MYB transcription factors drive evolutionary innovations in Arabidopsis fruit trichome patterning

Inter and intraspecific diversity has been classically described for the pattern of trichomes in fruits, which is presumably involved in plant adaptation. However, the mechanisms underlying this trait have been hardly addressed. Here we study natural populations of Arabidopsis thaliana showing trichome development in fruits and pedicels, phenotypes previously not described in Arabidopsis species. Genetic analyses indicate that the combination of alleles in three MALAMBRUNO (MAL) epistatic loci is necessary and sufficient to evolve these traits. The isolation of MAL loci reveals regulatory and structural mutations in three genes encoding transcription factors of the core regulatory network for trichome patterning. In addition, these traits and mutations mostly occur in an Iberian relict lineage, where they correlate with climate precipitation. Thus, we show that synergistic modifications of a transcription regulatory circuit, mediated by standing and new mutations, have enabled evolutionary innovations of fruit trichome patterning in A. thaliana.