Environment and HSP90 modulate MAPK stomatal developmental pathway

Abstract

Stomatal ontogenesis is a key element of plant adaptation aiming to control photosynthetic efficiency and water management under fluctuating environments 1,2,3. Development of stomata is guided by endogenous and environmental cues and is tightly coupled to overall plant growth 1,2,3. YODA signaling pathway is essential to stomatal lineage specification4,5,6 since it regulates the activities of transcription factors such as SPEECHLESS (SPCH)7,8,9,10. Heat-shock proteins 90 (HSP90s) are evolutionarily conserved molecular chaperones implicated in a broad range of signalling pathways being integrated in interaction networks with client proteins11,12,13,14. Herein, based on genetic, molecular, biochemical, and cell biological evidence we report that heat-stress conditions affect phosphorylation and deactivation of SPCH and modulate stomatal density. We show that genetic and physical interactions between HSP90s and YODA control stomatal patterning, distribution and morphology. We provide solid evidence that HSP90s play a major role in transducing the heat-stress response since they act upstream and downstream of YODA signalling, regulate the activity and nucleocytoplasmic distribution of MAPKs, and the activation of SPCH. Thus, HSPs control the stomatal development both under normal temperature and acute heat-stress conditions. Our results demonstrate that HSP90s couple stomatal formation and patterning to environmental cues providing an adaptive mechanism of heat-stress tolerance response and stomatal formation in Arabidopsis.