Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi

Lotus A. Lofgren, Nhu H. Nguyen, Rytas Vilgalys, Joske Ruytinx, Hui Ling Liao, Sara Branco, Alan Kuo, Kurt LaButti, Anna Lipzen, William Andreopoulos, Jasmyn Pangilinan, Robert Riley, Hope Hundley, Hyunsoo Na, Kerrie Barry, Igor V. Grigoriev, Jason E. Stajich, Peter G. Kennedy

Research output: Contribution to journalArticlepeer-review

Abstract

While there has been significant progress characterizing the ‘symbiotic toolkit’ of ectomycorrhizal (ECM) fungi, how host specificity may be encoded into ECM fungal genomes remains poorly understood. We conducted a comparative genomic analysis of ECM fungal host specialists and generalists, focusing on the specialist genus Suillus. Global analyses of genome dynamics across 46 species were assessed, along with targeted analyses of three classes of molecules previously identified as important determinants of host specificity: small secreted proteins (SSPs), secondary metabolites (SMs) and G-protein coupled receptors (GPCRs). Relative to other ECM fungi, including other host specialists, Suillus had highly dynamic genomes including numerous rapidly evolving gene families and many domain expansions and contractions. Targeted analyses supported a role for SMs but not SSPs or GPCRs in Suillus host specificity. Phylogenomic-based ancestral state reconstruction identified Larix as the ancestral host of Suillus, with multiple independent switches between white and red pine hosts. These results suggest that like other defining characteristics of the ECM lifestyle, host specificity is a dynamic process at the genome level. In the case of Suillus, both SMs and pathways involved in the deactivation of reactive oxygen species appear to be strongly associated with enhanced host specificity.

Original languageEnglish (US)
Pages (from-to)774-792
Number of pages19
JournalNew Phytologist
Volume230
Issue number2
DOIs
StatePublished - Apr 2021
Externally publishedYes

Bibliographical note

Funding Information:
We thank all members of the Consortium for use of genome sequences, encouragement and project feedback, staff at the Minnesota Super Computing Institute for computational assistance, H. Nielsen and the Signal P team, B. Stielow for use of genome data for the species and , J. Xu for use of genome data for the species , F. Martin for use of genome data for the species , , , , and B. Looney for use of genome data for the species and , B. Henrissat for the annotation and curation of Auxiliary Activity enzymes via the CAZy database. Special thanks to A. Certano and K‐H. Chen for extracting genomic DNA and RNA for several of the species used in this study. Comparative analyses were performed on the High‐Performance Computing Cluster at the University of California, Riverside, in the Institute of Integrative Genome Biology, supported by NSF DBI‐1429826 and NIH S10‐OD016290. JES is a CIFAR fellow in the Fungal Kingdom: Threats and Opportunities program. 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 US Department of Energy under contract no. DE‐AC02‐05CH11231. Project support was provided by a National Science Foundation Division of Environmental Biology grant (no. 1554375) to PGK and RV. Suillus G. morchelliformis H. stonoliferum T. ganbajun T. terrestris C. anzutake H. rufescens G. lividus R. compacta R. brevipies

Funding Information:
We thank all members of the Suillus Consortium for use of genome sequences, encouragement and project feedback, staff at the Minnesota Super Computing Institute for computational assistance, H. Nielsen and the Signal P team, B. Stielow for use of genome data for the species G.?morchelliformis and H.?stonoliferum, J. Xu for use of genome data for the species T.?ganbajun, F. Martin for use of genome data for the species T.?terrestris, C.?anzutake, H.?rufescens, G.?lividus, and B. Looney for use of genome data for the species R.?compacta and R.?brevipies, B. Henrissat for the annotation and curation of Auxiliary Activity enzymes via the CAZy database. Special thanks to A. Certano and K-H. Chen for extracting genomic DNA and RNA for several of the species used in this study. Comparative analyses were performed on the High-Performance Computing Cluster at the University of California, Riverside, in the Institute of Integrative Genome Biology, supported by NSF DBI-1429826 and NIH S10-OD016290. JES is a CIFAR fellow in the Fungal Kingdom: Threats and Opportunities program. 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 US Department of Energy under contract no. DE-AC02-05CH11231. Project support was provided by a National Science Foundation Division of Environmental Biology grant (no. 1554375) to PGK and RV.

Publisher Copyright:
© 2020 The Authors. New Phytologist © 2020 New Phytologist Foundation

Keywords

  • G-protein coupled receptors
  • Suillus
  • genomics
  • host specificity
  • secondary metabolites
  • small secreted proteins

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

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