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AtHDA15 attenuates COP1 via transcriptional quiescence, direct binding, and sub-compartmentalization during photomorphogenesis

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Abstract

Light is an essential environmental cue that determines the overall growth and development of plants. However, the molecular mechanisms underpinning the light signaling network are obscured by the epigenetic machinery where reversible acetylation and deacetylation play crucial roles in modulating light-regulated gene expression. In this paper, we demonstrate that HDA15 represses COP1, the master switch in the light signaling network, by deacetylation, protein interaction, and sub-compartmentalization. hda15 T-DNA mutant lines exhibited light hyposensitivity with significantly reduced HY5 and PIF3 transcript levels leading to long-hypocotyl phenotypes in the dark while its overexpression exhibited elevated HY5 transcripts and short hypocotyl phenotypes. In vivo and in vitro binding assays further show that HDA15 directly interacts with COP1 inside the nucleus modulating COP1’s repressive activities. Crossing hda15-t27 with cop1-4 mutants resulted in short-hypocotyl and dwarfed phenotypes, reminiscent of cop1-4 mutants suggesting COP1 is epistatic to HDA15. Although light signals the nucleocytoplasmic shuttling of HDA15, the presence of COP1 triggers its nuclear localization. A working model is presented elucidating the concerted interplay between HDA15 and COP1 under light and dark conditions.

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Data availability

The data supporting the findings of this study are available in the paper and from the corresponding author, MVA, upon request.

References

  • Alam SL, Sun J, Payne M, Welch BD, Blake BK, Davis DR, Meyer HH, Emr SD, Sundquist WI (2004) Ubiquitin interactions of NZF zinc fingers. EMBO J 23:1411–1421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alinsug MV, Yu CW, Wu K (2009) Phylogenetic analysis, subcellular localization, and expression patterns of RPD3/HDA1 family histone deacetylases in plants. BMC Plant Biol 9:37. https://doi.org/10.1186/1471-2229-9-37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alinsug MV, Chen FF, Luo M, Tai R, Jiang L, Wu K (2012) Subcellular localization of class II HDAs in Arabidopsis thaliana: nucleocytoplasmic shuttling of HDA15 is driven by light. PLoS One 7:e30846. https://doi.org/10.1371/journal.pone.0030846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alinsug MV, Radziejwoski A, Deocaris CC (2020) AtHDA15 binds directly to COP1 positively regulating photomorphogenesis. Biochem Biophysical Res Comm 533:806–812. https://doi.org/10.1016/j.bbrc.2020.09.089

    Article  CAS  Google Scholar 

  • Ausin I, Alonso-Blanco C, Martinez-Zapater JM (2004) Environmental regulation of flowering. Int J Dev Biol 49:689–705

    Article  Google Scholar 

  • Benhamed M, Bertrand C, Servet C, Zhou DX (2006) Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18:2893–2903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benhamed M, Martin-Magniette ML, Taconnat L, Bitton F, Servet C, De Clercq R, De Meyer B, Buysschaert C, Rombauts S, Villarroel R, Aubourg S, Beynon J, Bhalerao RP, Coupland G, Gruissem W, Menke FL, Weisshaar B, Renou JP, Zhou DX, Hilson P (2008) Genome-scale Arabidopsis promoter array identifies targets of the histone acetyltransferase GCN5. Plant J Cell Mol Biol 56:493–504

    Article  CAS  Google Scholar 

  • Charron JB, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21:3732–3748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218

    Article  CAS  PubMed  Google Scholar 

  • Gu D, Chen CY, Zhao M, Zhao L, Duan X, Duan J, Wu K, Liu X (2017) Identification of HDA15-PIF1 as a key repression module directing the transcriptional network of seed germination in the dark. Nucleic Acids Res 45:7137–7150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Zhou J, Elling AA, Charron JB, Deng XW (2008) Histone modifications and expression of light-regulated genes in Arabidopsis are cooperatively influenced by changing light conditions. Plant Physiol 147:2070–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holm M, Deng XW (1999) Structural organization and interactions of COP1, a light-regulated developmental switch. Plant Mol Biol 41:151–158

    Article  CAS  PubMed  Google Scholar 

  • Hook SS, Orian A, Cowley SM, Eisenman RN (2002) Histone deacetylase 6 binds polyubiquitin through its zinc finger (PAZ domain) and copurifies with deubiquitinating enzymes. Proc Nat Acad Sci USA 99:13425–13430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh HL, Okamoto H, Wang M, Ang LH, Matsui M, Goodman H, Deng XW (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14:1958–1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito A, Kawaguchi Y, Lai CH, Kovacs JJ, Higashimoto Y, Appella E, Yao TP (2002) MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO 21:6236–6245

    Article  CAS  Google Scholar 

  • Jang IC, Chung PJ, Hemmes H, Jung C, Chua NH (2011) Rapid and reversible light-mediated chromatin modifications of Arabidopsis phytochrome A locus. Plant Cell 23:459–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8:217–230

    Article  CAS  PubMed  Google Scholar 

  • Kovacs JJ, Cohen TJ, Yao TP (2005) Chaperoning steroid hormone signaling via reversible acetylation. Nucl Rec Sig 3:e004

    Article  Google Scholar 

  • Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global histone acetylation patterns to gene expression. Cell 117:721–733

    Article  CAS  PubMed  Google Scholar 

  • Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P (2009) Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinfo 25:2744–2750

    Article  CAS  Google Scholar 

  • Liu X, Chen CY, Wang KC, Luo M, Tai R, Yuan L, Zhao M, Yang S, Tian G, Cui Y, Hsieh HL, Wu K (2013) Phytochrome interacting FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell 25:1258–1273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Wei W, Zhu W, Su L, Xiong Z, Zhou M, Zheng Y, Zhou DX (2017) Histone deacetylase AtSRT1 links metabolic flux and stress response in Arabidopsis. Mol Plant 10:1510–1522

    Article  CAS  PubMed  Google Scholar 

  • Luxton GG, Gundersen GG (2007) HDAC6-pack: cortactin acetylation joins the brew. Dev Cell 13:161–162

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Lv S, Zhang C, Yang C (2013) Histone deacetylases and their functions in plants. Plant Cell Rep 32:465–478

    Article  CAS  PubMed  Google Scholar 

  • Matthias P, Yoshida M, Khochbin S (2008) HDAC6 a new cellular stress surveillance factor. Cell Cycle 7:7–10

    Article  CAS  PubMed  Google Scholar 

  • Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466

    Article  CAS  PubMed  Google Scholar 

  • Ouyang H, Ali YO, Ravichandran M, Dong A, Qiu W, MacKenzie F, Dhe-Paganon S, Arrowsmith CH, Zhai RG (2012) Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J Biol Chem 287:2317–2327

    Article  CAS  PubMed  Google Scholar 

  • Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes bZip protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11(22):2983–2995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, Jorgensen RA (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30:5036–5055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schenke D, Cai D, Scheel D (2014) Suppression of UV-B stress responses by flg22 is regulated at the chromatin level via histone modification. Plant Cell Environ 37:1716–1721

    Article  CAS  PubMed  Google Scholar 

  • Schübeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O’Neill LP, Turner BM, Delrow J (2004) The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18:1263–1271

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang Y, Liu X, Liu X, Li Y, Wu K, Hou X (2017) Arabidopsis NF-YCs mediate the light-controlled hypocotyl elongation via modulating histone acetylation. Mol Plant 10:260–273

    Article  CAS  PubMed  Google Scholar 

  • Tessadori F, van Zanten M, Pavlova P, Clifton R, Pontvianne F, Snoek LB, Millenaar FF, Schulkes RK, van Driel R, Voesenek LA, Spillane C, Pikaard CS, Fransz P, Peeters AJ (2009) Phytochrome B and histone deacetylase 6 control light-induced chromatin compaction in Arabidopsis thaliana. PLoS Genet 5:e1000638

    Article  PubMed  PubMed Central  Google Scholar 

  • Tran HT, Nimick M, Uhrig RG, Templeton G, Morrice N, Gourlay R, DeLong A, Moorhead GB (2012) Arabidopsis thaliana histone deacetylase 14 (HDA14) is an alpha-tubulin deacetylase that associates with PP2A and enriches in the microtubule fraction with the putative histone acetyltransferase ELP3. Plant J Cell Mol Biol 71:263–272

    Article  CAS  Google Scholar 

  • Valenzuela-Fernandez A, Cabrero JR, Serrador JM, Sanchez-Madrid F (2008) HDAC6: a key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol 18:291–297

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Alam SL, Meyer HH, Payne M, Stemmler TL, Davis DR, Sundquist WI (2003) Structure and ubiquitin interactions of the conserved zinc finger domain of Npl4. J Biol Chem 278:20225–20234

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Li S, Kim YJ, Zeng Q, Radziejwoski A, Wang L, Nomura Y, Nakagami H, Somers D (2021) TOC1 clock protein phosphorylation controls complex formation with NF-YB/C to repress hypocotyl growth. EMBO J 40(24):e108684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH (2008) BetaC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22:2564–2577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  CAS  PubMed  Google Scholar 

  • Yruela I, Moreno-Yruela C, Olsen CA (2021) Zn2+-dependent histone deacetylases in plants: structure and evolution. Trends Plant Sci 26(7):741–757

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Peng T, Chen CY, Ji R, Gu D, Li T, Zhang D, Tu YT, Wu K, Liu X (2019) HY5 interacts with the histone deacetylase HDA15 to repress hypocotyl cell elongation in photomorphogenesis. Plant Physiol 180:1450–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou R, Han L, Li G, Tong T (2009) Senescence delay and repression of p16INK4a by Lsh via recruitment of histone deacetylases in human diploid fibroblasts. Nucleic Acids Res 37:5183–5196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are grateful to the unwavering support of the various laboratory professors, mentors, colleagues, and staff for the conduct of this research. Special mention goes to Prof. Keqiang Wu and Prof. Hsu-Liang Hsieh of NTU and Prof. Jeong Joo Cheong of SNU for their guidance and access to their facilities. MVA is equally indebted to the scholarship and research fellowship grants funded by the Democratic Pacific Union, National Science Council of Taiwan, National Taiwan University, and Seoul National University.

Funding

This work was supported by the Democratic Pacific Union PhD studentship and research fellowship grants from the National Science Council of Taiwan, National Taiwan University, and Seoul National University to MVA.

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Authors and Affiliations

  1. Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei, Taiwan

    Malona V. Alinsug

  2. Center for Food & Bioconvergence, College of Agriculture & Life Sciences, Seoul National University, Seoul, South Korea

    Malona V. Alinsug

  3. Atomic Research Division, Philippine Nuclear Research Institute, Department of Science and Technology, Commonwealth Avenue, Diliman, 1101, Quezon City, Philippines

    Malona V. Alinsug & Custer C. Deocaris

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  1. Malona V. Alinsug
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Both authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by MVA and CCD. The first draft of the manuscript was written by MVA and CCD commented on previous versions of the manuscript. Both authors read and approved the final manuscript.

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Correspondence to Malona V. Alinsug.

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Communicated by Dawei Xue.

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Alinsug, M.V., Deocaris, C.C. AtHDA15 attenuates COP1 via transcriptional quiescence, direct binding, and sub-compartmentalization during photomorphogenesis. Plant Growth Regul 101, 145–158 (2023). https://doi.org/10.1007/s10725-023-01008-x

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