Publication

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

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 Lipszen,Roland Marmeisse,Elena Martino,Cluade 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,Mycorrhizal Genomics Initiative Consortium,Anders Tunlid,Igor V. Grigoriev,David S. Hibbett,Francis Martin 2015 February 23 Nature Genetics. doi:10.1038/ng.3223

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.

Highlights

Evolution of mycorrhizal symbiosis inferred from 49 fungal genomes
Figure 1. 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 and 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.
Distribution of symbiosis-upregulated genes of clusters I to VI into functional categories including MiSSPs and nonsecreted orphan genes no KOG

Figure 4. MiSSPs represent 16% of the symbiosis-upregulated transcripts in cluster V, a significant enrichment compared to their percentage in the total gene repertoire (i.e., 2%). CAZyme, carbohydrate-active enzymes; FOLyme, fungal oxidative lignin-degrading enzymes.




Citation

Kohler A., Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A, Copaert J, Copeland A, Costa MD, Doré J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Högberg N, Johansson T, Khouja HR, 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, Mycorrhizal Genomics Initiative Consortium, Tunlid A, Grigoriev IV, Hibbett DS, and Martin F. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics.  doi:10.1038/ng.3223



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