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Journal of Integrative Agriculture  2025, Vol. 24 Issue (10): 3719-3738    DOI: 10.1016/j.jia.2024.03.011
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Convergent and divergent signaling pathways in C3 rice and C4 foxtail millet crops in response to salt stress

Xinyu Man1*, Sha Tang1*, Yu Meng2*, Yanjia Gong2, Yanqing Chen1, Meng Wu2, Guanqing Jia1, Jun Liu1#, Xianmin Diao1#, Xiliu Cheng1#

1 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China

2 Hebei Agricultural University, Baoding 071001, China

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摘要  
盐胁迫是全球农业生产的制约因素。因此,利用耐盐植物已成为当前的研究热点。C4植物的耐盐性进化更频繁。然而,很少有研究探索C4作物谷子耐盐性的分子基础。在这项研究中,我们对盐胁迫下C3作物水稻和C4模式作物谷子进行转录组学和生理生化实验多重分析。我们的研究结果表明,在盐胁迫下,与C3作物水稻相比,C4作物谷子中脱落酸合成代谢加快,同时细胞分裂素的生物合成和信号传导受到抑制。盐胁迫加快C3水稻光合作用相关基因的快速下调以及净光合速率严重降低。在盐胁迫中,C3水稻和C4谷子中一些应激反应转录因子(TF),如AP2/ERF、WRKY和MYB变化显著。基于加权基因共表达网络分析(WGCNA),一个AP2/ERF转录因子- SiRSR1(Seita.3G044600)被鉴定为盐胁迫反应的关键调控因子。为了证实其功能,我们在水稻中通过CRISPR/Cas9基因编辑技术构建的OsRSR1敲除系,并在谷子中构建其上游抑制因子SiMIR172a过表达转基因植物(172a-OE),两者耐盐性均提高。总的来说,我们的研究不仅为谷子和水稻对盐胁迫反应的趋同调节提供了新的见解,而且揭示了它们对盐胁迫的不同信号网络。


Abstract  

Salt stress is a global constraint on agricultural production.  Therefore, the development of salt tolerant plants has become a current research hotspot.  While salt tolerance has evolved more frequently in C4 grass lineages, few studies have explored the molecular bases underlying salt stress tolerance in the C4 crop foxtail millet.  In this study, we used a multi-pronged approach spanning the omics analyses of transcriptomes and physiological analysis of the C3 crop rice and the C4 model crop foxtail millet to investigate their responses to salt stress.  The results revealed that compared to C3 rice, C4 foxtail millet has upregulated abscisic acid (ABA) and notably reduced CK biosynthesis and signaling transduction under salt stress.  Salt stress in C3 rice plants triggered rapid downregulation of photosynthesis related genes, which was coupled with severely reduced net photosynthetic rates.  In the salt-treated C3 rice and C4 foxtail millet, some stress responsive transcription factors (TFs), such as AP2/ERF, WRKY and MYB, underwent strong and distinct transcriptional changes.  Based on a weighted gene co-expression network analysis (WGCNA), the AP2/ERF transcription factor Rice Starch Regulator1 SiRSR1 (Seita.3G044600) was identified as a key regulator of the salt stress response.  To confirm its function, we generated OsRSR1-knockout lines using CRISPR/Cas9 genome editing in rice and its upstream repressor SimiR172a-overexpressing (172a-OE) transgenic plants in foxtail millet, which both showed increased salt tolerance.  Overall, this study not only provides new insights into the convergent regulation of the salt stress responses of foxtail millet and rice, but it also sheds light on the divergent signaling networks between them in response to salt stress

Keywords:  C3        C4        phytohormone        photosynthesis        transcriptional regulatory network        RSR1  
Received: 30 October 2023   Online: 02 March 2024   Accepted: 23 February 2024
Fund: This study was supported by the National Natural Science Foundation of China (32241042), the National Key R&D Program of China (2019YFD1000700 and 2019YFD1000703) and the Biological Breeding-National Science and Technology Major Project, China (2022ZD04017).

About author:  Xinyu Man, E-mail: shanying420@163.com; Sha Tang, E-mail: tangsha@caas.cn; Yu Meng, E-mail: my131sohu@126.com; #Correspondence Jun Liu, E-mail: liujun@caas.cn; Xianmin Diao, E-mail: diaoxianmin@caas.cn; Xiliu Cheng, E-mail: chengxiliu@caas.cn * These authors contributed equally to this study.

Cite this article: 

Xinyu Man, Sha Tang, Yu Meng, Yanjia Gong, Yanqing Chen, Meng Wu, Guanqing Jia, Jun Liu, Xianmin Diao, Xiliu Cheng. 2025. Convergent and divergent signaling pathways in C3 rice and C4 foxtail millet crops in response to salt stress. Journal of Integrative Agriculture, 24(10): 3719-3738.

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