Histone Deacetylase HDA9 and WRKY53 Transcription Factor Are Mutual Antagonists in Regulation of Plant Stress Response

Abstract

Epigenetic regulation of gene expression is important for plant adaptation to environmental changes. Previous results showed that Arabidopsis RPD3-like histone deacetylase HDA9 is known to function in repressing plant response to stress in Arabidopsis. However, how HDA9 targets to specific chromatin loci and controls gene expression networks involved in plant response to stress remains largely unclear. Here, we show that HDA9 represses stress tolerance response by interacting with and regulating the DNA binding and transcriptional activity of WRKY53, which functions as a high-hierarchy positive regulator of stress response. We found that WRKY53 is post-translationally modified by lysine acetylation at multiple sites, some of which are removed by HDA9, resulting in inhibition of WRKY53 transcription activity. Conversely, WRKY53 negatively regulates HDA9 histone deacetylase activity. Collectively, our results indicate that HDA9 and WRK53 are reciprocal negative regulators of each other's activities, illustrating how the functional interplay between a chromatin regulator and a transcription factor regulates stress tolerance in plants.

The diverse and unanticipated roles of histone deacetylase 9 in coordinating plant development and environmental acclimation

“…The transcription factors WRKY53 ( Chen et al , 2016 ; Zheng et al , 2020 ), ABI4, ABI3 ( Baek et al , 2020 , Khan et al , 2020 ), and HY5 ( Yang et al , 2020 ), the epigenome readers VP1/ABI3-LIKE 1 (VAL1) and VAL2 ( Zeng et al , 2020 ), the circadian clock Evening Complex (EC) transcription factor(s) ELF3 and possibly LUX ( Lee et al , 2019 ; Park et al , 2019 ), and AT-hook motif-containing protein AHL22 ( Yun et al , 2012 ) are currently the only confirmed HDA9-interacting proteins with DNA binding capacity ( Fig. 1 ).…”

“…1 ). In particular, the molecular mechanism of the HDA9–WRKY53 interaction is now understood in detail ( Zheng et al , 2020 ). Despite the limited number of confirmed HDA9 interactors, it is likely that HDA9 associates directly—or as part of a bigger HDAC multiprotein complex—with many more yet to be discovered DNA-binding factors.…”

“…HDA9 substrates include H3K9Ac, H3K14Ac, H3K18Ac, H3K27Ac, H3K36Ac, and H3K56Ac ( Kim et al , 2013 ; Van Zanten et al , 2014 ; Kang et al , 2015 ; Chen et al , 2016 ; Kim et al , 2016 ; Mayer et al , 2019 ; Park et al , 2019 ; van der Woude et al , 2019 ; Yang et al , 2020 ; Zeng et al , 2020 ; Zheng et al , 2020 ), but not H4 or H2A lysines ( Kim et al , 2016 ; Mayer et al , 2019 ). In addition, hda9 mutants display altered H3K9Me1, H3K9Me2, H3K27Me1, H3K27Me2, and H3K36Me2 levels ( Chen et al , 2016 ; Kim et al , 2016 ; Mayer et al , 2019 ; Zeng et al , 2020 ).…”

“…Despite the fact that some HDACs target non-histone protein substrates ( Hartl et al , 2017 ; Zheng et al , 2020 ), for a long time there was no evidence suggesting that HDA9 can deacetylate proteins other than histone H3, even though HDA9 has been detected in both the cytoplasm and the nucleus ( Kang et al , 2015 ; Ducos et al , 2017 ; Suzuki et al , 2018 ; Mayer et al , 2019 ; Yang et al , 2019 ). A recent study, however, demonstrated that HDA9 can remove acetyl groups and thereby negatively regulates the transcriptional activity of its interacting transcription factor protein WRKY53 ( Zheng et al , 2020 ). Pharmacological evidence showed that HDA9 is prone to proteasomal regulation ( Mayer et al , 2019 ) and it has been suggested that HDA9 may be associated with a CUL4-based E3 ligase ( Park et al , 2019 ).…”

“…1 ; Table 2 ). Moreover, HDA9 mediates responses to environmental signals such as salt, drought ( Zheng et al , 2016 ; Baek et al , 2020 ; Khan et al , 2020 ; Zheng et al , 2020 ), and warm temperatures ( Tasset et al , 2018 ; Shen et al , 2019 ; van der Woude et al , 2019 ).…”