Transcriptional Regulators of Plant Adaptation to Heat Stress

Abstract

Heat stress (HS) is becoming an increasingly large problem for food security as global warming progresses. As sessile species, plants have evolved different mechanisms to cope with the disruption of cellular homeostasis, which can impede plant growth and development. Here, we summarize the mechanisms underlying transcriptional regulation mediated by transcription factors, epigenetic regulators, and regulatory RNAs in response to HS. Additionally, cellular activities for adaptation to HS are discussed, including maintenance of protein homeostasis through protein quality control machinery, and autophagy, as well as the regulation of ROS homeostasis via a ROS-scavenging system. Plant cells harmoniously regulate their activities to adapt to unfavorable environments. Lastly, we will discuss perspectives on future studies for improving urban agriculture by increasing crop resilience to HS.

Keywords: ROS homeostasis; epigenetics; heat stress; histone modification; protein homeostasis; transcription factor.

Figure 1

The Heat Stress Response in Arabidopsis. HSFA1s function as central regulators orchestrating plant responses to heat stress (HS). HSFA1 expression is induced by heat, and HSFA1 activity is precisely modulated by various factors. Upon heat stress, HSFA1 is released from HSP70 and HSP90, leading to HSFA1 activation. In addition, the increases of cytoplasmic Ca²⁺ levels mediated by the Ca²⁺ channels, CNGCs, triggered by HS may be important for HSFA1 activation. Post-translational modifications, such as phosphorylation/SUMOylation/Ubiquitination regulate the activity of HSFA1 and DREB2A. HSFA2 as a target of HSFA1s is an important regulator of the expression of HSR genes through sustained H3K4 methylation. The miR398 inhibits the expression of ROS scavenger genes CSD1, CSD2, and CCS1, thereby promoting ROS accumulation, which subsequently activates HSFA1s. The miR165/166–PHB module regulates thermotolerance through at least two pathways: one involving direct transcriptional regulation of HSFs, with PHB modulating HSR transcription in an HSFA1-dependent manner; and another HSFA1-independent pathway, where PHB directly regulates the transcription of heat-inducible HSFA2. Additionally, PHB physically interacts with HSFA1s, influencing their transcriptional function. DREB2A is positively regulated by MBF1C and JUB1 in response to HS, whereas it is negatively regulated by GRF7 under normal conditions. In addition, DREB2A activity is enhanced by the NF-YA2/NFYB3/DBP3-1 complex. During HS, SIZ1 facilitates the SUMOylation of NF-YC10. The SUMO conjugation on NF-YC10 enhances its association with NF-YB3 via a SUMO-SIM interaction and improves the nuclear translocation of NFYB3. In the nucleus, the NF-YC10–NF-YB3 dimer binds to NF-YA2 to form an NF-YC trimeric complex to promote the transcription of HS-responsive genes. HS triggers the ER-localized transcription factors bZIP60 and bZIP28 to translocate into the nucleus and activate HSR expression. The circadian clock proteins RVE4 and RVE8 also can induce HSR gene expression in an HSFA1-independent way. Created with BioRender.com; accessed on 31 July 2023.

Figure 2

Schematic representation of regulators involved in Acquired thermotolerance (AT) in Arabidopsis. A mild heat stress (HS) can act as a priming cue and trigger enhanced tolerance to HS in the primed state. This primed state is maintained over time in a memory phase so that primed plants that encounter a second severe stress event are able to survive in contrast to nonprimed plants. Priming HS activates the expression of HSFA2 through HSFA1s, which are released from the HSP chaperone under priming HS and enter the nucleus. HSFA2 forms a heteromeric transcription factor complex with HSFA3, which activates the expression of HS memory genes or heat stress response (HSR) genes. Histone modifications play a critical role to regulate HS memory genes, including H3K27 demethylation by REF6, ELF6, JMJ30, and JMJ32; H3K4 trimethylation by COMPASS-like; and nucleosome positioning by the ATP-dependent chromatin remodeler complex consisting of FGT1, BRM, and ISWI. In addition, the FGT2/phosphatase-PLDa2/phospholipase complex and the miR156-SPL module are involved in the regulation of thermomemory genes in Arabidopsis. Created with BioRender.com; accessed on 31 July 2023.

Figure 3

Cell activities for keeping ROS and protein homeostasis. Upon heat stress, nuclear redox oxidation is sensed by HSFs. HSFs activate HSR genes, which are important for ROS scavenging and protein homeostasis. In addition, autophagy-related (ATG) protein ATG8 is rapidly translocated to the sites of swelling Golgi bodies. It recruits the clathrin component CLC2 to mediate the vesicle budding, which fuses with the vacuole. It facilitates the reassembly of the Golgi apparatus, thereby increasing thermotolerance. Created with BioRender.com; accessed on 31 July 2023.

Figure 4

Schematic representation of how plants respond to various heat stress (HS). HS changes membrane fluidity, which may be sensed by proteins, such as Ca²⁺ channels and receptor-like kinases, localized at the plasma membrane. After plants perceive temperature signals, a set of cell activities are activated, thereby conferring plant HS tolerance. Created with BioRender.com; accessed on 31 July 2023.