Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins

Pellegrin, Clement; Morin, Emmanuelle; Martin, Francis M.; Veneault-Fourrey, Claire

doi:10.3389/fmicb.2015.01278

Title: Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins

Journal Article · Wed Nov 18 00:00:00 EST 2015 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2015.01278· OSTI ID:1241128

Pellegrin, Clement ^[1]; Morin, Emmanuelle ^[2]; Martin, Francis M. ^[2]; Veneault-Fourrey, Claire ^[1]

Univ. de Lorraine, Vandoeuvre-les-Nancy (France); Institut National de la Recherche Agronomique, Champenoux (France)
Institut National de la Recherche Agronomique, Champenoux (France)

Fungi are major players in the carbon cycle in forest ecosystems due to the wide range of interactions they have with plants either through soil degradation processes by litter decayers or biotrophic interactions with pathogenic and ectomycorrhizal symbionts. Secretion of fungal proteins mediates these interactions by allowing the fungus to interact with its environment and/or host. Ectomycorrhizal (ECM) symbiosis independently appeared several times throughout evolution and involves approximately 80% of trees. Despite extensive physiological studies on ECM symbionts, little is known about the composition and specificities of their secretomes. In this study, we used a bioinformatics pipeline to predict and analyze the secretomes of 49 fungal species, including 11 ECM fungi, wood and soil decayers and pathogenic fungi to tackle the following questions: (1) Are there differences between the secretomes of saprophytic and ECM fungi? (2) Are small-secreted proteins (SSPs) more abundant in biotrophic fungi than in saprophytic fungi? and (3) Are there SSPs shared between ECM, saprotrophic and pathogenic fungi? We showed that the number of predicted secreted proteins is similar in the surveyed species, independently of their lifestyle. The secretome from ECM fungi is characterized by a restricted number of secreted CAZymes, but their repertoires of secreted proteases and lipases are similar to those of saprotrophic fungi. Focusing on SSPs, we showed that the secretome of ECM fungi is enriched in SSPs compared with other species. Most of the SSPs are coded by orphan genes with no known PFAM domain or similarities to known sequences in databases. Finally, based on the clustering analysis, we identified shared- and lifestyle-specific SSPs between saprotrophic and ECM fungi. The presence of SSPs is not limited to fungi interacting with living plants as the genome of saprotrophic fungi also code for numerous SSPs. As a result, ECM fungi shared lifestyle-specific SSPs likely involved in symbiosis that are good candidates for further functional analyses.

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Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1241128

Journal Information:: Frontiers in Microbiology, Vol. 6; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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References (87)

Comparative analysis of secretomes in basidiomycete fungi Alfaro, Manuel; Oguiza, José A.; Ramírez, Lucía Journal of Proteomics, Vol. 102 https://doi.org/10.1016/j.jprot.2014.03.001	journal	May 2014
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Cerato-Platanin Induces Resistance in Arabidopsis Leaves through Stomatal Perception, Overexpression of Salicylic Acid- and Ethylene-Signalling Genes and Camalexin Biosynthesis Baccelli, Ivan; Lombardi, Lara; Luti, Simone PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0100959	journal	June 2014
Secreted Fungal Effector Lipase Releases Free Fatty Acids to Inhibit Innate Immunity-Related Callose Formation during Wheat Head Infection Blümke, Antje; Falter, Christian; Herrfurth, Cornelia Plant Physiology, Vol. 165, Issue 1 https://doi.org/10.1104/pp.114.236737	journal	March 2014
The fungal cerato-platanin protein EPL1 forms highly ordered layers at hydrophobic/hydrophilic interfaces Bonazza, K.; Gaderer, R.; Neudl, S. Soft Matter, Vol. 11, Issue 9 https://doi.org/10.1039/C4SM02389G	journal	January 2015
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis Bonfante, Paola; Genre, Andrea Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1046	journal	July 2010
Carbohydrate-related enzymes of important Phytophthora plant pathogens Brouwer, Henk; Coutinho, Pedro M.; Henrissat, Bernard Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.08.011	journal	November 2014
Evolution of a subtilisin-like protease gene family in the grass endophytic fungus Epichloë festucae Bryant, Michelle K.; Schardl, Christopher L.; Hesse, Uljana BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-168	journal	January 2009
Manipulating the soil microbiome to increase soil health and plant fertility Chaparro, Jacqueline M.; Sheflin, Amy M.; Manter, Daniel K. Biology and Fertility of Soils, Vol. 48, Issue 5 https://doi.org/10.1007/s00374-012-0691-4	journal	May 2012
Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response Chisholm, Stephen T.; Coaker, Gitta; Day, Brad Cell, Vol. 124, Issue 4 https://doi.org/10.1016/j.cell.2006.02.008	journal	February 2006
Identification and characterization of a lipase gene from Antrodia cinnamomea Chu, Fang-Hua; Wang, Sheng-Yang; Lee, Li-Chiun Mycological Research, Vol. 112, Issue 12 https://doi.org/10.1016/j.mycres.2008.06.006	journal	December 2008
The Structure of the Elicitor Cerato-platanin (CP), the First Member of the CP Fungal Protein Family, Reveals a Double ψβ-Barrel Fold and Carbohydrate Binding de Oliveira, Aline L.; Gallo, Mariana; Pazzagli, Luigia Journal of Biological Chemistry, Vol. 286, Issue 20 https://doi.org/10.1074/jbc.M111.223644	journal	March 2011
Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete Hebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis Doré, Jeanne; Perraud, Marie; Dieryckx, Cindy New Phytologist, Vol. 208, Issue 4 https://doi.org/10.1111/nph.13546	journal	July 2015
The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi Eastwood, D. C.; Floudas, D.; Binder, M. Science, Vol. 333, Issue 6043, p. 762-765 https://doi.org/10.1126/science.1205411	journal	July 2011
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren Journal of Molecular Biology, Vol. 300, Issue 4 https://doi.org/10.1006/jmbi.2000.3903	journal	July 2000
Copsin, a Novel Peptide-based Fungal Antibiotic Interfering with the Peptidoglycan Synthesis Essig, Andreas; Hofmann, Daniela; Münch, Daniela Journal of Biological Chemistry, Vol. 289, Issue 50 https://doi.org/10.1074/jbc.M114.599878	journal	October 2014
Subtilisin-like proteases in plantâ€“pathogen recognition and immune priming: a perspective Figueiredo, Andreia; Monteiro, Filipa; Sebastiana, MÃ³nica Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00739	journal	December 2014
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes Floudas, Dimitrios; Binder, Manfred; Riley, Robert Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1221748	journal	June 2012
Forests trapped in nitrogen limitation - an ecological market perspective on ectomycorrhizal symbiosis Franklin, Oskar; Näsholm, Torgny; Högberg, Peter New Phytologist, Vol. 203, Issue 2 https://doi.org/10.1111/nph.12840	journal	May 2014
Deletion of S mgpi1 encoding a GPI-anchored protein suppresses sterility of the STRIPAK mutant ΔSmmob3 in the filamentous ascomycete S ordaria macrospora : GPI-anchored protein SmGPI1 of Sordaria macrospora Frey, Stefan; Lahmann, Yasmine; Hartmann, Thomas Molecular Microbiology, Vol. 97, Issue 4 https://doi.org/10.1111/mmi.13054	journal	May 2015
Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses Garcia, Kevin; Delaux, Pierre‐Marc; Cope, Kevin R. New Phytologist, Vol. 208, Issue 1 https://doi.org/10.1111/nph.13423	journal	April 2015
Soil moisture and plant residue addition interact in their effect on extracellular enzyme activity Geisseler, Daniel; Horwath, William R.; Scow, Kate M. Pedobiologia, Vol. 54, Issue 2 https://doi.org/10.1016/j.pedobi.2010.10.001	journal	March 2011
Filamentous plant pathogen effectors in action Giraldo, Martha C.; Valent, Barbara Nature Reviews Microbiology, Vol. 11, Issue 11 https://doi.org/10.1038/nrmicro3119	journal	October 2013
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses Hibbett, David S.; Matheny, P. Brandon BMC Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1741-7007-7-13	journal	March 2009
WoLF PSORT: protein localization predictor Horton, P.; Park, K. -J.; Obayashi, T. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm259	journal	May 2007
A phylogenomic approach to reconstructing the diversification of serine proteases in fungi Hu, G.; Leger, R. J. St. Journal of Evolutionary Biology, Vol. 17, Issue 6 https://doi.org/10.1111/j.1420-9101.2004.00786.x	journal	November 2004
CD-HIT Suite: a web server for clustering and comparing biological sequences Huang, Ying; Niu, Beifang; Gao, Ying Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btq003	journal	January 2010
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy Kloppholz, Silke; Kuhn, Hannah; Requena, Natalia Current Biology, Vol. 21, Issue 14 https://doi.org/10.1016/j.cub.2011.06.044	journal	July 2011
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G. Nature Genetics, Vol. 47, Issue 4 https://doi.org/10.1038/ng.3223	journal	February 2015
Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation Krijger, Jorrit-Jan; Thon, Michael R.; Deising, Holger B. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-722	journal	January 2014
Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem Lakshmanan, V.; Selvaraj, G.; Bais, H. P. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.245811	journal	July 2014
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs Lindahl, Björn D.; Tunlid, Anders New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13201	journal	December 2014
Hydrophobins: the protein-amphiphiles of filamentous fungi Linder, Markus B.; Szilvay, Géza R.; Nakari-Setälä, Tiina FEMS Microbiology Reviews, Vol. 29, Issue 5 https://doi.org/10.1016/j.femsre.2005.01.004	journal	November 2005
Harnessing ectomycorrhizal genomics for ecological insights Martin, Francis; Nehls, Uwe Current Opinion in Plant Biology, Vol. 12, Issue 4 https://doi.org/10.1016/j.pbi.2009.05.007	journal	August 2009
Reliability Measures for Membrane Protein Topology Prediction Algorithms Melén, Karin; Krogh, Anders; von Heijne, Gunnar Journal of Molecular Biology, Vol. 327, Issue 3 https://doi.org/10.1016/S0022-2836(03)00182-7	journal	March 2003
Small Signaling Peptides in Arabidopsis Development: How Cells Communicate Over a Short Distance Murphy, Evan; Smith, Stephanie; De Smet, Ive The Plant Cell, Vol. 24, Issue 8 https://doi.org/10.1105/tpc.112.099010	journal	August 2012
Independent Subtilases Expansions in Fungi Associated with Animals Muszewska, A.; Taylor, J. W.; Szczesny, P. Molecular Biology and Evolution, Vol. 28, Issue 12 https://doi.org/10.1093/molbev/msr176	journal	July 2011
Mastering ectomycorrhizal symbiosis: the impact of carbohydrates Nehls, U. Journal of Experimental Botany, Vol. 59, Issue 5 https://doi.org/10.1093/jxb/erm334	journal	February 2008
Erratum: Mechanisms of regulated unconventional protein secretion Nickel, Walter; Rabouille, Catherine Nature Reviews Molecular Cell Biology, Vol. 10, Issue 3 https://doi.org/10.1038/nrm2645	journal	March 2009
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes Plett, J. M.; Daguerre, Y.; Wittulsky, S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1322671111	journal	May 2014
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D. Current Biology, Vol. 21, Issue 14 https://doi.org/10.1016/j.cub.2011.05.033	journal	July 2011
Reconsidering mutualistic plant–fungal interactions through the lens of effector biology Plett, Jonathan M.; Martin, Francis Current Opinion in Plant Biology, Vol. 26 https://doi.org/10.1016/j.pbi.2015.06.001	journal	August 2015
Fungal Effectors and Plant Susceptibility Lo Presti, Libera; Lanver, Daniel; Schweizer, Gabriel Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-043014-114623	journal	April 2015
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi Riley, Robert; Salamov, Asaf A.; Brown, Daren W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 27 https://doi.org/10.1073/pnas.1400592111	journal	June 2014
The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry: Organic matter degradation by ectomycorrhizal fungi Rineau, Francois; Roth, Doris; Shah, Firoz Environmental Microbiology, Vol. 14, Issue 6 https://doi.org/10.1111/j.1462-2920.2012.02736.x	journal	March 2012
Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus Rineau, F.; Shah, F.; Smits, M. M. The ISME Journal, Vol. 7, Issue 10 https://doi.org/10.1038/ismej.2013.91	journal	June 2013
Filamentous pathogen effector functions: of pathogens, hosts and microbiomes Rovenich, Hanna; Boshoven, Jordi C.; Thomma, Bart PHJ Current Opinion in Plant Biology, Vol. 20 https://doi.org/10.1016/j.pbi.2014.05.001	journal	August 2014
Asynchronous origins of ectomycorrhizal clades of Agaricales Ryberg, Martin; Matheny, P. Brandon Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1735 https://doi.org/10.1098/rspb.2011.2428	journal	December 2011
Using Hierarchical Clustering of Secreted Protein Families to Classify and Rank Candidate Effectors of Rust Fungi Saunders, Diane G. O.; Win, Joe; Cano, Liliana M. PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029847	journal	January 2012
Microbial control over carbon cycling in soil Schimel, Joshua P.; Schaeffer, Sean M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00348	journal	January 2012
The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus Shah, Firoz; Rineau, Francois; Canbäck, Björn New Phytologist, Vol. 200, Issue 3 https://doi.org/10.1111/nph.12425	journal	July 2013
Genome-Wide Analysis in Three Fusarium Pathogens Identifies Rapidly Evolving Chromosomes and Genes Associated with Pathogenicity Sperschneider, Jana; Gardiner, Donald M.; Thatcher, Louise F. Genome Biology and Evolution, Vol. 7, Issue 6 https://doi.org/10.1093/gbe/evv092	journal	May 2015
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
Fungal Effector Proteins Stergiopoulos, Ioannis; de Wit, Pierre J. G. M. Annual Review of Phytopathology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.phyto.112408.132637	journal	September 2009
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments Talavera, Gerard; Castresana, Jose Systematic Biology, Vol. 56, Issue 4 https://doi.org/10.1080/10635150701472164	journal	August 2007
Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition Talbot, Jennifer M.; Bruns, Thomas D.; Smith, Dylan P. Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.10.004	journal	February 2013
Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa Tian, Chaoguang; Beeson, William T.; Iavarone, Anthony T. Proceedings of the National Academy of Sciences, Vol. 106, Issue 52 https://doi.org/10.1073/pnas.0906810106	journal	December 2009
Interspecies competition triggers virulence and mutability in Candida albicans–Pseudomonas aeruginosa mixed biofilms Trejo-Hernández, Abigail; Andrade-Domínguez, Andrés; Hernández, Magdalena The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.53	journal	April 2014
Fungal enzyme sets for plant polysaccharide degradation van den Brink, Joost; de Vries, Ronald P. Applied Microbiology and Biotechnology, Vol. 91, Issue 6, p. 1477-1492 https://doi.org/10.1007/s00253-011-3473-2	journal	July 2011
Establishing the roots of a relationship van Ooij, Christiaan Nature Reviews Microbiology, Vol. 9, Issue 9 https://doi.org/10.1038/nrmicro2642	journal	August 2011
Mutualistic interactions on a knife-edge between saprotrophy and pathogenesis Veneault-Fourrey, Claire; Martin, Francis Current Opinion in Plant Biology, Vol. 14, Issue 4 https://doi.org/10.1016/j.pbi.2011.03.022	journal	August 2011
Secretome of the Free-living Mycelium from the Ectomycorrhizal Basidiomycete Laccaria bicolor Vincent, Delphine; Kohler, Annegret; Claverol, Stephane Journal of Proteome Research, Vol. 11, Issue 1 https://doi.org/10.1021/pr200895f	journal	November 2011
A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals: Lipase as a virulence factor Voigt, Christian A.; Schäfer, Wilhelm; Salomon, Siegfried The Plant Journal, Vol. 42, Issue 3 https://doi.org/10.1111/j.1365-313X.2005.02377.x	journal	February 2005
Soil biodiversity and soil community composition determine ecosystem multifunctionality Wagg, C.; Bender, S. F.; Widmer, F. Proceedings of the National Academy of Sciences, Vol. 111, Issue 14 https://doi.org/10.1073/pnas.1320054111	journal	March 2014
Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field Wallander, Hakan; Nilsson, Lars Ola; Hagerberg, David New Phytologist, Vol. 151, Issue 3 https://doi.org/10.1046/j.0028-646x.2001.00199.x	journal	September 2001
Effector Biology of Plant-Associated Organisms: Concepts and Perspectives Win, J.; Chaparro-Garcia, A.; Belhaj, K. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 77, Issue 0 https://doi.org/10.1101/sqb.2012.77.015933	journal	January 2012
Carbohydrate-Active Enzymes in Pythium and Their Role in Plant Cell Wall and Storage Polysaccharide Degradation Zerillo, Marcelo M.; Adhikari, Bishwo N.; Hamilton, John P. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0072572	journal	September 2013
Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi Zhao, Zhongtao; Liu, Huiquan; Wang, Chenfang BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-6	journal	January 2014
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00921-1	journal	March 2021
Comparative mitochondrial genome analysis reveals intron dynamics and gene rearrangements in two Trametes species Chen, Cheng; Li, Qiang; Fu, Rongtao Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-82040-7	journal	January 2021
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi RWTH Aachen University https://doi.org/10.18154/rwth-2021-02761	text	January 2021
Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages Tedersoo, Leho; May, Tom W.; Smith, Matthew E. Mycorrhiza, Vol. 20, Issue 4 https://doi.org/10.1007/s00572-009-0274-x	journal	September 2009
Stable genetic transformation of the ectomycorrhizal fungus Pisolithus tinctorius Rodríguez-Tovar, Aída V.; Ruiz-Medrano, Roberto; Herrera-Martínez, Aseneth Journal of Microbiological Methods, Vol. 63, Issue 1 https://doi.org/10.1016/j.mimet.2005.02.016	journal	October 2005
Agrobacterium tumefaciens -mediated transformation as a tool for insertional mutagenesis in the symbiotic ectomycorrhizal fungus Hebeloma cylindrosporum Combier, Jean-Philippe; Melayah, Delphine; Raffier, Colette FEMS Microbiology Letters, Vol. 220, Issue 1 https://doi.org/10.1016/s0378-1097(03)00089-2	journal	March 2003
Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis Martin, Francis; Kohler, Annegret; Murat, Claude Nature, Vol. 464, Issue 7291 https://doi.org/10.1038/nature08867	journal	March 2010
Genetic basis for the establishment of endosymbiosis in Paramecium He, Ming; Wang, Jinfeng; Fan, Xinpeng The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-018-0341-4	journal	January 2019
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha Ruan, Xiaoxian; Wang, Zhen; Su, Yingjuan Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07198-0	journal	February 2022
The danger of mycorrhizal traps? Kuyper, Thomas W.; Kiers, E. Toby New Phytologist, Vol. 203, Issue 2 https://doi.org/10.1111/nph.12883	journal	June 2014
Overexpression of Laccaria bicolor aquaporin JQ585595 alters root water transport properties in ectomycorrhizal white spruce ( Picea glauca ) seedlings Xu, Hao; Kemppainen, Minna; El Kayal, Walid New Phytologist, Vol. 205, Issue 2 https://doi.org/10.1111/nph.13098	journal	October 2014
Abolishing Cell Wall Glycosylphosphatidylinositol-Anchored Proteins in Candida albicans Enhances Recognition by Host Dectin-1 Shen, Hui; Chen, Si Min; Liu, Wei Infection and Immunity, Vol. 83, Issue 7 https://doi.org/10.1128/iai.00097-15	journal	April 2015
The Irreversible Loss of a Decomposition Pathway Marks the Single Origin of an Ectomycorrhizal Symbiosis Wolfe, Benjamin E.; Tulloss, Rodham E.; Pringle, Anne PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0039597	journal	July 2012
Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling Churchland, Carolyn; Grayston, Sue J. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00261	journal	June 2014

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Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina Morin, Emmanuelle; Miyauchi, Shingo; San Clemente, Hélène New Phytologist, Vol. 222, Issue 3 https://doi.org/10.1111/nph.15687	journal	February 2019
Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae Almási, Éva; Sahu, Neha; Krizsán, Krisztina New Phytologist, Vol. 224, Issue 2 https://doi.org/10.1111/nph.16032	journal	June 2019
Manipulating the Expression of Small Secreted Protein 1 (Ssp1) Alters Patterns of Development and Metabolism in the White-Rot Fungus Pleurotus ostreatus Feldman, Daria; Amedi, Nadav; Carmeli, Shmuel Applied and Environmental Microbiology, Vol. 85, Issue 15 https://doi.org/10.1128/aem.00761-19	journal	May 2019
Apophysomyces variabilis: draft genome sequence and comparison of predictive virulence determinants with other medically important Mucorales Prakash, Hariprasath; Rudramurthy, Shivaprakash Mandya; Gandham, Prasad S. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4136-1	journal	September 2017
The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata Armaleo, Daniele; Müller, Olaf; Lutzoni, François BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5629-x	journal	July 2019
Comparative transcriptomics of Gymnosporangium spp. teliospores reveals a conserved genetic program at this specific stage of the rust fungal life cycle Tao, Si-Qi; Cao, Bin; Morin, Emmanuelle BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6099-x	journal	October 2019
Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis Challacombe, Jean F.; Hesse, Cedar N.; Bramer, Lisa M. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6358-x	journal	December 2019
Trees, fungi and bacteria: tripartite metatranscriptomics of a root microbiome responding to soil contamination Gonzalez, E.; Pitre, F. E.; Pagé, A. P. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0432-5	journal	March 2018
Arabidopsis thaliana responds to colonisation of Piriformospora indica by secretion of symbiosis-specific proteins Thürich, Johannes; Meichsner, Doreen; Furch, Alexandra C. U. PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0209658	journal	December 2018
Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response Lamacchia, Marina; Dyrka, Witold; Breton, Annick Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00471	journal	April 2016
Secretome Analysis from the Ectomycorrhizal Ascomycete Cenococcum geophilum de Freitas Pereira, Maíra; Veneault-Fourrey, Claire; Vion, Patrice Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00141	journal	February 2018
The Comparison of Expressed Candidate Secreted Proteins from Two Arbuscular Mycorrhizal Fungi Unravels Common and Specific Molecular Tools to Invade Different Host Plants Kamel, Laurent; Tang, Nianwu; Malbreil, Mathilde Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00124	journal	February 2017
The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics Vincent, Delphine; Rafiqi, Maryam; Job, Dominique Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01626	journal	January 2020
The Conifer Root and Stem Rot Pathogen (Heterobasidion parviporum): Effectome Analysis and Roles in Interspecific Fungal Interactions Wen, Zilan; Zeng, Zhen; Ren, Fei Microorganisms, Vol. 7, Issue 12 https://doi.org/10.3390/microorganisms7120658	journal	December 2019
Laccaria bicolor MiSSP8 is a small-secreted protein decisive for the establishment of the ectomycorrhizal symbiosis Pellegrin, Cl??ment; Daguerre, Yohann; Ruytinx, Joske Environmental Microbiology https://doi.org/10.1101/218131	journal	May 2019
The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata Armaleo, Daniele; Müller, Olaf; Lutzoni, François BioMed Central https://doi.org/10.14288/1.0380051	text	January 2019
Comparative transcriptomics of Gymnosporangium spp. teliospores reveals a conserved genetic program at this specific stage of the rust fungal life cycle Tao, Si-Qi; Cao, Bin; Morin, Emmanuelle https://doi.org/10.21203/rs.2.10143/v1	preprint	October 2019
Comparative transcriptomics of Gymnosporangium spp. teliospores reveals a conserved genetic program at this specific stage of the rust fungal life cycle Tao, Si-Qi; Cao, Bin; Morin, Emmanuelle Research Square [preprint] https://doi.org/10.21203/rs.2.10143/v2	posted_content	October 2019
Orchids and their mycorrhizal fungi: an insufficiently explored relationship Favre-Godal, Quentin; Gourguillon, Lorène; Lordel-Madeleine, Sonia Mycorrhiza, Vol. 30, Issue 1 https://doi.org/10.1007/s00572-020-00934-2	journal	January 2020
Unusual genome expansion and transcription suppression in ectomycorrhizal Tricholoma matsutake by insertions of transposable elements Min, Byoungnam; Yoon, Hyeokjun; Park, Julius PLOS ONE, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pone.0227923	journal	January 2020
The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata Daniele, Armaleo,; Olaf, Müller,; François, Lutzoni, BioMed Central https://doi.org/10.5167/uzh-175027	text	January 2019
Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita Hess, Jaqueline; Skrede, Inger; Chaib De Mares, Maryam Molecular Biology and Evolution https://doi.org/10.1093/molbev/msy179	journal	September 2018
Recent Insights on Biological and Ecological Aspects of Ectomycorrhizal Fungi and Their Interactions Mello, Antonietta; Balestrini, Raffaella Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00216	journal	February 2018

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