MUTE drives asymmetric divisions to form stomatal subsidiary cells in Crassulaceae succulents

Abstract

Amongst the evolutionary innovations of many succulents is a photosynthetic lifestyle, where stomatal gas exchange is decoupled from light-dependent carbon fixation. Stomatal complexes in the emerging succulent modelKalanchoë laxifloraconsist of two guard cells surrounded by three anisocytic subsidiary cells (SCs). Here, we show that these SCs shuttle ions and thus likely support stomatal movements. Furthermore, gene editing, reporter lines and protein overexpression implicate the stomatal transcription factor MUTE in facilitating additional rounds of asymmetric divisions that form SCs in succulents. This is opposite to the role of MUTE inArabidopsis thaliana, where it stops rather than induces asymmetric divisions, but reminiscent of MUTE’s SC-related function in grasses. Together, our work deciphers an intricate genetic mechanism that generates innovative stomatal morphology in Crassulaceae succulents.