Comparative and pan-genomic analyses of the endophytic fungus Pezicula neosporulosa (Helotiales, Ascomycota) from needles of the relict fir, Abies beshanzuensis, showed expansions of carbohydrate metabolism and secondary metabolite biosynthetic genes characteristic for unrelated plant-beneficial helotialean, such as dark septate endophytes and ericoid mycorrhizal fungi. The current species within the relatively young Pliocene genus Pezicula are predominantly saprotrophic, while P. neosporulosa lacks such features. To understand the genomic background of this putatively convergent evolution, we performed population analyses of 77 P. neosporulosa isolates. This revealed a mosaic structure of a dozen non-recombining and highly genetically polymorphic subpopulations with a unique mating system structure. We found that one idiomorph of a probably duplicated mat1-2 gene was found in putatively heterothallic isolates, while the other co-occurred with mat1-1 locus suggesting homothallic reproduction for these strains. Moreover, 24 and 81 genes implicated in plant cell-wall degradation and secondary metabolite biosynthesis, respectively, showed signatures of the balancing selection. These findings highlight the evolutionary pattern of the two gene families for allowing the fungus a rapid adaptation towards endophytism and facilitating diverse symbiotic interactions.
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M44 genomic data are available at the NCBI (BioProject number PRJNA517416, BioSample number SAMN10830013). This Whole Genome Sequencing (WGS) Project has been deposited at DDBJ/ENA/GenBank under the accession number SELE00000000. The raw genome resequencing data obtained have been deposited at the NCBI in the Short Read Archive database under the accession numbers SRR8568788-SRR8568862. Raw VCF files (SNP and indel variants) are available via Data Dryad (https://doi.org/10.5061/dryad.zs7h44j6x). The alignment and ML tree of mat1-2-1 were deposited in TreeBase (http://purl.org/phylo/treebase/phylows/study/TB2:S27214).
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Research in Yuan’s lab is financially supported by the Fundamental Research Funds for the Central Non-profit Research of the Chinese Academy of Forestry (CAFYBB2019ZA001-3) and the National Natural Science Foundation of China (No. 31722014 and 31772032). Research in Martin’s lab is supported by the Laboratory of Excellence ARBRE (ANR-11-LABX-0002-01) and the Beijing Advanced Innovation Center for Tree Breeding by Molecular Design. We extend our sincere gratitude to Dr. Primrose Boynton (Wheaton College, USA) and Dr. Fengyan Bai (State Key Laboratory of Mycology, Chinese Academy of Sciences) for useful discussions. We thank Dr Yougui Wu (Fengyangshan-Baishanzu National Nature Reserve, China) for providing basic information about the wild relict fir trees.
The authors declare no competing interests.
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Yuan, Z., Wu, Q., Xu, L. et al. Genomic landscape of a relict fir-associated fungus reveals rapid convergent adaptation towards endophytism. ISME J 16, 1294–1305 (2022). https://doi.org/10.1038/s41396-021-01176-6