Two alternatively spliced variants of ZmHSF12 regulate the balance of plant growth and heat tolerance in maize and Arabidopsis.

Heat shock factors (HSFs) are pivotal in regulating plant heat tolerance; however, the mechanisms HSFs employ in regulating transcription to maintain a balance of plant growth and heat tolerance are poorly understood. This study reports that two maize HSF12 knockout lines are more sensitive to heat stress. ZmHSF12 encodes two alternative spliced transcripts: ZmHSF12-1 and ZmHSF12-2; overexpression of ZmHSF12-2 enhances, whereas overexpression of ZmHSF12-1 decreases plant heat tolerance, indicating the distinct functions of these two transcripts in plant heat stress response. In addition, ZmHSF12-2 upregulates RAFFINOSE SYNTHASE (ZmRAFS) and CYTOKININ OXIDASE (ZmCKO2) gene expression, controlling raffinose and cytokinin concentration in the cell, enhancing plant heat tolerance and inhibiting plant growth. ZmHSF12-1 interacts with ZmHSF12-2 and represses the transcriptional regulation of ZmHSF12-2 on ZmCKO2 and ZmRAFS. Co-overexpression of ZmHSF12-1 and ZmHSF12-2 in Arabidopsis not only improved the heat tolerance of plants but also compensated for the growth defect phenotype of ZmHSF12-2 overexpressing Arabidopsis plants. These findings deepen our understanding of plant heat tolerance and significantly impact the scientific community. They support the potential application of co-overexpressing ZmHSF12-1 and ZmHSF12-2 to improve crop heat tolerance without causing growth retardation and yield compensation, thereby offering a promising avenue for crop improvement.