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Intracellular localization of histone deacetylase HDA6 in plants

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Abstract

Histone modification is an important epigenetic mechanism in eukaryotes. Histone acetyltransferase and deacetylase regulate histone acetylation levels antagonistically, leading to dynamic control of chromatin structure. One of the histone deacetylases, HDA6, is involved in gene silencing in the heterochromatin regions, chromocenter formation, and metabolic adaptation under drought stress. Although HDA6 plays an important role in chromatin control and response to drought stress, its intracellular localization has not been observed in detail. In this paper, we generated transformants expressing HDA6-GFP in the model plant, Arabidopsis thaliana, and the crops, rice, and cassava. We observed the localization of the fusion protein and showed that HDA6-GFP was expressed in the whole root and localized at the nucleus in Arabidopsis, rice, and cassava. Remarkably, HDA6-GFP clearly formed speckles that were actively colocalized with chromocenters in Arabidopsis root meristem. In contrast, such speckles were unlikely to be formed in rice or cassava. Because AtHDA6 directly binds to the acetate synthesis genes, which function in drought tolerance, we performed live imaging analyses to examine the cellular dynamics of pH in roots and the subnuclear dynamics of AtHDA6 responding to acetic acid treatment. The number of HDA6 speckles increased during drought stress, suggesting a role in contributing to drought stress tolerance.

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References

  • Allis CD, Jenuwein T (2016) The molecular hallmarks of epigenetic control. Nat Rev Genet 17:487–500

    Article  CAS  PubMed  Google Scholar 

  • Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earley KW, Pontvianne F, Wierzbicki AT, Blevins T, Tucker S, Costa-Nunes P, Pontes O, Pikaard CS (2010) Mechanisms of HDA6-mediated rRNA gene silencing: suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev 24:1119–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felle HH (2001) pH: signal and messenger in plant cells. Plant Biol 3:577–591

    Article  CAS  Google Scholar 

  • Geilfus CM (2017) The pH of the apoplast: dynamic factor with functional impact under stress. Mol Plant 10:1371–1386

    Article  CAS  PubMed  Google Scholar 

  • Gjetting SK, Ytting CK, Schulz A, Fuglsang AT (2012) Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J Exp Bot 63:3207–3218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grossmann G, Guo WJ, Ehrhardt DW, Frommer WB, Sit RV, Quake SR, Meier M (2011) The RootChip: an integrated microfluidic chip for plant science. Plant Cell 23:4234–4240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa J, Sakamoto Y, Nakagami S, Aida M, Sawa S, Matsunaga S (2016) Three-dimensional imaging of plant organs using a simple and rapid transparency technique. Plant Cell Physiol 57:462–472

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa J, Sakamoto T, Fujimoto S, Yamashita T, Suzuki T, Matsunaga S (2018) Auxin decreases chromatin accessibility through the TIRl/AFBs auxin signaling pathway in proliferative cells. Sci Rep 8:12

    Article  CAS  Google Scholar 

  • Hida H, Nishiyama H, Sawa S, Higashiyama T, Arata H (2015) Chemotaxis assay of plant-parasitic nematodes on a gel-filled microchannel device. Sens Actuat B-Chem 221:1483–1491

    Article  CAS  Google Scholar 

  • Hirakawa T, Hasegawa J, White CI, Matsunaga S (2017) RAD54 forms DNA repair foci in response to DNA damage in living plant cells. Plant J 90:372–382

    Article  CAS  PubMed  Google Scholar 

  • Hollender C, Liu ZC (2008) Histone deacetylase genes in Arabidopsis development. J Integrat Plant Biol 50:875–885

    Article  CAS  Google Scholar 

  • Kim JM, To TK, Seki M (2012) An epigenetic integrator: new insights into genome regulation, environmental stress responses and developmental controls by histone deacetylase 6. Plant Cell Physiol 53:794–800

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, To TK, Matsui A, Tanoi K, Kobayashi NI, Matsuda F, Habu Y, Ogawa D, Sakamoto T, Matsunaga S, Bashir K, Rasheed S, Ando M, Takeda H, Kawaura K, Kusano M, Fukushima A, Endo TA, Kuromori T, Ishida J, Morosawa T, Tanaka M, Torii C, Takebayashi Y, Sakakibara H, Ogihara Y, Saito K, Shinozaki K, Devoto A, Seki M (2017) Acetate-mediated novel survival strategy against drought in plants. Nat Plants 3:7

    Google Scholar 

  • Layat E, Sáez-Vásquez J, Tourmente S (2012) Regulation of Pol I-transcribed 45S rDNA and Pol III-transcribed 5S rDNA in Arabidopsis. Plant Cell Physiol 53:267–276

    Article  CAS  PubMed  Google Scholar 

  • Maluszynska J, Heslopharrison JS (1991) Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1:159–166

    Article  Google Scholar 

  • Massalha H, Korenblum E, Malitsky S, Shapiro OH, Aharoni A (2017) Live imaging of root-bacteria interactions in a microfluidics setup. Proc Natl Acad Sci USA 14:4549–4554

    Article  CAS  Google Scholar 

  • Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Tanaka K, Niwa Y, Watanabe Y, Nakamura K, Kimura T, Ishiguro S (2007) Improved gateway binary vectors: high-performance vectors for creation of fusion constructs in Transgenic analysis of plants. Biosci Biotechnol Biochem 71:2095–2100

    Article  CAS  PubMed  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 

  • Park J, Kurihara D, Higashiyama T, Arata H (2014) Fabrication of microcage arrays to fix plant ovules for long-term live imaging and observation. Sens Actuat B-Chem 191:178–185

    Article  CAS  Google Scholar 

  • Pontes O, Lawrence RJ, Silva M, Preuss S, Costa-Nunes P, Earley K, Neves N, Viegas W, Pikaard CS (2007) Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PLoS One 2:e1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, Vaucheret H, Scheid OM (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosa S, Ntoukakis V, Ohmido N, Pendle A, Abranches R, Shaw P (2014) Cell differentiation and development in Arabidopsis are associated with changes in histone dynamics at the single-cell level. Plant Cell 26:4821–4833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto T, Inui YT, Sotta N, Hirakawa T, Matsunaga TM, Fukao Y, Matsunaga S, Fujiwara T (2018) Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis. Nat Commun 9:5258

    Article  CAS  Google Scholar 

  • To TK, Kim JM, Matsui A, Kurihara Y, Morosawa T, Ishida J, Tanaka M, Endo T, Kakutani T, Toyoda T, Kimura H, Yokoyama S, Shinozaki K, Seki M (2011) Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet 7:14

    Article  CAS  Google Scholar 

  • Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976

    Article  CAS  PubMed  Google Scholar 

  • Utsumi Y, Utsumi C, Tanaka M, Ha VT, Matsui A, Takahashi S, Seki M (2017) Formation of friable embryogenic callus in cassava is enhanced under conditions of reduced nitrate, potassium and phosphate. PLoS One 12:e0180736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaillant I, Tutois S, Cuvillier C, Schubert I, Tourmente S (2007) Regulation of Arabidopsis thaliana 5S rRNA genes. Plant Cell Physiol 48:745–752

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (1997) Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol 113:559–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zentner GE, Henikoff S (2013) Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20:259–266

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by Japan Science and Technology Agency (JST) CREST Grant (JPMJCR13B4) and MXT/JSPS KAKENHI (15H05955, 15H05962 and 19H03259) to SM and by MXT/JSPS KAKENHI (18K14743) and the Sasakawa Scientific Research Grant from Japan Science Society to YS. We thank Huw Tyson, PhD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.

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Author notes

  1. Kazuki Kurita and Yuki Sakamoto equally contributed to this work.

Authors and Affiliations

  1. Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510, Japan

    Kazuki Kurita, Sota Naruse, Takuya Sakamoto & Sachihiro Matsunaga

  2. Research Institute for Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510, Japan

    Yuki Sakamoto, Tomoko M. Matsunaga & Sachihiro Matsunaga

  3. Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8602, Japan

    Hideyuki Arata & Tetsuya Higashiyama

  4. Plant Physiology Research Unit, Division of Plant and Microbial Sciences, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8602, Japan

    Yoshiki Habu

  5. Plant Genomic Network Research Team, RIKEN Centre for Sustainable Resource Science (CSRS), 1-7-22 Suehiro, Tsurumi, Yokohama, 230-0045, Japan

    Yoshinori Utsumi, Chikako Utsumi, Maho Tanaka, Satoshi Takahashi, Jong-Myong Kim & Motoaki Seki

  6. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Jong-Myong Kim

  7. Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

    Motoaki Seki

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  1. Kazuki Kurita
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  2. Yuki Sakamoto
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Correspondence to Sachihiro Matsunaga.

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Kurita, K., Sakamoto, Y., Naruse, S. et al. Intracellular localization of histone deacetylase HDA6 in plants. J Plant Res 132, 629–640 (2019). https://doi.org/10.1007/s10265-019-01124-8

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