POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis inArabidopsis thaliana

Abstract

. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/186916 doi: bioRxiv preprint first posted online Sep. 10, 2017; Author summaryPlant growth and development is influenced by a variety of external environmental cues.Ambient temperature affects almost all stages of plant development but the underlying molecular mechanisms remain largely unknown. In this paper, the authors show that histone deacetylation, one of the major chromatin remodeling processes, is essential for eliciting growth temperatureinduced responses in plants. The authors identify POWERDRESS, a protein known to interact with HISTONE DEACETYLASE 9, as a novel key player essential for eliciting high temperature induced responses in Arabidopsis. Another chromatin remodeling mechanism that is known to play a role in thermal response is the eviction of histone variant H2A.Z from nucleosomes. Through transcriptome studies the authors demonstrate an overlap between gene regulations conferred through PWR-mediated histone H3 deacetylation and that conferred via histone H2A.Z eviction/incorporation dynamics. This study identifies a key novel gene that is essential for plants to elicit high temperature responses and reveals close links between two seemingly distinct chromatin-remodeling processes in regulating gene expression in plants.

Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants

“…Epigenetic regulation is important for plant responses to cold stress. Previous interesting results indicate that chromatin remodelling mediated by H2A.Z is responsible for thermomorphogensis and the thermosensory activation of flowering (Kumar & Wigge, 2010;Kumar et al, 2012;Tasset et al, 2018). The cold-induced expression of CBFs is rapid and transient, peaking at 2-3 h after cold treatment (Thomashow, 1999).…”

Molecular pathways regulating elongation of aerial plant organs: a focus on light, the circadian clock, and temperature

“…The molecular mechanisms regulating thermomorphogenesis bear several similarities to those involved in shade responses, with PIF4, PIF7, and, to a lesser degree, PIF5 mediating the growth responses to both stimuli (Lorrain et al ., 2008; Koini et al ., 2009; Stavang et al ., 2009; Franklin et al ., 2011; Li et al ., 2012a; Sun et al ., 2012; Hayes et al ., 2014; de Wit et al ., 2015; Zhu et al ., 2016; Hayes et al ., 2017; Pantazopoulou et al ., 2017; Fiorucci et al ., 2019; Sharma et al ., 2019; van der Woude et al ., 2019; Chung et al ., 2020). In particular, enhanced auxin biosynthesis in cotyledons due to PIF‐mediated induction of YUC8 (and probably also other YUC genes) has been demonstrated to be critical for hypocotyl responses to elevated temperature (Figure 4) (Franklin et al ., 2011; Sun et al ., 2012; Lee et al ., 2014; Hayes et al ., 2017; Tasset et al ., 2018; Bellstaedt et al ., 2019; van der Woude et al ., 2019; Kim et al ., 2020). Furthermore, the epidermis plays a key role in transducing signals associated with both low R:FR and warm temperature responses (Procko et al ., 2016; Kim et al ., 2020).…”

“…While reduced phyB activity probably stabilizes PIF4 during thermomorphogenesis (Foreman et al ., 2011; Kumar et al ., 2012; Jung et al ., 2016; Legris et al ., 2016), this stabilization also depends on COP1/SPAs (Gangappa and Kumar, 2017; Lee et al ., 2020) as well as HEMERA (HMR), a co‐activator important for the induction of genes such as YUC8 and IAA19 in response to warm temperatures (Qiu et al ., 2019). The PIF4‐mediated induction of YUC8 in response to elevated temperature is also facilitated by epigenetic changes, as higher temperatures promote eviction of the repressive histone 2A (H2A) variant H2A.Z from chromatin, which enhances the activation of PIF‐targeted genes such as YUC8 (Kumar and Wigge, 2010; Kumar et al ., 2012; Tasset et al ., 2018; van der Woude et al ., 2019). The eviction of H2A.Z from YUC8 critically requires maintenance of low levels of histone 3 lysine 9/14 acetylation (H3K9/14ac) on this gene, which is carried out by a complex containing POWERDRESS (PWR) and HISTONE DEACETYLASE 9 (HDA9) and is facilitated by warmer temperatures via promotion of HDA9 accumulation (Chen et al ., 2016a; Kim et al ., 2016; Tasset et al ., 2018; Mayer et al ., 2019; van der Woude et al ., 2019).…”

“…The PIF4‐mediated induction of YUC8 in response to elevated temperature is also facilitated by epigenetic changes, as higher temperatures promote eviction of the repressive histone 2A (H2A) variant H2A.Z from chromatin, which enhances the activation of PIF‐targeted genes such as YUC8 (Kumar and Wigge, 2010; Kumar et al ., 2012; Tasset et al ., 2018; van der Woude et al ., 2019). The eviction of H2A.Z from YUC8 critically requires maintenance of low levels of histone 3 lysine 9/14 acetylation (H3K9/14ac) on this gene, which is carried out by a complex containing POWERDRESS (PWR) and HISTONE DEACETYLASE 9 (HDA9) and is facilitated by warmer temperatures via promotion of HDA9 accumulation (Chen et al ., 2016a; Kim et al ., 2016; Tasset et al ., 2018; Mayer et al ., 2019; van der Woude et al ., 2019).…”

“…For instance, on top of their roles in hypocotyl thermomorphogenesis, PIF4 and PIF7 are also essential for petiole growth responses to warm temperatures (Koini et al ., 2009; Stavang et al ., 2009; Franklin et al ., 2011; Sun et al ., 2012; Zhu et al ., 2016; Hayes et al ., 2017; Tasset et al ., 2018; Fiorucci et al ., 2019; Chung et al ., 2020). Additionally, the pwr‐2 and hda9‐1 mutants both exhibit defects in thermomorphogenic petiole elongation, suggesting that, as in hypocotyls, PWR/HDA9 may be necessary to facilitate the eviction of H2A.Z from YUC8 (Figure 6) (Tasset et al ., 2018; van der Woude et al ., 2019). Thermomorphogenic growth in both organs is also inhibited by UV‐B, although UVR8 appears to be somewhat less important for this response in petioles (Hayes et al ., 2017).…”