Light regulates chlorophyll homeostasis and photosynthesis via various molecular mechanisms in plants. The light regulation of transcription and protein stability of nuclear-encoded chloroplast proteins have been extensively studied, but how light regulation of mRNA metabolism affects abundance of nuclear-encoded chloroplast proteins and chlorophyll homeostasis remains poorly understood. Here we show that the blue light receptor cryptochrome 2 (CRY2) and the METTL16-type m⁶A writer FIONA1 (FIO1) regulate chlorophyll homeostasis in response to blue light. In contrast to the CRY2-mediated photo-condensation of the mRNA adenosine methylase (MTA), photoexcited CRY2 co-condenses FIO1 only in the presence of the CRY2-signalling protein SUPPRESSOR of PHYTOCHROME A (SPA1). CRY2 and SPA1 synergistically or additively activate the RNA methyltransferase activity of FIO1 in vitro, whereas CRY2 and FIO1, but not MTA, are required for the light-induced methylation and translation of the mRNAs encoding multiple chlorophyll homeostasis regulators in vivo. Our study demonstrates that the light-induced liquid–liquid phase separation of the photoreceptor/writer complexes is commonly involved in the regulation of photoresponsive changes of mRNA methylation, whereas the different photo-condensation mechanisms of the CRY/FIO1 and CRY/MTA complexes explain, at least partially, the writer-specific functions in plant photomorphogenesis.

光通过植物中的各种分子机制调节叶绿素稳态和光合作用。核编码的叶绿体蛋白的转录和蛋白质稳定性的光调节已被广泛研究，但 mRNA 代谢的光调节如何影响核编码的叶绿体蛋白的丰度和叶绿素稳态仍然知之甚少。在这里，我们表明蓝光受体隐花色素 2 （CRY2） 和 METTL16 型 m⁶A 写入器 FIONA1 （FIO1） 响应蓝光调节叶绿素稳态。与 CRY2 介导的 mRNA 腺苷甲基化酶 （MTA） 的光浓缩相反，光激发的 CRY2 仅在植物色素 A （SPA1） 的 CRY2 信号蛋白抑制因子存在下共冷凝 FIO1。CRY2 和 SPA1 在体外协同或相加激活 FIO1 的 RNA 甲基转移酶活性，而 CRY2 和 FIO1 而不是 MTA，是体内编码多个叶绿素稳态调节因子的 mRNA 的光诱导甲基化和翻译所必需的。我们的研究表明，光感受器/写入器复合物的光诱导液-液相分离通常参与 mRNA 甲基化光响应性变化的调节，而 CRY/FIO1 和 CRY/MTA 复合物的不同光冷凝机制至少部分解释了植物光形态发生中的写入器特异性功能。