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Arbuscular mycorrhizal fungi are soilborne microorganisms that form a mutualistic symbiotic association with most land plants. As obligate biotrophs these fungi are unable to complete their life cycle in the absence of the host plant. This symbiosis is increasingly being recognised as an integral and important part of natural ecosystems throughout the word. Because of the incalcitrance of arbuscular mycorrhizal fungi to grow in pure culture and consequently the difficulties in obtaining sufficiently large quantities of fungal material, the analysis of gene products has remained an extremely challenging but unexplored area. Until recently, little was known about the genomics of these fungi and it is only with the advent of powerful molecular techniques that it has been possible to venture research into their genetic makeup. This review surveys the most recent molecular genetics of arbuscular mycorrhizal fungi and their contributions to basic knowledge of the biology of this group of organisms.
Nuria Ferrol, Bert Bago, Philipp Franken, Armelle Gollotte, Manuel González-Guerrero, Lucy Alexandra Harrier, Luisa Lanfranco, Diederik van Tuinen, Vivienne Gianinazzi-Pearson Applied Mycology and Biotechnology Volume 4, 2004, Pages 379–403 http://dx.doi.org/10.1016/S1874-5334(04)80019-4
Arbuscular mycorrhizal fungi (AMF), which form an ancient and widespread mutualistic symbiosis with plants, are a crucial but still enigmatic component of the plant microbiome. Nowadays, their obligate biotrophy is no longer an obstacle to deciphering the role played by AMF in this fascinating symbiosis. The first genome-wide transcriptomic analysis of an AMF showed a metabolic complexity with no sign of massive gene loss, and the presence of genes for meiotic recombination suggests that AMF are not simple clonal organisms, as originally thought. New findings on suppression of host defenses and nutrient exchange processes have shed light on the mechanisms that contribute to such an intimate and long-lasting integration between living plant and fungal cells. Luisa Lanfranco, J Peter W Young Current Opinion in Plant Biology Volume 15, Issue 4, August 2012, Pages 454–461 http://dx.doi.org/10.1016/j.pbi.2012.04.003
L. bicolor was the first ectomycorrhizal fungus to have its genome sequenced. The second version of the assembly is now available at the JGI portal. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008 Mar 6;452(7183):88-92.
Arbuscular mycorrhizal fungi (AMF) represent an ecologically relevant and evolutionarily intriguing group of land plant symbionts, which produce multinucleated spores and hyphae that are currently thought to have propagated clonally for over 500 million years. This long-term absence of sex in AMF is a puzzling evolutionary feature that has sparked scientific interest for some time, but a provoking explanation for their successful evolutionary history in the absence of an obvious sexual cycle is that these organisms may have cryptic sex, or a parasexual life cycle, allowing them to recombine alleles and compensate for deleterious mutations. Interestingly, the recent acquisition of large sequence data from many AMF species can finally allow this hypothesis to be tested more extensively. In this perspective, we highlight emerging evidence based on sequence data for the potential of AMF to have sexual reproduction, and propose a number of routes that could be taken to further explore the presence (or absence thereof) of sex in this poorly studied, yet highly relevant, fungal group.
Rohan Riley, Nicolas Corradi Fungal Ecology Volume 6, Issue 1, February 2013, Pages 44–49
http://dx.doi.org/10.1016/j.funeco.2012.01.010
Within the framework of the Mycorrhizal Genomics Initiative, the JGI is sequencing aphylogenetically and ecologically diverse suite of mycorrhizal fungi (Basidiomycota and Ascomycota), which include the major clades of symbiotic species associating with trees and woody shrubs. Analyses of these genomes will provide insight into the diversity of mechanisms for the mycorrhizal symbiosis, including endo- and ectomycorrhiza. This scoop points to the official project page hosted on Mycorweb.
The Fungal Genetics Policy Committee invites you to attend the 27th Fungal Genetics Conference, sponsored by the Genetics Society of America. The meeting is held every two years at the Asilomar Conference Grounds, Pacific Grove, California (near Monterey, California). The conference will open on Tuesday evening, March 12 with an Opening Mixer from 7:30 pm – 10:30 pm and end on Sunday, March 17. Regine Kahmann will present the Perkins/Metzenberg Lecture on Saturday, March 16 at 6:30 pm, followed by the banquet and closing party. Chairs of the Scientific Program:
Katherine Borkovich, University of California, Riverside
Francis Martin, INRA, Nancy, France
The Molecular Mycorrhiza Meeting, one of the satellite meeting of the 10th European Nitrogen Fixation Congress (ENFC), will be held in Munich, Germany, the 6-7th September 2012. MMM will be the first event of a series initiated to satisfy the growing demand for a specialized scientific meeting covering the molecular genetic aspects of mycorrhiza. http://www.enfc2012.de/fileadmin/ENFC2011/PDF/Flyer_web.pdf
A genome-wide inventory of proteins involved in cell wall synthesis and remodeling has been obtained by taking advantage of the recently released genome sequence of the ectomycorrhizal Tuber melanosporum black truffle. Genes that encode cell wall biosynthetic enzymes, enzymes involved in cell wall polysaccharide synthesis or modification, GPI-anchored proteins and other cell wall proteins were identified in the black truffle genome. As a second step, array data were validated and the symbiotic stage was chosen as the main focus. Quantitative RT-PCR experiments were performed on 29 selected genes to verify their expression during ectomycorrhizal formation. The results confirmed the array data, and this suggests that cell wall-related genes are required for morphogenetic transition from mycelium growth to the ectomycorrhizal branched hyphae. Labeling experiments were also performed on T. melanosporum mycelium and ectomycorrhizae to localize cell wall components. Raffaella Balestrini, Fabiano Sillo, Annegret Kohler, Georg Schneider, Antonella Faccio, Emilie Tisserant, Francis Martin and Paola Bonfante CURRENT GENETICS
Volume 58, Number 3 (2012), 165-177 http://dx.doi.org/10.1007/s00294-012-0374-6
Biotrophic fungi interacting with plants establish long-term relationships with their hosts to fulfill their life cycles. In contrast to necrotrophs, they need to contend with the defense mechanisms of the plant to develop within the host and feed on living cells. It is generally accepted that microbial pathogens produce and deliver a myriad of effector proteins to hijack the cellular program of their hosts. Arbuscular mycorrhizal (AM) fungi are the most widespread biotrophs of plant roots. We investigated whether AM fungi use effector proteins to short-circuit the plant defense program. Here we show that Glomus intraradices secretes a protein, SP7, that interacts with the pathogenesis-related transcription factor ERF19 in the plant nucleus. ERF19 is highly induced in roots by the fungal pathogen Colletotrichum trifolii as well as by several fungal extracts, but only transiently during mycorrhiza colonization. When constitutively expressed in roots, SP7 leads to higher mycorrhization while reducing the levels of C. trifolii-mediated defense responses. Furthermore, expression of SP7 in the rice blast fungus Magnaporthe oryzae attenuates root decay symptoms. Taken together, these results suggest that SP7 is an effector that contributes to develop the biotrophic status of AM fungi in roots by counteracting the plant immune program. Silke Kloppholz, Hannah Kuhn, Natalia Requena Current Biology Volume 21, Issue 14, 26 July 2011, Pages 1204–1209 http://dx.doi.org/10.1016/j.cub.2011.06.044
Hydrophobins are morphogenetic, small secreted hydrophobic fungal proteins produced in response to changing development and environmental conditions. These proteins are important in the interaction between certain fungi and their hosts. In mutualistic ectomycorrhizal fungi several hydrophobins form a subclass of mycorrhizal-induced small secreted proteins that are likely to be critical in the formation of the symbiotic interface with host root cells. In this study, two genomes of the ectomycorrhizal basidiomycete Laccaria bicolor strains S238N-H82 (from North America) and 81306 (from Europe) were surveyed to construct a comprehensive genome-wide inventory of hydrophobins and to explore their characteristics and roles during host colonization. The S238N-H82 L. bicolor hydrophobin gene family is composed of 12 genes while the 81306 strain encodes nine hydrophobins, all corresponding to class I hydrophobins. The three extra hydrophobin genes encoded by the S238N-H82 genome likely arose via gene duplication and are bordered by transposon rich regions. Expression profiles of the hydrophobin genes of L. bicolor varied greatly depending on life stage (e.g. free living mycelium vs. root colonization) and on the host root environment. We conclude from this study that the complex diversity and range of expression profiles of the Laccaria hydrophobin multi-gene family have likely been a selective advantage for this mutualist in colonizing a wide range of host plants. Jonathan M. Plett et al. Fungal Genetics and Biology
Volume 49, Issue 3, March 2012, Pages 199–209 http://dx.doi.org/10.1016/j.fgb.2012.01.002
The ESTuber database (http://www.itb.cnr.it/estuber) includes 3,271 Tuber borchii expressed sequence tags (EST). Barbara Lazzari, Andrea Caprera, Cristian Cosentino, Alessandra Stella, Luciano Milanesiand Angelo Viotti BMC Bioinformatics 2007, 8(Suppl 1):S13 10.1186/1471-2105-8-S1-S13
The ectomycorrhizal basidiomycete Laccaria bicolor has a dual lifestyle with a transitory soil saprotrophic phase and a longer mutualistic interaction with tree roots. Recent evidence suggests that secreted proteins play key roles in host plant colonisation and symbiosis development. However, a limited number of secreted proteins have been characterized, and the full spectrum of effectors involved in the mycobiont invasion and survival remains unknown. We analyzed the extracellular proteins secreted in growth medium by free-living mycelium of L. bicolor as a proxy for its saprotrophic phase. The proteomic analyses (two-dimensional electrophoresis and shotgun proteomics) were substantiated by whole-genome expression transcript profiling on ectomycorrhizal roots. Among the 224 proteins identified were carbohydrate-acting enzymes likely involved in the cell wall remodelling linked to hyphal growth as well as secreted proteases possibly digesting soil organic compounds and/or fending off competitors, pathogens, and predators. Evidence of gene expression was found in ectomycorrhizal roots for 210 of them. These findings provide the first global view of the secretome of a mutualistic symbiont and shed some light on the mechanisms controlling cell wall remodelling during the hyphal growth. They also revealed many novel putative secreted proteins of unknown function, including one mycorrhiza-induced small secreted protein. Delphine Vincent, Annegret Kohler, Stephane Claverol, Emilie Solier, Johann Joets, Julien Gibon, Marc-Henri Lebrun, Christophe Plomion, and Francis Martin Journal of Proteome Research 2012, 11 (1), pp 157–171 http://dx.doi.org/10.1021/pr200895f
The arbuscular mycorrhizal symbiosis is arguably the most ecologically important eukaryotic symbiosis, yet it is poorly understood at the molecular level. To provide novel insights into the molecular basis of symbiosis-associated traits, we report the first genome-wide analysis of the transcriptome from Glomus intraradices DAOM 197198.
We generated a set of 25 906 nonredundant virtual transcripts (NRVTs) transcribed in germinated spores, extraradical mycelium and symbiotic roots using Sanger and 454 sequencing. NRVTs were used to construct an oligoarray for investigating gene expression.
We identified transcripts coding for the meiotic recombination machinery, as well as meiosis-specific proteins, suggesting that the lack of a known sexual cycle in G. intraradices is not a result of major deletions of genes essential for sexual reproduction and meiosis. Induced expression of genes encoding membrane transporters and small secreted proteins in intraradical mycelium, together with the lack of expression of hydrolytic enzymes acting on plant cell wall polysaccharides, are all features of G. intraradices that are shared with ectomycorrhizal symbionts and obligate biotrophic pathogens.
Our results illuminate the genetic basis of symbiosis-related traits of the most ancient lineage of plant biotrophs, advancing future research on these agriculturally and ecologically important symbionts. Tisserant et al. New Phytologist
Volume 193, Issue 3, pages 755–769, February 2012 http://dx.doi.org/10.1111/j.1469-8137.2011.03948.x
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Arbuscular mycorrhizal symbioses occur between fungi and the majority of plant species. They are important for plant nutrition, plant growth, protection from pathogens, plant diversity, nutrient cycling, and ecosystem processes. A key goal in research is to understand the molecular basis of the establishment, regulation, and functioning of the symbiosis. However, lack of knowledge on the genetics of the fungal side of this association has hindered progress. Here, we show how several key, recently discovered processes concerning the genetics of arbuscular mycorrhizal fungi could be essential for ultimately understanding the molecular genetics of this important symbiosis with plants.
Ian R. Sanders and Daniel Croll Annual Review of GeneticsVol. 44: 271-292 (Volume publication date December 2010) DOI: 10.1146/annurev-genet-102108-134239
Tuber melanosporum was the second ectomycorrhizal fungus whose genome has been sequenced. This copy of the genome was obtained from the Tuber Genome Browser at Genoscope. In order to allow comparative analyses with other fungal genomes sequenced by the Joint Genome Institute, a copy of this genome is incorporated into MycoCosm. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury JM, Ballario P, Bolchi A, Brenna A, Brun A, Buée M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, Hilselberger B, Iotti M, Marçais B, Mello A, Miranda M, Pacioni G, Quesneville H, Riccioni C, Ruotolo R, Splivallo R, Stocchi V, Tisserant E, Viscomi AR, Zambonelli A, Zampieri E, Henrissat B, Lebrun MH, Paolocci F, Bonfante P, Ottonello S, Wincker P. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature. 2010 Apr 15;464(7291):1033-8. Epub 2010 Mar 28.
Background The publicly available Laccaria bicolor genome sequence has provided a considerable genomic resource allowing systematic identification of transposable elements (TEs) in this symbiotic ectomycorrhizal fungus. Using a TE-specific annotation pipeline we have characterized and analyzed TEs in the L. bicolor S238N-H82 genome. Methodology/Principal Findings TEs occupy 24% of the 60 Mb L. bicolor genome and represent 25,787 full-length and partial copy elements distributed within 171 families. The most abundant elements were the Copia-like. TEs are not randomly distributed across the genome, but are tightly nested or clustered. The majority of TEs exhibits signs of ancient transposition except some intact copies of terminal inverted repeats (TIRS), long terminal repeats (LTRs) and a large retrotransposon derivative (LARD) element. There were three main periods of TE expansion in L. bicolor: the first from 57 to 10 Mya, the second from 5 to 1 Mya and the most recent from 0.5 Mya ago until now. LTR retrotransposons are closely related to retrotransposons found in another basidiomycete, Coprinopsis cinerea. Conclusions This analysis 1) represents an initial characterization of TEs in the L. bicolor genome, 2) contributes to improve genome annotation and a greater understanding of the role TEs played in genome organization and evolution and 3) provides a valuable resource for future research on the genome evolution within the Laccaria genus. Labbé J, Murat C, Morin E, Tuskan GA, Le Tacon F, et al. (2012) Characterization of Transposable Elements in the Ectomycorrhizal Fungus Laccaria bicolor. PLoS ONE 7(8): e40197. http://dx.doi.org/10.1371/journal.pone.0040197
List of fungi within the JGI Mycorrhizal Genomics Initiative whose genome has been released.
Arbuscular mycorrhizal (AM) fungi are involved in one of the most widespread plant–fungus interactions. A number of studies on the population dynamics of AM fungi have used mitochondrial (mt) DNA sequences, and yet mt AM fungus genomes are poorly known. To date, four mt genomes of three species of AM fungi are available, among which are two from Rhizophagus irregularis.
In order to study intra- and interstrain mt genome variability of R. irregularis, we sequenced and de novo assembled four additional mt genomes of this species. We used 454 pyrosequencing and Illumina technologies to directly sequence mt genomes from total genomic DNA.
The mt genomes are unique within each strain. Interstrain divergences in genome size, as a result of highly polymorphic intergenic and intronic sequences, were observed. The polymorphism is brought about by three types of variability generating element (VGE): homing endonucleases, DNA polymerase domain-containing open reading frames and small inverted repeats. Based on VGE positioning, mt sequences and nuclear markers, two subclades of R. irregularis were characterized.
The discovery of VGEs highlights the great intraspecific plasticity of the R. irregularis mt genome. VGEs allow the design of powerful mt markers for the typing and monitoring of R. irregularis strains in genetic and population studies. Damien Formey, Marion Molès, Alexandra Haouy, Bruno Savelli, Olivier Bouchez, Guillaume Bécard, Christophe Roux Volume 196, Issue 4, pages 1217–1227, December 2012 DOI: 10.1111/j.1469-8137.2012.04283.x
Gigaspora rosea is a member of the arbuscular mycorrhizal fungi (AMF; Glomeromycota) and a distant relative of Glomus species that are beneficial to plant growth. To allow for a better understanding of Glomeromycota, we have sequenced the mitochondrial DNA of G. rosea. A comparison with Glomus mitochondrial genomes reveals that Glomeromycota undergo insertion and loss of mitochondrial plasmid-related sequences and exhibit considerable variation in introns. The gene order between the two species is almost completely reshuffled. Furthermore, Gigaspora has fragmented cox1 and rns genes, and an unorthodox initiator tRNA that is tailored to decoding frequent UUG initiation codons. For the fragmented cox1 gene, we provide evidence that its RNA is joined via group I–mediated trans-splicing, whereas rns RNA remains in pieces. According to our model, the two cox1 precursor RNA pieces are brought together by flanking cox1 exon sequences that form a group I intron structure, potentially in conjunction with the nad5 intron 3 sequence. Finally, we present analyses that address the controversial phylogenetic association of Glomeromycota within fungi. According to our results, Glomeromycota are not a separate group of paraphyletic zygomycetes but branch together with Mortierellales, potentially also Harpellales. Maryam Nadimi, Denis Beaudet, Lise Forget, Mohamed Hijri and B. Franz Lang Mol Biol Evol (2012)
http://dx.doi.org/10.1093/molbev/mss088
•Arbuscular mycorrhizal fungi (AMF) are ubiquitous organisms that benefit ecosystems through the establishment of an association with the roots of most plants: the mycorrhizal symbiosis. Despite their ecological importance, however, these fungi have been poorly studied at the genome level.
•In this study, total DNA from the AMF Gigaspora margarita was subjected to a combination of 454 and Illumina sequencing, and the resulting reads were used to assemble its mitochondrial genome de novo. This genome was annotated and compared with those of other relatives to better comprehend the evolution of the AMF lineage.
•The mitochondrial genome of G. margarita is unique in many ways, exhibiting a large size (97 kbp) and elevated GC content (45%). This genome also harbors molecular events that were previously unknown to occur in fungal mitochondrial genomes, including trans-splicing of group I introns from two different genes coding for the first subunit of the cytochrome oxidase and for the small subunit of the rRNA.
•This study reports the second published genome from an AMF organelle, resulting in relevant DNA sequence information from this poorly studied fungal group, and providing new insights into the frequency, origin and evolution of trans-spliced group I introns found across the mitochondrial genomes of distantly related organisms. Adrian Pelin, Jean-François Pombert, Alessandra Salvioli, Linda Bonen, Paola Bonfante, Nicolas Corradi New Phytologist
Volume 194, Issue 3, pages 836–845, May 2012 http://dx.doi.org/10.1111/j.1469-8137.2012.04072.x
As obligate symbionts of most land plants, arbuscular mycorrhizal fungi (AMF) have a crucial role in ecosystems, but to date, in the absence of genomic data, their adaptive biology remains elusive. In addition, endobacteria are found in their cytoplasm, the role of which is unknown. In order to investigate the function of the Gram-negative Candidatus Glomeribacter gigasporarum, an endobacterium of the AMF Gigaspora margarita, we sequenced its genome, leading to an ~1.72-Mb assembly. Phylogenetic analyses placed Ca. G. gigasporarum in the Burkholderiaceae whereas metabolic network analyses clustered it with insect endobacteria. This positioning of Ca. G. gigasporarum among different bacterial classes reveals that it has undergone convergent evolution to adapt itself to intracellular lifestyle. The genome annotation of this mycorrhizal-fungal endobacterium has revealed an unexpected genetic mosaic where typical determinants of symbiotic, pathogenic and free-living bacteria are integrated in a reduced genome. Ca. G. gigasporarum is an aerobic microbe that depends on its host for carbon, phosphorus and nitrogen supply; it also expresses type II and type III secretion systems and synthesizes vitamin B12, antibiotics- and toxin-resistance molecules, which may contribute to the fungal host's ecological fitness. Ca. G. gigasporarum has an extreme dependence on its host for nutrients and energy, whereas the fungal host is itself an obligate biotroph that relies on a photosynthetic plant. Our work represents the first step towards unraveling a complex network of interphylum interactions, which is expected to have a previously unrecognized ecological impact. Stefano Ghignone, Alessandra Salvioli, Iulia Anca, Erica Lumini, Giuseppe Ortu, Luca Petiti, Stéphane Cruveiller, Valeria Bianciotto, Pietro Piffanelli, Luisa Lanfranco and Paola Bonfante The ISME Journal (2012) 6, 136–145 http://dx.doi.org/10.1038/ismej.2011.110
Soil-borne mutualistic fungi, such as the ectomycorrhizal fungi, have helped shape forest communities worldwide over the last 180 million years through a mutualistic relationship with tree roots in which the fungal partner provides a large array of nutrients to the plant host in return for photosynthetically derived sugars. This exchange is essential for continued growth and productivity of forest trees, especially in nutrient-poor soils. To date, the signals from the two partners that mediate this symbiosis have remained uncharacterized. Here we demonstrate that MYCORRHIZAL iNDUCED SMALL SECRETED PROTEIN 7 (MiSSP7), the most highly symbiosis-upregulated gene from the ectomycorrhizal fungus Laccaria bicolor, encodes an effector protein indispensible for the establishment of mutualism. MiSSP7 is secreted by the fungus upon receipt of diffusible signals from plant roots, imported into the plant cell via phosphatidylinositol 3-phosphate-mediated endocytosis, and targeted to the plant nucleus where it alters the transcriptome of the plant cell. L. bicolor transformants with reduced expression of MiSSP7 do not enter into symbiosis with poplar roots. MiSSP7 resembles effectors of pathogenic fungi, nematodes, and bacteria that are similarly targeted to the plant nucleus to promote colonization of the plant tissues and thus can be considered a mutualism effector. Jonathan M. Plett, Minna Kemppainen, Shiv D. Kale, Annegret Kohler, Valérie Legué, Annick Brun, Brett M. Tyler, Alejandro G. Pardo, Francis Martin Current Biology Volume 21, Issue 14, 26 July 2011, Pages 1197–1203 http://dx.doi.org/10.1016/j.cub.2011.05.033
Biotrophy is a pervasive trait that evolved independently in plant pathogenic fungi and oomycetes. Comparative genomics of the first sequenced biotrophic pathogens highlight remarkable convergences, including gene losses in the metabolism of inorganic nitrogen, inorganic sulphur, and thiamine, and genes encoding carbohydrate active enzymes and secondary metabolism enzymes. Some biotrophs, but not all, display marked increases in overall genome size because of a proliferation of retrotransposons. I argue here that the release of constraints on transposon activity is driven by the advantages conferred by the genetic variability that results from transposition, in particular by the creation and diversification of broad palettes of effector genes. Increases in genome size and gene losses are the consequences of this trade-off. Genes that are not necessary for growth on a plant disappeared, but we still do not know what lost functions make some of these pathogens obligate.
Via Kamoun Lab @ TSL
The functional complexity of the Tuber melanosporum transcriptome has not yet been fully elucidated. Here, we applied high-throughput Illumina RNA-sequencing (RNA-Seq) to the transcriptome of T. melanosporum at different major developmental stages, that is free-living mycelium, fruiting body and ectomycorrhiza.
Sequencing of cDNA libraries generated a total of c. 24 million sequence reads representing > 882 Mb of sequence data. To construct a coverage signal profile across the genome, all reads were then aligned to the reference genome assembly of T. melanosporum Mel28.
We were able to identify a substantial number of novel transcripts, antisense transcripts, new exons, untranslated regions (UTRs), alternative upstream initiation codons and upstream open reading frames.
This RNA-Seq analysis allowed us to improve the genome annotation. It also provided us with a genome-wide view of the transcriptional and post-transcriptional mechanisms generating an increased number of transcript isoforms during major developmental transitions in T. melanosporum. E. Tisserant, C. Da Silva, A. Kohler, E. Morin, P. Wincker, F. Martin New Phytologist
Special Issue: Featured papers on ‘Unearthing the truffle genome’
Volume 189, Issue 3, pages 883–891, February 2011 http://dx.doi.org/10.1111/j.1469-8137.2010.03597.x
Recent sequencing projects have provided deep insight into fungal lifestyle-associated genomic adaptations. Here we report on the 25 Mb genome of the mutualistic root symbiont Piriformospora indica (Sebacinales, Basidiomycota) and provide a global characterization of fungal transcriptional responses associated with the colonization of living and dead barley roots. Extensive comparative analysis of the P. indica genome with other Basidiomycota and Ascomycota fungi that have diverse lifestyle strategies identified features typically associated with both, biotrophism and saprotrophism. The tightly controlled expression of the lifestyle-associated gene sets during the onset of the symbiosis, revealed by microarray analysis, argues for a biphasic root colonization strategy of P. indica. This is supported by a cytological study that shows an early biotrophic growth followed by a cell death-associated phase. About 10% of the fungal genes induced during the biotrophic colonization encoded putative small secreted proteins (SSP), including several lectin-like proteins and members of a P. indica-specific gene family (DELD) with a conserved novel seven-amino acids motif at the C-terminus. Similar to effectors found in other filamentous organisms, the occurrence of the DELDs correlated with the presence of transposable elements in gene-poor repeat-rich regions of the genome. This is the first in depth genomic study describing a mutualistic symbiont with a biphasic lifestyle. Our findings provide a significant advance in understanding development of biotrophic plant symbionts and suggest a series of incremental shifts along the continuum from saprotrophy towards biotrophy in the evolution of mycorrhizal association from decomposer fungi Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, et al. (2011) PLoS Pathog 7(10): e1002290 http://dx.doi.org/10.1371/journal.ppat.1002290
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