Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Comparative genomics reveals a dynamic genome evolution in the ectomycorrhizal milk-cap (Lactarius) mushrooms

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.18143· OSTI ID:1961160
 [1];  [2];  [3];  [3];  [3];  [4];  [5];  [3];  [3];  [3];  [6];  [3];  [7];  [8];  [9];  [10];  [11];  [7];  [1]
  1. Beijing Forestry Univ. (China); French National Research Institute for Agriculture, Food and Environment (INRAE), Champenoux (France); Universite de Lorraine, Champenoux (France)
  2. French National Research Institute for Agriculture, Food and Environment (INRAE), Champenoux (France); Universite de Lorraine, Champenoux (France); Chinese Academy of Sciences, Kunming (China)
  3. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Aix-Marseille Univ., Marseille (France)
  5. Max Planck Institute for Plant Breeding Research, Cologne (Germany)
  6. French National Research Institute for Agriculture, Food and Environment (INRAE), Champenoux (France)
  7. Chinese Academy of Sciences, Kunming (China)
  8. Beijing Forestry Univ. (China)
  9. Technical Univ. of Denmark, Lyngby (Denmark)
  10. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  11. Southern Woods Nursery, Christchurch (New Zealand)

Ectomycorrhizal fungi play a key role in forests by establishing mutualistic symbioses with woody plants. Genome analyses have identified conserved symbiosis-related traits among ectomycorrhizal fungal species, but the molecular mechanisms underlying host specificity remain poorly known. We sequenced and compared the genomes of seven species of milk-cap fungi (Lactarius, Russulales) with contrasting host specificity. We also compared these genomes with those of symbiotic and saprotrophic Russulales species, aiming to identify genes involved in their ecology and host specificity. The size of Lactarius genomes is significantly larger than other Russulales species, owing to a massive accumulation of transposable elements and duplication of dispensable genes. As expected, their repertoire of genes coding for plant cell wall-degrading enzymes is restricted, but they retained a substantial set of genes involved in microbial cell wall degradation. Notably, Lactarius species showed a striking expansion of genes encoding proteases, such as secreted ectomycorrhiza-induced sedolisins. A high copy number of genes coding for small secreted LysM proteins and Lactarius-specific lectins were detected, which may be linked to host specificity. This study revealed a large diversity in the genome landscapes and gene repertoires within Russulaceae. The known host specificity of Lactarius symbionts may be related to mycorrhiza-induced species-specific genes, including secreted sedolisins.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1961160
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 1 Vol. 235; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (65)

Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages journal September 2009
Reconstructing the evolutionary history of gypsy retrotransposons in the Périgord black truffle (Tuber melanosporum Vittad.) journal March 2016
A studentized permutation test for the non-parametric Behrens–Fisher problem journal June 2007
The Chromosome-Based Rubber Tree Genome Provides New Insights into Spurge Genome Evolution and Rubber Biosynthesis journal February 2020
Fungal lectins: structure, function and potential applications journal October 2013
Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis journal March 2010
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum journal September 2016
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists journal February 2015
Phased diploid genome assembly with single-molecule real-time sequencing journal October 2016
The rubber tree genome reveals new insights into rubber production and species adaptation journal May 2016
Unearthing the roots of ectomycorrhizal symbioses journal October 2016
Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits journal October 2020
Mediation of plant–mycorrhizal interaction by a lectin receptor-like kinase journal July 2019
Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle journal November 2018
Megaphylogeny resolves global patterns of mushroom evolution journal March 2019
Climatic controls of decomposition drive the global biogeography of forest-tree symbioses journal May 2019
Phylogenomic evolutionary surveys of subtilase superfamily genes in fungi journal March 2017
Identification of a Chitinase-modifying Protein from Fusarium verticillioides : TRUNCATION OF A HOST RESISTANCE PROTEIN BY A FUNGALYSIN METALLOPROTEASE journal August 2011
CLANS: a Java application for visualizing protein families based on pairwise similarity journal July 2004
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs journal June 2015
regioneR: an R/Bioconductor package for the association analysis of genomic regions based on permutation tests journal September 2015
Application of the MAFFT sequence alignment program to large data—reexamination of the usefulness of chained guide trees journal July 2016
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference journal May 2019
MCMCtreeR: functions to prepare MCMCtree analyses and visualize posterior ages on trees journal July 2019
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms journal May 2018
ModelTest-NG: A New and Scalable Tool for the Selection of DNA and Protein Evolutionary Models journal August 2019
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
Interactive Tree Of Life (iTOL) v4: recent updates and new developments journal April 2019
Isolation and Characterization of a Lectin from the Mushroom, Lactarius deliciosus journal June 1991
Synergistic Action of a Metalloprotease and a Serine Protease from Fusarium oxysporum f. sp. lycopersici Cleaves Chitin-Binding Tomato Chitinases, Reduces Their Antifungal Activity, and Enhances Fungal Virulence journal September 2015
Characterization of a Lectin from Lactarius deterrimus (Research on the Possible Involvement of the Fungal Lectin in Recognition between Mushroom and Spruce during the Early Stages of Mycorrhizae Formation) journal February 1993
Lentinula edode s tlg1 Encodes a Thaumatin-Like Protein That Is Involved in Lentinan Degradation and Fruiting Body Senescence journal April 2006
Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs: Regulation of gene expression in ectomycorrhiza journal January 2001
Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi journal January 2016
A highly conserved metalloprotease effector enhances virulence in the maize anthracnose fungusColletotrichum graminicola journal April 2016
Evolutionary history of mycorrhizal symbioses and global host plant diversity journal January 2018
Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates journal January 2018
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics journal March 2018
Dual function of a secreted fungalysin metalloprotease inUstilago maydis journal June 2018
Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina journal February 2019
Rapid evolution in plant–microbe interactions – an evolutionary genomics perspective journal March 2020
Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi journal February 2021
Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyper‐diverse lineage of mushroom‐forming fungi journal December 2021
Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism journal December 2010
Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity journal August 2020
Mycorrhizal syntheses between Lactarius spp. section Deliciosi and Pinus spp. and the effects of grazing insects in Yunnan, China journal June 2019
Molecular Mechanisms of Natural Rubber Biosynthesis journal June 2020
Evolution of the Mode of Nutrition in Symbiotic and Saprotrophic Fungi in Forest Ecosystems journal November 2021
LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons journal January 2008
The landscape of transposable elements in the finished genome of the fungal wheat pathogen Mycosphaerella graminicola journal January 2014
Gene family expansions and contractions are associated with host range in plant pathogens of the genus Colletotrichum journal August 2016
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy journal August 2015
Repbase Update, a database of repetitive elements in eukaryotic genomes journal June 2015
Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles journal June 2016
Metatranscriptomic Study of Common and Host-Specific Patterns of Gene Expression between Pines and Their Symbiotic Ectomycorrhizal Fungi in the Genus Suillus journal October 2016
LysM Effectors: Secreted Proteins Supporting Fungal Life journal December 2013
Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins journal November 2015
Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius–Pinus Symbioses journal August 2021
A Comprehensive Phylogenetic and Bioinformatics Survey of Lectins in the Fungal Kingdom journal June 2021
Worldwide phylogeny of Lactarius section Deliciosi inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences journal November 2007
Gene family expansions and contractions are associated with host range in plant pathogens of the genus Colletotrichum collection January 2016