doi: 10.1086/337477 Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592. doi: 10.1038/ nature02039

720


Ramu SK, Peng H-M, Cook DR (2002) Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Molecular Plant– Microbe Interactions 15, 522–528. Rienties IM, Vink J, Borst JW, Russinova E, de Vries SC (2005) The Arabidopsis SERK1 protein interacts with the AAA-ATPase AtCDC48, the 14–3-3 protein GF14λ and the PP2C phosphatase KAPP. Planta 221, 394–405. doi: 10.1007/s00425-004-1447-7 Sagan M, Duc G (1996) Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20, 229–245. Sagan M, Gresshoff PM (1996) Developmental mapping of nodulation events in Pea (Pisum sativum L.) using supernodulating plant genotypes and bacterial variability reveals both plant and Rhizobium control of nodulation regulation. Plant Science 117, 167–179. doi: 10.1016/0168-9452(96)04411-1 Santos R, Hérouart D, Sigaud S, Touati D, Puppo A (2001) Oxidative burst in alfalfa–Sinorhizobium meliloti symbiotic interaction. Molecular Plant–Microbe Interactions 14, 86–89. Sargent L, Huang SZ, Rolfe BG, Djordjevic MA (1987) Split root assays using Trifolium subterraneum shows that Rhizobium infection induces a systemic response that can inhibit nodulation of another invasive Rhizobium strain. Applied and Environmental Microbiology 53, 1611–1619. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402, 191–195. doi: 10.1038/46058 Schmidt JS, Harper JE, Hoffman TK, Bent AF (1999) Regulation of soybean nodulation independent of ethylene signaling. Plant Physiology 119, 951–959. doi: 10.1104/pp.119.3.951 Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucinerich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology 58, 809–822. doi: 10.1007/s11103005-8102-y Schlaman HRM, Horvath B, Vigenboom E, Okker RGH, Lugtenberg BJJ (1991) Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar vicae. Journal of Bacteriology 173, 4277–4287. Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a clavata1-like receptor kinase. Science 299, 109–112. doi: 10.1126/science.1077937 Shah K, Gadella TWJ Jr, van Erp H, Hecht V, de Vries SC (2001) Subcellular localization and oligomerization of the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein. Journal of Molecular Biology 309, 641–655. doi: 10.1006/jmbi.2001.4706 Sharma VK, Carles C, Fletcher JC (2003) Maintenance of stem cell populations in plants. Proceedings of the National Academy of Sciences USA 100, 11 823–11 829. doi: 10.1073/pnas.1834206100 Shaw SL, Long SR (2003a) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiology 131, 976–984. doi: 10.1104/pp.005546 Shaw SL, Long SR (2003b) Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiology 132, 2196–2204. doi: 10.1104/pp.103.021113 Shrihari PC, Sakamoto K, Inubushi K, Akao S (2000) Interaction between supernodulating or non-nodulating mutants of soybean and two arbuscular mycorrhizal fungi. Mycorrhiza 10, 101–106. doi: 10.1007/s005720000064 Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789–1791. doi: 10.1126/science.1111025

M. Kinkema et al.

Solaiman MZ, Senoo K, Kawaguchi M, Imaizumi-Anraku H, Akao S, Tanaka A, Obata H (2000) Characterization of mycorrhizas formed by Glomus sp. on roots of hypernodulating mutants of Lotus japonicus. Journal of Plant Research 113, 443–448. doi: 10.1007/PL00013953 Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences USA 92, 2647–2651. Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annual Review of Microbiology 54, 257–288. doi: 10.1146/annurev.micro.54.1.257 Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics and functional genomics of legume nodulation. Current Opinion in Plant Biology 9, 110–121. doi: 10.1016/j.pbi.2006.01.005 Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, et al. (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962. doi: 10.1038/nature00841 Suganuma N, Yamauchi H, Yamamoto K (1995) Enhanced production of ethylene by soybean roots after inoculation with Bradyrhizobium japonicum. Plant Science 111, 163–168. doi: 10.1016/0168-9452 (95)04239-Q Tang W, Ezcurra I, Muschietti J, McCormick S (2002) A cysteinerich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. The Plant Cell 14, 2277–2287. doi: 10.1105/tpc.003103 Thimann KV (1936) On the physiology of the formation of nodules on legume roots. Proceedings of the National Academy of Sciences USA 22, 511–514. Timmers ACJ, Auriac M-C, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium–Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126, 3617–3628. Truchet G, Roche P, Lerouge P, Vasse J, Camut S, Debilly F, Prome JC, Dénarié J (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670–673. doi: 10.1038/351670a0 van Brussel AAN, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJJ, Kijne JW (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257, 70–72. van Loon LC, Bakker PA, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36, 453–483. doi: 10.1146/annurev.phyto.36.1.453 van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiology 140, 1494–1506. doi: 10.1104/pp.105.075879 van Spronsen PC, Tak T, Rood AMM, van Brussel AAN, Kijne JW, Boot KJM (2003) Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Molecular Plant– Microbe Interactions 16, 83–91. Vasse J, de Billy F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti–alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566. doi: 10.1046/j.1365-313X.1993.04030555.x Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2 -fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant and Soil 266, 205–230. doi: 10.1007/s11104-005-0871-1 Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y (2000a) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biology & Biochemistry 32, 589–595. doi: 10.1016/S0038-0717(99)00155-8



Vierheilig H, Maier W, Wyss U, Samson J, Strack D, Piché Y (2000b) Cyclohexenone derivative- and phosphate-levels in split root systems and their role in the systemic suppression of mycorrhization in precolonized barley plants. Journal of Plant Physiology 157, 593–599. Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Denarie J, Long SR (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proceedings of the National Academy of Sciences USA 97, 13 407–13 412. doi: 10.1073/pnas.230439797 Walker SA, Viprey V, Downie JA (2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proceedings of the National Academy of Sciences USA 97, 13 413–13 418. doi: 10.1073/ pnas.230440097 Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40, 428–438. doi: 10.1111/j.1365-313X.2004.02219.x Weerasinghe R, Bird DMcK, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proceedings of the National Academy of Sciences USA 102, 3147–3152. doi: 10.1073/pnas.0407926102 Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, de Bruijn FJ, Stougaard J, Szczyglowski K (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal 23, 97–114. doi: 10.1046/j.1365-313x.2000.00799.x

721

Wu C, Dickstein R, Carry AJ, Norris JH (1996) The auxin transport inhibitor N-(1-Naphthyl)phthalamic acid elicits pseudonodules on non-nodulating mutants of white sweet clover. Plant Physiology 110, 501–510. Xie Z-P, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vögeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybean. Plant Physiology 108, 1519–1525. Xie Z-P, Staehelin C, Wiemken A, Boller T (1996) Ethylene responsiveness of soybean cultivars characterized by leaf senescence, chitinase induction and nodulation. Journal of Plant Physiology 149, 690–694. Xie Z-P, Muller J, Wiemken A, Broughton WJ, Boller T (1998) Nod factors and tri-iodobenzoic acid stimulate mycorrhizal colonization and affect carbohydrate partitioning in mycorrhizal roots of Lablab purpureus. New Phytologist 139, 361–366. doi: 10.1046/j.14698137.1998.00186.x Yamamoto E, Caglar H, Knap HT (2000) Molecular characterization of two soybean homologs of Arabidopsis thaliana CLAVATA1 from the wild type and fasciation mutant. Biochimica et Biophysica Acta 1491, 333–340.

Manuscript received 17 March 2006, accepted 22 May 2006

http://www.publish.csiro.au/journals/fpb

Legume nodulation - CiteSeerX

Legume nodulation - CiteSeerX

Suggest Documents

Molecular mechanisms controlling legume autoregulation of nodulation

Nodulation in the Legume Biofuel Feedstock Tree ... - Springer Link

Nodulation Studies in the Model Legume Medicago ... - APS Journals

Nodulation Studies in the Model Legume Medicago ... - APS Journals

Legume Aeschynomene evenia - CiteSeerX

Cowpea, a Multifunctional Legume - CiteSeerX

Nodulation Suppression by Rhizobium leguminosarum bv ... - CiteSeerX

Rhizobium Ieguminosarum nodulation gene (nod ... - CiteSeerX

Legume perspectives 2 (PDF) - International Legume Society

Legume Inoculants and Quality Control - CiteSeerX

species legume

Nodulation, arbuscular mycorrhizal colonization

Regulation and symbiotic significance of nodulation outer ... - CiteSeerX

intercropping legume and non- legume, an innovative ...

Rhizobium-Legume Associations - NCBI

perspectives - International Legume Society

Rhizobium legume symbiosis.pdf

Rhizobial Nodulation Factors Stimulate Mycorrhizal

Non-rhizobial nodulation in legumes

perspectives - International Legume Society

Ureide-Producing Legume - NCBI

perspectives - International Legume Society

Legume Futures Report 4.5 Impacts of legume-related policy ...

Decomposition from legume and non-legume crop residues: Effects on