POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana

Celine Tasset, Avilash Singh Yadav, Sridevi Sureshkumar, Rupali Singh, Lennard van der Woude, Maxim Nekrasov, David Tremethick, Martijn van Zanten, Sureshkumar Balasubramanian

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19 Citations (Scopus)

Abstract

Ambient temperature affects plant growth and even minor changes can substantially impact crop yields. The underlying mechanisms of temperature perception and response are just beginning to emerge. Chromatin remodeling, via the eviction of the histone variant H2A.Z containing nucleosomes, is a critical component of thermal response in plants. However, the role of histone modifications remains unknown. Here, through a forward genetic screen, we identify POWERDRESS (PWR), a SANT-domain containing protein known to interact with HISTONE DEACETYLASE 9 (HDA9), as a novel factor required for thermomorphogenesis in Arabidopsis thaliana. We show that mutations in PWR impede thermomorphogenesis, exemplified by attenuated warm temperature-induced hypocotyl/petiole elongation and early flowering. We show that inhibitors of histone deacetylases diminish temperature-induced hypocotyl elongation, which demonstrates a requirement for histone deacetylation in thermomorphogenesis. We also show that elevated temperature is associated with deacetylation of H3K9 at the +1 nucleosomes of PHYTOCHROME INTERACTING FACTOR4 (PIF4) and YUCCA8 (YUC8), and that PWR is required for this response. There is global misregulation of genes in pwr mutants at elevated temperatures. Meta-analysis revealed that genes that are misregulated in pwr mutants display a significant overlap with genes that are H2A.Z-enriched in their gene bodies, and with genes that are differentially expressed in mutants of the components of the SWR1 complex that deposits H2A.Z. Our findings thus uncover a role for PWR in facilitating thermomorphogenesis and suggest a potential link between histone deacetylation and H2A.Z nucleosome dynamics in plants.

Original languageEnglish
Article numbere1007280
Number of pages21
JournalPLoS Genetics
Volume14
Issue number3
DOIs
Publication statusPublished - 1 Mar 2018

Cite this

Tasset, Celine ; Singh Yadav, Avilash ; Sureshkumar, Sridevi ; Singh, Rupali ; van der Woude, Lennard ; Nekrasov, Maxim ; Tremethick, David ; van Zanten, Martijn ; Balasubramanian, Sureshkumar. / POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana. In: PLoS Genetics. 2018 ; Vol. 14, No. 3.
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abstract = "Ambient temperature affects plant growth and even minor changes can substantially impact crop yields. The underlying mechanisms of temperature perception and response are just beginning to emerge. Chromatin remodeling, via the eviction of the histone variant H2A.Z containing nucleosomes, is a critical component of thermal response in plants. However, the role of histone modifications remains unknown. Here, through a forward genetic screen, we identify POWERDRESS (PWR), a SANT-domain containing protein known to interact with HISTONE DEACETYLASE 9 (HDA9), as a novel factor required for thermomorphogenesis in Arabidopsis thaliana. We show that mutations in PWR impede thermomorphogenesis, exemplified by attenuated warm temperature-induced hypocotyl/petiole elongation and early flowering. We show that inhibitors of histone deacetylases diminish temperature-induced hypocotyl elongation, which demonstrates a requirement for histone deacetylation in thermomorphogenesis. We also show that elevated temperature is associated with deacetylation of H3K9 at the +1 nucleosomes of PHYTOCHROME INTERACTING FACTOR4 (PIF4) and YUCCA8 (YUC8), and that PWR is required for this response. There is global misregulation of genes in pwr mutants at elevated temperatures. Meta-analysis revealed that genes that are misregulated in pwr mutants display a significant overlap with genes that are H2A.Z-enriched in their gene bodies, and with genes that are differentially expressed in mutants of the components of the SWR1 complex that deposits H2A.Z. Our findings thus uncover a role for PWR in facilitating thermomorphogenesis and suggest a potential link between histone deacetylation and H2A.Z nucleosome dynamics in plants.",
author = "Celine Tasset and {Singh Yadav}, Avilash and Sridevi Sureshkumar and Rupali Singh and {van der Woude}, Lennard and Maxim Nekrasov and David Tremethick and {van Zanten}, Martijn and Sureshkumar Balasubramanian",
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Tasset, C, Singh Yadav, A, Sureshkumar, S, Singh, R, van der Woude, L, Nekrasov, M, Tremethick, D, van Zanten, M & Balasubramanian, S 2018, 'POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana', PLoS Genetics, vol. 14, no. 3, e1007280. https://doi.org/10.1371/journal.pgen.1007280

POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana. / Tasset, Celine; Singh Yadav, Avilash; Sureshkumar, Sridevi; Singh, Rupali; van der Woude, Lennard; Nekrasov, Maxim; Tremethick, David; van Zanten, Martijn; Balasubramanian, Sureshkumar.

In: PLoS Genetics, Vol. 14, No. 3, e1007280, 01.03.2018.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Singh, Rupali

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AU - Tremethick, David

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AU - Balasubramanian, Sureshkumar

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