Abstract
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. 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.
| Original language | English |
|---|---|
| Pages (from-to) | 2294-2309 |
| Number of pages | 16 |
| Journal | New Phytologist |
| Volume | 233 |
| Issue number | 5 |
| DOIs | |
| State | Published - Mar 2022 |
| Externally published | Yes |
Funding
This research was supported by the Genomic Science Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research as part of the Plant Microbe Interfaces Scientific Focus Area, at the Oak Ridge National Laboratory. The Oak Ridge National Laboratory is managed by UT‐Battelle, LLC, for the US Department of Energy under contract DE‐AC05‐00OR22725. The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under contract no. DE‐AC02‐05CH11231. This was done within the framework of the Community Sequencing Program #1974 ‘1KFG: Deep Sequencing of Ecologically‐relevant Dikarya’ and the Community Sequencing Program #305 ‘Mycorrhizal Genomics Initiative’. Research in the Martin laboratory is also funded by the Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE; grant ANR‐11‐LABX‐0002‐01), the Region Lorraine Research Council and the European Commission (European Regional Development Fund). BL would like to thank the Laboratory of Excellence ARBRE for a visiting researcher grant. Thanks are also due to Daniel Lindner at the USFS Northern Research Station and Otto Miettinen at the University of Helsinki for taxonomic expertise and sample support. We would like to thank Prof. Joseph Spatafora and Rytas Vilgalys for their support for this project, as well as the managing editor and anonymous reviewers for constructive comments. The authors declare there are no competing interests.