HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion

Lennard C. Van Der Woude; Giorgio Perrella; Basten L. Snoek; Mark Van Hoogdalem; Ondřej Novák; Marcel C. Van Verk; Heleen N. Van Kooten; Lennert E. Zorn; Rolf Tonckens; Joram A. Dongus; Myrthe Praat; Evelien A. Stouten; Marcel C.G. Proveniers; Elisa Vellutini; Eirini Patitaki; Umidjon Shapulatov; Wouter Kohlen; Sureshkumar Balasubramanian; Karin Ljung; Alexander R. Van Der Krol; Sjef Smeekens; Eirini Kaiserli; Martijn Van Zanten

doi:10.1073/pnas.1911694116

HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion

Lennard C. Van Der Woude, Giorgio Perrella, Basten L. Snoek, Mark Van Hoogdalem, Ondřej Novák, Marcel C. Van Verk, Heleen N. Van Kooten, Lennert E. Zorn, Rolf Tonckens, Joram A. Dongus, Myrthe Praat, Evelien A. Stouten, Marcel C.G. Proveniers, Elisa Vellutini, Eirini Patitaki, Umidjon Shapulatov, Wouter Kohlen, Sureshkumar Balasubramanian, Karin Ljung, Alexander R. Van Der KrolSjef Smeekens, Eirini Kaiserli, Martijn Van Zanten

School of Biological Sciences

Research output: Contribution to journal › Article › Research › peer-review

109 Citations (Scopus)

Abstract

Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatinmodifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.

Original language	English
Pages (from-to)	25343-25354
Number of pages	12
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	50
DOIs	https://doi.org/10.1073/pnas.1911694116
Publication status	Published - 10 Dec 2019

Keywords

Arabidopsis
H2A.Z
HDA9
Shade avoidance
Thermomorphogenesis

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10.1073/pnas.1911694116

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Van Der Woude, L. C., Perrella, G., Snoek, B. L., Van Hoogdalem, M., Novák, O., Van Verk, M. C., Van Kooten, H. N., Zorn, L. E., Tonckens, R., Dongus, J. A., Praat, M., Stouten, E. A., Proveniers, M. C. G., Vellutini, E., Patitaki, E., Shapulatov, U., Kohlen, W., Balasubramanian, S., Ljung, K., ... Van Zanten, M. (2019). HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion. Proceedings of the National Academy of Sciences of the United States of America, 116(50), 25343-25354. https://doi.org/10.1073/pnas.1911694116

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title = "HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion",

abstract = "Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatinmodifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.",

keywords = "Arabidopsis, H2A.Z, HDA9, Shade avoidance, Thermomorphogenesis",

author = "{Van Der Woude}, {Lennard C.} and Giorgio Perrella and Snoek, {Basten L.} and {Van Hoogdalem}, Mark and Ond{\v r}ej Nov{\'a}k and {Van Verk}, {Marcel C.} and {Van Kooten}, {Heleen N.} and Zorn, {Lennert E.} and Rolf Tonckens and Dongus, {Joram A.} and Myrthe Praat and Stouten, {Evelien A.} and Proveniers, {Marcel C.G.} and Elisa Vellutini and Eirini Patitaki and Umidjon Shapulatov and Wouter Kohlen and Sureshkumar Balasubramanian and Karin Ljung and {Van Der Krol}, {Alexander R.} and Sjef Smeekens and Eirini Kaiserli and {Van Zanten}, Martijn",

year = "2019",

month = dec,

day = "10",

doi = "10.1073/pnas.1911694116",

language = "English",

volume = "116",

pages = "25343--25354",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Van Der Woude, LC, Perrella, G, Snoek, BL, Van Hoogdalem, M, Novák, O, Van Verk, MC, Van Kooten, HN, Zorn, LE, Tonckens, R, Dongus, JA, Praat, M, Stouten, EA, Proveniers, MCG, Vellutini, E, Patitaki, E, Shapulatov, U, Kohlen, W, Balasubramanian, S, Ljung, K, Van Der Krol, AR, Smeekens, S, Kaiserli, E & Van Zanten, M 2019, 'HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 50, pp. 25343-25354. https://doi.org/10.1073/pnas.1911694116

HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion. / Van Der Woude, Lennard C.; Perrella, Giorgio; Snoek, Basten L. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 50, 10.12.2019, p. 25343-25354.

Research output: Contribution to journal › Article › Research › peer-review

TY - JOUR

T1 - HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion

AU - Van Der Woude, Lennard C.

AU - Perrella, Giorgio

AU - Snoek, Basten L.

AU - Van Hoogdalem, Mark

AU - Novák, Ondřej

AU - Van Verk, Marcel C.

AU - Van Kooten, Heleen N.

AU - Zorn, Lennert E.

AU - Tonckens, Rolf

AU - Dongus, Joram A.

AU - Praat, Myrthe

AU - Stouten, Evelien A.

AU - Proveniers, Marcel C.G.

AU - Vellutini, Elisa

AU - Patitaki, Eirini

AU - Shapulatov, Umidjon

AU - Kohlen, Wouter

AU - Balasubramanian, Sureshkumar

AU - Ljung, Karin

AU - Van Der Krol, Alexander R.

AU - Smeekens, Sjef

AU - Kaiserli, Eirini

AU - Van Zanten, Martijn

PY - 2019/12/10

Y1 - 2019/12/10

N2 - Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatinmodifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.

AB - Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatinmodifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.

KW - Arabidopsis

KW - H2A.Z

KW - HDA9

KW - Shade avoidance

KW - Thermomorphogenesis

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U2 - 10.1073/pnas.1911694116

DO - 10.1073/pnas.1911694116

M3 - Article

C2 - 31767749

AN - SCOPUS:85076340419

SN - 0027-8424

VL - 116

SP - 25343

EP - 25354

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 50

ER -

HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion

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Keywords

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The transgenerational effect of thermosensing in plants

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HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion

Abstract

Keywords

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The transgenerational effect of thermosensing in plants

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