WRKY53 negatively regulates rice cold tolerance at the booting stage by fine-tuning anther gibberellin levels

Abstract

Abstract Cold tolerance at the booting (CTB) stage is a major factor limiting rice (Oryza sativa L.) productivity and geographical distribution. A few cold-tolerance genes have been identified, but they either need to be overexpressed to result in CTB or cause yield penalties, limiting their utility for breeding. Here, we characterize the function of the cold-induced transcription factor WRKY53 in rice. The wrky53 mutant displays increased CTB, as determined by higher seed setting. Low temperature is associated with lower gibberellin (GA) contents in anthers in the wild type but not in the wrky53 mutant, which accumulates slightly more GA in its anthers. WRKY53 directly binds to the promoters of GA biosynthesis genes and transcriptionally represses them in anthers. In addition, we uncover a possible mechanism by which GA regulates male fertility: SLENDER RICE1 (SLR1) interacts with and sequesters two critical transcription factors for tapetum development, UNDEVELOPED TAPETUM1 (UDT1), and TAPETUM DEGENERATION RETARDATION (TDR), and GA alleviates the sequestration by SLR1, thus allowing UDT1 and TDR to activate transcription. Finally, knocking out WRKY53 in diverse varieties increases cold tolerance without a yield penalty, leading to a higher yield in rice subjected to cold stress. Together, these findings provide a target for improving CTB in rice.