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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.

SUBMITTER: Yuan Z

PROVIDER: S-EPMC9038928 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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

Yuan Zhilin Z Wu Qi Q Xu Liangxiong L Druzhinina Irina S IS Stukenbrock Eva H EH Nieuwenhuis Bart P S BPS Zhong Zhenhui Z Liu Zhong-Jian ZJ Wang Xinyu X Cai Feng F Kubicek Christian P CP Shan Xiaoliang X Wang Jieyu J Shi Guohui G Peng Long L Martin Francis M FM

The ISME journal 20211216 5

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 l ...[more]

PMID: 34916613

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Project description:Geographically separated populations can convergently adapt to the same selection pressure. Convergent evolution at the level of a gene may arise via three distinct modes. The selected alleles can (1) have multiple independent mutational origins, (2) be shared due to shared ancestral standing variation, or (3) spread throughout subpopulations via gene flow. We present a model-based, statistical approach that utilizes genomic data to detect cases of convergent adaptation at the genetic level, identify the loci involved and distinguish among these modes. To understand the impact of convergent positive selection on neutral diversity at linked loci, we make use of the fact that hitchhiking can be modeled as an increase in the variance in neutral allele frequencies around a selected site within a population. We build on coalescent theory to show how shared hitchhiking events between subpopulations act to increase covariance in allele frequencies between subpopulations at loci near the selected site, and extend this theory under different models of migration and selection on the same standing variation. We incorporate this hitchhiking effect into a multivariate normal model of allele frequencies that also accounts for population structure. Based on this theory, we present a composite-likelihood-based approach that utilizes genomic data to identify loci involved in convergence, and distinguishes among alternate modes of convergent adaptation. We illustrate our method on genome-wide polymorphism data from two distinct cases of convergent adaptation. First, we investigate the adaptation for copper toxicity tolerance in two populations of the common yellow monkey flower, Mimulus guttatus We show that selection has occurred on an allele that has been standing in these populations prior to the onset of copper mining in this region. Lastly, we apply our method to data from four populations of the killifish, Fundulus heteroclitus, that show very rapid convergent adaptation for tolerance to industrial pollutants. Here, we identify a single locus at which both independent mutation events and selection on an allele shared via gene flow, either slightly before or during selection, play a role in adaptation across the species' range.

Project description:In our study, we aimed to explore the genomic and phenotypic traits of Priestia megaterium strain B1, which was isolated from root material of healthy apple plants, to adapt to the endophytic lifestyle and promote plant growth. We identified putative genes encoding proteins involved in chemotaxis, flagella biosynthesis, biofilm formation, secretory systems, detoxification, transporters, and transcription regulation. Furthermore, B1 exhibited both swarming and swimming motilities, along with biofilm formation. Both genomic and physiological analyses revealed the potential of B1 to promote plant growth through the production of indole-3-acetic acid and siderophores, as well as the solubilization of phosphate and zinc. To deduce potential genomic features associated with endophytism across members of P. megaterium strains, we conducted a comparative genomic analysis involving 27 and 31 genomes of strains recovered from plant and soil habitats, respectively, in addition to our strain B1. Our results indicated a closed pan genome and comparable genome size of strains from both habitats, suggesting a facultative host association and adaptive lifestyle to both habitats. Additionally, we performed a sparse Partial Least Squares Discriminant Analysis to infer the most discriminative functional features of the two habitats based on Pfam annotation. Despite the distinctive clustering of both groups, functional enrichment analysis revealed no significant enrichment of any Pfam domain in both habitats. Furthermore, when assessing genetic elements related to adaptation to endophytism in each individual strain, we observed their widespread presence among strains from both habitats. Moreover, all members displayed potential genetic elements for promoting plant growth.IMPORTANCEBoth genomic and phenotypic analyses yielded valuable insights into the capacity of P. megaterium B1 to adapt to the plant niche and enhance its growth. The comparative genomic analysis revealed that P. megaterium members, whether derived from soil or plant sources, possess the essential genetic machinery for interacting with plants and enhancing their growth. The conservation of these traits across various strains of this species extends its potential application as a bio-stimulant in diverse environments. This significance also applies to strain B1, particularly regarding its application to enhance the growth of plants facing apple replant disease conditions.

Dataset Information

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

Publications

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

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