Tissue-specific accumulation of pH-sensing phosphatidic acid determines plant stress tolerance

First author: Wenyu Li; Affiliations: Nanjing Agricultural University (南京农业大学): Nanjing, China

Corresponding author: Wenhua Zhang

The signalling lipid phosphatidic acid (PA; 脂质磷脂酸) is involved in regulating various fundamental biological processes in plants. However, the mechanisms of PA action remain poorly understood because currently available methods for monitoring PA fail to determine the precise spatio-temporal dynamics of this messenger in living cells and tissues of plants. Here, we have developed PAleon, a PA-specific optogenetic biosensor (光遗传学生物传感器) that reports the concentration and dynamics of bioactive PA at the plasma membrane based on Förster resonance energy transfer (FRET; 荧光共振能量转移). PAleon was sensitive enough to monitor physiological concentrations of PA in living cells and to visualize PA dynamics at subcellular resolution in tissues when they were challenged with abscisic acid (ABA) and salt stress. PAleon bioimaging revealed kinetics and tissue specificity of salt stress-triggered PA accumulation. Compared with wild-type Arabidopsis, the pldα1 mutant lacking phospholipase Dα1 (PLDα1) for PA generation showed delayed and reduced PA accumulation. Comparative analysis of wild type and pldα1 mutant indicated that cellular pH-modulated PA interaction with target proteins and PLD/PA-mediated salt tolerance. Application of the PA biosensor PAleon uncovered specific spatio-temporal PA dynamics in plant tissues. Our findings suggest that PA signalling integrates with cellular pH dynamics to mediate plant response to salt stress.

信号脂质磷脂酸PA参与了植物中多个基础的生物学进程。然而，由于目前的技术不够成熟，不能精确定量该信号分子在植物活细胞和组织中的时空动态，因此我们对于该信号分子的作用分子机制还不是很了解。本文中，作者开发了一个叫做PAleon的PA特异性光遗传学生物传感器，能够基于荧光共振能量转移精确报道质膜上活性PA的浓度和动态波动。PAleon十分敏感，足以检测活细胞中的PA生理浓度，并且能够在脱落酸ABA或盐胁迫处理的组织中在亚细胞层面可视化PA的波动。PAleon生物成像揭示了盐胁迫诱导的PA积累的动力学与组织特异性。与野生型拟南芥相比，pldα1突变体缺失了用于生成PA的磷脂酶Dα1，因此突变体表现出PA的积累延迟并减少。野生型与pldα1突变体的比较分析显示细胞内pH调节PA与靶蛋白的互作以及PLD/PA介导的盐耐受性。本文作用通过利用PA生物感应器PAleon发现了植物组织中特异性的PA时空动态波动。本文的研究说明PA信号转导整合细胞内的pH动态介导植物对于盐胁迫的响应。

通讯：章文华（http://dangan.njau.edu.cn/info/1024/1136.htm)

个人简介：1983-1987年，南京农业大学，学士；1987-1990年，南京农业大学，硕士；1998-2001年，南京农业大学，博士；2001-2004年，美国堪萨斯州立大学，博士后。

研究方向：1. 盐、低温、干旱和病害诱导的基因克隆、表达，及其功能和调节，作物抗逆性分子遗传改良与调控；2. 磷脂和胞内信使转导逆境信号的细胞和分子生物学机理；3. 花粉萌发、花粉管伸长的分子基础，植物的育性研究；4. 作物油脂组分、耐储的品质改良。

doi: https://doi.org/10.1038/s41477-019-0497-6

Journal: Nature Plants

Published date: August 26, 2019