Cao Yiming, Zhang Jiaxin, Zhao Zhong, Tang Guiliang, Yan Jun
School of Life Sciences, East China Normal University, Shanghai 200241, China.
CAS Center for Excellence in Molecular Plant Sciences, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230027, China.
Plant Cell. 2025 Jun 4;37(6). doi: 10.1093/plcell/koaf092.
Plants have evolved a complex regulatory network to cope with heat stress (HS), which includes microRNAs (miRNAs). However, the roles of the entire miRNA biogenesis machinery in HS responses remain unclear. Here, we show that HS induces the majority of miRNAs primarily through the enhanced nuclear localization of HYPONASTIC LEAVES 1 (HYL1), rather than by upregulating MIR gene transcription in Arabidopsis (Arabidopsis thaliana). Disruption of miRNA biogenesis increases plant susceptibility to HS. We also demonstrate that HYL1 phosphorylation modulates its nuclear localization during HS, which is critical for miRNA induction and thermotolerance. MAP KINASE3 (MPK3) phosphorylates and stabilizes the phosphatase C-TERMINAL DOMAIN PHOSPHATASE-LIKE 1 (CPL1), while CPL1 inhibits MPK3 activity, creating a feedback loop that regulates HYL1 phosphorylation. Disruption of MPK3 function results in increased nuclear HYL1 levels and miRNA production, conferring enhanced HS tolerance to mpk3 mutants. These findings reveal a mechanism by which plants enhance miRNA biogenesis during HS, offering insights into the regulatory networks that govern plant thermotolerance.
植物已经进化出一个复杂的调控网络来应对热胁迫（HS），其中包括 microRNA（miRNA）。然而，整个 miRNA 生物合成机制在热胁迫响应中的作用仍不清楚。在这里，我们表明热胁迫主要通过增强拟南芥中 HYPONASTIC LEAVES 1（HYL1）的核定位来诱导大多数 miRNA，而不是通过上调 MIR 基因转录。miRNA 生物合成的破坏会增加植物对热胁迫的敏感性。我们还证明，HYL1 磷酸化在热胁迫期间调节其核定位，这对 miRNA 诱导和耐热性至关重要。丝裂原活化蛋白激酶 3（MPK3）磷酸化并稳定磷酸酶 C 末端结构域磷酸酶样 1（CPL1），而 CPL1 抑制 MPK3 活性，形成一个调节 HYL1 磷酸化的反馈环。MPK3 功能的破坏导致核 HYL1 水平和 miRNA 产生增加，赋予 mpk3 突变体增强的热胁迫耐受性。这些发现揭示了植物在热胁迫期间增强 miRNA 生物合成的机制，为控制植物耐热性的调控网络提供了见解。
