Brassinosteroid-signaling kinase 4 activates mitogen-activated protein kinase 4 to enhance cold stress tolerance in maize.

The Plant Cell Pub Date : 2025-09-30 DOI:10.1093/plcell/koaf234

Chen Zhang,Guangdong Li,Yitian Pan,Qian Li,Yadan Miao,Yang Xiang,Aying Zhang

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Abstract

Cold stress limits the growth, development and yield of maize (Zea mays L.). Mitogen-activated protein kinases (MAPKs) play important roles in response to cold stress. However, besides the canonical MAPK cascades, it is unclear whether other kinases directly activate MAPKs under cold stress. Here, we identified brassinosteroid-signaling kinase 4 (ZmBSK4) as an upstream kinase of ZmMAPK4 in regulating cold tolerance. Functional analysis demonstrated that ZmMAPK4 and ZmBSK4 positively regulate cold tolerance in maize. ZmBSK4 directly interacts with and phosphorylates ZmMAPK4 at Ser-171. This Ser-171 phosphorylation augments ZmMAPK4 kinase activity and improves maize cold tolerance. Furthermore, we identified two ZmMAPK4-interacting substrates: the two basic helix-loop-helix (bHLH) transcription factors ZmbHLH111 and ZmbHLH181. ZmMAPK4 phosphorylates ZmbHLH111 and ZmbHLH181. Ser-171 phosphorylation enhances ZmMAPK4-mediated phosphorylation of ZmbHLH111 and ZmbHLH181, which promotes their transcriptional activity. Then, ZmbHLH111 and ZmbHLH181 induce the expression of the cold-responsive genes Zea mays dehydration response element binding protein1.2/1.4/1.9/1.10 (ZmDREB1.2/1.4/1.9/1.10), thereby enhancing cold tolerance in maize. Taken together, ZmBSK4 phosphorylating ZmMAPK4 at Ser-171 enhances ZmMAPK4-mediated phosphorylation of ZmbHLH111 and ZmbHLH181, which promotes their activity, ultimately triggering the expression of the cold-responsive ZmDREB1 genes and enhancing maize cold tolerance. Our results reveal a non-canonical MAPK regulatory mechanism for enhancing cold tolerance in maize.

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油菜素类固醇信号激酶4激活丝裂原活化蛋白激酶4，增强玉米的冷胁迫耐受性。

冷胁迫限制了玉米的生长发育和产量。丝裂原活化蛋白激酶（MAPKs）在低温胁迫反应中起重要作用。然而，除了典型的MAPK级联反应外，尚不清楚是否有其他激酶在冷胁迫下直接激活MAPK。在这里，我们确定了油菜素类固醇信号激酶4 （ZmBSK4）是ZmMAPK4的上游激酶，参与调节耐寒性。功能分析表明，ZmMAPK4和ZmBSK4正调控玉米的耐寒性。ZmBSK4直接与ZmMAPK4相互作用并磷酸化Ser-171位点。Ser-171磷酸化增强了ZmMAPK4激酶活性，提高了玉米的耐寒性。此外，我们鉴定了两个与zmmapk4相互作用的底物：两个基本的螺旋-环-螺旋（bHLH）转录因子ZmbHLH111和ZmbHLH181。ZmMAPK4磷酸化ZmbHLH111和ZmbHLH181。Ser-171磷酸化增强了zmmapk4介导的ZmbHLH111和ZmbHLH181的磷酸化，从而促进了它们的转录活性。然后，ZmbHLH111和ZmbHLH181诱导玉米脱水反应元件结合蛋白1.2/1.4/1.9/1.10 （ZmDREB1.2/1.4/1.9/1.10）基因的表达，从而增强玉米的耐寒性。综上所述，ZmBSK4磷酸化ZmMAPK4 Ser-171位点可以增强ZmMAPK4介导的ZmbHLH111和ZmbHLH181的磷酸化，从而促进它们的活性，最终触发ZmDREB1基因的表达，增强玉米的耐寒性。我们的研究结果揭示了一个非规范的MAPK调控机制，以增强玉米的耐寒性。

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The Plant Cell

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