Selection processes in simple sequence repeats suggest a correlation with their genomic location: insights from a fungal model system

Paolo Gonthier, Fabiano Sillo, Elisa Lagostina, Angela Roccotelli, Olga Santa Cacciola, Jan Stenlid, Matteo Garbelotto

Adaptive processes shape the evolution of genomes and the diverse functions of different genomic regions are likely to have an impact on the trajectory and outcome of this evolution. The main underlying hypothesis of this study is that the evolution of Simple Sequence Repeats (SSRs) is correlated with the evolution of the genomic region in which they are located, resulting in differences of motif size, number of repeats, and levels of polymorphisms. These differences should be clearly detectable when analyzing the frequency and type of SSRs within the genome of a species, when studying populations within a species, and when comparing closely related sister taxa. By coupling a genome-wide SSR survey in the genome of the plant pathogenic fungus Heterobasidion irregulare with an analysis of intra- and interspecific variability of 39 SSR markers in five populations of the two sibling species H. irregulare and H. annosum, we investigated mechanisms of evolution of SSRs. Results showed a clear dominance of trirepeats and a selection against other repeat number, i.e. di- and tetranucleotides, both in regions inside Open Reading Frames (ORFs) and upstream 5' untranslated region (5'UTR). Locus per locus AMOVA showed SSRs both inside ORFs and upstream 5'UTR were more conserved within species compared to SSRs in other genomic regions, suggesting their evolution is constrained by the functions of the regions they are in. Principal coordinates analysis (PCoA) indicated that even if SSRs inside ORFs were less polymorphic than those in intergenic regions, they were more powerful in differentiating species. These findings indicate SSRs evolution undergoes a directional selection pressure comparable to that of the ORFs they interrupt and to that of regions involved in regulatory functions. Our work linked the variation and the type of SSRs with regions upstream 5'UTR, putatively harbouring regulatory elements, and shows that the evolution of SSRs might be affected by their location in the genome. Additionally, this study provides a first glimpse on a possible molecular basis for fast adaptation to the environment mediated by SSRs.