Dephosphorylation of bZIP59 by PP2A ensures appropriate shade avoidance response in Arabidopsis

Changes in light quality and quantity experienced by many shade-intolerant plants grown in close proximity lead to transcriptional reprogramming and shade avoidance syndrome (SAS). Despite the importance of phosphorylation-dependent signaling in cellular physiology, phosphorylation events during SAS are largely unknown. Here, we examined shade-regulated phosphorylation events in Arabidopsis using quantitative phosphoproteomics. We confirmed shade-induced dephosphorylation of bZIP59, a basic region/leucine zipper motif (bZIP) transcription factor. Shade treatment promotes the nuclear localization of bZIP59, which can be mimicked by mutation of the phosphorylation sites on bZIP59. Phenotypic analysis identified that bZIP59 negatively regulated shade-induced hypocotyl elongation. bZIP59 repressed the shade-induced activation of certain growth-related genes, while shade increased the DNA binding of bZIP59. Furthermore, the protein phosphatase 2A (PP2A) mediated de-phosphorylation of bZIP59. Our study characterized a previously unidentified mechanism by which the phyB-PP2A-bZIP59 regulatory module integrates shade signals and transcriptomes, broadening our knowledge of phosphorylation strategies for rapid adaptation to shade.

许多密植的不耐阴植物所经历的光质与光量变化，会诱发转录重编程与避荫综合征（shade avoidance syndrome, SAS）。尽管依赖磷酸化的信号转导在细胞生理过程中至关重要，但避荫过程中的磷酸化事件迄今仍鲜有报道。本研究借助定量磷酸化蛋白质组学，分析了拟南芥中受遮荫调控的磷酸化事件。我们验证了遮荫诱导的碱性亮氨酸拉链（basic region/leucine zipper motif, bZIP）转录因子bZIP59的去磷酸化过程。遮荫处理可促进bZIP59的核定位，该效应可通过突变bZIP59的磷酸化位点进行模拟。表型分析结果显示，bZIP59负调控遮荫诱导的下胚轴伸长。bZIP59可抑制部分生长相关基因的遮荫诱导激活，而遮荫则会增强bZIP59的DNA结合能力。此外，蛋白磷酸酶2A（protein phosphatase 2A, PP2A）介导了bZIP59的去磷酸化过程。本研究阐明了一种此前未被揭示的调控机制：phyB-PP2A-bZIP59调控模块可整合遮荫信号与转录组，拓宽了我们对植物快速适应遮荫的磷酸化调控策略的认知。