Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

Miyauchi, Shingo; Kiss, Enikő; Kuo, Alan; Drula, Elodie; Kohler, Annegret; Sánchez-García, Marisol; Morin, Emmanuelle; Andreopoulos, Bill; Barry, Kerrie W.; Bonito, Gregory; Buée, Marc; Carver, Akiko; Chen, Cindy; Cichocki, Nicolas; Clum, Alicia; Culley, David; Crous, Pedro W.; Fauchery, Laure; Girlanda, Mariangela; Hayes, Richard D.; Kéri, Zsófia; LaButti, Kurt; Lipzen, Anna; Lombard, Vincent; Magnuson, Jon; Maillard, François; Murat, Claude; Nolan, Matt; Ohm, Robin A.; Pangilinan, Jasmyn; de Freitas Pereira, Maíra; Perotto, Silvia; Peter, Martina; Pfister, Stephanie; Riley, Robert; Sitrit, Yaron; Stielow, J. Benjamin; Szöllősi, Gergely; Žifčáková, Lucia; Štursová, Martina; Spatafora, Joseph W.; Tedersoo, Leho; Vaario, Lu-Min; Yamada, Akiyoshi; Yan, Mi; Wang, Pengfei; Xu, Jianping; Bruns, Tom; Baldrian, Petr; Vilgalys, Rytas; Dunand, Christophe; Henrissat, Bernard; Grigoriev, Igor V.; Hibbett, David; Nagy, László G.; Martin, Francis M.

doi:10.1038/s41467-020-18795-w

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

Journal Article · Mon Oct 12 00:00:00 EDT 2020 · Nature Communications

DOI:https://doi.org/10.1038/s41467-020-18795-w· OSTI ID:1713294

^[1]; Kiss, Enikő ^[2]; Kuo, Alan ^[3]; Drula, Elodie ^[4]; Kohler, Annegret ^[1]; Sánchez-García, Marisol ^[5]; Morin, Emmanuelle ^[1]; Andreopoulos, Bill ^[3]; Barry, Kerrie W. ^[3]; Bonito, Gregory ^[6]; Buée, Marc ^[1]; Carver, Akiko ^[3]; Chen, Cindy ^[3]; Cichocki, Nicolas ^[1]; Clum, Alicia ^[3]; Culley, David ^[7]; Crous, Pedro W. ^[8]; ^[1]; Girlanda, Mariangela ^[9]; ^[3] more »

Univ. of Lorraine, Champenoux (France)
Biological Research Centre, Szeged (Hungary)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Architecture et Fonction des Macromolecules Biologiques, Marseille (France)
Clark Univ., Worcester, MA (United States)
Michigan State Univ., East Lansing, MI (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Westerdijk Fungal Biodiversity Inst., Utrecht (Netherlands)
Univ. of Torino (Italy)
Swiss Federal Inst. for Forest, Snow and Landscape Research, Birmensdorf (Switzerland)
Ben-Gurion Univ. of The Negev (Israel)
Czech Academy of Sciences, Prague (Czech Republic)
Oregon State Univ., Corvallis, OR (United States)
Univ. of Tartu (Estonia)
Univ. of Helsinki (Finland)
Shinshu Univ., Nagano (Japan)
Kunming Medical Univ., Yunnan (China)
McMaster Univ., Hamilton, ON (Canada)
Univ. of California, Berkeley, CA (United States)
Duke Univ., Durham, NC (United States)
Univ. of Toulouse (France); National Centre for Scientific Research (CNRS), Toulouse (France)
Architecture et Fonction des Macromolecules Biologiques, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Univ. of Lorraine, Champenoux (France); Beijing Forestry Univ. (China)

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: European Research Council (ERC); Hungarian Academy of Sciences; Laboratory of Excellence ARBRE; National Research, Development and Innovation; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1713294

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 11; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (87)

ggplot2 Wickham, Hadley Springer New York, NY https://doi.org/10.1007/978-0-387-98141-3	book	January 2009
Evolution of Ectomycorrhizal Symbiosis in Plants Tedersoo, Leho; Brundrett, Mark C. Biogeography of Mycorrhizal Symbiosis https://doi.org/10.1007/978-3-319-56363-3_19	book	June 2017
Ectomycorrhizal Fungal Lineages: Detection of Four New Groups and Notes on Consistent Recognition of Ectomycorrhizal Taxa in High-Throughput Sequencing Studies Tedersoo, Leho; Smith, Matthew E. Biogeography of Mycorrhizal Symbiosis https://doi.org/10.1007/978-3-319-56363-3_6	book	January 2017
Characterization of the carbohydrase productions of an ectomycorrhizal fungus, Tricholoma matsutake Kusuda, Mizuho; Ueda, Mitsuhiro; Miyatake, Kazutaka Mycoscience, Vol. 49, Issue 5 https://doi.org/10.1007/S10267-008-0423-7	journal	October 2008
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
Fungal Genomics Kuo, Alan; Bushnell, Brian; Grigoriev, Igor V. Fungi, Vol. 70, p. 1-52 https://doi.org/10.1016/B978-0-12-397940-7.00001-X	book	May 2014
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages Domazet-Lošo, Tomislav; Brajković, Josip; Tautz, Diethard Trends in Genetics, Vol. 23, Issue 11 https://doi.org/10.1016/j.tig.2007.08.014	journal	November 2007
Signs of sex: what we know and how we know it Schurko, Andrew M.; Neiman, Maurine; Logsdon, John M. Trends in Ecology & Evolution, Vol. 24, Issue 4 https://doi.org/10.1016/j.tree.2008.11.010	journal	April 2009
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
The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis Martin, F.; Aerts, A.; Ahrén, D. Nature, Vol. 452, Issue 7183 https://doi.org/10.1038/nature06556	journal	March 2008
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
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Hybrid error correction and de novo assembly of single-molecule sequencing reads Koren, Sergey; Schatz, Michael C.; Walenz, Brian P. Nature Biotechnology, Vol. 30, Issue 7 https://doi.org/10.1038/nbt.2280	journal	July 2012
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum Peter, Martina; Kohler, Annegret; Ohm, Robin A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12662	journal	September 2016
A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms Werner, Gijsbert D. A.; Cornwell, William K.; Sprent, Janet I. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5087	journal	June 2014
Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts Nagy, László G.; Ohm, Robin A.; Kovács, Gábor M. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5471	journal	July 2014
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
Phased diploid genome assembly with single-molecule real-time sequencing Chin, Chen-Shan; Peluso, Paul; Sedlazeck, Fritz J. Nature Methods, Vol. 13, Issue 12 https://doi.org/10.1038/nmeth.4035	journal	October 2016
Unearthing the roots of ectomycorrhizal symbioses Martin, Francis; Kohler, Annegret; Murat, Claude Nature Reviews Microbiology, Vol. 14, Issue 12 https://doi.org/10.1038/nrmicro.2016.149	journal	October 2016
The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen Nicolás, César; Martin-Bertelsen, Tomas; Floudas, Dimitrios The ISME Journal, Vol. 13, Issue 4 https://doi.org/10.1038/s41396-018-0331-6	journal	December 2018
Contemporaneous radiations of fungi and plants linked to symbiosis Lutzoni, François; Nowak, Michael D.; Alfaro, Michael E. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07849-9	journal	December 2018
Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria Sipos, György; Prasanna, Arun N.; Walter, Mathias C. Nature Ecology & Evolution, Vol. 1, Issue 12 https://doi.org/10.1038/s41559-017-0347-8	journal	October 2017
Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle Murat, Claude; Payen, Thibaut; Noel, Benjamin Nature Ecology & Evolution, Vol. 2, Issue 12 https://doi.org/10.1038/s41559-018-0710-4	journal	November 2018
Megaphylogeny resolves global patterns of mushroom evolution Varga, Torda; Krizsán, Krisztina; Földi, Csenge Nature Ecology & Evolution, Vol. 3, Issue 4 https://doi.org/10.1038/s41559-019-0834-1	journal	March 2019
Unique and common traits in mycorrhizal symbioses Genre, Andrea; Lanfranco, Luisa; Perotto, Silvia Nature Reviews Microbiology, Vol. 18, Issue 11 https://doi.org/10.1038/s41579-020-0402-3	journal	July 2020
In silico definition of new ligninolytic peroxidase sub-classes in fungi and putative relation to fungal life style Mathé, Catherine; Fawal, Nizar; Roux, Christophe Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-56774-4	journal	December 2019
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
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
Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi Krizsán, Krisztina; Almási, Éva; Merényi, Zsolt Proceedings of the National Academy of Sciences, Vol. 116, Issue 15 https://doi.org/10.1073/pnas.1817822116	journal	March 2019
Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Soltis, D. E.; Soltis, P. S.; Morgan, D. R. Proceedings of the National Academy of Sciences, Vol. 92, Issue 7 https://doi.org/10.1073/pnas.92.7.2647	journal	March 1995
Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism Taylor, T. N.; Hass, H.; Kerp, H. Mycologia, Vol. 97, Issue 1 https://doi.org/10.1080/15572536.2006.11832862	journal	March 2005
r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock Sanderson, M. J. Bioinformatics, Vol. 19, Issue 2 https://doi.org/10.1093/bioinformatics/19.2.301	journal	January 2003
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
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
High-quality sequence clustering guided by network topology and multiple alignment likelihood Miele, Vincent; Penel, Simon; Daubin, Vincent Bioinformatics, Vol. 28, Issue 8 https://doi.org/10.1093/bioinformatics/bts098	journal	February 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Paradis, Emmanuel; Schliep, Klaus Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty633	journal	July 2018
Functional convergence in the decomposition of fungal necromass in soil and wood Maillard, François; Schilling, Jonathan; Andrews, Erin FEMS Microbiology Ecology, Vol. 96, Issue 2 https://doi.org/10.1093/femsec/fiz209	journal	December 2019
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
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
Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities Nagy, László G.; Riley, Robert; Tritt, Andrew Molecular Biology and Evolution, Vol. 33, Issue 4 https://doi.org/10.1093/molbev/msv337	journal	December 2015
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
PATRIC, the bacterial bioinformatics database and analysis resource Wattam, Alice R.; Abraham, David; Dalay, Oral Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1099	journal	November 2013
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 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
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
TreeFix: Statistically Informed Gene Tree Error Correction Using Species Trees Wu, Yi-Chieh; Rasmussen, Matthew D.; Bansal, Mukul S. Systematic Biology, Vol. 62, Issue 1 https://doi.org/10.1093/sysbio/sys076	journal	November 2012
First evidences that the ectomycorrhizal fungus Paxillus involutus mobilizes nitrogen and carbon from saprotrophic fungus necromass: Do ectomycorrhizal fungi degrade brown rot fungi? Akroume, Emila; Maillard, François; Bach, Cyrille Environmental Microbiology, Vol. 21, Issue 1 https://doi.org/10.1111/1462-2920.14440	journal	November 2018
Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis Pellegrin, Clément; Daguerre, Yohann; Ruytinx, Joske Environmental Microbiology, Vol. 21, Issue 10 https://doi.org/10.1111/1462-2920.14727	journal	July 2019
The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis Kang, Heng; Chen, Xin; Kemppainen, Minna Environmental Microbiology, Vol. 22, Issue 4 https://doi.org/10.1111/1462-2920.14959	journal	April 2020
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data Yu, Guangchuang; Smith, David K.; Zhu, Huachen Methods in Ecology and Evolution, Vol. 8, Issue 1 https://doi.org/10.1111/2041-210X.12628	journal	September 2016
Complex multicellularity in fungi: evolutionary convergence, single origin, or both?: Complex multicellularity in Fungi Nagy, László G.; Kovács, Gábor M.; Krizsán, Krisztina Biological Reviews, Vol. 93, Issue 4 https://doi.org/10.1111/brv.12418	journal	April 2018
Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes Tedersoo, Leho; Bahram, Mohammad Biological Reviews, Vol. 94, Issue 5 https://doi.org/10.1111/brv.12538	journal	May 2019
Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae Matheny, P. Brandon; Aime, M. Catherine; Bougher, Neale L. Journal of Biogeography, Vol. 36, Issue 4 https://doi.org/10.1111/j.1365-2699.2008.02055.x	journal	April 2009
Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest Lindahl, Björn D.; Ihrmark, Katarina; Boberg, Johanna New Phytologist, Vol. 173, Issue 3 https://doi.org/10.1111/j.1469-8137.2006.01936.x	journal	November 2006
Ectomycorrhizal fungi and the biotrophy–saprotrophy continuum Koide, Roger T.; Sharda, Jori N.; Herr, Joshua R. New Phytologist, Vol. 178, Issue 2 https://doi.org/10.1111/j.1469-8137.2008.02401.x	journal	April 2008
Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems Bödeker, Inga T. M.; Clemmensen, Karina E.; de Boer, Wietse New Phytologist, Vol. 203, Issue 1 https://doi.org/10.1111/nph.12791	journal	April 2014
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
Mycorrhizal ecology and evolution: the past, the present, and the future van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13288	journal	February 2015
Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors Shah, Firoz; Nicolás, César; Bentzer, Johan New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13722	journal	November 2015
Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters Pellitier, Peter T.; Zak, Donald R. New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14598	journal	May 2017
Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus Op De Beeck, Michiel; Troein, Carl; Peterson, Carsten New Phytologist, Vol. 218, Issue 1 https://doi.org/10.1111/nph.14971	journal	January 2018
Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists Martino, Elena; Morin, Emmanuelle; Grelet, Gwen-Aëlle New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14974	journal	January 2018
Evolutionary history of mycorrhizal symbioses and global host plant diversity Brundrett, Mark C.; Tedersoo, Leho New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.14976	journal	January 2018
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics Strullu-Derrien, Christine; Selosse, Marc-André; Kenrick, Paul New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15076	journal	March 2018
The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development Zhang, Feng; Anasontzis, George E.; Labourel, Aurore New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15113	journal	April 2018
Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota Chang, Ying; Desirò, Alessandro; Na, Hyunsoo New Phytologist, Vol. 222, Issue 1 https://doi.org/10.1111/nph.15613	journal	January 2019
Exploring the role of ectomycorrhizal fungi in soil carbon dynamics Zak, Donald R.; Pellitier, Peter T.; Argiroff, WilliamA. New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15679	journal	February 2019
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
Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization Plett, Jonathan M.; Plett, Krista L.; Wong‐Bajracharya, Johanna New Phytologist, Vol. 228, Issue 2 https://doi.org/10.1111/nph.16759	journal	September 2020
Phylogeny-Aware Gap Placement Prevents Errors in Sequence Alignment and Evolutionary Analysis Loytynoja, A.; Goldman, N. Science, Vol. 320, Issue 5883 https://doi.org/10.1126/science.1158395	journal	June 2008
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
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest Clemmensen, K. E.; Bahr, A.; Ovaskainen, O. Science, Vol. 339, Issue 6127 https://doi.org/10.1126/science.1231923	journal	March 2013
Global diversity and geography of soil fungi Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei Science, Vol. 346, Issue 6213 https://doi.org/10.1126/science.1256688	journal	November 2014
Mycorrhizal Fungi as Mediators of Soil Organic Matter Dynamics Frey, Serita D. Annual Review of Ecology, Evolution, and Systematics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110617-062331	journal	November 2019
Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4750-6	journal	May 2018
Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles Castanera, Raúl; López-Varas, Leticia; Borgognone, Alessandra PLOS Genetics, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pgen.1006108	journal	June 2016
Correction: Metatranscriptomic Study of Common and Host-Specific Patterns of Gene Expression between Pines and Their Symbiotic Ectomycorrhizal Fungi in the Genus Suillus Liao, Hui-Ling; Chen, Yuan; Vilgalys, Rytas PLOS Genetics, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pgen.1007742	journal	October 2018
Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology English, Adam C.; Richards, Stephen; Han, Yi PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0047768	journal	November 2012
Fossil ectomycorrhizae from the Middle Eocene Lepage, Ben A.; Currah, Randolph S.; Stockey, Ruth A. American Journal of Botany, Vol. 84, Issue 3 https://doi.org/10.2307/2446014	journal	March 1997
Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of Homobasidiomycetes Hibbett, David S.; Grimaldi, David; Donoghue, Michael J. American Journal of Botany, Vol. 84, Issue 7 https://doi.org/10.2307/2446289	journal	July 1997
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
Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins Pellegrin, Clement; Morin, Emmanuelle; Martin, Francis M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01278	journal	November 2015
Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan Figshare https://doi.org/10.6084/m9.figshare.c.4108949	collection	January 2018

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Additional file 3 of Disease-induced changes in plant microbiome assembly and functional adaptation Gao, Min; Xiong, Chao; Gao, Cheng figshare https://doi.org/10.6084/m9.figshare.16625387.v1	dataset	January 2021
Additional file 1 of Whole genome sequencing and analysis of Armillaria gallica Jzi34 symbiotic with Gastrodia elata Cai, Jinlong; Muhammad, Ikram; Chen, Bilian figshare https://doi.org/10.6084/m9.figshare.23084013.v1	dataset	January 2023
Additional file 1 of Evolutionary history of arbuscular mycorrhizal fungi and genomic signatures of obligate symbiosis Rosling, Anna; Eshghi Sahraei, Shadi; Kalsoom Khan, Faheema figshare https://doi.org/10.6084/m9.figshare.25929209	dataset	January 2024

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