Mitochondrial VOLTAGE-DEPENDENT ANION CHANNEL 3 regulates stomatal closure by abscisic acid signaling

Haixia Qin, Wenqi Yang, Zile Liu, Yi Ouyang, Xiao Wang, Haiyang Duan, Bing Zhao, Shujie Wang, Junli Zhang, Yuankai Chang, Kun Jiang, Ke Yu and Xuebin Zhang
Henan University, Kaifeng 475004, China

In Arabidopsis, stomatal closure mediated by abscisic acid (ABA) is redundantly controlled by ABA receptors and subclass III SnRK2s. Among those, the roles of PYR1, PYL2 and SnRK2.6 are more prominent. A recent discovery shows that ABA-induced accumulation of reactive oxygen species (ROS) in mitochondria could promote stomatal closure. By analyzing stomatal movements in an array of single and higher order mutants, we revealed that a mitochondrial protein VDAC3 jointly regulates ABA-mediated stomatal closure with ABA receptors and SnRK2s, by affecting cellular and mitochondrial ROS accumulation. VDAC3 interacts with nine out of fourteen ABA receptors and all three subclass III SnRK2s. Single mutation in VDAC3, ABA receptors (except PYR1 and PYL2) or SnRK2.2/2.3 had little effect on ABA-mediated stomatal closure. However, knocking out PYR1, PYL1/2/4/8 or SnRK2.2/2.3 in vdac3 resulted in significantly delayed or attenuated ABA-mediated stomatal closure, despite the presence of other ABA receptors or SnRK2s conferring redundant functions. We found that cellular and mitochondrial accumulation of ROS induced by ABA was altered in vdac3pyl1. Moreover, supplement of H2O2 restored ABA-induced stomatal closure in mutants with decreased stomatal sensitivity to ABA. Our work uncovers that VDAC3 ensures redundant control of ABA-mediated stomatal closure by canonical ABA signaling components.