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

Submergence stress tolerance is a complex trait governed by multiple loci. Because of its wide distribution across arid and humid regions, Arabidopsis thaliana offers an opportunity to explore the genetic components and their action mechanisms underlying plant adaptation to submergence stress. In this study, using map-based cloning we identified WRKY22 that activates RAP2.12, a locus previously identified to contribute to the submergence stress response, to regulate plant humid adaptation possibly through ethylene signal transduction in Arabidopsis. WRKY22 expression is inhibited by ARABIDOPSIS RESPONSE REGULATORs (ARRs) but activated by the WRKY70 transcription factor. In accessions from humid environments, a two-nucleotide deletion in the WRKY22 promoter region prevents binding of phosphorylated ARRs, thereby maintaining its high expression. Loss of the ARR-binding element in the WRKY22 promoter underwent strong positive selection during colonization of A. thaliana in the humid Yangtze River basin. However, the WRKY70-binding motif in the WRKY22 promoter shows no variation between accessions from humid and arid regions. These findings together establish a novel signaling axis wherein WRKY22 plays a key role in regulating the adaptive response that enables A. thaliana to colonize contrasting habitats. Notably, we further showed functional conservation of this locus in Brassica napus, suggesting that modulating this axis might be useful in the breeding of flood-tolerant crop varieties.