Adaptive protein evolution through length variation in short tandem repeats

Abstract

Intrinsically disordered protein regions are of high importance for temperature sensing and immune responses in plants. Tracts of identical amino acids accumulate in these regions and can vary in length over generations due to expansions and retractions of short tandem repeats at the genomic level. However, little attention has been paid to what extent length variation is shaped by natural selection. By environmental association analysis on 2,514 length variable tracts in 770 whole-genome sequenced wild Arabidopsis thaliana we show that length variation in glutamine and asparagine amino acid homopolymers, as well as in interaction hotspots, correlate with local bio-climatic habitat. We determined experimentally that the promoter activity of a light-stress gene depended on polyglutamine length variants in a disordered transcription factor. Our results show that length variations impact protein function and are substantially shaped by natural selection. Length variants modulating protein function at a global genomic scale has implications for understanding protein evolution and eco-evolutionary biology.