Short heat shock factor A2 confers heat sensitivity inArabidopsis: Insights into heat resistance and growth balance

Cells prevent heat damage through a highly conserved canonical heat stress response (HSR) in which heat shock factors (HSFs) bind heat shock elements (HSEs) to activate heat shock proteins (HSPs). Plants generate short HSFs that originate from HSF splicing variants, but little is known about S-HSFs. Although an enhanced canonical HSR confers thermotolerance, its hyperactivation inhibits plant growth. How this process is prevented to ensure proper plant growth has not been determined. Here, we report thatArabidopsisS-HsfA2, S-HsfA4c, and S-HsfB1 confer extreme heat (45°C) sensitivity and represent new kinds of HSF with a unique truncated DNA-binding domain (tDBD) that binds a new heat-regulated element (HRE). The HRE conferred a minimal promoter response to heat and exhibited heat stress sensing and transmission patterns. We used S-HsfA2 to investigate whether and how S-HSFs prevent hyperactivation of the canonical HSR.HSP17.6B,a direct target gene of HsfA2, conferred thermotolerance, but its overexpression caused HSR hyperactivation. We revealed that S-HsfA2 alleviated this hyperactivation in two different ways. 1) S-HsfA2 negatively regulatesHSP17.6B viathe HRE-HRE-like element, thus constructing a noncanonical HSR (S-HsfA2-HRE-HSP17.6B) to antagonistically repress HsfA2-activatedHSP17.6Bexpression. 2) S-HsfA2 binds to the DBD of HsfA2 to prevent HsfA2 from binding to HSEs, eventually attenuating HsfA2-activatedHSP17.6Bpromoter activity. Overall, our findings underscore the biological importance of S-HSFs, namely, preventing plant heat tolerance hyperactivation to maintain proper growth.