A distinct foliar pigmentation pattern formed by activator-repressor gradients upstream of an anthocyanin-activating R2R3-MYB

The emergence of novel traits is often preceded by a potentiation phase, when all the genetic components necessary for producing the trait are assembled. However, elucidating these potentiating factors is challenging. We have previously shown that an anthocyanin-activating R2R3-MYB, STRIPY, triggers the emergence of a distinct foliar pigmentation pattern in the monkeyflower Mimulus verbenaceus. Here, using forward and reverse genetics approaches, we identify three potentiating factors that pattern STRIPY expression: MvHY5, a master regulator of light signaling that activates STRIPY and is expressed throughout the leaf, and two leaf developmental regulators, MvALOG1 and MvTCP5, that are expressed in opposing gradients along the leaf proximodistal axis and negatively regulate STRIPY. These results provide strong empirical evidence that phenotypic novelties can be potentiated through incorporation into preexisting genetic regulatory networks and highlight the importance of positional information in patterning the novel foliar stripe. [Display omitted] •STRIPY is an activator of anthocyanin biosynthesis in a distinct mediolateral leaf stripe•Three leaf developmental regulators form a pre-pattern that determines STRIPY expression•MvHY5 activates STRIPY and is expressed throughout the leaf•MvALOG1 and MvTCP5 negatively regulate STRIPY and are expressed in opposing gradients Determining how novel phenotypes originate is a central question in evolution. LaFountain et al. use forward and reverse genetics approaches to identify three leaf developmental regulators that are co-opted to pattern a distinct foliar anthocyanin stripe in the monkeyflower species Mimulus verbenaceus.