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

Abstract

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.

Authors:
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Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Genomics Division
Sponsoring Org.:
USDOE Office of Science (SC). Joint Genome Inst.; USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1242700
Report Number(s):
LBNL-177846
Journal ID: ISSN 1061-4036; ir:177846
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Nature Genetics
Additional Journal Information:
Journal Volume: 47; Journal Issue: 4; Journal ID: ISSN 1061-4036
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

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., and Martin, Francis. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. United States: N. p., 2015. Web. doi:10.1038/ng.3223.
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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. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. United States. https://doi.org/10.1038/ng.3223
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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., and Martin, Francis. Mon . "Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists". United States. https://doi.org/10.1038/ng.3223. https://www.osti.gov/servlets/purl/1242700.
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@article{osti_1242700,
title = {Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists},
author = {Kohler, Annegret and Kuo, Alan and Nagy, Laszlo G. and Morin, Emmanuelle and Barry, Kerrie W. and Buscot, Francois and Canbäck, Björn and Choi, Cindy and Cichocki, Nicolas and Clum, Alicia and Colpaert, Jan and Copeland, Alex and Costa, Mauricio D. and Doré, Jeanne and Floudas, Dimitrios and Gay, Gilles and Girlanda, Mariangela and Henrissat, Bernard and Herrmann, Sylvie and Hess, Jaqueline and Högberg, Nils and Johansson, Tomas and Khouja, Hassine-Radhouane and LaButti, Kurt and Lahrmann, Urs and Levasseur, Anthony and Lindquist, Erika A. and Lipzen, Anna and Marmeisse, Roland and Martino, Elena and Murat, Claude and Ngan, Chew Y. and Nehls, Uwe and Plett, Jonathan M. and Pringle, Anne and Ohm, Robin A. and Perotto, Silvia and Peter, Martina and Riley, Robert and Rineau, Francois and Ruytinx, Joske and Salamov, Asaf and Shah, Firoz and Sun, Hui and Tarkka, Mika and Tritt, Andrew and Veneault-Fourrey, Claire and Zuccaro, Alga and Tunlid, Anders and Grigoriev, Igor V. and Hibbett, David S. and Martin, Francis},
abstractNote = {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.},
doi = {10.1038/ng.3223},
journal = {Nature Genetics},
number = 4,
volume = 47,
place = {United States},
year = {Mon Feb 23 00:00:00 EST 2015},
month = {Mon Feb 23 00:00:00 EST 2015}
}
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https://doi.org/10.1038/ng.3223
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Figures / Tables:

Figure 1 Figure 1: Evolution of mycorrhizal symbiosis inferred from 49 fungal genomes. The tree is a chronogram estimated with r8s on the basis of a maximum-likelihood phylogeny inferred with RAxML. Nodes receiving less than maximal support in all analyses are indicated with asterisks. Curved arrows indicate alternate placements for Ustilaginomycotina andmore » Auriculariales (Supplementary Fig. 2). Mean ages (ma) are indicated adjacent to selected nodes. Circles indicate observed (right of tree) and reconstructed (left) copy numbers for selected genes encoding enzymes involved in decay of lignin (POD and GLX; blue circles) or crystalline cellulose (GH6, GH7 and LPMO; beige circles). Absence of gene copies is indicated with ‘x’. Areas of circles are proportional to gene copy numbers. (Copy numbers are indicated for internal nodes; gene counts in terminal taxa are shown in Supplementary Table 9.) Selected clades are labeled at internal nodes; ‘st.’ indicates the stem node for a taxon. Shading of terminal taxon names indicates nutritional modes (as shown in the key). Solid red triangles, estimated origins of ECM or ERM and ORM mycorrhizal symbioses; unfilled red triangle, alternate reconstruction with a single origin of ECM in Boletales and at least one reversal to saprotrophy; colored triangles below the geological timescale, ages of major ECM hosts based on fossils (solid triangles) and molecular-clock estimates (unfilled triangles); light-gray shading, temporal period when the origins of ECM are most plausible. Orch/eric/endomyc, orchid, ericoid or endomycorrhizae; litter/soil/other, litter, soil or other saprotroph; Cryog., Cryogenian; Ediac., Ediacaran; Cam., Cambrian; Ord., Ordovician; Sil., Silurian; Dev., Devonian; Carb., Carboniferous; Per., Permian; Tri., Triassic; Jur., Jurassic; Cret., Cretaceous; Cen., Cenozoic. Abbreviations for taxon names are defined in Supplementary Note.« less
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    Distribution, Characteristics, and Regulatory Potential of Long Noncoding RNAs in Brown-Rot Fungi
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    • Borgognone, Alessandra; Sanseverino, Walter; Aiese Cigliano, Riccardo
    • International Journal of Genomics, Vol. 2019
    • DOI: 10.1155/2019/9702342

    Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins
    journal, November 2016

    Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi
    text, January 2018

    Globally distributed root endophyte Phialocephala subalpina links pathogenic and saprophytic lifestyles
    text, January 2016

    • Schlegel, Markus; Münsterkötter, Martin; Güldener, Ulrich
    • BioMed Central
    • DOI: 10.7892/boris.98176

    Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots
    journal, January 2018

    • Kohout, Petr; Charvátová, Markéta; Štursová, Martina
    • The ISME Journal, Vol. 12, Issue 3
    • DOI: 10.1038/s41396-017-0027-3

    FGMP: assessing fungal genome completeness
    journal, April 2019

    Evolutionary history of versatile-lipases from Agaricales through reconstruction of ancestral structures
    journal, January 2017

    Description of the first fungal dye-decolorizing peroxidase oxidizing manganese(II)
    journal, May 2015

    • Fernández-Fueyo, Elena; Linde, Dolores; Almendral, David
    • Applied Microbiology and Biotechnology, Vol. 99, Issue 21
    • DOI: 10.1007/s00253-015-6665-3

    Chemical changes in organic matter after fungal colonization in a nitrogen fertilized and unfertilized Norway spruce forest
    journal, July 2017

    Data on the genome analysis of the wild edible mushroom, Russula griseocarnosa
    journal, August 2019

    The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen
    journal, December 2018

    • Nicolás, César; Martin-Bertelsen, Tomas; Floudas, Dimitrios
    • The ISME Journal, Vol. 13, Issue 4
    • DOI: 10.1038/s41396-018-0331-6

    Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why?
    journal, March 2019

    • Bunn, Rebecca A.; Simpson, Dylan T.; Bullington, Lorinda S.
    • The ISME Journal, Vol. 13, Issue 8
    • DOI: 10.1038/s41396-019-0403-2

    European mushroom assemblages are darker in cold climates
    journal, June 2019

    A meta-analysis of global fungal distribution reveals climate-driven patterns
    journal, November 2019

    Distribution and diversity of enzymes for polysaccharide degradation in fungi
    journal, March 2017

    Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi
    journal, April 2018

    Genome sequence of the cauliflower mushroom Sparassis crispa (Hanabiratake) and its association with beneficial usage
    journal, October 2018

    Genome sequence analysis of the fairy ring-forming fungus Lepista sordida and gene candidates for interaction with plants
    journal, April 2019

    Defence priming in Arabidopsis – a Meta-Analysis
    journal, September 2019

    Intrinsic cooperativity potentiates parallel cis-regulatory evolution
    journal, April 2018

    • Sorrells, Trevor R.; Johnson, Amanda N.; Howard, Conor J.
    • eLife
    • DOI: 10.1101/301234

    Influence of Ammonium on Formation of Mineral-Associated Organic Carbon by an Ectomycorrhizal Fungus
    journal, March 2019

    • Wang, Tao; Tian, Zhaomo; Tunlid, Anders
    • Applied and Environmental Microbiology, Vol. 85, Issue 10
    • DOI: 10.1128/aem.03007-18

    Draft Genome Sequence of Tuber borchii Vittad., a Whitish Edible Truffle
    journal, June 2018

    Draft Genome Sequence of the Ectomycorrhizal Ascomycete Sphaerosporella brunnea
    journal, December 2019

    • Benucci, Gian Maria Niccolò; Haridas, Sajeet; Labutti, Kurt
    • Microbiology Resource Announcements, Vol. 8, Issue 50
    • DOI: 10.1128/mra.00857-19

    Distribution, Characteristics, and Regulatory Potential of Long Noncoding RNAs in Brown-Rot Fungi
    journal, May 2019

    • Borgognone, Alessandra; Sanseverino, Walter; Aiese Cigliano, Riccardo
    • International Journal of Genomics, Vol. 2019
    • DOI: 10.1155/2019/9702342

    FGMP: assessing fungal genome completeness
    journal, April 2019

    Diversity and evolution of ABC proteins in mycorrhiza-forming fungi
    journal, December 2015

    • Kovalchuk, Andriy; Kohler, Annegret; Martin, Francis
    • BMC Evolutionary Biology, Vol. 15, Issue 1
    • DOI: 10.1186/s12862-015-0526-7

    Expansion and diversification of the MSDIN family of cyclic peptide genes in the poisonous agarics Amanita phalloides and A. bisporigera
    journal, December 2016

    Evolutionary history of versatile-lipases from Agaricales through reconstruction of ancestral structures
    journal, January 2017

    Genome sequence of the ectophytic fungus Ramichloridium luteum reveals unique evolutionary adaptations to plant surface niche
    journal, September 2017

    Comparative genomics of Coniophora olivacea reveals different patterns of genome expansion in Boletales
    journal, November 2017

    Genome of lethal Lepiota venenata and insights into the evolution of toxin-biosynthetic genes
    journal, March 2019

    Grouping of multicopper oxidases in Lentinula edodes by sequence similarities and expression patterns
    journal, September 2015

    Trees, fungi and bacteria: tripartite metatranscriptomics of a root microbiome responding to soil contamination
    journal, March 2018

    Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles
    journal, June 2016

    Molecular fungal community and its decomposition activity in sapwood and heartwood of 13 temperate European tree species
    journal, February 2019

    Genome and secretome of Chondrostereum purpureum correspond to saprotrophic and phytopathogenic life styles
    journal, March 2019

    A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy
    journal, March 2016

    A New Oidiodendron maius Strain Isolated from Rhododendron fortunei and its Effects on Nitrogen Uptake and Plant Growth
    journal, August 2016

    Microbial Taxa Distribution Is Associated with Ecological Trophic Cascades along an Elevation Gradient
    journal, October 2017

    Commentary: Fungal lifestyle reflected in serine protease repertoire
    journal, March 2018

    Two P1B-1-ATPases of Amanita strobiliformis With Distinct Properties in Cu/Ag Transport
    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
    journal, January 2019

    Explorative Meta-Analysis of 377 Extant Fungal Genomes Predicted a Total Mycobiome Functionality of 42.4 Million KEGG Functions
    journal, February 2020

    Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus
    journal, March 2020

    • Casarrubia, Salvatore; Martino, Elena; Daghino, Stefania
    • Frontiers in Microbiology, Vol. 11
    • DOI: 10.3389/fmicb.2020.00341

    Editorial: Transport in Plant Microbe Interactions
    journal, June 2016

    Algae and fungi move from the past to the future
    journal, July 2019

    Structural plasticity in root-fungal symbioses: diverse interactions lead to improved plant fitness
    journal, December 2018

    • Kariman, Khalil; Barker, Susan Jane; Tibbett, Mark
    • PeerJ, Vol. 6
    • DOI: 10.7717/peerj.6030
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