Abstract
Histone deacetylases (HDACs) are important regulators that participate in plant growth and development. HISTONE DEACETYLASE 9 (HDA9), HISTONE DEACETYLASE 6 (HDA6) and FLOWERING LOCUS D (FLD) are reported to be involved in flowering regulation, stress response and other regulation in Arabidopsis, but whether and how there is a protein relationship between them in Chinese cabbage (Brassica rapa L. ssp. pekinensis) is still unknown. In this study, BrFLD, two members of BrHDA6, and BrHDA9 were cloned from Brassica rapa and ubiquitously expressed in roots, stems, cauline leaves, flower buds and opening flowers. Those genes exhibited their highest transcript levels in cauline leaves and lowest levels in stems or flower buds. BrFLD and two BrHDA6s were highly induced by long-day photoperiod, but BrHDA9 was highly induced by short-day. The genes are diel regulated and have different patterns across the photoperiods. Yeast two-hybrid assays and glutathione S-transferase (GST) pull-down assays revealed that the BrFLD protein interacts with the two BrHAD6 proteins but not with the BrHDA9 protein, and no interaction was detected between BrHDA9 and the two BrHDA6s. Further research showed that the SWIRM domain of BrFLD and the C-domain of BrHDA6 are the key domains involved in these interactions. This result suggested that HDAC genes are regulated by photoperiod and participate in autonomous pathway control flowering time through integration with FLD or regulate flowering independently of FLD.
Similar content being viewed by others
Data availability
The data supporting the conclusions of this study are included within the article.
References
Ausín I, Alonso-Blanco C, Jarillo JA, Ruiz-García L, Martínez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36:162–166
Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops what did we learn from Arabidopsis? Curr Opin Biotech 32:121–129
Chen LT, Luo M, Wang YY, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353
Fornara F, Montaigu AD, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141: 550–550
Gu X, Jiang D, Yang W, Jacob Y, Michaels SD, He Y (2011) Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. Plos Genet 7:e1002366
Guan-Peng MA, Da-Qin ZH, Tian-Wen WA, Lin-Bi ZH, Gui-Lian LI (2019) BBX32 interacts with AGL24 involved in flowering time control in Chinese cabbage (Brassica rapa L. ssp pekinensis). Not Bot Horti Agrobot 47:34
He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302:1751–1754
Hollender C, Liu Z (2008) Histone deacetylase genes in Arabidopsis development. J Integr Plant Biol 50:875–885
Jiang D, Yang W, He Y, Amasino RM (2007) Arabidopsis relatives of the human lysine-specific Demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19:2975–2987
Jiang W, Wei D, Zhou W, Wang Z, Tang Q (2018) HDA9 interacts with the promoters of SOC1 and AGL24 involved in flowering time control in Brassica juncea. Biochem Bioph Res Co 499:519–523
Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, Hasegawa PM (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 53:530–540
Kang MJ, Jin HS, Noh YS, Noh B (2015a) Repression of flowering under a noninductive photoperiod by the HDA 9-AGL 19-FT module in Arabidopsis. New Phytol 206:281–294
Kang MJ, Jin HS, Noh YS, Noh B (2015b) Repression of flowering under a noninductive photoperiod by the HDA 9-AGL19-FT module in Arabidopsis. New Phytol 206:281–294
Kim W, Latrasse D, Servet C, Zhou DX (2013) Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19. Biochem Biophy Res Commun 432:394–398
Lenfant N, Hotelier T, Velluet E, Bourne Y, Marchot P, Chatonnet A (2012) ESTHER, the database of the α/β-hydrolase fold superfamily of proteins: tools to explore diversity of functions. Nucleic Acids Res 41:D423–D429
Lin J, Hung FY, Ye C, Hong L, Shih YH, Wu K, Li QQ (2020) HDA6-dependent histone deacetylation regulates mRNA polyadenylation in Arabidopsis. Genome Res 30:1407–1417
Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97
Liu X, Yang S, Zhao M, Luo M, Yu CW, Chen CY, Wu K (2014) Transcriptional repression by histone deacetylases in plants. Mol Plant 7:764–772
Liu J, Zhang H, Lian X, Converse R, Zhu L (2016) Identification of interacting motifs between armadillo repeat containing 1 (ARC1) and Exocyst 70 A1 (Exo70A1) proteins in Brassica oleracea. Protein J 35:34–43
Luo M, Tai R, Yu CW, Yang S, Chen CY, Lin WD, Wu K (2015) Regulation of flowering time by the histone deacetylase HDA 5 in Arabidopsis. Plant J 82:925–936
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:636–641
Pandey R, MuÈller 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
Putterill J, Varkonyi-Gasic E (2016) FT and florigen long-distance flowering control in plants. Curr Opin Plant Biol 33:77–82
Sakharkar AJ, Vetreno RP, Zhang H, Kokare DM, Crews FT, Pandey SC (2016) A role for histone acetylation mechanisms in adolescent alcohol exposure-induced deficits in hippocampal brain-derived neurotrophic factor expression and neurogenesis markers in adulthood. Brain Struct Funct 221:4691–4703
Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468
To TK, Kim JM, Matsui KY, 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:e1002055
van Zanten M, Zöll C, Wang Z, Philipp C, Carles A, Li Y, Kornet NG, Liu Y, Soppe WJ (2014) HISTONE DEACETYLASE 9 represses seedling traits in Arabidopsis thaliana dry seeds. Plant J 80:475–488
Verhage L, Angenent GC, Immink RGH (2014) Research on floral timing by ambient temperature comes into blossom. Trends Plant Sci 19:583–591
Wang Z, Cao H, Chen F, Liu Y (2014) The roles of histone acetylation in seed performance and plant development. Plant Physiol Bioch 84:125–133
Wu K, Zhang L, Zhou C, Yu CW, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59:225–234
Yang H, Liu X, Xin M, Du J, Hu Z, Peng H, Rossi V, Sun Q, Ni Z, Yao Y, Du JHZ (2016) Genome-wide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development. Plant Cell 28:629–645
Yu CW, Liu X, Luo M, Chen C, Lin X, Tian G, Cui Y, Wu K (2011) HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol 156:173–184
Yu CW, Chang KY, Wu K (2016) Genome-wide analysis of gene regulatory networks of the FVE-HDA6-FLD complex in Arabidopsis. Front Plant Sci 7:555
Xiao D, Zhang NW, Zhao JJ, Bonnema G, Hou XL (2012) Validation of reference genes for real-time quantitative PCR normalisation in non-heading Chinese cabbage. Funct Plant Biol 39:342–350
Xu Y, Li Q, Yuan L, Huang Y, Hung FY, Wu K, Yang S (2022) MSI1 and HDA6 function interdependently to control flowering time via chromatin modifications. Plant J 109:831–843
Zhang X, Meng L, Liu B, Hu Y, Cheng F, Liang J, Mark GM, Wang X, Wu J (2015) A transposon insertion in FLOWERING LOCUS T is associated with delayed flowering in Brassica rapa. Plant Sci 241:211–220
Zheng Y, Ding Y, Sun X, Xie S, Wang D, Liu X, Su L, Wei W, Pan L, Zhou DX (2016) Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 67:1703–1713
Zhou JX, Du P, Liu ZW, Feng C, Cai XW, He XJ (2021) FVE promotes RNA-directed DNA methylation by facilitating the association of RNA polymerase V with chromatin. Plant J 107:467–479
Acknowledgements
This work was financially supported by the Project of Guizhou Science and Technology Department (Project No: [2020]1Y089, [2019]2392), the Research Program of Guizhou Academy of Agricultural Sciences (Project No: [2018]5768-11)
Author information
Authors and Affiliations
Contributions
DZ and GM conceived and designed the experiments. GM drafted the manuscript. LZ and LL performed the experiments and analyzed the data. DZ guided the experiments and provided advices. All authors read and approved the submitted manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ma, G., Zhou, L., Liu, L. et al. Expression patterns of HDA9, HDA6 and FLD in Chinese cabbage (Brassica rapa L. ssp. pekinensis) under different photoperiods and their protein interactions. Braz. J. Bot 46, 549–561 (2023). https://doi.org/10.1007/s40415-023-00897-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-023-00897-6