College of Chemistry, Chemical Engineering and Resource Utilization, Northeast Forestry University, Harbin 150040, China.
Key Laboratory of Forest Plant Ecology, Ministry of Education, Northeast Forestry University, Harbin 150040, China.
Plant Cell. 2024 Oct 3;36(10):4557-4575. doi: 10.1093/plcell/koae224.
Identifying the essential factors and underlying mechanisms regulating plant heat stress (HS) responses is crucial for mitigating the threat posed by HS on plant growth, development, distribution, and productivity. In this study, we found that the Arabidopsis (Arabidopsis thaliana) super-killer2 (ski2) dicer-like4 (dcl4) mutant, characterized by RNA processing defects and the accumulation of abundant 22-nt small interfering RNAs derived from protein-coding transcripts, displayed significantly increased expression levels of HS-responsive genes and enhanced thermotolerance. These traits primarily resulted from the suppression of SMAX1-LIKE4 (SMXL4) and SMXL5, which encode 2 putative transcriptional regulators that belong to the SMXL protein family. While smxl4 and smxl5 single mutants were similar to wild type, the smxl4 smxl5 double mutant displayed substantially heightened seedling thermotolerance. Further investigation demonstrated that SMXL4 and SMXL5 repressed the transcription of HEAT-SHOCK TRANSCRIPTION FACTOR A2 (HSFA2), encoding a master regulator of thermotolerance, independently of ethylene-response factor-associated amphiphilic repression motifs. Moreover, SMXL4 and SMXL5 interacted with HSFA1d and HSFA1e, central regulators sensing and transducing HS stimuli, and antagonistically affected their transactivation activity. In addition, HSFA2 directly bound to the SMXL4 and SMXL5 promoters, inducing their expression during recovery from HS. Collectively, our findings elucidate the role of the SMXL4/SMXL5-HSFA2 regulatory module in orchestrating plant thermotolerance under HS.
鉴定调控植物热应激（HS）响应的基本因素和潜在机制对于减轻 HS 对植物生长、发育、分布和生产力的威胁至关重要。在这项研究中，我们发现拟南芥（Arabidopsis thaliana）超级杀手 2（ski2）双链 RNA 酶样 4（dcl4）突变体表现出明显增加的 HS 响应基因表达水平和增强的耐热性，其特征是 RNA 加工缺陷和大量源自蛋白质编码转录物的 22nt 小干扰 RNA 的积累。这些特征主要归因于 SMAX1-LIKE4（SMXL4）和 SMXL5 的抑制，它们编码属于 SMXL 蛋白家族的 2 个假定转录调节剂。虽然 smxl4 和 smxl5 单突变体与野生型相似，但 smxl4 smxl5 双突变体表现出明显增强的幼苗耐热性。进一步研究表明，SMXL4 和 SMXL5 独立于乙烯反应因子相关的两亲性抑制基序抑制热休克转录因子 A2（HSFA2）的转录，HSFA2 编码耐热性的主调控因子。此外，SMXL4 和 SMXL5 与 HSFA1d 和 HSFA1e 相互作用，HSFA1d 和 HSFA1e 是感知和转导 HS 刺激的中央调节剂，并拮抗地影响它们的转录激活活性。此外，HSFA2 直接结合到 SMXL4 和 SMXL5 启动子上，在从 HS 恢复期间诱导其表达。总之，我们的研究结果阐明了 SMXL4/SMXL5-HSFA2 调控模块在 HS 下协调植物耐热性的作用。
