The Histone-Modifying Complex PWR/HOS15/HD2C Epigenetically Regulates Cold Tolerance

Abstract

Cold stress is a major environmental stress that severely affects plant growth and crop productivity. Arabidopsis (Arabidopsis thaliana) HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE15 (HOS15) is a substrate receptor of the CULLIN4based CLR4 ubiquitin E3 ligase complex, which epigenetically regulates cold tolerance by degrading HISTONE DEACETYLASE2C (HD2C) to switch from repressive to permissive chromatin structure in response to cold stress. In this study, we characterized a HOS15-binding protein, POWERDRESS (PWR), and analyzed its function in the cold stress response. PWR loss-of-function plants (pwr) showed lower expression of cold-regulated (COR) genes and sensitivity to freezing. PWR interacts with HD2C through HOS15, and cold-induced HD2C degradation by HOS15 is diminished in the pwr mutant. The association of HOS15 and HD2C to promoters of cold-responsive COR genes was dependent on PWR. Consistent with these observations, the high acetylation levels of histone H3 by cold-induced and HOS15-mediated HD2C degradation were significantly reduced in pwr under cold stress. PWR also interacts with C-repeat element-binding factor transcription factors to modulate their cold-induced binding to the promoter of COR genes. Collectively, our data signify that the PWR-HOS15-HD2C histone-modifying complex regulates the expression of COR genes and the freezing tolerance of plants. Cold stress is one of the major environmental factors that seriously limits the growth and productivity of plants. To overcome this constraint, plants have developed effective ways to increase resistance to cold stress and freezing. Cold acclimation is a process that increases freezing tolerance upon exposure to low but nonfreezing temperatures. This process involves the activation or expression of cold-regulated (COR) genes and consequent physiological and biochemical changes in response to cold stress (Guo et al., 2018; Ding et al., 2019). Over the past two decades, various effectors and regulators of stress signaling pathways have been identified (Guo et al., 2018; Liu et al., 2018b; Zhang et al., 2019; Tang et al., 2020). One of the best-characterized mechanisms is the C-REPEAT ELEMENT-BINDING FACTORS (CBFs; also known as DEHYDRATION RESPONSIVE ELEMENT-BINDING proteins [DREB]: CBF1/DREB1B, CBF2/DREB1C, and CBF3/DREB1A) transcription factor-dependent cold signaling pathway (Chinnusamy et al., 2007; Guo et al., 2018; Liu et al., 2018a). These CBF transcription factors are APETALA2-like DNAbinding domain proteins that bind to the conserved C-REPEAT ELEMENT/DEHYDRATION RESPONSIVE ELEMENT (CRT/DRE) on the promoter regions of COR genes, such as COR15A, COR47, and COR78, and induce

Cauliflower mosaic virus P6 Dysfunctions Histone Deacetylase HD2C to Promote Virus Infection

“…Consistently, the deposition of histone acetylation on these genes was increased in the P6 overexpression lines than in the wild-type ( Figure 6 c). Previous reports had demonstrated that HD2C was involved in many abiotic stresses like salt, heat, and cold stress [ 19 , 21 , 56 ]. Therefore, further studies are needed to investigate how CaMV facilitates the hosts to survive these stresses through histone deacetylation.…”

“…In response to heat stress, HD2C was proved to regulate heat-responsive genes by physically cooperating with chromatin remodeling complex like SWI/SNF [ 19 ]. HD2C had also been identified as a core factor in chromatin structure switching from repressed to active status in response to cold stress, whose degradation was facilitated by interacting with HOS15, a substrate receptor of CULLIN4 (CUL4) -based E3 ubiquitin ligase complex, under cold stress [ 20 , 21 , 22 ]. Although the function of HD2C in abiotic stress was extensively studied, its functions in biotic stress have remained unclear.…”

Multifaceted Chromatin Structure and Transcription Changes in Plant Stress Response

“…The histone deacetylase inhibitor Trichostatin A and DNA methylation inhibitor 5-Aza-2′-Deoxycytidine alter the expression of cold-induced genes in Arabidopsis thaliana, enhancing its cold tolerance [ 44 ], and in response to cold stress, histone H3 acetylation-mediated chromatin remodeling is necessary for transcriptional activation of a cold-inducible rice gene, OsDREB1b [ 45 ]. The POWERDRESS (PWR)-HOS15-HD2C complex in Arabidopsis negatively regulates the expression of COR genes through H3 deacetylation and repressive chromatin structure [ 25 , 46 ], whereas the histone deacetylase HD2C is degraded by the PWR-HOS15 complex, resulting in transcriptional activation of COR genes ( RD29A and COR15A / 47 / 78 ) under cold stress, by facilitating H3 acetylation and the permissive chromatin structure. In cold-treated banana ( Musa acuminata ) fruits, the increased levels of H3 and H4 acetylation in the promoters of ω-3 fatty acid desaturase genes ( MaFADs ) are correlated with the enhanced transcription of ω-3 MaFADs ; the MaMYB4 transcription factor negatively regulates the transcription of ω-3 MaFADs by recruiting the histone deacetylase MaHDA2 [ 47 ].…”

“…Similarly, the rice AGO2 is associated with the enhanced H3K4me3 and the reduced H3K27me3 levels of the BG3 gene to facilitate its expression under salinity stress through chromatin modifications [ 75 ]. The PWR proteins also constitute a chromatin-remodeling complex with either HOS15 and HD2C, or HDA9 and ABI4 to repress the cold-responsive RD29A and COR15A / 47 / 78 or the drought-responsive CYP707A1/2 genes, respectively in Arabidopsis [ 46 , 87 ]. In addition, histone modifiers and transcription regulators together coordinate chromatin dynamics and gene expression, allowing alternative nucleosome configurations at transcription sites [ 10 , 11 , 12 , 13 ].…”

HD2-type histone deacetylases: unique regulators of plant development and stress responses

“…Study demonstrated that HOS15 acts as a DCAF protein and interacts with and degrades the HD2C protein via ubiquitination and proteasome-mediated degradation, thus modulating the expression of cold-responsive (COR) genes under freezing stress in Arabidopsis (Park, et al 2018). Lim, et al (2020) studied the function of the HOS15 binding protein, POWERDRESS (PWR) in response to cold stress. This study showed that HOS15 interacts with HD2C with the help of PWR at the promoter region of COR genes, thus mediating the degradation of HD2C, leading to the upregulation of COR genes as a part of the cold stress response.…”