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

TL;DR

This study reveals how the MUTE gene helps form specialized cells around stomata in Crassulaceae succulents, using a new model species.

Contribution

The paper identifies MUTE's novel role in driving asymmetric divisions to create stomatal subsidiary cells in Crassulaceae.

Findings

MUTE facilitates asymmetric divisions to form three anisocytic subsidiary cells in Crassulaceae stomata.

Kalanchoë laxiflora is established as a model for studying succulent stomatal development.

MUTE's function in Crassulaceae contrasts with its role in Arabidopsis but aligns with its function in grasses.

Abstract

Among the evolutionary innovations of many succulents is a photosynthetic lifestyle, where stomatal gas exchange is decoupled from light-dependent carbon fixation. Many Crassulaceae leaf succulents form a stomatal morphotype consisting of kidney-shaped guard cells surrounded by three anisocytic subsidiary cells (SCs), whose function and development remained unknown. Here, we established Kalanchoë laxiflora as a developmental model. Potassium staining suggested SCs to shuttle osmolytes and support turgor-driven stomatal movements. Gene editing, reporter lines, protein overexpression, and RNA sequencing implicated the stomatal transcription factor MUTE in facilitating the additional rounds of asymmetric divisions required to form SCs in succulents. This is opposite to the role of MUTE in Arabidopsis thaliana, where it stops rather than induces asymmetric divisions but reminiscent of MUTE’s subsidiary cell–related function in grasses. Our work firmly establishes K. laxiflora as a model for succulent development and deciphers an intricate genetic mechanism that generates innovative stomatal morphology in Crassulaceae succulents.

Crassulaceae MUTE guides asymmetric divisions to form stomatal subsidiary cells in succulents.

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