J Integr Plant Biol ›› 2025, Vol. 67 ›› Issue (9): 2388-2400.DOI: 10.1111/jipb.13963

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  • 收稿日期:2024-11-19 接受日期:2025-06-06 出版日期:2025-09-01 发布日期:2025-09-02

TaIRE1-mediated unconventional splicing of the TabZIP60 mRNA and the miR172 precursor regulates heat stress tolerance in wheat

Haoran Li1†, Zhen Qin2†, Xiaoli Geng3†, Jie Cao1, Xinyang Yuan1, Huiru Peng1, Yingyin Yao1, Zhaorong Hu1, Weilong Guo1, Yumei Zhang4, Jie Liu1, Vincenzo Rossi5, Ive De Smet6,7, Zhongfu Ni1, Qixin Sun1 and Mingming Xin1*   

  1. 1. Frontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis Utilization (MOE), China Agricultural University, Beijing 100193, China
    2. State Key Laboratory for Crop Stress Resistance and High‐Efficiency Production, College of Agronomy, Northwest A&F University, Yangling, Shaanxi 712100, China
    3. State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China
    4. Qingdao Agricultural University, Qingdao 266109, China
    5. Council for Agricultural Research and Economics, Research Centre for Cereal and Industrial Crops, Bergamo 24126, Italy
    6. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent B‐9052, Belgium
    7. VIB Center for Plant Systems Biology, Ghent B‐9052, Belgium

    †These authors contribute equally to this work.
    *Correspondence: Mingming Xin (mingmingxin@cau.edu.cn)
  • Received:2024-11-19 Accepted:2025-06-06 Online:2025-09-01 Published:2025-09-02
  • Supported by:
    This work was supported by the National Natural Science of China (U22A20471), Sci‐Tech Special Project of Inner Mongolia (NMKJXM202201).

Abstract: 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.

Key words: heat stress tolerance, miR172, TabZIP60, TaIRE1, wheat

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