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

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

doi:10.1038/ng.3223

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

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

Research output: Contribution to journal › Article › peer-review

802 Citations (Scopus)

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.

Original language	English
Pages (from-to)	410-415
Number of pages	6
Journal	Nature Genetics
Volume	47
Issue number	4
DOIs	https://doi.org/10.1038/ng.3223
Publication status	Published - Apr 2015

Keywords

Base Sequence
Evolution, Molecular
Gene Deletion
Gene Expression Regulation, Fungal/genetics
Genome, Fungal/genetics
Molecular Sequence Data
Mycorrhizae/genetics
Phylogeny
Plant Diseases/genetics
Plant Roots/microbiology
Selection, Genetic
Symbiosis/genetics
Virulence/genetics

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10.1038/ng.3223

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Kohler, A., Kuo, A., Nagy, L. G., Morin, E., Barry, K. W., Buscot, F., Canbäck, B., Choi, C., Cichocki, N., Clum, A., Colpaert, J., Copeland, A., Costa, M. D., Doré, J., Floudas, D., Gay, G., Girlanda, M., Henrissat, B., Herrmann, S., ... Grigoriev, I. V. (2015). Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics, 47(4), 410-415. https://doi.org/10.1038/ng.3223

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. / Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. In: Nature Genetics. 2015 ; Vol. 47, No. 4. pp. 410-415.

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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. ",

keywords = "Base Sequence, Evolution, Molecular, Gene Deletion, Gene Expression Regulation, Fungal/genetics, Genome, Fungal/genetics, Molecular Sequence Data, Mycorrhizae/genetics, Phylogeny, Plant Diseases/genetics, Plant Roots/microbiology, Selection, Genetic, Symbiosis/genetics, Virulence/genetics",

author = "Annegret Kohler and Alan Kuo and Nagy, {Laszlo G} and Emmanuelle Morin and Barry, {Kerrie W} and Francois Buscot and Bj{\"o}rn Canb{\"a}ck and Cindy Choi and Nicolas Cichocki and Alicia Clum and Jan Colpaert and Alex Copeland and Costa, {Mauricio D} and Jeanne Dor{\'e} and Dimitrios Floudas and Gilles Gay and Mariangela Girlanda and Bernard Henrissat and Sylvie Herrmann and Jaqueline Hess and Nils H{\"o}gberg and Tomas Johansson and Hassine-Radhouane Khouja and Kurt LaButti and Urs Lahrmann and Anthony Levasseur and Lindquist, {Erika A} and Anna Lipzen and Roland Marmeisse and Elena Martino and Claude Murat and Ngan, {Chew Y} and Uwe Nehls and Plett, {Jonathan M} and Anne Pringle and Ohm, {Robin A} and Silvia Perotto and Martina Peter and Robert Riley and Francois Rineau and Joske Ruytinx and Asaf Salamov and Firoz Shah and Hui Sun and Mika Tarkka and Andrew Tritt and Claire Veneault-Fourrey and Alga Zuccaro and Anders Tunlid and Grigoriev, {Igor V}",

year = "2015",

month = apr,

doi = "10.1038/ng.3223",

language = "English",

volume = "47",

pages = "410--415",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Publishing Group",

number = "4",

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Kohler, A, Kuo, A, Nagy, LG, Morin, E, Barry, KW, Buscot, F, Canbäck, B, Choi, C, Cichocki, N, Clum, A, Colpaert, J, Copeland, A, Costa, MD, Doré, J, Floudas, D, Gay, G, Girlanda, M, Henrissat, B, Herrmann, S, Hess, J, Högberg, N, Johansson, T, Khouja, H-R, LaButti, K, Lahrmann, U, Levasseur, A, Lindquist, EA, Lipzen, A, Marmeisse, R, Martino, E, Murat, C, Ngan, CY, Nehls, U, Plett, JM, Pringle, A, Ohm, RA, Perotto, S, Peter, M, Riley, R, Rineau, F, Ruytinx, J, Salamov, A, Shah, F, Sun, H, Tarkka, M, Tritt, A, Veneault-Fourrey, C, Zuccaro, A, Tunlid, A & Grigoriev, IV 2015, 'Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists', Nature Genetics, vol. 47, no. 4, pp. 410-415. https://doi.org/10.1038/ng.3223

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.

In: Nature Genetics, Vol. 47, No. 4, 04.2015, p. 410-415.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

AU - Kohler, Annegret

AU - Kuo, Alan

AU - Nagy, Laszlo G

AU - Morin, Emmanuelle

AU - Barry, Kerrie W

AU - Buscot, Francois

AU - Canbäck, Björn

AU - Choi, Cindy

AU - Cichocki, Nicolas

AU - Clum, Alicia

AU - Colpaert, Jan

AU - Copeland, Alex

AU - Costa, Mauricio D

AU - Doré, Jeanne

AU - Floudas, Dimitrios

AU - Gay, Gilles

AU - Girlanda, Mariangela

AU - Henrissat, Bernard

AU - Herrmann, Sylvie

AU - Hess, Jaqueline

AU - Högberg, Nils

AU - Johansson, Tomas

AU - Khouja, Hassine-Radhouane

AU - LaButti, Kurt

AU - Lahrmann, Urs

AU - Levasseur, Anthony

AU - Lindquist, Erika A

AU - Lipzen, Anna

AU - Marmeisse, Roland

AU - Martino, Elena

AU - Murat, Claude

AU - Ngan, Chew Y

AU - Nehls, Uwe

AU - Plett, Jonathan M

AU - Pringle, Anne

AU - Ohm, Robin A

AU - Perotto, Silvia

AU - Peter, Martina

AU - Riley, Robert

AU - Rineau, Francois

AU - Ruytinx, Joske

AU - Salamov, Asaf

AU - Shah, Firoz

AU - Sun, Hui

AU - Tarkka, Mika

AU - Tritt, Andrew

AU - Veneault-Fourrey, Claire

AU - Zuccaro, Alga

AU - Tunlid, Anders

AU - Grigoriev, Igor V

PY - 2015/4

Y1 - 2015/4

N2 - 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.

AB - 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.

KW - Base Sequence

KW - Evolution, Molecular

KW - Gene Deletion

KW - Gene Expression Regulation, Fungal/genetics

KW - Genome, Fungal/genetics

KW - Molecular Sequence Data

KW - Mycorrhizae/genetics

KW - Phylogeny

KW - Plant Diseases/genetics

KW - Plant Roots/microbiology

KW - Selection, Genetic

KW - Symbiosis/genetics

KW - Virulence/genetics

U2 - 10.1038/ng.3223

DO - 10.1038/ng.3223

M3 - Article

C2 - 25706625

VL - 47

SP - 410

EP - 415

JO - Nature Genetics

JF - Nature Genetics

SN - 1061-4036

IS - 4

ER -

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

Abstract

Keywords

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