High nucleotide substitution rates associated with retrotransposon proliferation drive dynamic secretome evolution in smut pathogens

Abstract

Transposable elements (TEs) play a pivotal role in shaping diversity in eukaryotic genomes. The covered smut pathogen on barley, Ustilago hordei, encountered a recent genome expansion. Using long reads, we assembled genomes of 6 U. hordei strains and 3 sister species, to study this genome expansion. We found that larger genome sizes can mainly be attributed to long terminal repeat retrotransposons (LTR-RTs) of the Copia and Gypsy superfamilies. From the studied smuts, LTR-RTs proliferated the most recently and to the furthest extent in the U. hordei genome, in which they make up for 19.5% of the genome. Interestingly, the extent of TE proliferation in different smut species is positively correlated to the mating-type locus size, which is largest in U. hordei with up to ~560 kb. TE transposition within the mating-type loci and their flanking regions are mating-type specific, which is likely due to the very low recombination activity in this region. Furthermore, LTR-RT proliferation was found to be associated with higher nucleotide substitution levels, as genes in genome regions that are rich in dynamic LTR-RTs display higher nucleotide substitution levels. The high nucleotide substitution rate particularly affected the evolution of genes encoding secreted proteins as substitutions more frequently led to amino acid alterations. The mechanism behind this increase in nucleotide substitution rate remains elusive, but seems not to be a consequence of the repeat-induced point mutation (RIP) mechanism, as genes and LTR-RTs did not display typical RIP substitutions.