The calcium transporter ANNEXIN1 mediates cold-induced calcium signaling and freezing tolerance in plants

The transient elevation of cytosolic free calcium concentration ([Ca2+]cyt) induced by cold stress is a well-established phenomenon; however, the underlying mechanism remains elusive. Here, we report that the Ca2+-permeable transporter ANNEXIN1 (AtANN1) mediates cold-triggered Ca2+ influx and freezing tolerance in Arabidopsis thaliana. The loss of function of AtANN1 substantially impaired freezing tolerance, reducing the cold-induced [Ca2+]cyt increase and upregulation of the cold-responsive CBF and COR genes. Further analysis showed that the OST1/SnRK2.6 kinase interacted with and phosphorylated AtANN1, which consequently enhanced its Ca2+ transport activity, thereby potentiating Ca2+ signaling. Consistent with these results and freezing sensitivity of ost1 mutants, the cold-induced [Ca2+]cyt elevation in the ost1-3 mutant was reduced. Genetic analysis indicated that AtANN1 acts downstream of OST1 in responses to cold stress. Our data thus uncover a cascade linking OST1-AtANN1 to cold-induced Ca2+ signal generation, which activates the cold response and consequently enhances freezing tolerance in Arabidopsis.

冷胁迫诱导的胞质游离钙离子浓度（[Ca²⁺]cyt）瞬时升高是公认的生物学现象，但其潜在机制仍尚不明确。本研究报道，拟南芥（Arabidopsis thaliana）钙离子通透转运蛋白膜联蛋白1（AtANN1）可介导冷触发的钙内流与抗冻性。AtANN1功能缺失会显著削弱植株的抗冻性，降低冷诱导的[Ca²⁺]cyt升高以及冷响应CBF和COR基因的上调水平。进一步分析显示，OST1/SnRK2.6激酶可与AtANN1相互作用并对其进行磷酸化，从而增强AtANN1的钙离子转运活性，进而强化钙信号通路。与上述研究结果及ost1突变体的冷敏感性一致，ost1-3突变体中冷诱导的[Ca²⁺]cyt升高同样被显著削弱。遗传分析表明，AtANN1在冷胁迫应答过程中作用于OST1的下游。综上，本研究揭示了一条将OST1-AtANN1与冷诱导钙信号生成相连的级联通路，该通路可激活冷响应过程，最终提升拟南芥的抗冻性。