IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52033-x.html
   My bibliography  Save this article

Phosphorylation activates master growth regulator DELLA by promoting histone H2A binding at chromatin in Arabidopsis

Author

Listed:
  • Xu Huang

    (Duke University)

  • Rodolfo Zentella

    (Duke University
    Plant Science Research Unit
    North Carolina State University)

  • Jeongmoo Park

    (Duke University
    Syngenta)

  • Larry Reser

    (University of Virginia)

  • Dina L. Bai

    (University of Virginia)

  • Mark M. Ross

    (University of Virginia)

  • Jeffrey Shabanowitz

    (University of Virginia)

  • Donald F. Hunt

    (University of Virginia
    University of Virginia)

  • Tai-ping Sun

    (Duke University)

Abstract

DELLA proteins are conserved master growth regulators that play a central role in controlling plant development in response to internal and environmental cues. DELLAs function as transcription regulators, which are recruited to target promoters by binding to transcription factors (TFs) and histone H2A via their GRAS domain. Recent studies showed that DELLA stability is regulated post-translationally via two mechanisms, phytohormone gibberellin-induced polyubiquitination for its rapid degradation, and Small Ubiquitin-like Modifier (SUMO)-conjugation to increase its accumulation. Moreover, DELLA activity is dynamically modulated by two distinct glycosylations: DELLA-TF interactions are enhanced by O-fucosylation, but inhibited by O-linked N-acetylglucosamine (O-GlcNAc) modification. However, the role of DELLA phosphorylation remains unclear as previous studies showing conflicting results ranging from findings that suggest phosphorylation promotes or reduces DELLA degradation to others indicating it has no effect on its stability. Here, we identify phosphorylation sites in REPRESSOR OF ga1-3 (RGA, an AtDELLA) purified from Arabidopsis by mass spectrometry analysis, and show that phosphorylation of two RGA peptides in the PolyS and PolyS/T regions enhances RGA activity by promoting H2A binding and RGA association with target promoters. Notably, phosphorylation does not affect RGA-TF interactions or RGA stability. Our study has uncovered a molecular mechanism of phosphorylation-induced DELLA activity.

Suggested Citation

  • Xu Huang & Rodolfo Zentella & Jeongmoo Park & Larry Reser & Dina L. Bai & Mark M. Ross & Jeffrey Shabanowitz & Donald F. Hunt & Tai-ping Sun, 2024. "Phosphorylation activates master growth regulator DELLA by promoting histone H2A binding at chromatin in Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52033-x
    DOI: 10.1038/s41467-024-52033-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52033-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-52033-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Kohji Murase & Yoshinori Hirano & Tai-ping Sun & Toshio Hakoshima, 2008. "Gibberellin-induced DELLA recognition by the gibberellin receptor GID1," Nature, Nature, vol. 456(7221), pages 459-463, November.
    2. Weimin Ni & Shou-Ling Xu & Eduardo González-Grandío & Robert J. Chalkley & Andreas F. R. Huhmer & Alma L. Burlingame & Zhi-Yong Wang & Peter H. Quail, 2017. "PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3," Nature Communications, Nature, vol. 8(1), pages 1-11, August.
    3. Miyako Ueguchi-Tanaka & Motoyuki Ashikari & Masatoshi Nakajima & Hironori Itoh & Etsuko Katoh & Masatomo Kobayashi & Teh-yuan Chow & Yue-ie C. Hsing & Hidemi Kitano & Isomaro Yamaguchi & Makoto Matsuo, 2005. "GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin," Nature, Nature, vol. 437(7059), pages 693-698, September.
    4. Asako Shimada & Miyako Ueguchi-Tanaka & Toru Nakatsu & Masatoshi Nakajima & Youichi Naoe & Hiroko Ohmiya & Hiroaki Kato & Makoto Matsuoka, 2008. "Structural basis for gibberellin recognition by its receptor GID1," Nature, Nature, vol. 456(7221), pages 520-523, November.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Mohamed Mahameed & Pengli Wang & Shuai Xue & Martin Fussenegger, 2022. "Engineering receptors in the secretory pathway for orthogonal signalling control," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Hideki Yoshida & Ko Hirano & Kenji Yano & Fanmiao Wang & Masaki Mori & Mayuko Kawamura & Eriko Koketsu & Masako Hattori & Reynante Lacsamana Ordonio & Peng Huang & Eiji Yamamoto & Makoto Matsuoka, 2022. "Genome-wide association study identifies a gene responsible for temperature-dependent rice germination," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Jia Zhou & Qinli Hu & Xinlong Xiao & Deqiang Yao & Shenghong Ge & Jin Ye & Haojie Li & Rujie Cai & Renyang Liu & Fangang Meng & Chao Wang & Jian-Kang Zhu & Mingguang Lei & Weiman Xing, 2021. "Mechanism of phosphate sensing and signaling revealed by rice SPX1-PHR2 complex structure," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Youra Hwang & Soeun Han & Chan Yul Yoo & Liu Hong & Chenjiang You & Brandon H. Le & Hui Shi & Shangwei Zhong & Ute Hoecker & Xuemei Chen & Meng Chen, 2022. "Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Ruth Jean Ae Kim & De Fan & Jiangman He & Keunhwa Kim & Juan Du & Meng Chen, 2024. "Photobody formation spatially segregates two opposing phytochrome B signaling actions of PIF5 degradation and stabilization," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Bihai Shi & Amelia Felipo-Benavent & Guillaume Cerutti & Carlos Galvan-Ampudia & Lucas Jilli & Geraldine Brunoud & Jérome Mutterer & Elody Vallet & Lali Sakvarelidze-Achard & Jean-Michel Davière & Ale, 2024. "A quantitative gibberellin signaling biosensor reveals a role for gibberellins in internode specification at the shoot apical meristem," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Yage Ding & Cristina Tous & Jaehoon Choi & Jingyao Chen & Wilson W. Wong, 2024. "Orthogonal inducible control of Cas13 circuits enables programmable RNA regulation in mammalian cells," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Yuqing He & Yingjun Yu & Xiling Wang & Yumei Qin & Chen Su & Lei Wang, 2022. "Aschoff’s rule on circadian rhythms orchestrated by blue light sensor CRY2 and clock component PRR9," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Chanhee Kim & Yongmin Kwon & Jaehoon Jeong & Minji Kang & Ga Seul Lee & Jeong Hee Moon & Hyo-Jun Lee & Youn-Il Park & Giltsu Choi, 2023. "Phytochrome B photobodies are comprised of phytochrome B and its primary and secondary interacting proteins," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52033-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.