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Molecular systematics and population genomics of the tree-pathogenic fungus Grosmannia clavigera Massoumi Alamouti, Sepideh

Abstract

Ophiostomatoid fungi increasingly damage forests, but understanding their interactions with vectors and hosts is hampered by uncertainty over the validity of genera, relationships between genera, and species boundaries. To address some of these issues, I first generated a new multigene dataset from 67 taxa that represent the genus Grosmannia and other related genera. The multigene phylogeny resolved the Grosmannia fungi into a clade that was separated from previously intermixed species of the genera Ambrosiella and Raffaelea, and that corresponded to distinct ecological niches and vector associates, i.e. bark versus wood-boring beetles. Second, I generated and used 15 gene genealogies to define species boundaries in G. clavigera. This destructive pine pathogen is vectored by two beetle species: mountain and Jeffrey pine beetles (MPB, JPB). MPB and its fungal associates have expanded into the largest epidemic in western North American history. I identified two phylogenetic species: Gs and Gc. Gc is present in the phylogenetically close Pinus species ponderosa and jeffreyi, which are infested by localized populations of their respective beetles. In contrast, Gs is an exclusive associate of MPB and its primary host P. contorta, although it is found in other pine species in current epidemic regions. These results suggest that host-tree species and beetle population dynamics are important factors in the genetic divergence and diversity of fungal associates in the beetle-tree ecosystems. Finally, we generated new genomic sequences for eleven Gs and Gc strains to further assess evidence for divergence in these fungi as they adapt to different pine species, and to find genes that may be involved in species divergence. Aligning these genome sequences to the reference genome, we identified 103,430 SNPs that supported the Gs and Gc lineages and divided each lineage into two subclades. Genome-wide scans identified truncated genes and potential pseudogenes that differed between Grosmannia lineages, as well as seven genes that show evidence of positive selection. The seven genes are involved in secondary metabolism and in detoxifying host-tree defense chemicals (e.g. polyketide synthases, oxidoreductases), and their variants may reflect adaptation to the specific chemistries of P. contorta, ponderosa, and jeffreyi.

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