State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences and School of Advanced Agricultural Sciences, Peking University, Beijing 100871, China.
Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China.
Plant Cell. 2021 Jul 2;33(5):1506-1529. doi: 10.1093/plcell/koab060.
Light-dependent seed germination is a vital process for many seed plants. A decisive event in light-induced germination is degradation of the central repressor PHYTOCHROME INTERACTING FACTOR 1 (PIF1). The balance between gibberellic acid (GA) and abscisic acid (ABA) helps to control germination. However, the cellular mechanisms linking PIF1 turnover to hormonal balancing remain elusive. Here, employing far-red light-induced Arabidopsis thaliana seed germination as the experimental system, we identified PLANTACYANIN (PCY) as an inhibitor of germination. It is a blue copper protein associated with the vacuole that is both highly expressed in mature seeds and rapidly silenced during germination. Molecular analyses showed that PIF1 binds to the miR408 promoter and represses miR408 accumulation. This in turn posttranscriptionally modulates PCY abundance, forming the PIF1-miR408-PCY repression cascade for translating PIF1 turnover to PCY turnover during early germination. Genetic analysis, RNA-sequencing, and hormone quantification revealed that PCY is necessary and sufficient to maintain the PIF1-mediated seed transcriptome and the low-GA-high-ABA state. Furthermore, we found that PCY domain organization and regulation by miR408 are conserved features in seed plants. These results revealed a cellular mechanism whereby PIF1-relayed external light signals are converted through PCY turnover to internal hormonal profiles for controlling seed germination.
光依赖性种子萌发是许多种子植物的重要过程。光诱导萌发的一个决定性事件是降解中央抑制剂 PHYTOCHROME INTERACTING FACTOR 1（PIF1）。赤霉素（GA）和脱落酸（ABA）之间的平衡有助于控制萌发。然而，将 PIF1 周转与激素平衡联系起来的细胞机制仍然难以捉摸。在这里，我们以远红光诱导的拟南芥种子萌发为实验系统，鉴定出 PLANTACYANIN（PCY）是一种抑制萌发的物质。它是一种与液泡相关的蓝色铜蛋白，在成熟种子中高度表达，并在萌发过程中迅速沉默。分子分析表明，PIF1 结合 miR408 启动子并抑制 miR408 的积累。这反过来又在后转录水平上调节 PCY 的丰度，形成 PIF1-miR408-PCY 抑制级联，将 PIF1 周转转化为早期萌发过程中的 PCY 周转。遗传分析、RNA-seq 和激素定量分析表明，PCY 是维持 PIF1 介导的种子转录组和低 GA-高 ABA 状态所必需的。此外，我们发现 PCY 结构域组织和 miR408 的调节是种子植物的保守特征。这些结果揭示了一种细胞机制，通过该机制，PIF1 传递的外部光信号通过 PCY 周转转化为内部激素图谱，从而控制种子萌发。
