Light regulates stomatal development by modulating paracrine signaling from inner tissues

Shenqi Wang,Rini Rahiman,Yuan Kai Yeo,Xin Yang,On Sun Lau,Grace Sheen Yee Lee,Zimin Zhou

doi:10.1038/s41467-021-23728-2

Shenqi Wang, Rini Rahiman + Show 5 more

Open Access

https://doi.org/10.1038/s41467-021-23728-2

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Abstract

Developmental outcomes are shaped by the interplay between intrinsic and external factors. The production of stomata—essential pores for gas exchange in plants—is extremely plastic and offers an excellent system to study this interplay at the cell lineage level. For plants, light is a key external cue, and it promotes stomatal development and the accumulation of the master stomatal regulator SPEECHLESS (SPCH). However, how light signals are relayed to influence SPCH remains unknown. Here, we show that the light-regulated transcription factor ELONGATED HYPOCOTYL 5 (HY5), a critical regulator for photomorphogenic growth, is present in inner mesophyll cells and directly binds and activates STOMAGEN. STOMAGEN, the mesophyll-derived secreted peptide, in turn stabilizes SPCH in the epidermis, leading to enhanced stomatal production. Our work identifies a molecular link between light signaling and stomatal development that spans two tissue layers and highlights how an environmental signaling factor may coordinate growth across tissue types.

Highlights

Developmental outcomes are shaped by the interplay between intrinsic and external factors
To investigate the role of HYPOCOTYL 5 (HY5) in light-regulated stomatal development, we carried out a detailed analysis of stomatal production in Arabidopsis with varying HY5 levels under a series of light intensities
These results suggest a positive role of HY5 in promoting stomatal development under the light

Summary

Introduction

Developmental outcomes are shaped by the interplay between intrinsic and external factors. We show that the light-regulated transcription factor ELONGATED HYPOCOTYL 5 (HY5), a critical regulator for photomorphogenic growth, is present in inner mesophyll cells and directly binds and activates STOMAGEN. The bZIP transcription factor ELONGATED HYPOCOTYL 5 (HY5), a central component in light signal transduction, plays a prominent role in promoting photomorphogenic growth[23,24]. In the dark, it is targeted by the ubiquitin E3 ligase, CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1), for degradation, and inactivation of COP1 by light-induced photoreceptors leads to the accumulation of HY5 under light[25,26]. How light signals are linked to SPCH and dynamically induce stomatal production remain unresolved

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