Fungal ecology catches fire

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Phenotypic variability: underlying mechanisms and limits do matter

‘A more fundamental question is whether the pattern observed at a regional level is the result of species adaptation to site-specific conditions through the emergence of local ecotypes, or of structural and

The interest in the hydraulic architecture of trees, and the interplay between xylem anatomical characteristics and dimensions, its hydraulic conductance and water transport through the plant, stretches back to Leonardo da Vinci’s observations and Huber’s (1928) first systematic measurements of a constant area of conductive sapwood across the entire length of the tree and of a close correspondence with the amount of leaf area supported. Apart from the pure interest in the inner workings of plant self-organization, the study of hydraulic architecture has since demonstrated its role in key tree and ecosystem processes as a result of (1) the close association between gaseous-phase and liquid-phase conductances (i.e. between stomatal and hydraulic conductances, responsible for leaf water loss and replenishment, respectively), and important effects on CO2 availability and photosynthetic rates (Brodribb et al., 2005), (2) the requirements imposed by hydraulic constraints on growth allocation between tree parts, which affects both primary production (through allocation to transpiring foliage) and net ecosystem production (through allocation to shortlived, easily decomposed fine roots; Litton et al., 2007) and (3) xylem and foliage vulnerability to extreme events, whenever the limits imposed by plant hydraulic architecture and stomatal behaviour are exceeded, resulting in extreme tissue dehydration and foliage dieback (MartıńezVilalta & Pinõl, 2002). Several studies have demonstrated the variability of plant hydraulic architecture both between and within species, which is reflected in the huge variability in tree form and function across scales. It has been suggested that the observed differences could mirror the variability in environmental conditions experienced by different species and individuals, resulting in an optimal behaviour under the pressure of evolutionary processes (Magnani et al., 2002). In this issue of New Phytologist, Martıńez-Vilalta et al., (pp. 353–364) explore the geographic pattern of hydraulic architecture in Pinus sylvestris, which, because of its wide

The Authors (2009) Journal compilation New Phytologist (2009)

functional acclimation and phenotypic plasticity.’

natural range as well as its ecological and productive relevance, has been the subject of a number of related studies and can be therefore viewed as a de facto model species in forest tree functional and evolutionary ecology. Seen in the context of this large body of studies on the geographic and genetic variability of functional traits, the article provides not only new valuable information (in terms of parameters explored and their correlation and trade-offs), but also important hints of how evolutionary strategies could differ at the intraspecific and interspecific levels, and for different traits and processes. The authors did not find evidence at the intraspecific level of some of the associations and trade-offs between hydraulic traits that have been commonly reported across species. An interesting case in point is the observation of a lack of variability across the entire latitudinal range explored (from Finland to Spain and southern Italy) in xylem vulnerability to embolism, which is determined by tracheid fine anatomical features (Hacke & Jansen, 2009) and appears to determine the minimum water potential the plant can tolerate (Jacobsen et al., 2007). By contrast, large interspecific differences in vulnerability to xylem cavitation have been found among coniferous and other evergreen species (Maherali et al., 2004), which were related to mean annual precipitation. A similar pattern has been recently observed among a range of shrub species (Bhaskar et al., 2007), after accounting for phylogenetic effects. Can the limited variability reported here for P. sylvestris populations (and for P. ponderosa, described by Maherali & DeLucia, 2000) be extended to the entire genus, as suggested by Martıńez-Vilalta et al. (2004)? A similar homeostatic canalization in the face of environmental variability has been reported for Quercus wislizenii adult trees by Matzner et al. (2001),

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but further research is needed on other species before any general conclusions can be drawn. Two other crucial questions are raised by the analysis of Martıńez-Vilalta and colleagues, both of which are related to the interpretation of the observed pattern at a regional level and to the design of future studies. In order to avoid the confounding effects of the correlation commonly observed between climatic variables, the authors bundle several of them together, through a principal component analysis, into an index of climate dryness. This was found to be closely related to a number of functional parameters, such as the ratio between transpiring foliage and branch sapwood area (AL : AS). Indeed, the geographic variability across Europe in AL : AS has been variously attributed in the past to the effects of evaporative demand (Berninger et al., 1995) or temperature (Palmroth et al., 1999), both contributing to the new dryness index. It would be important, however, to disentangle the effects of individual variables, as their trajectories in response to future climate change could differ. This is no easy task, as truly manipulative studies are hardly feasible in slow-growing forest trees. The only way forward lies in the careful design of future regional studies, which should locate study plots on the basis not of their geographic distribution, but of a homogeneous exploration of the climate space (e.g. temperature · drought combinations). A more fundamental question is whether the pattern observed at the regional level is the result of species adaptation to site-specific conditions through the emergence of local ecotypes, or of structural and functional acclimation and phenotypic plasticity. This has great ecological and evolutionary significance. On the one hand, if the variability currently observed was the result of continuous acclimation to variable conditions, we could expect local individuals to keep changing in response to future climate change and for pine trees from Germany to resemble their Spanish kin in a few decades’ time without a reduction in population fitness or an increase in vulnerability. The opposite would be true if observed differences were the result of selection and therefore genetically encoded, as they could provide optimal fitness under present, but not future, conditions (Magnani et al., 2002). Under an evolutionary perspective, a large phenotypic plasticity could be explained by the variety of environmental conditions experienced by trees over their lifetime, which would prevent stabilizing selection from prevailing (Bradshaw, 1965). Which process does prevail? As an example, Palmroth et al. (1999) also reported a close relationship between the leaf-to-sapwood area ratio of different P. sylvestris provenances and annual temperature. Interestingly, the same relationship was observed in situ and in a common garden experiment, considering the temperature at the site of seed origin. This would suggest a strong genetic control and a general lack of phenotypic plasticity for this hydraulic trait

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Fig. 1 Schematic representation of the possible response of plant functional traits to environmental variables across regional transects (thin line) or to prevailing conditions at the site of seed origin in common garden experiments (thick line). Four possible cases can be distinguished: (a) a parallel response at the two scales is indicative of directional selection and long-term adaptation to local conditions; (b) by contrast, a lack of variability in common garden experiments suggests that the pattern observed at the regional level is the result of acclimation to site conditions; (c) contrasting responses at the two scales demonstrate a strong genetic · environment interaction, eliciting further studies on the genetic control of phenotypic plasticity; (d) finally, a limited variability of the trait across both scales (e.g. for minimum water potential homeostasis, constant vulnerability to embolism) demonstrates canalization as a result of homeostatic processes.

(see Fig. 1). This contrasts with other key functional traits reported by Oleksyn et al. (2003). In an analysis of foliage nutrient concentration in P. sylvestris from different geographic origins, the geographic pattern recorded in situ (determined by the interaction between ecotypic adaptation and acclimation to local conditions) was found to differ substantially from that observed under constant environmental conditions in a common garden experiment (determined only by ecotypic adaptation). How can future experiments try and disentangle the role of adaptation and acclimation, and help us predict the impact of future conditions on forest tree function and vulnerability? Only a combination of in situ and ex situ measurements can provide the answer to this question, exploiting the network of provenance trials established with a different purpose by forest services over the years. The answer could differ depending on the trait and scale considered, as hinted by Martıńez-Vilalta and colleagues. Federico Magnani DCA, University of Bologna, via Fanin 46 I-40127, Bologna, Italy (tel +39 051 2096466; email [email protected])


New Phytologist References Berninger F, Mencuccini M, Nikinmaa E, Grace J, Hari P. 1995. Evaporative demand determines branchiness of Scots pine. Oecologia 102: 164–168. Bhaskar R, Valiente-Banuet V, Ackerly DD. 2007. Evolution of hydraulic traits in closely related species pairs from mediterranean and nonmediterranean environments of North America. New Phytologist 176: 718–726. Bradshaw AD. 1965. Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13: 115–155. Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B. 2005. Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist 165: 839–846. Hacke UG, Jansen S. 2009. Embolism resistance of three boreal conifer species varies with pit structure. New Phytologist 182: 675–686. Huber B. 1928. Weitere Untersuchungen uber das Wasserleitungssystem der Pfanzen. Jahrbu¨cher fu¨r wissenschaftliche Botanik 67: 877–959. Jacobsen AL, Pratt RB, Ewers FW, Davis SD. 2007. Cavitation resistance among 26 chaparral species of Southern California. Ecological Monographs 77: 99–115. Litton CM, Raich JW, Ryan MG. 2007. Carbon allocation in forest ecosystems. Global Change Biology 13: 2089–2109. Magnani F, Grace J, Borghetti M. 2002. Adjustment of tree structure in response to the environment under hydraulic constraints. Functional Ecology 16: 385–393. Maherali H, DeLucia EH. 2000. Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiology 20: 859–867. Maherali H, Pockman WT, Jackson RB. 2004. Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85: 2184–2199. Martıńez-Vilalta J, Pinõl J. 2002. Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. Forest Ecology and Management 161: 247–256. Martıńez-Vilalta J, Sala A, Pinõl J. 2004. The hydraulic architecture of Pinaceae. A review. Plant Ecology 171: 3–13. Martıńez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nole` A, Poyatos R, Ripullone F, Sass-Klaassen U, Zweifel R. 2009. Hydraulic adjustment of Scots pine across Europe. New Phytologist 184: 353–364. Matzner SL, Rice KJ, Richards JH. 2001. Intra-specific variation in xylem cavitation in interior live oak (Quercus wislizenii A. DC.). Journal of Experimental Botany 52: 783–789. Oleksyn J, Reich PB, Zytkowiak R, Karolewski P, Tjoelker MG. 2003. Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations. Oecologia 136: 220–235. Palmroth S, Berninger F, Nikinmaa E, Lloyd J, Pulkkinen P, Hari P. 1999. Structural adaptation rather than water conservation was observed in Scots pine over a range of wet to dry climates. Oecologia 121: 302–309. Key words: acclimation, adaptation, drought, hydraulic architecture, phenotypic plasticity, xylem embolism.

Fungal ecology catches fire Progress in science is episodic and uneven; some fields get hot while others dwindle. Fungal ecology is undergoing an observationally driven boom, resulting from the application of pyrosequencing technology. Three papers in the current issue of New Phytologist (Bueé et al., 449–456; Jumpponen ¨ pik et al., 424–437) illustrate the state & Jones, 438–448; O


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of the science, using 454 sequencing of clone libraries derived from PCR-amplified ribosomal RNA (rRNA) genes to characterize fungal communities. The volume of data in these studies is staggering; Bueé et al. generated 166 000 ¨ pik et al. and Jumpponen & Jones anasequences, while O lyzed 125 000 and 18 000 sequences, respectively. The flood of data from these and similar studies provides ecologists with opportunities to describe fungal communities in greater detail than ever before. At the same time, the new technology challenges the taxonomic community to provide resources for molecular identification and to consider how (or whether) the rapidly accumulating sequence data can be used for species discovery and description.

¨ pik et al., Jumpponen & Jones and ‘The studies of O Bueé et al. prompted us to ask whether ecology or taxonomy is currently leading the way in the discovery of new taxa, and also to assess the growth of the molecular database for taxon identification.’

¨ pik et al. targeted partial nuclear small subunit (18S) O rRNA genes in arbuscular mycorrhizal fungi (Glomeromycota) in the roots of ten different plant species in a 10 · 10m plot. The plants were divided into generalists, which can be found in a wide range of habitat types, and forest specialists. The fungal sequences were assigned to 48 Virtual Taxa (VT), defined as groups with sequence similarity of at least 97%. Forest specialist plants harboured much higher diversity of Glomeromycota than generalists; 22 VT were limited to forest specialists, while only one VT was restricted to generalist species. A phylogenetic tree of the VT suggests that there have been multiple transitions between association with forest specialists and generalists in the evolution of Glomeromycota (although Glomus group A appears to be particularly rich in taxa associated with generalists, while the Acaulosporaceae and Glomus group C are represented almost entirely by VT associated with forest specialists; see ¨ pik et al. Similarly, cluster analyFig. 1 contained within O sis of the fungal communities of plant hosts yielded a topology that separates VT associated with forest specialists and generalists into distinct groups, but that conflicts with current views of angiosperm phylogeny (e.g. the forest specialist Galeobdolon luteum and the generalist Veronica chamaedrys are in separate clusters, although both are members of the ¨ pik et al.). In sum, the Lamiales; Fig. 3, contained within O ¨ pik et al. suggests that there are co-adapted work of O pools of forest-specialist Glomeromycota and plants, and that habitat preference may be a more important driver of


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host–fungus associations than host or fungus phylogeny, at least over very broad evolutionary scales. The other studies are largely in the realm of descriptive ecology and molecular natural history (this is not intended as a criticism). Jumpponen & Jones and Bueé et al. both used sequences of the internal transcribed spacer (ITS) region of nuclear rRNA genes, which has become the de facto fungal barcode locus for most Dikarya (Basidiomycota and Ascomycota; Seifert, 2008). Jumpponen & Jones studied the fungal community in the phyllosphere (including epiphytes and endophytes) of a single tree species, Quercus macrocarpa, which was sampled in urban and rural environments. Richness and diversity of the phyllosphere fungal communities were greater in the rural habitats than in the urban habitats. Bueé et al. characterized fungal diversity in forest soils associated with six different dominant tree species. An important finding of Bueé et al. was that use of a custom-curated sequence database enabled many more sequences to be identified than a wholesale BLAST analysis of the notoriously error-prone GenBank database (Nilsson et al., 2006). Ecologists are naturally excited about the promise of pyrosequencing methods for describing fungal communities, but systematists should also consider how the outpouring of data from molecular ecological studies impacts their discipline. At a basic level, taxonomy has two complementary goals: (1) discovery and description of new taxa (including clades), and (2) provision of resources for ¨ pik et al., Jumpponen & identification. The studies of O Jones and Bueé et al. prompted us to ask whether ecology or taxonomy is currently leading the way in the discovery of new taxa, and also to assess the growth of the molecular database for taxon identification. To evaluate progress in species description, we surveyed new names for species (i.e. excluding infraspecific taxa and combinations) of Ascomycota, Basidiomycota and Glomeromycota recorded in the Index of Fungi (published every 6 months by CABI) from 2000 to 2009 (Table 1). The

overall rate of species discovery has been fairly level for the last 10 yr, with an average of 1223 new species described per year, mostly Ascomycota. In 2008, the last year for which complete data are available, 1009 species were described. These figures probably overestimate the rate of species discovery somewhat, because of redescriptions of previously published taxa, which have been estimated to occur at a rate of one synonym for every 2.5 truly novel descriptions (Hawksworth, 1991). It is very difficult to estimate how many undescribed species of fungi have been detected by molecular ecologists in ¨ pik et al., Jumpponen & recent years, but the data from O Jones and Bueé et al. provide a hint about the magnitude of taxon discovery that is occurring. Jumpponen & Jones assigned their sequences to 689 operational taxonomic units (OTUs) based on a 95% sequence identity criterion, including 329 singletons and 360 nonsingletons. A BLAST analysis of the nonsingletons found that 214 OTUs had no matches in GenBank at the 95% identity level, and the top hits for 26 of the remaining OTUs were not identified to species level (Suppl. Table S2, provided as part of Jumpponen & Jones). Thus, c. 240 OTUs could not be referred to a named species. This is a conservative figure, because it excludes the 329 singleton OTUs that evidently were not subjected to BLAST analysis. Bueé et al. pooled their sequences into c. 1000 OTUs using a 97% sequence identity criterion and then used the program MEGAN to place the sequences at the least-inclusive level possible in the NCBI taxonomy (Huson et al., 2007). MEGAN placed about 76 000 sequences into 111 taxa identified at the species level, while the remaining 90 000 sequences were placed into 65 more inclusive groups (i.e. genera, families, etc.; Bueé et al., Suppl. Table S2). If one assumes an approximate correspondence between species assigned by MEGAN and OTUs, based on a 97% similarity cut-off, then c. 890 of the OTUs found by Bueé et al. could not be identified to the species level. Collectively, these two ecological studies

Table 1 Rates of species description and sequence deposition Year

Ascomycota (%)

Basidiomycota (%)

Glomeromycota (%)

All groups (%)

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 Total

746, 142 (19) 841, 198 (24) 815, 121 (15) 913, 162 (18) 916, 279 (30) 687, 220 (32) 779, 237 (30) 947, 225 (24) 709, 230 (32) 260, 61 (23) 7613, 1875 (25)

427, 74 (17) 439, 93 (21) 387, 74 (19) 459, 77 (17) 545, 104 (19) 283, 67 (24) 356, 58 (16) 426, 95 (22) 296, 41 (14) 89, 18 (20) 3707, 701 (19)

4, 2 (50) 2, 0 (0) 9, 0 (0) 3, 2 (67) 8, 4 (50) 2, 1 (50) 4, 2 (50) 2, 2 (100) 4, 1 (25) 6, 2 (33) 44, 16 (36)

1177, 218 (19) 1282, 291 (23) 1211, 195 (16) 1375, 241 (18) 1469, 387 (26) 972, 288 (27) 1139, 297 (26) 1375, 322 (23) 1009, 272 (27) 355, 81 (23) 11 364, 2592 (23)

The first number in columns 2–5 indicates the number of new species names recorded in the Index of Fungi during one year (excluding infraspecific taxa, duplicate names and combinations); the second number is the number of names recorded in each year that are now represented by sequences of any locus in GenBank, as of 08 ⁄ 26 ⁄ 2009.



New Phytologist detected at least 1130 potentially novel taxa, which exceeds the total number of species of Ascomycota, Basidiomycota and Glomeromycota described by the entire taxonomic community in 2008 (Table 1). ¨ pik et al. compared their Glomeromycota 18S O sequences with sequences in a reference database, containing 243 predefined VT, called MaarjAM (http://moritz. ¨ pik et al. concluded that all 48 of botany.ut.ee/maarjam/). O the VT that they detected were already represented in MaarjAM (potentially novel VT were observed, but these were interpreted as sequencing artifacts). Nevertheless, the composition of MaarjAM clearly indicates that most new taxa of Glomeromycota are being discovered as environmental sequences. One hundred and eighty-four (76%) of the VT in MaarjAM are composed of sequences known only from molecular environmental surveys, which is > 4 times the total number of new species of Glomeromycota reported in the Index of Fungi over the last 10 yr combined (Table 1). Of course, some of the unidentified sequences may simply represent described species that have not yet been subjected to molecular analysis, but it is unlikely that many of the unidentified OTUs are in this category. As of this writing, the GenBank taxonomy browser reports that 19 848 fungal species are represented in the database. This is almost 20% of the c. 100 000 species of fungi that have been described (Kirk et al., 2008), assuming no redundancy or error, but it is only 0.6–1.3% of the 1.5–3.5 million fungal species that have been estimated to exist (Hawksworth, 2001; O’Brien et al., 2005). Therefore, most of the unidentified molecular OTUs probably represent undescribed taxa. Growing the database for molecular identification should be a priority for fungal taxonomists (Ko˜ljalg et al., 2005). We were interested in knowing what proportion of new species descriptions are coupled with deposition of reference sequences, so we created a Perl script to query the GenBank taxonomy for new species names reported in the Index of Fungi. Overall, 23% of the species recorded from 2000 to 2009 are represented by sequences in GenBank (Table 1). Twenty-five per cent of the names from 2005 to 2009 have sequences compared with 20% from 2000 to 2004. This suggests a modest increase in the rate of sequencing associated with species description over the last 10 yr. On the other hand, there is a growing backlog of relatively recent type material that has not been sequenced, now comprising 8772 species described since 2000. We conclude that molecular ecological studies, especially those using pyrosequencing, are now – or will soon be – detecting significantly more undescribed species of fungi than traditional taxonomic studies. Furthermore, molecular species discovery has the potential to accelerate dramatically, while taxonomy seems to have reached a plateau (Table 1). The disconnect between species description and deposition of sequences is particularly troubling. Even as the total number of named sequences in GenBank increases,


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the gap between the number of described species and reference sequences is widening. To narrow the gap, it will be necessary to intensify efforts to obtain sequences from reference collections (herbaria) and culture collections (Brock et al., 2008) and to urge authors of new names to deposit reference sequences. Journals and funding agencies could help in this regard, by insisting that new species descriptions be accompanied by sequence data whenever possible. Until now, fungal molecular ecologists have operated largely as consumers of resources generated by taxonomists, specifically databases of named sequences, classifications and voucher materials. However, the taxonomic community is clearly challenged to provide adequate resources for molecular identification, and appears to be falling behind ecologists in the discovery of new taxa. Given this situation, it may be appropriate to consider inverting the traditional relationship between taxonomy and ecology, and to ask whether taxonomists, in their quest to document the global diversity of fungi, should not become consumers of the products of ecological studies. In short, it may be time to take a serious look at formal species description based on environmental sequences. To an extent, this work has already begun; molecular ecologists routinely identify OTUs using sequences, but these entities are not being formally classified as species and therefore they do not enter Index Fungorum or other downstream taxonomic databases, such as MycoBank, GBIF, Species2000 and the Encyclopedia of Life. This is unfortunate because the concept of species, controversial though it may be, is deeply ingrained in the ways that humans perceive biodiversity, and species-based classifications impact such disparate fields as pathology (diagnosis), conservation biology (biodiversity hot spots) and comparative biology (key innovations). Tremendous discoveries are being made through molecular ecology, but the failure to classify molecular OTUs as species limits our ability to bring these discoveries to bear on disciplines outside fungal ecology. Adoption of sequence-based species description would represent a major shift for fungal taxonomy. For some, the loss of morphological descriptions could be disconcerting. Techniques such as fluorescent in situ hybridization (FISH) could be used to visualize taxa in the environment, and phylogeny-based character optimizations could be used to predict diverse properties of unseen organisms, but many taxa might never be directly observed. Another potential problem with sequence-based species description is that the duality of sequence-based taxonomy and specimen-based taxonomy could create synonyms, but this is nothing new for mycologists, who are accustomed to dealing with parallel naming of anamorphs and teleomorphs. We are not advocating adoption of a uniform global standard for species delimitation based on a particular gene or sequence similarity score. Indeed, the requirements for molecular species description will probably vary from group


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to group (Seifert et al., 2007) and should be based on the taxonomic judgement of experts. All we suggest is that the taxonomic community, together with ecologists and bioinformaticians, engage in a conversation about the possibility for sequence-based taxon description. If it is determined that this is desirable, then it will be necessary to propose language to modernize the International Code of Botanical Nomenclature (McNeill et al., 2006), which sets the rules by which fungi are named. David S. Hibbett1*, Anders Ohman1 and Paul M. Kirk2 1

Biology Department, Clark University, Worcester, MA 01610, USA; 2 CABI UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK (*Author for correspondence: tel 1-508-793-7332; email [email protected])

References Brock PM, Do¨ring H, Bidartondo MI. 2008. How to know unknown fungi: the role of a herbarium. New Phytologist 181: 719–724. Bueé M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F. 2009. 454 pyrosequencing analyses of forest soils reveal an unexpected high fungal diversity. New Phytologist 184: 449–456. Hawksworth DL. 1991. The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycological Research 95: 641–655. Hawksworth DL. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research 105: 1422–1432. Huson DH, Auch AF, Qi J, Schuster SC. 2007. MEGAN analysis of metagenomic data. Genome Research 17: 377–386. Jumpponen A, Jones KL. 2009. Massively parallel 454-sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytologist 184: 438–448. Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008. Dictionary of the Fungi, 10th ed. Wallingford, UK: CABI. Ko˜ljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E et al. 2005. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytologist 166: 1063–1068. McNeill J, Barrie FR, Burdet HM, Demoulin V, Hawksworth DL, Marhold K, Nicolson DH, Prado J, Silva PC, Skog JE et al. 2006. International Code of Botanical Nomenclature (Vienna Code) adopted by the Seventeenth International Botanical Congress Vienna, Austria, July 2005. Ruggell, Liechtenstein: Gantner Verlag. Nilsson RH, Ryberg M, Kristianssin E, Abarenkov K, Larsson KH. 2006. Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1: e59. O’Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R. 2005. Fungal community analysis by large-scale sequencing of environmental samples. Applied and Environmental Microbiology 71: 5544–5550. ¨ pik M, Metsis M, Daniell TJ, Zobel M, Moora M. 2009. Large-scale O parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytologist 184: 424–437. Seifert KA. 2008. Integrating DNA barcoding into the mycological sciences. Persoonia 21: 162–166. Seifert KA, Samson RA, deWaard JR, Houbraken J, Le´vesque CA, Moncalvo JM, Louis-Seize G, Hebert PDN. 2007. Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. Proceedings of the National Academy of Sciences, USA 104: 3901–3906.


Key words: biological nomenclature, endophytes, mycorrhizas, systematic, taxonomy.

Three birds with one stone: moas, heteroblasty and the New Zealand flora An intriguing article in this issue of New Phytologist (pp. 495–501 by Fadzly and colleagues) is relevant to at least three interesting issues in plant evolutionary biology. Although understandably somewhat short on data, it raises a new hypothesis on the co-evolution of plants and their now-extinct moa herbivores in New Zealand. As such it adds to the small body of research on assessing plant traits in a palaeoecological context; it is also an example of the use of accessory pigments to alter leaf appearance, thereby reducing herbivory; and it adds fuel to the controversy of the function of heteroblasty in New Zealand plants.

‘Perhaps the greatest challenge in using such evidence to test hypotheses of herbivory is that a successful defense will exclude the plant from the diet, and accompanying evidence that the species in question was present in the palaeoflora consumed by the moa may be lacking.’

First, some brief background on moas and the New Zealand flora. Moas evolved on the North and South Islands from ratite ancestors, most closely related to Australian emus and cassowaries (Worthy & Holdaway, 2002). Ten species in six genera are recognized from the Pleistocene; some species were restricted to higher-altitude habitats; and most species were restricted to the South Island. The giant moas, of the genus Dinormis, which stretched to heights of >3 m, lived in forest on both islands. They fed on the foliage of shrubs and trees within their reach and were capable of ingesting fairly tough tissue by grinding it in very large gizzards. The last of the moas became extinct in the 15th century, presumably primarily as a result of hunting pressure by the Maori. The New Zealand flora is distinctive for its diversity and endemism, for the high incidence of divarication in shrubs and juvenile trees (10% of all native woody species; Greenwood & Atkinson, 1977) and for the high frequency of


New Phytologist heteroblasty (some 200 tree species; Cockayne, 1912). Many species produce leaves of remarkably different morphology and appearance at different life history stages. Lancewood (Pseudopanax crassifolius), examined by Fadzly et al., is one of many such heteroblastic species in the New Zealand flora. Divarication and heteroblasty occur in the floras of islands in general (Carlquist, 1965), although their incidence is greatest in New Zealand. The functions of divarication and heteroblasty in New Zealand plants, and the selection pressures that have led to their evolution, have long been controversial matters, going back to the 19th century (Hill, 1913). Some have argued for physiological functions, as reductions in stress from wind or radiation (the literature is well-reviewed in the article). More recently, divarication has been viewed as an adaptation to reduce herbivory by moas (Greenwood & Atkinson, 1977). Fadzly and colleagues extend this argument to the appearance of leaves in lancewood. Seedling leaves are narrow and mottled with dull brown splotches (as a result of the production of anthocyanins along with the chlorophylls), and look similar to leaf litter to our perception. Juvenile leaves are linear, with sharply toothed margins, and each is highlighted by a light-coloured patch. Adult leaves produce oblong leaves of normal appearance. Fadzly et al. argue that the seedling leaves are camouflaged, thereby avoiding herbivory by moas, and that the juvenile leaves are aposematic, with teeth ‘advertised’ by the coloured patches, and also would have been avoided by moas. The normal adult leaves are produced above heights that could be reached by the giant moas. This is a novel hypothesis, explaining the evolution of heteroblasty in lancewood, and is perhaps relevant to other species. The authors provide two lines of evidence to support it. The first is that a closely related lancewood, on a nearby island group that did not have moas, produces leaves with little heteroblasty and a normal green appearance at all stages. A second line of evidence is based on the results of a detailed optical analysis of the lancewood leaves, showing clear differences in appearance that would have been perceived by moas, if we can accept that their visual physiology was similar to that of the related ostrich (a reasonable assumption). These birds would easily have detected the colour ⁄ contrast differences in the leaves of juveniles (and avoided them) and seedlings (not recognized them). They also show that the optical properties of leaves of the Chatham Islands plants are identical to those of normal green leaves of plants in the New Zealand flora. Ideas of colour changes leading to camouflage or warning have generally been limited to animals. However, leaf mottling was recognized by Stone (1979) as a mechanism for camouflage, and this idea was reviewed extensively by Givnish (1990). Mottling is a form of variegation in leaves, and silvery variegation reduces herbivory (Soltau et al., 2009). As for warning coloration, Lev-Yadun (2001) was the first to


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advocate its role in advertising thorns, part of a larger argument for aposematism in plants, and Fadzly and colleagues applied these concepts to the moa ‘problem’. Colour variations in seedling and juvenile leaves are partly a result of the production of anthocyanins in sectors of the leaf. Although the majority of research on anthocyanin function in leaves has investigated senescence (Archetti et al., 2009), there is growing evidence for a multitude of antiherbivory functions of anthocyanins in leaves, at all developmental stages (Lev-Yadun & Gould, 2008). The moa– lancewood interaction is a contribution to this new, but rapidly expanding, research area. However, anthocyanins have known photoprotective and antioxidative activities, and a co-evolutionary role in defense does not exclude the possibility of a physiological role (Lev-Yadun & Gould, 2008). Lastly, the hypothesis of camouflage ⁄ aposematism and moa herbivory is another example of the need to look at the palaeoecological conditions under which traits were selected, because extinction of a major guild of interactors, such as herbivores, may obscure our understanding of their selective advantage. The now classical example of the Pleistocene extinction of large herbivores (or ‘gomphotheres’) was argued by Janzen & Martin (1982), as the loss of the major selection agents in the evolution of large fruited and seeded trees in Central and North America. In a case similar to moas and New Zealand plants, Givnish et al. (1994) argued that thorn-like prickles in Cyanea evolved several times in the Hawaiian Archipelago in response to flightless avian browsers. Although they built a robust phylogeny showing the multiple appearances of spines, particularly on the older islands, they had no direct evidence of defense against herbivory. The fundamental problem of such palaeoecological hypotheses is how to critically test them. Janzen & Martin (1982) used evidence from a thorough examination of the literature, and they employed a modern substitute of the extinct gomphotheres: the horse. Fadzley et al. used the evidence of actual leaf optical properties along with the comparison of a sibling species from a non-moa island group, but presented no direct evidence of defense against herbivory. There is actually quite a substantial amount of information available on moas from the recent fossil record, including sexual dimorphism, nesting behavior, vocalizations, feeding and diet. In addition, there is an impressive amount of data available on plants and plant organs consumed by moas, based on gizzard function and content and, particularly, coprolites. Wood et al. (2008) showed (based on coprolite analysis) plant consumption by at least two moa species at a site on the South Island. Another list of plants in the moa diet was compiled from analysis of gizzard contents from another South Island site (Horrocks et al., 2004). Coprolites and gizzard contents allow identification of both the moa species and what they ate. DNA extracted from tissues provides identity of the moa species involved (Baker et al., 2005). Perhaps the greatest challenge


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in using such evidence to test hypotheses of herbivory is that a successful defense will exclude the plant from the diet, and accompanying evidence that the species in question was present in the palaeoflora consumed by the moa may be lacking. Thus, data from a single species of moa from a locality with evidence of plant communities present at that time will be necessary to test more critically this antiherbivory hypothesis. The large exotic invasive herbivores now in New Zealand are not a substitute for the moa and do not contribute to our understanding of these ecological interactions. Despite the limitations of the evidence presented by Fadzly et al., and the difficulty of obtaining more direct evidence on the browsing habits of emus, the hypothesis raised by them, explaining the evolution of heteroblasty in the New Zealand flora, will stimulate more research on the subject and will illuminate other work in palaeoecology, the roles of leaf display in evolution and the functions of anthocyanins in leaves. In that way the authors have clearly struck three birds with a single stone. David Lee1* and Kevin Gould2 1

Department of Biological Sciences, Florida International University, Miami, FL 33199, USA; 2School of Biological Sciences, Victoria University of Wellington, Wellington 6140, New Zealand (*Author for correspondence: tel +1 305 348 3111; email [email protected])

References Archetti M, Do¨ring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PJ et al. 2009. Unraveling the evolution of autumn colours: an interdisciplinary approach. Trends in Ecology and Evolution 24: 166–173. Baker AJ, Huynen LJ, Haddrath O, Millar CD, Lambert DM. 2005. Reconstructing the tempo and mode of evolution in an extinct clade of birds with ancient DNA: the giant moas of New Zealand. Proceedings of the National Academy of Sciences, USA 102: 8257–8262.

Carlquist S. 1965. Island life. New York, NY, USA: Natural History Press. Cockayne L. 1912. Observations concerning evolution, derived from ecological studies in New Zealand. Transactions and Proceedings of the New Zealand Institute 44: 1–50. Fadzly N, Jack C, Schaefer HM, Burns KC. 2009. Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytologist 184: 495–501. Givnish TJ. 1990. Leaf mottling: relation to growth form and leaf phenology and possible role as camouflage. Functional Ecology 4: 463–474. Givnish TJ, Sytsma KJ, Smith JF, Hahn WJ. 1994. Thorn-like prickles and heterophylla in Cyanea: adaptations to extinct avian browsers on Hawaii? Proceedings of the National Academy of Sciences, USA 91: 2810–2814. Greenwood RM, Atkinson IAE. 1977. Evolution of divaricating plants in New Zealand in relation to moa browsing. Proceedings of the New Zealand Ecological Society 24: 21–33. Hill H. 1913. The moa – legendary, historical and geographical: why and when the moa disappeared. Transactions and Proceedings of the Royal Society of New Zealand 46: 330–351. Horrocks M, D’Costa D, Wallace R, Gardner R, Kondo R. 2004. Plant remains in coprolites: diet of a subalpine moa (Dinornithiformes) from southern New Zealand. Emu 104: 149–156. Janzen DH, Martin PS. 1982. Neotropical anachronisms: the fruits the gomphotheres ate. Science 215: 19–27. Lev-Yadun S. 2001. Aposematic (warning) coloration associated with thorns in higher plants. Journal of Theoretical Biology 210: 285–388. Lev-Yadun S, Gould KS. 2008. Role of anthocyanins in plant defense. In: Gould KS, Davies KM, Winefield C, eds. Life’s colorful solutions: the biosynthesis, functions and applications of anthocyanins. Berlin, Germany: Springer Verlag, 21–48. Soltau U, Do¨tterl S, Liede-Schumann S. 2009. Leaf variegation in Caladium steudneriifolium (Araceae): a case of mimicry? Evolutionary Ecology 23: 503–512. Stone BC. 1979. Protective coloration of young leaves in certain Malaysian palms. Biotropica 11: 126. Wood JR, Rawlence NJ, Rogers GM, Austin JJ, Worthy TH, Cooper A. 2008. Coprolite deposits reveal the diet and ecology of the extinct New Zealand megaherbivore moa (Aves, Dinornithiformes). Quarternary Science Review 27: 2593–2602. Worthy TH, Holdaway RN. 2002. The lost world of the moa. Bloomington, IN, USA: Indiana University Press. Key words: aposematic coloration, camouflage, coevolution, divarication, heteroblasty, moas.

Meetings Parasitic plants tap into the main stream 10th World Congress on Parasitic Plants, Kusadasi, Turkey, June 2009 Parasitic plants can exhibit such unusual biology that they sometimes have not even been recognized as plants. Such


was the report of Jay Bolin (Old Dominion University, Norfolk, VA, USA), at the recent gathering of the International Parasitic Plant Society in Kusadasi, in his recounting of the first descriptions of holoparasitic species in the Hydnoraceae family. Although there were plenty of presentations highlighting the specialized anatomy and communication exhibited by parasitic plants, this meeting was marked by an increasing sense of the common themes shared between parasitic plants and other plant species. In one example, Marc-Andre´ Selosse (CNRS, Montpellier,


New Phytologist France) described striking parallels between parasitic plants and mycoheterotrophic and mixotrophic species that dine on fungi (Selosse & Roy, 2009). Also, as described later, the signaling molecule detected by some parasitic plants to locate their hosts has turned out to be a new plant hormone. This report will focus on research of broader interest to plant scientists; so many excellent presentations cannot be included. Nevertheless, it is noteworthy that the parasitic plant congresses are characterized by all manner of diversity. Over 100 participants represented 37 different countries from around the globe and the presentations described work on dozens of parasitic species. Every aspect of parasitic plant biology was under consideration, including ecology, evolution, population biology, biochemistry, physiology, and interactions with hosts and pathogens. The conservation of rare parasitic species was discussed, but a larger number of presentations focused on control of weedy species of the genera Striga and Orobanche, which decimate crops across Africa, the Mediterranean and the Middle East regions. Taxonomy was also on the agenda, and Danny Joel (Agricultural Research Organization, New Ya’ar, Israel) reviewed the evidence for renaming several Orobanche species to Phelipanche. Although there was no consensus for immediately adopting the name change, the use of both names in the literature is already reaching the point that researchers would be wise to use both names in keyword searches.

‘…an intriguing question is whether Striga and Orobanche produce their own strigolactones: if not, how do they control branching; if yes, how can they still respond in such a sensitive manner to strigolactones of hosts’ root exudates?’

The life-or-death decision to germinate An important step in the life cycle of all obligate parasitic plants is their germination in the right place and at the right time, enabling them to establish the connection they require to survive. The root parasitic Orobanche and Striga spp. use the so-called germination stimulants – secreted by the roots of their hosts – to achieve this. The best studied class of these stimulants is the strigolactones. Ground-breaking work of Koichi Yoneyama et al. (Utsunomiya University, Utsunomiya, Japan) on the analysis of strigolactones in the root exudate of many plant species has opened up


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possibilities to study their importance and regulation in greater detail. Kaori Yoneyama (Teikyo University, Utsunomiya, Japan) showed that there is substantial genetic variation in the strigolactone profile exuded by maize varieties. Moreover, she was able to correlate the composition of the exudate to the resistance ⁄ susceptibility towards Striga. Also in rice, there is a substantial genetic variation in strigolactone production, with concentrations in the exudate differing by 100-fold or more between varieties, as presented by Muhammad Jamil (Wageningen University, Wageningen, the Netherlands). Both reports have important implications for resistance breeding as genetic variation allows for selection to improve Striga resistance. This raises the important issue of host specificity, which may be influenced from two sides: the sensitivity of (species or ecotypes or races of) the parasite for different germination stimulants; and ⁄ or the production of different mixtures of germination stimulants by different hosts (species and varieties). Anna Hoeniges (‘Vasile Goldis’ Western University, Arad, Romania) compared the strigolactone production of a number of hosts of weedy and nonweedy broomrapes, postulating how host specificity (or the lack thereof) has arisen in several Orobanche spp. The efforts to identify the strigolactone receptor in Orobanche and Striga that were briefly mentioned by Harro Bouwmeester (Wageningen University, Wageningen, the Netherlands) will hopefully help to shed more light on the mechanism of host specificity. With regard to parasitic weed control, interesting new results were presented in relation to the germination stimulants. Tadao Asami et al. (University of Tokyo, Japan) presented a poster detailing the synthesis of strigolactone biosynthesis inhibitors with the objective of blocking germination stimulant production by crops to make these crops less susceptible to Striga or Orobanche. Of course, it is also of great interest for scientific purposes to have such selective inhibitors. In a similar vein, the long-known fact that increased fertilization leads to Striga suppression was explained in presentations by Muhammad Jamil (Wageningen University, Wageningen, the Netherlands) and Kaori Yoneyama (Teikyo University, Utsunomiya, Japan), reporting a strong negative correlation between the amount of nitrogen and ⁄ or phosphate application and the concentration of strigolactones in the exudate of rice. These concentration differences correlated well with Striga performance: the lower the nutrient availability, the higher the germination-inducing capacity of the exudate and the more Striga attachment ⁄ emergence in a pot experiment.

Do parasitic plants have a hormone problem? One of the most exciting discoveries of the last year was the fact that strigolactones were shown to be a new class of plant


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hormones (Gomez-Roldan et al., 2008; Umehara et al., 2008). This was the second surprise about strigolactones in recent years, with Akiyama et al. discovering, in 2005, that the strigolactones are – in addition to germination stimulants for root parasitic plants – also host-finding factors for the symbiotic arbuscular mycorrhizal fungi (Akiyama et al., 2005). Several of the co-authors contributing to the discovery of the hormonal function of the strigolactones (Koichi Yoneyama, Utsonomiya University, Utsunomiya, Japan; Satoko Yoshida, RIKEN, Yokehama, Japan; and Harro Bouwmeester, University of Wageningen, Wageningen, the Netherlands) attended the meeting. Harro presented a review of this exciting development, explaining how it was enabled by the discovery that the strigolactones are biosynthetically derived from the carotenoids through the action of a carotenoid-cleaving enzyme (Matusova et al., 2005). The search for mutants in such enzymes quickly resulted in the discovery that some ramosus (rms) mutants in pea and dwarf (d) mutants in rice, which are mutated in a CCD7 or a CCD8 enzyme, do not produce detectable amounts of strigolactones. Also in Arabidopsis, bioassays with Orobanche or Striga seeds suggest that the more axillary branching (max) mutants, max3 and max4 (mutated in a CCD7 or a CCD8 enzyme, respectively) do not produce strigolactones. However, as the names of these mutants suggest, they exhibit a morphological phenotype: abnormally high branching (pea, Arabidopsis) or high tillering (rice) (Fig. 1). The mutants could be restored to the wild-type phenotype by the application of the synthetic strigolactone, GR24, showing that strigolactones (or a close derivative thereof) represent the so-called branching inhibiting signal (BIS) that was postulated to exist many years before (Booker et al., 2004). Exciting opportunities for parasitic plant research that arise from this discovery are the fact that there are a number of other rms, d (or high-tillering dwarf (htd )) and max mutants available. The Arabidopsis max1 mutant, for example, has a mutation in a cytochrome P450, yet the branched phenotype of this mutant and the genetic evidence suggests that the mutant is not making the BIS. With regard to perception of the strigolactones, the d3, max2 and rms4 mutants are of particular interest. These mutants do make BIS but do not perceive it, resulting in the branched ⁄ tillered phenotype, which cannot be restored to the wild-type phenotype. These mutants are deficient in an F-Box receptor-like protein that is similar to transport inhibitor response 1 (TIR1), a protein involved in auxin perception ⁄ signal transduction. The fact that this F-Box protein is involved in the perception of the BIS in plants makes it a good candidate for the perception of strigolactones in Orobanche and Striga seeds. Harro Bouwmeester (University of Wageningen, Wageningen, the Netherlands) showed preliminary results of binding studies with biotinylated-


GR24 to MAX2, which were carried out in collaboration with Binne Zwanenburg (University of Nijmegen, Nijmegen, the Netherlands) and Ottoline Leyser (University of York, UK). Considering that the strigolactones seem ubiquitous in the plant kingdom, an intriguing question is whether Striga and Orobanche produce their own strigolactones: if not, how do they control branching; if yes, how can they still respond in such a sensitive manner to strigolactones of hosts’ root exudates? Undoubtedly, this will be an area of great interest for the parasitic plant community in the next couple of years.

Parasitic plants join the genomics club While genomic resources have been amassed for model plants and major crops over the past decade, few gene sequences have been available for parasites. This situation is now changing as at least two projects are poised to release substantial amounts of parasite sequence data. Jim Westwood (Virginia Tech, Blacksburg, VA, USA) and Claude dePamphilis (Penn State University, State College, PA, USA) described a project funded by the US National Science Foundation that is in the process of sequencing

Fig. 1 Wild-type (left) and ramosus mutant rms1 (right) of pea (seeds courtesy of Catherine Rameau, INRA, Versailles, France) showing the branched phenotype of the mutant and the lower infection with Orobanche crenata. Photo courtesy of Radoslava Matusova, Wageningen University, the Netherlands.


New Phytologist expressed sequence tags (ESTs) from several key stages of the life cycles of three species: Triphysaria versicolor, Striga hermonthica and Orobanche (syn. Phelipanche) aegyptiaca. These members of the family Orobanchaceae span the continuum from facultative parasite to achlorophyllous holoparasite and provide a framework for understanding the evolution of parasitism. The first sets of genes produced by this project comprise approximately 31 000 unigenes from shoots of S. hermonthica and 24 000 unigenes from preemerged tissues of O. aegyptiaca. In a separate project, Satoko Yoshida (RIKEN, Yokehama, Japan) reported the pending public release of 17 000 unigenes derived from multiple stages of S. hermonthica. Although a substantial data set of haustorial development-related genes for T. versicolor has been available for a few years (Torres et al., 2005), this new influx marks a milestone in parasitic plant research. The immediate impact of new parasite sequences will probably be felt by researchers working on parasite biochemistry, physiology and host–parasite communication. This includes the work on seed germination described earlier, as well as studies, such as that being conducted by Thomas Pe´ron (University of Nantes, Nantes, France) to understand how the parasite uses vacuolar invertase and sucrose synthase to maintain strong sink strength relative to its host. Studies of host resistance have already harnessed host genomic resources to describe global gene expression in response to parasitism (Karolina Lis, University of Virginia, Charlottesville, VA, USA) and identified new resistance mechanisms (Kan Huang, University of Virginia, Charlottesville, VA, USA; Gre´gory Montiel, University of Nantes, Nantes, France), but having parasite sequences will enable even more sophisticated understanding of the host–parasite interaction. The trickle of parasite sequence data is now a stream and will probably soon become a flood as additional sequences become available from Striga, Orobanche and other parasitic species. This will provide abundant opportunities for


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comparing gene structure and function across plants exhibiting a great diversity of morphologies. This should be of interest to a wide variety of plant scientists who would like to know how their favorite gene has been modified in a parasitic plant lineage. James H. Westwood1* and Harro Bouwmeester2 1

Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA, USA; 2 Laboratory of Plant Physiology, Wageningen University, Wageningen, The Netherlands (*Author for correspondence: tel +1 540 231 7519; email [email protected])

References Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824– 827. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O. 2004. Max3 ⁄ ccd7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Current biology 14: 1232– 1238. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC et al. 2008. Strigolactone inhibition of shoot branching. Nature 455: 189–194. Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ. 2005. The strigolactone germination stimulants of the plant-parasitic striga and orobanche spp are derived from the carotenoid pathway. Plant Physiology 139: 920–934. Selosse M-A, Roy M. 2009. Green plants that feed on fungi: facts and questions about mixotrophy. Trends in Plant Science 14: 64–70. Torres M, Tomilov A, Tomilova N, Reagan R, Yoder J. 2005. Pscroph, a parasitic plant est database enriched for parasite associated transcripts. BMC Plant Biol 5: 24. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K et al. 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195–200. Key words: Orobanche, parasitic plant, Phelipanche, Striga, strigolactones.


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