Bioengineering for robust tolerance against cold and drought stresses via co-overexpressing three Cu-miRNAs in major food crops

• Published in: Cell reports (Cambridge) 2024-10, Vol.43 (10), p.114828, Article 114828
• Main Authors: Hong, Zheyuan, Xu, Hang, Shen, Yuxin, Liu, Chuanjia, Guo, Fu, Muhammad, Sajid, Zhang, Yaqi, Niu, Hongbin, Li, Shengping, Zhou, Weijun, Wu, Liang
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Bioengineering - methods; cold stress; Cold Temperature; Copper - metabolism; CP: Plants; crop improvement; Crops, Agricultural - genetics; drought; Droughts; flavonoid; Gene Expression Regulation, Plant; laccase; Laccase - genetics; Laccase - metabolism; lignin; maize; MicroRNAs - genetics; MicroRNAs - metabolism; miRNA; Oryza - genetics; Oryza - growth & development; Plants, Genetically Modified; rice; Stress, Physiological - genetics; wheat; Zea mays - genetics; Zea mays - metabolism
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2024.114828

Environmental stresses threaten global food security by reducing major crop productivity. MicroRNAs (miRNAs), a class of small non-coding RNAs, function as master regulators of gene expression in plants. In this study, we co-overexpressed three copper-miRNAs (miR397, miR408, and miR528) in three major food crops (referred to as 3miR-OE), which simultaneously silenced several target laccase genes, resulting in reduced lignin contents but increased flavonoid metabolites. Importantly, we observed that, compared to wild-type and single miRNA overexpression lines, the 3miR-OE transgenic Japonica and Indica rice exhibited significantly enhanced tolerance against cold and drought stresses throughout the growth period. In addition, 3miR-OE transgenic maize and wheat also exhibited robust resistance to cold and water-deficit conditions, suggesting that co-overexpressing three Cu-miRNAs is a powerful tool for improving resilience to abiotic stresses across diverse crops. Altogether, we have developed a bioengineering strategy to maintain crop growth and yield under unfavorable environmental conditions. [Display omitted] •Several LAC genes are targeted by miR397, miR408, and miR528•Co-overexpression of three Cu-miRNAs modifies lignin biosynthesis and flavonoid metabolites•Cu-miRNA co-overexpression endows major food crops with tolerance to cold and drought stress•Simultaneous manipulation of miRNAs is a potential approach to improve crop agronomic traits Hong et al. demonstrate that co-overexpression of three Cu-miRNAs in rice, wheat, and maize alters lignin and flavonoid content and enhances cold- and drought stress tolerance. They develop a strategy to maintain crop growth and yield under unfavorable environmental conditions that could address escalating crop demand due to climate change.