Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom-forming fungi

Looney, Brian; Miyauchi, Shingo; Morin, Emmanuelle; Drula, Elodie; Courty, Pierre Emmanuel; Kohler, Annegret; Kuo, Alan; LaButti, Kurt; Pangilinan, Jasmyn; Lipzen, Anna; Riley, Robert; Andreopoulos, William; He, Guifen; Johnson, Jenifer; Nolan, Matt; Tritt, Andrew; Barry, Kerrie W.; Grigoriev, Igor V.; Nagy, László G.; Hibbett, David; Henrissat, Bernard; Matheny, P. Brandon; Labbé, Jesse; Martin, Francis M.

doi:10.1111/nph.17892

Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom-forming fungi

Journal Article · Fri Dec 03 00:00:00 EST 2021 · New Phytologist

DOI:https://doi.org/10.1111/nph.17892· OSTI ID:1856713

^[1]; ^[2]; Morin, Emmanuelle ^[2]; ^[3]; ^[4]; ^[2]; ^[5]; ^[5]; Pangilinan, Jasmyn ^[5]; Lipzen, Anna ^[5]; ^[5]; Andreopoulos, William ^[5]; He, Guifen ^[5]; Johnson, Jenifer ^[5]; Nolan, Matt ^[5]; Tritt, Andrew ^[5]; ^[5]; ^[6]; ^[7]; ^[1] more »

Clark Univ., Worcester, MA (United States)
Univ. de Lorraine, Champenoux (France)
Aix‐Marseille Univ. (France); USC1408 Architecture et Fonction des Macromolécules Biologiques (AFMB), Marseille (France)
Univ. de Bourgogne Franche‐Comté, Dijon (France)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Biological Research Centre, Szeged (Hungary); Eötvös Loránd Univ., Budapest (Hungary)
Aix‐Marseille Univ. (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. de Lorraine, Champenoux (France); Beijing Forestry Univ. (China)

The ectomycorrhizal (ECM) symbiosis has independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic signatures of the transition to the ECM habit within the hyperdiverse Russulaceae. We present comparative analyses of the genomic architecture and the total and secreted gene repertoires of 18 species across the order Russulales, of which 13 are newly sequenced, including a representative of a saprotrophic member of Russulaceae, Gloeopeniophorella convolvens. The genomes of ECM Russulaceae are characterized by a loss of genes for plant cell wall-degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of small secreted proteins (SSPs) with TE ‘nests’, or dense aggregations of TEs. Here, some PCWDEs have been retained or even expanded, mostly in a species-specific manner. The genome of G. convolvens possesses some characteristics of ECM genomes (e.g. loss of some PCWDEs, TE expansion, reduction in secondary metabolism clusters). Functional specialization in ECM decomposition may drive diversification. Accelerated gene evolution predates the evolution of the ECM habit, indicating that changes in genome architecture and gene content may be necessary to prime the evolutionary switch.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

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

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

OSTI ID:: 1856713

Alternate ID(s):: OSTI ID: 1855295

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 5 Vol. 233; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
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synteny
transposable elements

Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom-forming fungi

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