Allelic variation in the promoter of WRKY22 enhances humid adaptation of Arabidopsis thaliana

• Published in: Molecular plant 2024-11
• Main Authors: Liang, Ruyun, Tan, Luna, Guo, Xiang, Lou, Shangling, Dan, Xuming, Han, Yu, Zeng, Cheng, Zhang, Han, Yang, Kai, Chen, Liyang, Liang, Xin, Liu, Meng, Guo, Mengyun, Yin, Kangqun, Tang, Si, Song, Yan, Gao, Xuemeng, Gu, Shaobo, Hou, Jing, Yao, Yingjun, Zhang, Ruijia, Yan, Jin, Fu, Wensen, Li, Xuerui, Hu, Yongqi, Liu, Yao, Liu, Wei, Wu, Qiusai, Yan, Zhen, Jia, Weitao, Hu, Binhua, Wang, Jing, Liu, Jianquan, Liu, Huanhuan
• Format: Article
• Language: English
• Subjects: ARRs; Natural variation; RAP2.12; submergence tolerance; WRKY22; WRKY70
• ISSN: 1674-2052; 1752-9867; 1752-9867
• DOI: 10.1016/j.molp.2024.11.013

Submergence tolerance is a complex trait governed by multiple genetic loci. Arabidopsis thaliana, widely distributed from arid to humid regions, offers an opportunity to explore the underlying genetic components and their interactive mechanisms. In this study, we utilized map-based cloning techniques to identify the WRKY22 genetic locus, which activates RAP2.12, a locus identified previously, possibly through ethylene signal transduction. WRKY22 expression is inhibited by ARRs but activated by the WRKY70 transcription factors. The cooperative interaction between these regulators enhances A. thaliana’s ability to adapt more effectively to contrasting habitats. A two-nucleotide deletion in the WRKY22 promoter region prevents its inhibition by phosphorylated ARRs, maintaining its high expression in humid accessions. This WRKY22 allele without ARRs binding element underwent strong natural selection during the southeastern colonization of A. thaliana to the humid Yangtze River basin. However, the WRKY70-activated WT box in the WRKY22 promoter region shows no variation between humid and arid accessions. These findings together establish one previously unreported molecular module composed by multiple regulators, with WRKY22 playing a key role in the ecological shift of A. thaliana. Expanding upon the identified locus, we overexpressed BnaC2.WRKY22 in Brassica napus and successfully achieved a significant improvement in submergence tolerance, highlighting a functional conservatism of this gene across related species. This further demonstrates the potential for transferring knowledge from model plants to crops for the breeding of flood-tolerant crop varieties. Our study revealed a two-nucleotide TA deletion allele of WRKY22 that facilitates adaptation to humid environments in Arabidopsis thaliana. This TA deletion allele of WRKY22 underwent strong natural selection, blocking ARRs’ inhibition and enabling WRKY70 to effectively activate WRKY22, thereby conferring submergence tolerance. Overexpressing BnaC2.WRKY22 also enhances submergence tolerance in Brassica napus, suggesting its potential for breeding flood-tolerant crops.