Loss of a glutaredoxin gene underlies parallel evolution of trichome pattern in Antirrhinum

Abstract

Most angiosperms produce trichomes--epidermal hairs that have protective or more specialised roles. In almost all species trichomes are multicellular and, in the majority, secretory. Despite the importance of multicellular trichomes for plant protection and as a source of high-value products, little is known about the mechanisms that control their development. Here we use natural variation between Antirrhinum (snapdragon) species to examine how trichome distribution is regulated and has evolved. We show that a single gene, Hairy (H), which is needed to repress trichome fate, underlies variation in trichome distribution patterns between all Antirrhinum species except one. H encodes an epidermis-specific glutaredoxin and trichome distribution within individual plants reflects the location of H expression. Gene phylogenies and functional tests suggest that H gained its trichome-repressing role late in eudicot evolution and that Antirrhinum species with widespread trichomes evolved multiple times from a largely bald ancestor though independent losses of H activity. We also find evidence for an evolutionary reversal involving a suppressor mutation, and for a pleiotropic effect of H that might constrain the evolution of trichome patterns.