YODA-HSP90 module regulates phosphorylation-dependent inactivation of SPEECHLESS to control stomatal development under acute heat stress in Arabidopsis

First author: Despina Samakovli; Affiliations: Palacky University Olomouc (帕拉斯基大学): Olomouc, Czech

Corresponding author: Despina Samakovli

Stomatal ontogenesis, patterning, and function are hallmarks of environmental plant adaptation, especially to conditions limiting plant growth such as elevated temperatures and reduced water availability. The specification and distribution of a stomatal cell lineage and its terminal differentiation to guard cells requires a master regulatory protein phosphorylation cascade initiated by the YODA mitogen-activated protein kinase kinase kinase. YODA signaling results in the activation of MITOGEN-ACTIVATED PROTEIN KINASEs (MPK3 and MPK6), which confer regulation of transcription factors including SPEECHLESS (SPCH). Herein, we report that acute heat stress affects the phosphorylation and deactivation of SPCH and modulates stomatal density. By using complementary molecular, genetic, biochemical and cell biology approaches we provide solid evidence that HEAT SHOCK PROTEINS 90 (HSP90) play a crucial role in transducing heat-stress response through YODA cascade. Genetic studies revealed that YODA and HSP90.1 are epistatic, and they likely function linearly in the same developmental pathway regulating stomata formation. HSP90s interact with YODA, affect its cellular polarization, and modulate the phosphorylation of downstream targets, like MPK6 and SPCH, under both normal and heat-stress conditions. Thus, HSP90-mediated specification and differentiation of stomatal cell lineage couples stomatal development to environmental cues providing an adaptive mechanism to plant heat-stress response.

气孔的器官发生、模式建成以及功能是植物对于环境适应的标志，尤其是对于植物生长不适的环境，比如说温度的升高或是可利用水的减少。气孔细胞系的特化和分布以及最终分化为保卫细胞需要一个由YODA丝裂原激活的蛋白激酶激酶激酶起始的主调控蛋白磷酸化级联。YODA信号转导会导致丝裂原活化的蛋白激酶MPK3和MPK6的激活，从而赋予了包括SPCH在内的转录因子的调控。通过利用互补的分子、遗传、生化和细胞生物学试验，作者发现热激蛋白HSP90在YODA级联介导的植物热应激反应传导过程中发挥关键作用。遗传学研究显示YODA和HSP90.1存在上位性效应，并且可能线性作用于同一个发育通路上，从而调控气孔的形成。HSP90在正常或热胁迫条件下都能够与YODA互作，影响其在细胞水平的极性定位，调控下游包括MPK6和SPCH在内的靶标的磷酸化。因此，HSP90介导的气孔细胞系的特化和分化将气孔发育与环境条件联系到一起，为植物热激响应的适应性机制提供了一条途径。

doi: https://doi.org/10.1016/j.molp.2020.01.001

Journal: Molecular Plant

Published date: January 10, 2020