Copy number variation introduced by a massive mobile element underpins global thermal adaptation in a fungal wheat pathogen

Abstract

Copy number variation (CNV) can drive rapid evolution in changing environments. In microbial pathogens, such adaptation is a key factor underpinning epidemics and colonization of new niches. However, the genomic determinants of such adaptation remain poorly understood. Here, we systematically investigate CNVs in one of the largest to date genome sequencing dataset spanning a worldwide collection of 1109 genomes from the major wheat pathogenZymoseptoria tritici. We found overall strong purifying selection acting on most CNVs. Genomic defense mechanisms likely accelerated gene loss over episodes of continental colonization. Local adaptation along climatic gradients was facilitated by CNVs affecting secondary metabolite production and gene loss in general. One of the strongest candidates for climatic adaptation is a highly conserved gene of the NAD-dependent Sirtuin family. The Sirtuin CNV locus localizes to an ~68-kb Starship mobile element unique to the species carrying genes highly expressed during plant infection. The element has likely lost the ability to transpose, demonstrating how the ongoing domestication of cargo-carrying selfish elements can contribute to selectable variation within populations. Our work highlights how standing variation in gene copy numbers at the global scale is a major factor driving climatic and metabolic adaptation in microbial species.

Evolutionary genomics reveals variation in structure and genetic content implicated in virulence and lifestyle in the genusGaeumannomyces

“…Recently the Starship superfamily was identified as specific to and widespread in ascomycetes and, aside from the characteristic ‘captain’ tyrosine recombinase gene, each Starship contains a highly variable cargo (Gluck-Thaler et al 2022). Mobilisation of cargo genes by Starships has been linked to the acquisition of various adaptive traits in fungal species, such as metal resistance (Urquhart et al 2022), formaldehyde resistance (Urquhart et al 2023a), virulence (McDonald et al 2019), climatic adaptation (Tralamazza et al 2023) and lifestyle switching (Gluck-Thaler et al 2022). However, Starships are not inherently beneficial to the fungal host.…”

Systematic identification of cargo-mobilizing genetic elements reveals new dimensions of eukaryotic diversity

“…Mobile element density is also typically negatively correlated with meiotic recombination rates ( 88 ). Fungal lineages with highly active RIP machinery and high recombination rates may therefore be less suitable hosts for larger CMEs ( 89 , 90 ). Finally, differences in Starship distributions may be explained through stochastic processes that underlie element emergence, expansion and contraction.…”

Systematic identification of cargo-carrying genetic elements reveals new dimensions of eukaryotic diversity

“…Mobile element density is also typically negatively correlated with meiotic recombination rates (84) . Fungal lineages with highly active RIP machinery and high recombination rates may therefore be less suitable hosts for larger CCEs (85,86) . Finally, differences in Starship distributions may be explained through stochastic processes that underlie element emergence, expansion and contraction.…”