Needles in fungal haystacks : discovery of a putative a-factor pheromone and a unique mating strategy in the Leotiomycetes

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Authors

Wilson, Andi M.
Coetzee, Martin Petrus Albertus
Wingfield, Michael J.
Wingfield, Brenda D.

Journal Title

Journal ISSN

Volume Title

Publisher

Public Library of Science

Abstract

The Leotiomycetes is a hugely diverse group of fungi, accommodating a wide variety of important plant and animal pathogens, ericoid mycorrhizal fungi, as well as producers of antibiotics. Despite their importance, the genetics of these fungi remain relatively understudied, particularly as they don’t include model taxa. For example, sexual reproduction and the genetic mechanisms that underly this process are poorly understood in the Leotiomycetes. We exploited publicly available genomic and transcriptomic resources to identify genes of the mating-type locus and pheromone response pathway in an effort to characterize the mating strategies and behaviors of 124 Leotiomycete species. Our analyses identified a putative a-factor mating pheromone in these species. This significant finding represents the first identification of this gene in Pezizomycotina species outside of the Sordariomycetes. A unique mating strategy was also discovered in Lachnellula species that appear to have lost the need for the primary MAT1-1-1 protein. Ancestral state reconstruction enabled the identification of numerous transitions between homothallism and heterothallism in the Leotiomycetes and suggests a heterothallic ancestor for this group. This comprehensive catalog of mating-related genes from such a large group of fungi provides a rich resource from which in-depth, functional studies can be conducted in these economically and ecologically important species.

Description

DATA AVAILABILITY STATEMENT : A total of 124 genomes as well as various RNA seq datasets were used for this manuscript. All of this data was downloaded specifically for this manuscript from the NCBI’s Genome and SRA databases. All the relevant accession numbers can be found in S1 Table.
SUPPORTING INFORMATION : FIGURE S1. Determining the length of the mature repeat in the α-factor pheromone using Hymenoscyphus occultus as an example. FIGURE S2. Comparison between the maximum likelihood tree generated using a concatenated supermatrix of 72 genes and the maximum likelihood supertree generated using the 72 individual gene regions combined using ASTRAL. FIGURE S3. Ancestral state reconstruction of the Leotiomycete mating strategies. FIGURE S4. The diversity of the Leotiomycete a-factor pheromone in the Ploettnerulaceae, Drepanopezizaceae, Mollisiaceae, Erysiphaceae, Hyaloscyphaceae, Helotiaceae and Lachnaceae. FIGURE S5. The conservation of the Sclerotiniaceae and Rutstroemiaceae a-factor pheromones. FIGURE S6. Gene alignments and RNAseq mappings of the ste2 gene from Hymenoscyphus species. TABLE S1. Species included in this study, with NCBI Genome and RNAseq accession numbers. TABLE S2. NCBI accession numbers for the various gene and protein sequences used in BLASTn and tBLASTn analyses. TABLE S3. Presence and absence of both pheromone factors and additional functional information of the α-factor pheromone. TABLE S4. Expression of housekeeping genes, MAT genes, pheromone genes and pheromone receptor genes. FILE S1. Genomes that were excluded from the analyses. FILE S2. A pheromone sequences from a variety of Sordariomycetes & yeasts. FILE S3. CAAX/CpAX proteins (<100aa) from B. cinerea, B. sinoalli, S. sclerotiorum,M. fructicola, R. commune, A. resinae and P. destructans. FILE S4. Character state statistics from the ancestral state reconstruction analyses. FILE S5. MAT1-1-13 sequences from Rhynchosporium species. FILE S6. Species that were classified as “undetermined” with regards to their sexual strategy. FILE S7. Explanations regarding the sexual strategy determinations in species with both MAT1-1- and MAT1-2-associated genes. FILE S8. Alpha pheromone sequences for all Leotiomycetes (GBK). FILE S9. Alpha pheromone sequences for all Leotiomycetes (FASTA). FILE S10. A pheromone sequences for all Leotiomycetes.

Keywords

Leotiomycetes, Antibiotics, Model taxa, Genes, SDG-03: Good health and well-being, SDG-15: Life on land

Sustainable Development Goals

SDG-03:Good heatlh and well-being
SDG-15:Life on land

Citation

Wilson, A.M., Coetzee, M.P.A., Wingfield, M.J. & Wingfield, B.D. (2023) Needles in fungal haystacks: Discovery of a putative a-factor pheromone and a unique mating strategy in the Leotiomycetes. PLoS One 18(10): e0292619. https://DOI.org/10.1371/journal.pone.0292619.