Fruit ripening depends on the accurate control of ripening-related genes expression, with histone deacetylases (HDACs) playing crucial roles in transcriptional regulation. However, the functions of HDACs in fruit maturation remain largely unexplored. Here, we show that SlHDA7 acts as a suppressor of fruit ripening and functions as an H4ac HDAC in tomato. Deletion of SlHDA7 accelerated fruit ripening, while overexpression of SlHDA7 delayed the maturation process. Additionally, ethylene production and carotenoid biosynthesis significantly increased in slhda7 mutant fruits but decreased in SlHDA7-overexpressing fruits. Furthermore, SlHDA7 repress the expression of ethylene production and signaling, carotenoid metabolism, cell wall modification, and transcriptional regulation-related genes. RT-qPCR and ChIP-qPCR analyses indicated that SlHDA7 may deacetylate H4ac, leading to reduced transcript levels of ACO1, GGPPS2, Z-ISO, EXP1, and XYL1 mRNA, consequently suppressing fruit ripening. Moreover, SlHDA7 suppresses fruit ripening by targeting specific ripening-associated transcription factors (TFs) like RIN, FUL1, and ERF.E1, ultimately leading to delayed ripening and prolonged fruit shelf life. In summary, our findings indicate that SlHDA7 negatively modulates tomato fruit maturation by adjusting H4ac levels of these ripening-associated genes and key TFs.
Acknowledgements
This work was funded by the National Natural Science Foundation of China (Nos. 32272782, 32302625, and 32101567), Guangdong Basic and Applied Basic Research Foundation (Nos. 2023A1515010369 and 2022A1515010518), South China Botanical Garden, Chinese Academy of Sciences (Granted No: QNXM-202306), and Innovative Team Project of Guangdong Universities (Nos. 2022KCXTD051), Guangdong Science and Technology Plan Project (Grant No: 2023B1212060046).
Author contributions
G.J. designed the experiments. Y.Z., Z.L., and H.H. performed the experiments. Y.Z. and G.J. wrote the paper. X.D., Y.J., X.S., and H.Q. edited the manuscript. All authors discussed and approved the final manuscript.
Data availability
The RNA-Seq data have been deposited in the Dryad in the following repository (
https://datadryad.org/stash/share/dFeS6NvPQK_xhouVJUpnPQYRN2R5VkjHNAvbqiel2R8).
Conflict of interests
The authors declare no competing interests.
Supplementary data
Supplementary data is available at Horticulture Research online.
| [1] |
Klee HJ, Giovannoni JJ. Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet. 2011; 45:41-59
|
| [2] |
Deng L, Yang T, Li Q. et al. Tomato MED25 regulates fruit ripening by interacting with EIN3-like transcription factors. Plant Cell. 2023; 35:1038-57
|
| [3] |
Shan W, Kuang JF, Wei W. et al. MaXB3 modulates MaNAC2, MaACS1, and MaACO1 stability to repress ethylene biosynthesis during banana fruit ripening. Plant Physiol. 2020; 184:1153-71
|
| [4] |
Brumos J. Gene regulation in climacteric fruit ripening. Curr Opin Plant Biol. 2021; 63:6224-36
|
| [5] |
Berger SL, Kouzarides T, Shiekhattar R. et al. An operational definition of epigenetics. Genes Dev. 2009; 23:781-3
|
| [6] |
Allis CD, Jenuwein T. The molecular hallmarks of epigenetic control. Nat Rev Genet. 2016; 17:487-500
|
| [7] |
Giovannoni J, Cuong N, Ampofo B. et al. The epigenome and transcriptional dynamics of fruit ripening. Annu Rev Genet. 2017; 68:61-84
|
| [8] |
Zhong S, Fei ZJ, Chen YR. et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol. 2013; 31:154-9
|
| [9] |
Liu R, How-Kit A, Stammitti L. et al. A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc Natl Acad Sci USA. 2015; 112:10804-9
|
| [10] |
Cheng J, Niu Q, Zhang B. et al. Downregulation of RdDM during strawberry fruit ripening. Genome Res. 2018; 19:212
|
| [11] |
Huang H, Liu RE, Niu QF. et al. Global increase in DNA methylation during orange fruit development and ripening. Proc Natl Acad Sci USA. 2019; 116:1430-6
|
| [12] |
Lang Z, Wang YH, Tang K. et al. Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc Natl Acad Sci USA. 2017; 114:E4511-9
|
| [13] |
Li Z, Jiang GX, Liu XC. et al. Histone demethylase SlJMJ6 promotes fruit ripening by removing H3K27 methylation of ripening-related genes in tomato. New Phytol. 2020; 227:1138-56
|
| [14] |
Ding X, Liu XC, Jiang GX. et al. SlJMJ7 orchestrates tomato fruit ripening via crosstalk between H3K4me3 and DML2-mediated DNA demethylation. New Phytol. 2021; 233:1202-19
|
| [15] |
Verdone L, Agricola E, Caserta M. et al. Histone acetylation in gene regulation. Brief Funct Genomics. 2006; 5:209-21
|
| [16] |
Pandey R, Müller A, Napoli CA. et al. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 2002; 30:5036-55
|
| [17] |
Hollender C, Liu Z. Histone deacetylase genes in Arabidopsis development. J Integr Plant Biol. 2008; 50:875-85
|
| [18] |
Chhun T, Chong SY, Park BS. et al. HSI2 repressor recruits MED13 and HDA6 to down-regulate seed maturation gene expression directly during Arabidopsis early seedling growth. Plant Cell Physiol. 2016; 57:1689-706
|
| [19] |
Tian L, Chen ZJ. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc Natl Acad Sci USA. 2001; 98:7647-7
|
| [20] |
Zhou JJ, Liang Y, Niu QK. et al. The Arabidopsis general transcription factor TFIIB1 (AtTFIIB1) is required for pollen tube growth and endosperm development. J Exp Bot. 2013; 64:2205-18
|
| [21] |
Xu CR, Liu C, Wang YL. et al. Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc Natl Acad Sci USA. 2005; 102:14469-74
|
| [22] |
Liu C, Li LC, Chen WQ. et al. HDA18 affects cell fate in Arabidopsis root epidermis via histone acetylation at four kinase genes. Plant Cell. 2013; 25:257-69
|
| [23] |
Kang MJ, Jin HS, Noh YS. et al. Repression of flowering under a noninductive photoperiod by the HDA9-AGL19-FT module in Arabidopsis. New Phytol. 2015; 206:281-94
|
| [24] |
Bollier N, Sicard A, Leblond J. et al. At-MINI ZINC FINGER2 and Sl-INHIBITOR of MERISTEM ACTIVITY, a conserved missing link in the regulation of floral meristem termination in Arabidopsis and tomato. Plant Cell. 2018; 30:83-100
|
| [25] |
Chen X, Lu L, Mayer KS. et al. POWERDRESS interacts with HISTONE DEACETYLASE 9 to promote aging in Arabidopsis. elife. 2016; 5:e17214
|
| [26] |
Luo M, Yu CW, Chen FF. et al. Histone deacetylase HDA6 is functionally associated with AS1 in repression of KNOX genes in Arabidopsis. PLoS Genet. 2012; 8:e1003114
|
| [27] |
Han YC, Kuang JF, Chen JY. et al. Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol. 2016; 171:1070-84
|
| [28] |
Guo JE, Hu ZL, Zhu MK. et al. The tomato histone deacetylase SlHDA1 contributes to the repression of fruit ripening and carotenoid accumulation. Sci Rep. 2017; 7:7930
|
| [29] |
Guo JE, Hu ZL, Yu XH. et al. A histone deacetylase gene, SlHDA3, acts as a negative regulator of fruit ripening and carotenoid accumulation. Plant Cell Rep. 2018; 37:125-35
|
| [30] |
Li X, Guo W, Li JC. et al. Histone acetylation at the promoter for the transcription factor PuWRKY31 affects sucrose accumulation in pear fruit. Plant Physiol. 2020; 182:2035-46
|
| [31] |
Zhang Z, Wang B, Wang S. et al. Genome-wide target mapping shows histone deacetylase complex1 regulates cell proliferation in cucumber fruit. Plant Physiol. 2020; 182:167-84
|
| [32] |
Hu Y, Han ZY, Wang T. et al. Ethylene response factor MdERF4 and histone deacetylase MdHDA19 suppress apple fruit ripening through histone deacetylation of ripening-related genes. Plant Physiol. 2022; 188:2166-81
|
| [33] |
Guo JE. Histone deacetylase gene SlHDT1 regulates tomato fruit ripening by affecting carotenoid accumulation and ethylene biosynthesis. Plant Sci. 2022; 318:111235
|
| [34] |
Deng H, Chen Y, Liu ZY. et al. SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the co-repressor TOPLESS and histone deacetylases to repress key ripening genes. Plant Cell. 2022; 34:1250-72
|
| [35] |
Guo JE, Hu Z, Li F. et al. Silencing of histone deacetylase SlHDT3 delays fruit ripening and suppresses carotenoid accumulation in tomato. Plant Sci. 2017; 265:29-38
|
| [36] |
Tang D, Philippe G, Lang Z. Fruit development and epigenetic modifications. New Phytol. 2020; 228:839-44
|
| [37] |
Zhao LM, Lu JX, Zhang JX. et al. Identification and characterization of histone deacetylases in tomato (Solanum lycopersicum). Front Plant Sci. 2015; 5:760
|
| [38] |
Lee K, Lee HY, Back K. Rice histone deacetylase 10 and Arabidopsis histone deacetylase 14 genes encode N-acetylserotonin deacetylase, which catalyzes conversion of N-acetylserotonin into serotonin, a reverse reaction for melatonin biosynthesis in plants. J Pineal Res. 2018; 64:e12460
|
| [39] |
Zhao ML, Wang W, Nie H. et al. In silico structure prediction and inhibition mechanism studies of AtHDA 14 as revealed by homology modeling, docking, molecular dynamics simulation. Comput Biol. 2018; 75:120-30
|
| [40] |
Yruela I, Moreno-Yruela C, Olsen CA. Zn2+-dependent histone deacetylases in plants: structure and evolution. Trends Plant Sci. 2021; 26:741-57
|
| [41] |
Yu XH, Gao Q, Chen GP. et al. SlHDA5, a tomato histone deacetylase gene, is involved in responding to salt, drought, and ABA. Plant Mol Biol Report. 2018; 36:36-44
|
| [42] |
Li X, Wang X, Zhang Y. et al. Regulation of fleshy fruit ripening: from transcription factors to epigenetic modifications. Hort Res. 2022; 9:uhac013
|
| [43] |
Dai X, Bai YH, Zhao LH. et al. H2A.Z represses gene expression by modulating promoter nucleosome structure and enhancer histone modifications in Arabidopsis. Mol Plant. 2018; 11:635-5
|
| [44] |
Zheng Y, Ding Y, Sun X. et al. Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot. 2016; 67:1703-13
|
| [45] |
Li S, Chen KS, Grierson D. A critical evaluation of the role of ethylene and MADS transcription factors in the network controlling fleshy fruit ripening. New Phytol. 2019; 221:1724-41
|
| [46] |
Liu MC, Diretto G, Pirrello J. et al. The chimeric repressor version of an ethylene response factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol. 2014; 203:206-18
|
| [47] |
Li S, Chen KS, Grierson D. et al. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycopersicum). Plant Physiol Biochem. 2017; 118:235-44
|
| [48] |
Jia H, Xie ZQ, Wang C. et al. Abscisic acid, sucrose, and auxin coordinately regulate berry ripening process of the Fujiminori grape. Funct Integr Genomics. 2017; 17:441-57
|
| [49] |
Martin-Pizarro C, Vallarino JG, Osorio S. et al. The NAC transcription factor FaRIF controls fruit ripening in strawberry. Plant Cell. 2021; 33:1574-93
|
| [50] |
Bemer M, Karlova AR, Ballester YM. et al. The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell. 2012; 24:4437-51
|
| [51] |
Ito Y, Nishizawa-Yokoi A, Endo M. et al. Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nat Plants. 2017; 3:866-74
|
| [52] |
Fujisawa M, Nakano T, Shima Y. et al. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell. 2013; 25:371-86
|
| [53] |
Fujisawa M, Shima Y, Nakagawa H. et al. Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins. Plant Cell. 2014; 26:89-101
|
| [54] |
Li S, Zhu B, Pirrello J. et al. Roles of RIN and ethylene in tomato fruit ripening and ripening-associated traits. New Phytol. 2020; 226:460-75
|
| [55] |
Wang Z, Wang SB, Li DW. et al. Optimized paired-sgRNA/Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit. Plant Biotechnol J. 2018; 16:1424-33
|
| [56] |
Jiang G, Zeng J, Li ZW. et al. Redox regulation of the NOR transcription factor is involved in the regulation of fruit ripening in tomato. Plant Physiol. 2020; 183:671-85
|
| [57] |
Gao Y, Wei W, Zhao XD. et al. A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Hort Res. 2018; 5:75
|
| [58] |
Chung MY, Vrebalov J, Alba R. et al. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 2010; 64:936-47
|
| [59] |
Forth D, Pyke KA. The suffulta mutation in tomato reveals a novel method of plastid replication during fruit ripening. J Exp Bot. 2006; 57:1971-9
|
| [60] |
Sun QQ, Zhang N, Wang JF. et al. Melatonin promotes ripening and improves quality of tomato fruit during postharvest life. J Exp Bot. 2015; 66:657-68
|
| [61] |
Mayer KS, Chen XS, Sanders D. et al. HDA9-PWR-HOS15 is a core histone deacetylase complex regulating transcription and development. Plant Physiol. 2019; 180:342-55
|