Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.; Morin, Emmanuelle; Barry, Kerrie W.; Buscot, Francois; Canbäck, Björn; Choi, Cindy; Cichocki, Nicolas; Clum, Alicia; Colpaert, Jan; Copeland, Alex; Costa, Mauricio D.; Doré, Jeanne; Floudas, Dimitrios; Gay, Gilles; Girlanda, Mariangela; Henrissat, Bernard; Herrmann, Sylvie; Hess, Jaqueline; Högberg, Nils; Johansson, Tomas; Khouja, Hassine-Radhouane; LaButti, Kurt; Lahrmann, Urs; Levasseur, Anthony; Lindquist, Erika A.; Lipzen, Anna; Marmeisse, Roland; Martino, Elena; Murat, Claude; Ngan, Chew Y.; Nehls, Uwe; Plett, Jonathan M.; Pringle, Anne; Ohm, Robin A.; Perotto, Silvia; Peter, Martina; Riley, Robert; Rineau, Francois; Ruytinx, Joske; Salamov, Asaf; Shah, Firoz; Sun, Hui; Tarkka, Mika; Tritt, Andrew; Veneault-Fourrey, Claire; Zuccaro, Alga; Tunlid, Anders; Grigoriev, Igor V.; Hibbett, David S.; Martin, Francis

doi:10.1038/ng.3223

Title: Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Journal Article · 23 February 2015 · Nature Genetics

DOI: https://doi.org/10.1038/ng.3223 · OSTI ID:1242700

Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.; Morin, Emmanuelle; Barry, Kerrie W.; Buscot, Francois; Canbäck, Björn; Choi, Cindy; Cichocki, Nicolas; Clum, Alicia;

; Copeland, Alex; Costa, Mauricio D.; Doré, Jeanne; Floudas, Dimitrios; Gay, Gilles; Girlanda, Mariangela; Henrissat, Bernard; Herrmann, Sylvie; Hess, Jaqueline more »

To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall-degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.

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

Sponsoring Organization:: USDOE Office of Science (SC). Joint Genome Inst.; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1242700

Report Number(s):: LBNL-177846; ir:177846

Journal Information:: Nature Genetics, Vol. 47, Issue 4; ISSN 1061-4036

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Influence of Ammonium on Formation of Mineral-Associated Organic Carbon by an Ectomycorrhizal Fungus Wang, Tao; Tian, Zhaomo; Tunlid, Anders Applied and Environmental Microbiology, Vol. 85, Issue 10 https://doi.org/10.1128/aem.03007-18	journal	March 2019
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Genome Sequence of the Edible Cultivated Mushroom Lentinula edodes (Shiitake) Reveals Insights into Lignocellulose Degradation Chen, Lianfu; Gong, Yuhua; Cai, Yingli PLOS ONE, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pone.0160336	journal	August 2016
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Description of the first fungal dye-decolorizing peroxidase oxidizing manganese(II) Fernández-Fueyo, Elena; Linde, Dolores; Almendral, David Applied Microbiology and Biotechnology, Vol. 99, Issue 21 https://doi.org/10.1007/s00253-015-6665-3	journal	May 2015
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RiPEIP1, a gene from the arbuscular mycorrhizal fungus Rhizophagus irregularis, is preferentially expressed in planta and may be involved in root colonization Fiorilli, Valentina; Belmondo, Simone; Khouja, Hassine Radhouane Mycorrhiza, Vol. 26, Issue 6 https://doi.org/10.1007/s00572-016-0697-0	journal	April 2016
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Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics Bravo, Armando; York, Thomas; Pumplin, Nathan Nature Plants, Vol. 2, Issue 2 https://doi.org/10.1038/nplants.2015.208	journal	January 2016
Dimensions of biodiversity in the Earth mycobiome Peay, Kabir G.; Kennedy, Peter G.; Talbot, Jennifer M. Nature Reviews Microbiology, Vol. 14, Issue 7 https://doi.org/10.1038/nrmicro.2016.59	journal	June 2016
The fungus that came in from the cold: dry rot’s pre-adapted ability to invade buildings Balasundaram, S. V.; Hess, J.; Durling, M. B. The ISME Journal, Vol. 12, Issue 3 https://doi.org/10.1038/s41396-017-0006-8	journal	January 2018
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Distribution and diversity of enzymes for polysaccharide degradation in fungi Berlemont, Renaud Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00258-w	journal	March 2017
Genome sequence analysis of the fairy ring-forming fungus Lepista sordida and gene candidates for interaction with plants Takano, Tomoyuki; Yamamoto, Naoki; Suzuki, Tomohiro Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-42231-9	journal	April 2019
Soil metaproteomics reveals an inter-kingdom stress response to the presence of black truffles Zampieri, Elisa; Chiapello, Marco; Daghino, Stefania Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25773	journal	May 2016
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
A systematic revision of the ectomycorrhizal genus Laccaria from Korea Cho, Hae Jin; Park, Myung Soo; Lee, Hyun Mycologia, Vol. 110, Issue 5 https://doi.org/10.1080/00275514.2018.1507542	journal	September 2018
Restriction of plant roots in boreal forest organic soils affects the microbial community but does not change the dominance from ectomycorrhizal to saprotrophic fungi Sietiö, Outi-Maaria; Santalahti, Minna; Putkinen, Anuliina FEMS Microbiology Ecology, Vol. 95, Issue 9 https://doi.org/10.1093/femsec/fiz133	journal	August 2019
Divergent and Convergent Evolution of Fungal Pathogenicity Shang, Yanfang; Xiao, Guohua; Zheng, Peng Genome Biology and Evolution, Vol. 8, Issue 5 https://doi.org/10.1093/gbe/evw082	journal	April 2016
A plant perspective on nitrogen cycling in the rhizosphere Moreau, Delphine; Bardgett, Richard D.; Finlay, Roger D. Functional Ecology, Vol. 33, Issue 4 https://doi.org/10.1111/1365-2435.13303	journal	March 2019
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A new promising phylogenetic marker to study the diversity of fungal communities: The Glycoside Hydrolase 63 gene Pérez-Izquierdo, L.; Morin, E.; Maurice, J. P. Molecular Ecology Resources, Vol. 17, Issue 6 https://doi.org/10.1111/1755-0998.12678	journal	May 2017
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No support for the emergence of lichens prior to the evolution of vascular plants Nelsen, Matthew P.; Lücking, Robert; Boyce, C. Kevin Geobiology, Vol. 18, Issue 1 https://doi.org/10.1111/gbi.12369	journal	November 2019
Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi Looney, Brian P.; Ryberg, Martin; Hampe, Felix Molecular Ecology, Vol. 25, Issue 2 https://doi.org/10.1111/mec.13506	journal	January 2016
Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity Lahrmann, Urs; Strehmel, Nadine; Langen, Gregor New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13411	journal	April 2015
Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? Fernandez, Christopher W.; Kennedy, Peter G. New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13648	journal	September 2015
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
Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates Looney, Brian P.; Meidl, Peter; Piatek, Marek J. New Phytologist, Vol. 218, Issue 1 https://doi.org/10.1111/nph.15001	journal	January 2018
Ericoid plant species and Pinus sylvestris shape fungal communities in their roots and surrounding soil Sietiö, Outi-Maaria; Tuomivirta, Tero; Santalahti, Minna New Phytologist, Vol. 218, Issue 2 https://doi.org/10.1111/nph.15040	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
Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization Fournier, Joëlle; Imanishi, Leandro; Chabaud, Mireille New Phytologist, Vol. 219, Issue 3 https://doi.org/10.1111/nph.15216	journal	May 2018
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
Resource‐ratio theory predicts mycorrhizal control of litter decomposition Smith, Gabriel R.; Wan, Joe New Phytologist, Vol. 223, Issue 3 https://doi.org/10.1111/nph.15884	journal	May 2019
Dual‐mycorrhizal plants: their ecology and relevance Teste, François P.; Jones, Melanie D.; Dickie, Ian A. New Phytologist, Vol. 225, Issue 5 https://doi.org/10.1111/nph.16190	journal	October 2019
Trichoderma reesei Dehydrogenase, a Pyrroloquinoline Quinone-Dependent Member of Auxiliary Activity Family 12 of the Carbohydrate-Active Enzymes Database: Functional and Structural Characterization Turbe-Doan, Annick; Record, Eric; Lombard, Vincent Applied and Environmental Microbiology, Vol. 85, Issue 24 https://doi.org/10.1128/aem.00964-19	journal	December 2019
Involutin Is an Fe ³⁺ Reductant Secreted by the Ectomycorrhizal Fungus Paxillus involutus during Fenton-Based Decomposition of Organic Matter Shah, Firoz; Schwenk, Daniel; Nicolás, César Applied and Environmental Microbiology, Vol. 81, Issue 24 https://doi.org/10.1128/aem.02312-15	journal	October 2015
Draft Genome Sequence of the Ectomycorrhizal Ascomycete Sphaerosporella brunnea Benucci, Gian Maria Niccolò; Haridas, Sajeet; Labutti, Kurt Microbiology Resource Announcements, Vol. 8, Issue 50 https://doi.org/10.1128/mra.00857-19	journal	December 2019
Evolutionary dynamics of host specialization in wood-decay fungi Krah, Franz-Sebastian; Bässler, Claus; Heibl, Christoph BMC Evolutionary Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12862-018-1229-7	journal	August 2018
Filamentous ascomycete genomes provide insights into Copia retrotransposon diversity in fungi Donnart, Tifenn; Piednoël, Mathieu; Higuet, Dominique BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3795-2	journal	May 2017
Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor Daguerre, Y.; Levati, E.; Ruytinx, J. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4114-7	journal	September 2017
Oak displays common local but specific distant gene regulation responses to different mycorrhizal fungi Bouffaud, Marie-Lara; Herrmann, Sylvie; Tarkka, Mika T. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-06806-5	journal	June 2020
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Comparative Genomics of the Ectomycorrhizal Sister Species Rhizopogon vinicolor and Rhizopogon vesiculosus (Basidiomycota: Boletales) Reveals a Divergence of the Mating Type B Locus Mujic, Alija Bajro; Kuo, Alan; Tritt, Andrew G3: Genes\|Genomes\|Genetics, Vol. 7, Issue 6 https://doi.org/10.1534/g3.117.039396	journal	April 2017
Diversity and Enzyme Activity of Ectomycorrhizal Fungal Communities Following Nitrogen Fertilization in an Urban-Adjacent Pine Plantation Ning, Chen; Mueller, Gregory; Egerton-Warburton, Louise Forests, Vol. 9, Issue 3 https://doi.org/10.3390/f9030099	journal	February 2018
Globally distributed root endophyte Phialocephala subalpina links pathogenic and saprophytic lifestyles Markus, Schlegel,; Martin, Münsterkötter,; Ulrich, Güldener, ETH Zurich https://doi.org/10.3929/ethz-b-000124732	text	January 2016
The inseparability of sampling and time and its influence on attempts to unify the molecular and fossil records Hopkins, Melanie J.; Bapst, David W.; Simpson, Carl ETH Zurich https://doi.org/10.3929/ethz-b-000311010	text	January 2018
Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi Kameshwar, Ayyappa Kumar Sista; Qin, Wensheng Taylor & Francis https://doi.org/10.6084/m9.figshare.6741647.v1	text	January 2018
Structure‐guided design combined with evolutionary diversity led to the discovery of the xylose‐releasing exo‐xylanase activity in the glycoside hydrolase family 43 Zanphorlin, Letícia Maria; Morais, Mariana Abrahão Bueno; Diogo, José Alberto Biotechnology and Bioengineering https://doi.org/10.1002/bit.26899	journal	February 2019
Molecular Signalling During the Ectomycorrhizal Symbiosis Pellegrin, Clément; Martin, Francis; Veneault-Fourrey, Claire Biology of the Fungal Cell https://doi.org/10.1007/978-3-030-05448-9_6	book	January 2019
Comparative genomics and expression levels of hydrophobins from eight mycorrhizal genomes Rineau, F.; Lmalem, H.; Ahren, D. Mycorrhiza, Vol. 27, Issue 4 https://doi.org/10.1007/s00572-016-0758-4	journal	January 2017
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
Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi Knapp, Dániel G.; Németh, Julianna B.; Barry, Kerrie Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-24686-4	journal	April 2018
Delayed fungal evolution did not cause the Paleozoic peak in coal production Nelsen, Matthew P.; DiMichele, William A.; Peters, Shanan E. Proceedings of the National Academy of Sciences, Vol. 113, Issue 9 https://doi.org/10.1073/pnas.1517943113	journal	January 2016
Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi Sista Kameshwar, Ayyappa Kumar; Qin, Wensheng Mycology, Vol. 9, Issue 2 https://doi.org/10.1080/21501203.2017.1419296	journal	December 2017
ChIP-ping the branches of the tree: functional genomics and the evolution of eukaryotic gene regulation Marinov, Georgi K.; Kundaje, Anshul Briefings in Functional Genomics, Vol. 17, Issue 2 https://doi.org/10.1093/bfgp/ely004	journal	February 2018
Comparative Genomics of Pathogenic and Nonpathogenic Beetle-Vectored Fungi in the Genus Geosmithia Schuelke, Taruna A.; Wu, Guangxi; Westbrook, Anthony Genome Biology and Evolution, Vol. 9, Issue 12 https://doi.org/10.1093/gbe/evx242	journal	November 2017
Intrinsic cooperativity potentiates parallel cis-regulatory evolution Sorrells, Trevor R.; Johnson, Amanda N.; Howard, Conor J. eLife https://doi.org/10.1101/301234	journal	April 2018
Incipient local adaptation in a fungus: evolution of heavy metal tolerance through allelic and copy-number variation Bazzicalupo, Anna L.; Ruytinx, Joske; Ke, Yi-Hong bioRxiv https://doi.org/10.1101/832089	posted_content	November 2019
Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome Pérez‐Izquierdo, Leticia; Zabal‐Aguirre, Mario; González‐Martínez, Santiago C. Journal of Ecology, Vol. 107, Issue 4 https://doi.org/10.1111/1365-2745.13202	journal	February 2019
Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter: Seasonal dynamics of a soil microbial community Žifčáková, Lucia; Větrovský, Tomáš; Howe, Adina Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.13026	journal	October 2015
Oak extractive-induced stress reveals the involvement of new enzymes in the early detoxification response of Phanerochaete chrysosporium: Early fungal responses to oak extractives Fernández-González, Antonio José; Valette, Nicolas; Kohler, Annegret Environmental Microbiology, Vol. 20, Issue 10 https://doi.org/10.1111/1462-2920.14409	journal	October 2018
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
Time to re-think fungal ecology? Fungal ecological niches are often prejudged Selosse, Marc-André; Schneider-Maunoury, Laure; Martos, Florent New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14983	journal	January 2018
Ectomycorrhizal host specificity in a changing world: can legacy effects explain anomalous current associations? Lofgren, Lotus; Nguyen, Nhu H.; Kennedy, Peter G. New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15008	journal	February 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 inconspicuous gatekeeper: endophytic Serendipita vermifera acts as extended plant protection barrier in the rhizosphere Sarkar, Debika; Rovenich, Hanna; Jeena, Ganga New Phytologist, Vol. 224, Issue 2 https://doi.org/10.1111/nph.15904	journal	June 2019
Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition Fernandez, Christopher W.; See, Craig R.; Kennedy, Peter G. New Phytologist, Vol. 226, Issue 2 https://doi.org/10.1111/nph.16269	journal	November 2019
Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum , endophytically colonise roots of non‐ectomycorrhizal plants in natural environments Schneider‐Maunoury, Laure; Deveau, Aurélie; Moreno, Myriam New Phytologist, Vol. 225, Issue 6 https://doi.org/10.1111/nph.16321	journal	December 2019
De novo transcriptomic assembly and profiling of Rigidoporus microporus during saprotrophic growth on rubber wood Oghenekaro, Abbot O.; Raffaello, Tommaso; Kovalchuk, Andriy BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2574-9	journal	March 2016
Comparative genomics of Coniophora olivacea reveals different patterns of genome expansion in Boletales Castanera, Raúl; Pérez, Gúmer; López-Varas, Leticia BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4243-z	journal	November 2017
Genome description of Phlebia radiata 79 with comparative genomics analysis on lignocellulose decomposition machinery of phlebioid fungi Mäkinen, Mari; Kuuskeri, Jaana; Laine, Pia BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5817-8	journal	May 2019
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
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Mixotrophy in mycorrhizal plants: Extracting carbon from mycorrhizal networks Selosse, Marc-André; Bocayuva, Melissa Faust; Kasuya, Maria Catarina Megumi Molecular Mycorrhizal Symbiosis https://doi.org/10.1002/9781118951446.ch25	book	January 2016
Analysis of basidiomycete pigments in situ by Raman spectroscopy Tauber, James P.; Matthäus, Christian; Lenz, Claudius Journal of Biophotonics, Vol. 11, Issue 6 https://doi.org/10.1002/jbio.201700369	journal	March 2018
Genome sequence of the cauliflower mushroom Sparassis crispa (Hanabiratake) and its association with beneficial usage Kiyama, Ryoiti; Furutani, Yoshiyuki; Kawaguchi, Kayoko Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34415-6	journal	October 2018
Fungal evolution: major ecological adaptations and evolutionary transitions Naranjo‐Ortiz, Miguel A.; Gabaldón, Toni Biological Reviews https://doi.org/10.1111/brv.12510	journal	April 2019
Mycorrhizal symbioses: today and tomorrow Sędzielewska‐Toro, Kinga; Delaux, Pierre‐Marc New Phytologist, Vol. 209, Issue 3 https://doi.org/10.1111/nph.13820	journal	January 2016
Mycorrhizal fungi affect orchid distribution and population dynamics McCormick, Melissa K.; Whigham, Dennis F.; Canchani-Viruet, Armando New Phytologist, Vol. 219, Issue 4 https://doi.org/10.1111/nph.15223	journal	May 2018
Nitrogen and phosphate metabolism in ectomycorrhizas Nehls, Uwe; Plassard, Claude New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15257	journal	June 2018
Black root rot: a long known but little understood disease Nel, W. J.; Duong, T. A.; Beer, Z. W. Plant Pathology, Vol. 68, Issue 5 https://doi.org/10.1111/ppa.13011	journal	March 2019
Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms Plett, Jonathan M.; Martin, Francis M. The Plant Journal, Vol. 93, Issue 4 https://doi.org/10.1111/tpj.13802	journal	January 2018
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The genome of Rhizophagus clarus HR1 reveals a common genetic basis for auxotrophy among arbuscular mycorrhizal fungi Kobayashi, Yuuki; Maeda, Taro; Yamaguchi, Katsushi BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4853-0	journal	June 2018
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
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European mushroom assemblages are darker in cold climates. Krah, Franz-Sebastian; Buentgen, Ulf; Schaefer, Hanno Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.43443	text	January 2019
Ibotenic Acid Biosynthesis in the Fly Agaric Is Initiated by Glutamate Hydroxylation Obermaier, Sebastian; Müller, Michael Angewandte Chemie International Edition, Vol. 59, Issue 30 https://doi.org/10.1002/anie.202001870	journal	June 2020
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Mineral surface-reactive metabolites secreted during fungal decomposition contribute to the formation of soil organic matter: Fungal metabolites for soil carbon stabilization Wang, Tao; Tian, Zhaomo; Bengtson, Per Environmental Microbiology, Vol. 19, Issue 12 https://doi.org/10.1111/1462-2920.13990	journal	December 2017
Broad‐specificity GH131 β‐glucanases are a hallmark of fungi and oomycetes that colonize plants Anasontzis, George E.; Lebrun, Marc‐Henri; Haon, Mireille Environmental Microbiology, Vol. 21, Issue 8 https://doi.org/10.1111/1462-2920.14596	journal	April 2019
Mixotrophy everywhere on land and in water: the grand écart hypothesis Selosse, Marc-André; Charpin, Marie; Not, Fabrice Ecology Letters, Vol. 20, Issue 2 https://doi.org/10.1111/ele.12714	journal	December 2016
Distribution, Characteristics, and Regulatory Potential of Long Noncoding RNAs in Brown-Rot Fungi Borgognone, Alessandra; Sanseverino, Walter; Aiese Cigliano, Riccardo International Journal of Genomics, Vol. 2019 https://doi.org/10.1155/2019/9702342	journal	May 2019
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Globally distributed root endophyte Phialocephala subalpina links pathogenic and saprophytic lifestyles Schlegel, Markus; Münsterkötter, Martin; Güldener, Ulrich BioMed Central https://doi.org/10.7892/boris.98176	text	January 2016
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Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots Kohout, Petr; Charvátová, Markéta; Štursová, Martina The ISME Journal, Vol. 12, Issue 3 https://doi.org/10.1038/s41396-017-0027-3	journal	January 2018
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Evolutionary history of versatile-lipases from Agaricales through reconstruction of ancestral structures Barriuso, Jorge; Martínez, María Jesús BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-016-3419-2	journal	January 2017
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Description of the first fungal dye-decolorizing peroxidase oxidizing manganese(II) Fernández-Fueyo, Elena; Linde, Dolores; Almendral, David Applied Microbiology and Biotechnology, Vol. 99, Issue 21 https://doi.org/10.1007/s00253-015-6665-3	journal	May 2015
Chemical changes in organic matter after fungal colonization in a nitrogen fertilized and unfertilized Norway spruce forest Nicolás, César; Almeida, Juan P.; Ellström, Magnus Plant and Soil, Vol. 419, Issue 1-2 https://doi.org/10.1007/s11104-017-3324-8	journal	July 2017
Data on the genome analysis of the wild edible mushroom, Russula griseocarnosa Yu, Fei; Liang, Junfeng Data in Brief, Vol. 25 https://doi.org/10.1016/j.dib.2019.104295	journal	August 2019
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
Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? Bunn, Rebecca A.; Simpson, Dylan T.; Bullington, Lorinda S. The ISME Journal, Vol. 13, Issue 8 https://doi.org/10.1038/s41396-019-0403-2	journal	March 2019
European mushroom assemblages are darker in cold climates Krah, Franz-Sebastian; Büntgen, Ulf; Schaefer, Hanno Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10767-z	journal	June 2019
A meta-analysis of global fungal distribution reveals climate-driven patterns Větrovský, Tomáš; Kohout, Petr; Kopecký, Martin Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13164-8	journal	November 2019
Distribution and diversity of enzymes for polysaccharide degradation in fungi Berlemont, Renaud Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00258-w	journal	March 2017
Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi Knapp, Dániel G.; Németh, Julianna B.; Barry, Kerrie Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-24686-4	journal	April 2018
Genome sequence of the cauliflower mushroom Sparassis crispa (Hanabiratake) and its association with beneficial usage Kiyama, Ryoiti; Furutani, Yoshiyuki; Kawaguchi, Kayoko Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34415-6	journal	October 2018
Genome sequence analysis of the fairy ring-forming fungus Lepista sordida and gene candidates for interaction with plants Takano, Tomoyuki; Yamamoto, Naoki; Suzuki, Tomohiro Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-42231-9	journal	April 2019
Defence priming in Arabidopsis – a Meta-Analysis Westman, Sara M.; Kloth, Karen J.; Hanson, Johannes Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-49811-9	journal	September 2019
Intrinsic cooperativity potentiates parallel cis-regulatory evolution Sorrells, Trevor R.; Johnson, Amanda N.; Howard, Conor J. eLife https://doi.org/10.1101/301234	journal	April 2018
Influence of Ammonium on Formation of Mineral-Associated Organic Carbon by an Ectomycorrhizal Fungus Wang, Tao; Tian, Zhaomo; Tunlid, Anders Applied and Environmental Microbiology, Vol. 85, Issue 10 https://doi.org/10.1128/aem.03007-18	journal	March 2019
Draft Genome Sequence of Tuber borchii Vittad., a Whitish Edible Truffle Murat, Claude; Kuo, Alan; Barry, Kerrie W. Genome Announcements, Vol. 6, Issue 25 https://doi.org/10.1128/genomea.00537-18	journal	June 2018
Draft Genome Sequence of the Ectomycorrhizal Ascomycete Sphaerosporella brunnea Benucci, Gian Maria Niccolò; Haridas, Sajeet; Labutti, Kurt Microbiology Resource Announcements, Vol. 8, Issue 50 https://doi.org/10.1128/mra.00857-19	journal	December 2019
Distribution, Characteristics, and Regulatory Potential of Long Noncoding RNAs in Brown-Rot Fungi Borgognone, Alessandra; Sanseverino, Walter; Aiese Cigliano, Riccardo International Journal of Genomics, Vol. 2019 https://doi.org/10.1155/2019/9702342	journal	May 2019
FGMP: assessing fungal genome completeness Cissé, Ousmane H.; Stajich, Jason E. BMC Bioinformatics, Vol. 20, Issue 1 https://doi.org/10.1186/s12859-019-2782-9	journal	April 2019
Diversity and evolution of ABC proteins in mycorrhiza-forming fungi Kovalchuk, Andriy; Kohler, Annegret; Martin, Francis BMC Evolutionary Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12862-015-0526-7	journal	December 2015
Expansion and diversification of the MSDIN family of cyclic peptide genes in the poisonous agarics Amanita phalloides and A. bisporigera Pulman, Jane A.; Childs, Kevin L.; Sgambelluri, R. Michael BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3378-7	journal	December 2016
Evolutionary history of versatile-lipases from Agaricales through reconstruction of ancestral structures Barriuso, Jorge; Martínez, María Jesús BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-016-3419-2	journal	January 2017
Genome sequence of the ectophytic fungus Ramichloridium luteum reveals unique evolutionary adaptations to plant surface niche Wang, Bo; Liang, Xiaofei; Gleason, Mark L. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4118-3	journal	September 2017
Comparative genomics of Coniophora olivacea reveals different patterns of genome expansion in Boletales Castanera, Raúl; Pérez, Gúmer; López-Varas, Leticia BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4243-z	journal	November 2017
Genome of lethal Lepiota venenata and insights into the evolution of toxin-biosynthetic genes Lüli, Yunjiao; Cai, Qing; Chen, Zuo H. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5575-7	journal	March 2019
Genome description of Phlebia radiata 79 with comparative genomics analysis on lignocellulose decomposition machinery of phlebioid fungi Mäkinen, Mari; Kuuskeri, Jaana; Laine, Pia BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5817-8	journal	May 2019
Grouping of multicopper oxidases in Lentinula edodes by sequence similarities and expression patterns Sakamoto, Yuichi; Nakade, Keiko; Yoshida, Kentaro AMB Express, Vol. 5, Issue 1 https://doi.org/10.1186/s13568-015-0151-2	journal	September 2015
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
Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression Book, Adam J.; Lewin, Gina R.; McDonald, Bradon R. PLOS Biology, Vol. 14, Issue 6 https://doi.org/10.1371/journal.pbio.1002475	journal	June 2016
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
Genome Sequence of the Edible Cultivated Mushroom Lentinula edodes (Shiitake) Reveals Insights into Lignocellulose Degradation Chen, Lianfu; Gong, Yuhua; Cai, Yingli PLOS ONE, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pone.0160336	journal	August 2016
Molecular fungal community and its decomposition activity in sapwood and heartwood of 13 temperate European tree species Leonhardt, Sabrina; Hoppe, Björn; Stengel, Elisa PLOS ONE, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pone.0212120	journal	February 2019
Genome and secretome of Chondrostereum purpureum correspond to saprotrophic and phytopathogenic life styles Reina, Rocio; Kellner, Harald; Hess, Jaqueline PLOS ONE, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pone.0212769	journal	March 2019
A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy Tang, Nianwu; San Clemente, Hélène; Roy, Sébastien Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00233	journal	March 2016
A New Oidiodendron maius Strain Isolated from Rhododendron fortunei and its Effects on Nitrogen Uptake and Plant Growth Wei, Xiangying; Chen, Jianjun; Zhang, Chunying Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01327	journal	August 2016
Microbial Taxa Distribution Is Associated with Ecological Trophic Cascades along an Elevation Gradient Yao, Fei; Yang, Shan; Wang, Zhirui Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02071	journal	October 2017
Commentary: Fungal lifestyle reflected in serine protease repertoire da Silva, Ronivaldo R. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00467	journal	March 2018
Two P1B-1-ATPases of Amanita strobiliformis With Distinct Properties in Cu/Ag Transport Beneš, Vojtěch; Leonhardt, Tereza; Sácký, Jan Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00747	journal	April 2018
Dead or Alive; or Does It Really Matter? Level of Congruency Between Trophic Modes in Total and Active Fungal Communities in High Arctic Soil Wutkowska, Magdalena; Vader, Anna; Mundra, Sunil Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03243	journal	January 2019
Explorative Meta-Analysis of 377 Extant Fungal Genomes Predicted a Total Mycobiome Functionality of 42.4 Million KEGG Functions Starke, Robert; Capek, Petr; Morais, Daniel Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00143	journal	February 2020
Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus Casarrubia, Salvatore; Martino, Elena; Daghino, Stefania Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00341	journal	March 2020
Editorial: Transport in Plant Microbe Interactions Courty, Pierre-Emmanuel; Wipf, Daniel Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00809	journal	June 2016
Differential Gene Expression in Rhododendron fortunei Roots Colonized by an Ericoid Mycorrhizal Fungus and Increased Nitrogen Absorption and Plant Growth Wei, Xiangying; Chen, Jianjun; Zhang, Chunying Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01594	journal	October 2016
Algae and fungi move from the past to the future Bonfante, Paola eLife, Vol. 8 https://doi.org/10.7554/elife.49448	journal	July 2019
Structural plasticity in root-fungal symbioses: diverse interactions lead to improved plant fitness Kariman, Khalil; Barker, Susan Jane; Tibbett, Mark PeerJ, Vol. 6 https://doi.org/10.7717/peerj.6030	journal	December 2018
Additional file 10 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443143	dataset	January 2021
Additional file 11 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443146.v1	dataset	January 2021
Additional file 12 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443149.v1	dataset	January 2021
Additional file 13 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443152.v1	dataset	January 2021
Additional file 14 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443155	dataset	January 2021
Additional file 15 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443158	dataset	January 2021
Additional file 16 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443161.v1	dataset	January 2021
Additional file 17 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443164.v1	dataset	January 2021
Additional file 8 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443188.v1	dataset	January 2021
Additional file 9 of Genome sequencing and comparative genomic analysis of highly and weakly aggressive strains of Sclerotium rolfsii, the causal agent of peanut stem rot Yan, Liying; Wang, Zhihui; Song, Wanduo figshare https://doi.org/10.6084/m9.figshare.14443191	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