Li Haoran, Qin Zhen, Geng Xiaoli, Cao Jie, Yuan Xinyang, Peng Huiru, Yao Yingyin, Hu Zhaorong, Guo Weilong, Zhang Yumei, Liu Jie, Rossi Vincenzo, De Smet Ive, Ni Zhongfu, Sun Qixin, Xin Mingming
Frontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis Utilization (MOE), China Agricultural University, Beijing, 100193, China.
State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, College of Agronomy, Northwest A&F University, Yangling, 712100, Shaanxi, China.
J Integr Plant Biol. 2025 Sep;67(9):2388-2400. doi: 10.1111/jipb.13963. Epub 2025 Jul 3.
INOSITOL-REQUIRING ENZYME 1 (IRE1) is conserved in plants and mammals to regulate stress responses. Here, we found that TaIRE1 is involved in the unconventional splicing of cell membrane-localized TabZIP60 messenger RNA (mRNA), which results in a nucleus resident protein form (TabZIP60s), and enhanced heat stress tolerance. Transcriptome analysis together with binding element prediction revealed 121 high-confidence targets of TabZIP60s responsive to heat stress in wheat (Triticum aestivum), including heat shock protein genes. Interestingly, we found that an asparagine to glutamic acid substitution, located next to DNA-binding domain of TabZIP60s, results in reduced binding affinity and transcriptional activity to downstream targets, and this heat stress tolerance inferior allele was positively selected during modern wheat breeding programs in China, possibly due to their negative effects on yield potential. Finally, we showed that TaIRE1 is also responsible for the mis-cleavage of miR172 precursors, and consequently contribute to heat stress tolerance. To the best of our knowledge, this represents the first report showing that, like in mammals, IRE1 also regulates miRNA cleavage in response to heat stress in plants. Together, this coordinate control of two signaling pathways provides new insights into heat stress tolerance regulation in wheat.
肌醇需求酶1（IRE1）在植物和哺乳动物中保守存在以调节应激反应。在此，我们发现TaIRE1参与细胞膜定位的TabZIP60信使核糖核酸（mRNA）的非常规剪接，这导致一种定位于细胞核的蛋白形式（TabZIP60s），并增强了热胁迫耐受性。转录组分析结合结合元件预测揭示了小麦（Triticum aestivum）中121个对热胁迫有反应的TabZIP60s的高可信度靶标，包括热休克蛋白基因。有趣的是，我们发现位于TabZIP60s DNA结合结构域旁边的天冬酰胺到谷氨酸的替换导致对下游靶标的结合亲和力和转录活性降低，并且这种热胁迫耐受性较差的等位基因在中国现代小麦育种计划中被正向选择，这可能是由于它们对产量潜力有负面影响。最后，我们表明TaIRE1也负责miR172前体的错误切割，从而有助于热胁迫耐受性。据我们所知，这是第一份表明，与哺乳动物一样，IRE1也在植物中调节响应热胁迫的miRNA切割的报告。总之，这两种信号通路的协同控制为小麦热胁迫耐受性调控提供了新见解。
