The Heat shock factor 20-HSF4-Cellulose synthase A2 module regulates heat stress tolerance in maize

Ze Li; Zerui Li; Yulong Ji; Chunyu Wang; Shufang Wang; Yiting Shi; Jie Le; Mei Zhang

doi:10.1093/plcell/koae106

The Heat shock factor 20-HSF4-Cellulose synthase A2 module regulates heat stress tolerance in maize

Plant Cell. 2024 Apr 4:koae106. doi: 10.1093/plcell/koae106. Online ahead of print.

Authors

Ze Li^{1

2}, Zerui Li^{1

2}, Yulong Ji^{1

2}, Chunyu Wang^{1

2}, Shufang Wang¹, Yiting Shi³, Jie Le^{1

2}, Mei Zhang^{1

2}

Affiliations

¹ Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
² University of Chinese Academy of Sciences, Beijing 100049, China.
³ State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing 100193, China.

PMID: 38573521
DOI: 10.1093/plcell/koae106

Abstract

Temperature shapes the geographical distribution and behavior of plants. Understanding the regulatory mechanisms underlying the plant heat response is important for developing climate-resilient crops, including maize (Zea mays). To identify transcription factors that may contribute to the maize heat response, we generated a dataset of short- and long-term transcriptome changes following a heat treatment time course in the inbred line B73. Co-expression network analysis highlighted several transcription factors, including the class B2a heat shock factor (HSF) ZmHSF20. Zmhsf20 mutant seedlings exhibited enhanced tolerance to heat stress. Furthermore, DNA affinity purification sequencing and Cleavage Under Targets and Tagmentation (CUT&Tag) assays demonstrated that ZmHSF20 binds to the promoters of Cellulose synthase A2 (ZmCesA2) and three class A Hsf genes, including ZmHsf4, repressing their transcription. We showed that ZmCesA2 and ZmHSF4 promote the heat response, with ZmHSF4 directly activating ZmCesA2 transcription. In agreement with the transcriptome analysis, ZmHSF20 inhibited cellulose accumulation and repressed the expression of cell wall-related genes. Importantly, the Zmhsf20 Zmhsf4 double mutant exhibited decreased thermotolerance, placing ZmHsf4 downstream of ZmHsf20. We proposed an expanded model of the heat stress response in maize, whereby ZmHSF20 lowers seedling heat tolerance by repressing ZmHsf4 and ZmCesA2, thus balancing seedling growth and defense.