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Journal of Integrative Agriculture
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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 Agricultural University of Hebei, Baoding 071001China

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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C3作物水稻相比,C4作物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谷子一些应激反应转录因子(TF),如AP2/ERFWRKYMYB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- SiRSR1Seita.3G044600)被鉴定为盐胁迫反应的关键调因子。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. Salt tolerance evolves more frequently in C4 grass lineages.  However, few studies have been carried out to explore the molecular bases underlying salt stress tolerance in C4 crop foxtail millet.  In this study, we performed a multi-pronged approach spanning the omics analyses of transcriptomes and physiological analysis of C3 crop rice and C4 model crop foxtail millet in response to salt stress.  Our results revealed specifically compared to C3 rice, C4 foxtail millet has upregulated 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 by severely decreased net photosynthetic rates.  In the salt-threatened 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 weighted gene co-expression network analysis (WGCNA), an AP2/ERF transcription factor Rice Starch Regulator1 SiRSR1 (Seita.3G044600) was identified as a key regulator of salt stress response.  To confirmed its function, we generated OsRSR1-knockout lines with CRISPR/Cas9 genome editing in rice and its upstream repressor SiMIR172a-overexpressing (172a-OE) transgenic plants in foxtail millet, which increased salt tolerance.  Overall, our study not only provided new insights into the convergent regulation of salt stress responses of foxtail millet and rice, but also shed light on the divergent signaling networks between them in response to salt stress.
Keywords:  C3              C4                    phytohormone                    photosynthesis                    transcriptional regulatory network                    RSR1  
Online: 25 March 2024  
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 work.

Cite this article: 

Xinyu Man, Sha Tang, Yu Meng, Yanjia Gong, Yanqing Chen, Meng Wu, Guanqing Jia, Jun Liu, Xianmin Diao, Xiliu Cheng. 2024. Convergent and divergent signaling pathways in C3 rice and C4 foxtail millet crops in response to salt stress. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.03.011

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