Domestication-related changes at PvMYB26 reduce pod shattering in common bean and shed light on the origins of agriculture in the Americas

Abstract

Domestication imposed radical selection pressures on plants, transforming them into crops that support global populations today. Here, we investigate the loss of seed dispersal via pod shattering during common bean (Phaseolus vulgaris L.) domestication. We identified PvMYB26 mutations in all three main gene pools of common bean, including an 8 kb deletion in Middle American lines eliminating the gene's transcription start site and promoter; a frameshift/truncation deletion in the independently domesticated Andean population; and another frameshift/truncation insertion in the genetic background of the "undomesticated" debouckii population. Mutants with the 8 kb deletion express PvMYB26 at <1% of the level of wild types and produce 44% less pod lignin. RNA in situ hybridization and fluorescence microscopy show that PvMYB26 is expressed in the lignified fiber layer of pods, while mutants show no visible expression and have a greatly reduced fiber layer. Sequencing of 327 accessions revealed that the mutation is nearly diagnostic for domestication status among Middle American common bean and identified a 125 kb hard selective sweep, indicating the gene's importance in domestication. The main Andean frameshift mutation is found in 84.5% of Andean domesticates but 0% of wild lines, while the debouckii truncation was identified in six domesticated lines of Race Peru, suggesting a third proto-domestication of common bean may have occurred in Ecuador and/or northern Peru. Wild haplotypes most like Middle American domesticates are found in eastern Jalisco, Mexico, strongly suggesting West-Central Mexico as the site of common bean domestication and the rise of agriculture in Middle America.

Keywords: MYB26; Phaseolus vulgaris L.; Plant domestication; crop evolution; fruit dehiscence; population genetics.