Loss of cold tolerance is conferred by absence of the WRKY34 promoter fragment during tomato evolution

Natural evolution has resulted in reduced cold tolerance in cultivated tomato (Solanum lycopersicum). Herein, we perform a combined analysis of ATAC-Seq and RNA-Seq in cold-sensitive cultivated tomato and cold-tolerant wild tomato (S. habrochaites). We identify that WRKY34 has the most significant association with differential chromatin accessibility and expression patterns under cold stress. We find that a 60 bp InDel in the WRKY34 promoter causes differences in its transcription and cold tolerance among 376 tomato accessions. This 60 bp fragment contains a GATA cis-regulatory element that binds to SWIBs and GATA29, which synergistically suppress WRKY34 expression under cold stress. Moreover, WRKY34 interferes with the CBF cold response pathway through regulating transcription and protein levels. Our findings emphasize the importance of polymorphisms in cis-regulatory regions and their effects on chromatin structure and gene expression during crop evolution. Cold tolerance has lost during tomato natural evolution. Here, the authors report that absence of a 60 bp promoter fragment in the WRKY34 gene results in loss of cold tolerance in domesticated tomato varieties, and reveal how this natural variation can affect cold tolerance.