Autophagy controls reactive oxygen species homeostasis in guard cells that is essential for stomatal opening
Autophagy controls reactive oxygen species homeostasis in guard cells that is essential for stomatal opening
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DOI：
10.1073/pnas.1910886116
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发表时间：
2019-09
期刊：
影响因子：
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通讯作者：
S. Yamauchi;S. Mano;Kazusato Oikawa;Kazumi Hikino;Kosuke M. Teshima;Y. Kimori;M. Nishimura;K. Shimazaki;A. Takemiya
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文献类型：
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作者：
S. Yamauchi;S. Mano;Kazusato Oikawa;Kazumi Hikino;Kosuke M. Teshima;Y. Kimori;M. Nishimura;K. Shimazaki;A. Takemiya
意义 活性氧 (ROS) 是关键的信号分子，在调节气孔运动以应对应激条件方面发挥着重要作用。然而，气孔保卫细胞中基础细胞ROS水平如何调节尚不清楚。我们的结果表明，自噬通过消除氧化的过氧化物酶体来维持ROS稳态，从而优化光合作用二氧化碳固定和植物生长的气孔开放。这项研究为保卫细胞中ROS稳态的调节机制以及植物过氧化物酶体特异性自噬（即pexophagy）的生理意义提供了见解。活性氧（ROS）作为关键信号分子，抑制气孔开放并促进气孔关闭，以应对不同的环境胁迫。然而，保卫细胞如何维持基础细胞内ROS水平尚不清楚。本研究旨在确定自噬在维持保卫细胞基础 ROS 水平中的作用。我们分离出了拟南芥自噬相关 2 (atg2) 突变体，该突变体在响应光和低 CO2 浓度时气孔开放受损。其他自噬基因（包括 ATG5、ATG7、ATG10 和 ATG12）的破坏也会导致类似的气孔缺陷。 atg 突变体在保卫细胞中持续积累高水平的 ROS，抗坏血酸和谷胱甘肽等抗氧化剂可挽救 ROS 积累和气孔开放。此外，atg 突变增加了保卫细胞中过氧化物酶体的数量和聚集，并且使用过氧化物酶体靶向 H2O2 传感器 HyPer 观察到，这些过氧化物酶体表现出 ROS 清除剂过氧化氢酶活性降低和过氧化氢 (H2O2) 升高。此外，使用2-羟基-3-丁酸（一种产生过氧化物酶体H2O2的乙醇酸氧化酶的抑制剂）可以减少ROS的积累。我们的结果表明，自噬通过消除氧化的过氧化物酶体来控制保卫细胞 ROS 稳态，从而允许气孔打开。
Significance Reactive oxygen species (ROS) are key signaling molecules that play an important role in the regulation of stomatal movements in response to stress conditions. However, how basal cellular ROS levels are regulated in stomatal guard cells is not yet known. Our results revealed that autophagy maintains ROS homeostasis by eliminating oxidized peroxisomes, which allows the optimization of stomatal opening for photosynthetic CO2 fixation and plant growth. This study provides insights on regulatory mechanisms of ROS homeostasis in guard cells and the physiological significance of plant peroxisome-specific autophagy, that is, pexophagy. Reactive oxygen species (ROS) function as key signaling molecules to inhibit stomatal opening and promote stomatal closure in response to diverse environmental stresses. However, how guard cells maintain basal intracellular ROS levels is not yet known. This study aimed to determine the role of autophagy in the maintenance of basal ROS levels in guard cells. We isolated the Arabidopsis autophagy-related 2 (atg2) mutant, which is impaired in stomatal opening in response to light and low CO2 concentrations. Disruption of other autophagy genes, including ATG5, ATG7, ATG10, and ATG12, also caused similar stomatal defects. The atg mutants constitutively accumulated high levels of ROS in guard cells, and antioxidants such as ascorbate and glutathione rescued ROS accumulation and stomatal opening. Furthermore, the atg mutations increased the number and aggregation of peroxisomes in guard cells, and these peroxisomes exhibited reduced activity of the ROS scavenger catalase and elevated hydrogen peroxide (H2O2) as visualized using the peroxisome-targeted H2O2 sensor HyPer. Moreover, such ROS accumulation decreased by the application of 2-hydroxy-3-butynoate, an inhibitor of peroxisomal H2O2-producing glycolate oxidase. Our results showed that autophagy controls guard cell ROS homeostasis by eliminating oxidized peroxisomes, thereby allowing stomatal opening.