Genomic landscape of a relict fir-associated fungus reveals rapid convergent adaptation towards endophytism

Abstract

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.

Additions to the Knowledge of the Genus Pezicula (Dermateaceae, Helotiales, Ascomycota) in China

“…The strain VDBF-2 isolated from Vaccinium dunalianum in Yunnan Province showed strong antagonistic effects against plant pathogens and wood-decaying fungi [ 30 ]. Based on comparative and pan-genomic analyses of the endophytic P. neosporulosa , an example of convergent genomic adaptation to endophytism was revealed, mostly determined by enzymes involved in carbohydrate metabolism and secondary metabolite biosynthesis [ 53 ].…”

Changes of endophytic microbial community in Rhododendron simsii roots under heat stress and its correlation with leaf physiological indicators

“…Pezicula ericae in the genus of Pezicula is considered one of the Ericoid mycorrhizal fungi that can obtain N and phosphorus from complex organic matter to meet its own growth needs, as well as to transfer nutrients to the plant to promote its growth and development and to resist stress ( Walker et al, 2011 ). Another species of this genus, Pezicula neosporulosa, is involved in the metabolism of carbohydrates and the synthesis of enzymes that affect the secondary metabolites of plant and can provide nutrients to plant ( Yuan et al, 2022 ). In addition, fungi within genus Acidothermus have been shown to hydrolyze insoluble digestible cellulose and produce soluble products, that can use trifluoroacetic acid to hydrolyze their products into monosaccharides ( Liu, N. et al, 2022 ).…”