Transcriptional Profiling Reveals a Time-of-Day-Specific Role of REVEILLE 4/8 in Regulating the First Wave of Heat Shock-Induced Gene Expression in Arabidopsis

• Published in: The Plant cell 2019-10, Vol.31 (10), p.2353-2369
• Main Authors: Li, Bingjie, Gao, Zhihua, Liu, Xinye, Sun, Daye, Tang, Wenqiang
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Circadian Clocks - genetics; Circadian Clocks - physiology; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Gene Expression Regulation, Plant - genetics; Gene Ontology; Heat Shock Transcription Factors - genetics; Heat Shock Transcription Factors - metabolism; Heat-Shock Response - genetics; Heat-Shock Response - physiology; Hot Temperature; Large-Scale Biology; Promoter Regions, Genetic; Protein Binding - genetics; RNA-Seq; Signal Transduction - genetics; Stress, Physiological - genetics; Thermotolerance - genetics; Thermotolerance - physiology; Transcription Factors - genetics; Transcription Factors - metabolism; Transcriptional Activation - genetics; Transcriptional Activation - physiology
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1105/tpc.19.00519

Although much is known about plant responses to heat shock (HS), how plants sense high temperature and the primary HS signal transduction pathway leading to HS-regulated gene expression are still poorly understood. To identify primary transcription factors that mediate HS-regulated gene expression and their target genes, RNA sequencing was performed to detect genes whose expression is rapidly altered by HS in Arabidopsis ( ). The results showed several genes were induced after only 5 min of HS treatment, suggesting that HS signaling occurs very rapidly. Analysis of the -elements in the promoters of genes upregulated by 10 min of HS treatment identified HEAT SHOCK FACTOR A1s (HSFA1s) and circadian clock proteins REVEILLE4 (RVE4) and RVE8 as essential transcription factors that independently mediate early HS-induced gene expression. Using and mutants, we identified subsets of HSFA1s- or RVE4/8-dependent early HS-induced genes and showed RVE4/8 regulate plant thermotolerance partially by regulating the expression of downstream transcription factors ( ) and , specifically around noon. These findings reveal a potential transcriptional regulatory hierarchy governing the first wave of HS-induced gene expression. They also provided important insight into the mechanism by which the circadian clock gates thermotolerance and prepares plants for exposure to high temperatures during the day.