The Role of NAD-dependent Deacetylase SRT in Plant Epigenetic Inheritance Regulation

doi:10.13560/j.cnki.biotech.bull.1985.2022-0971

Abstract

Abstract:

Sirtuin（SRT）is one of nicotinamide adenine dinucleotide（NAD）-dependent protein deacetylases being highly homologous to yeast silencing information regulator 2（Sir2）. In eukaryotes, SRT regulates chromosome stability, gene transcription and the activity status of related proteins by catalyzing the deacetylation of specific or non-histone lysine（Lys）residues. Studies have shown that SRT-mediated deacetylation plays an important role in plant metabolism, growth and development, and stress response. In this review, the identification, structure and classification, biological evolution, epigenetic regulation mechanism and biological processes of SRT in plants are summarized, and its future research directions are also prospected, aiming to provide a basis for future research on SRT-mediated epigenetic biological processes in plant.

Key words: NAD, deacetylase, epigenetics, growth and development, stress response

WEI Ming WANG Xin-yu WU Guo-qiang ZHAO Meng. The Role of NAD-dependent Deacetylase SRT in Plant Epigenetic Inheritance Regulation[J]. Biotechnology Bulletin, 2023, 39(4): 59-70.

Figures/Tables 4

Table 1 SRT gene families in different plant species

物种 Species	基因名称Gene name	蛋白长度 Protein length/aa	分子量 Mw/kD	等电点 pI	亚细胞定位 Subcellular localization	参考文献 Reference
拟南芥Arabidopsis thaliana	AtSRT1	473	52.64	8.54	Nucleus	[22]
拟南芥Arabidopsis thaliana	AtSRT2	376	41.87	9.08	Mitochondria	[22]
水稻Oryza sativa	OsSRT1	483	53.90	9.38	Nucleus	[23-24]
水稻Oryza sativa	OsSRT2	393	43.47	8.79	Mitochondria	[23-24]
葡萄Vitis vinifera	VvSRT1	467	52.04	9.24	/	[25]
葡萄Vitis vinifera	VvSRT2	382	41.99	9.09	/	[25]
番茄Solanum lycopersicum	SlSRT1	472	52.50	9.10	Nucleus	[26-27]
番茄Solanum lycopersicum	SlSRT2	389	43.06	8.97	Mitochondria	[26-27]
大豆Glycine max	GmSRT1	393	43.46	9.40	Mitochondria chloroplast	[28-29]
	GmSRT2	392	43.21	9.32	Mitochondria chloroplast
	GmSRT3	434	48.21	9.11	Nucleus chloroplast
	GmSRT4	479	53.20	9.15	Nucleus cytoplasm
地钱Marchantia polymorpha	MpSIRT4	377	41.22	8.36	Mitochondria	[30]
	MpSIRT5	285	30.75	7.02	/
	MpSIRT6	379	41.39	7.60	Nucleus cytosol
玉米Zea mays	ZmSRT1	437	49.05	9.31	/	[31]
玉米Zea mays	ZmSRT2	351	39.19	8.91	/	[31]
茶树Camellia sinensis	CsSRT1	566	63.46	9.29	Nucleus	[32]
	CsSRT2	460	51.36	8.82	Chloroplast
	CsSRT3	479	53.39	9.11	Chloroplast
	CsSRT4	177	19.77	9.58	Nucleus
石斛Dendrobium officinale	DoSRT1	409	45.50	8.19	Nucleus	[33]
石斛Dendrobium officinale	DoSRT2	279	30.82	7.04	Nucleus	[33]
白梨Pyrus bretschneideri	PbSRT1	484	54.13	9.27	Nucleus cytoplasm	[34]
白梨Pyrus bretschneideri	PbSRT2	394	43.46	8.80	Chloroplast vacuole	[34]
大麻Cannabis sativa	CsSRT1	484	53.61	9.04	Nucleus chloroplast	[35]
大麻Cannabis sativa	CsSRT2	397	43.49	8.37	Nucleus chloroplast	[35]
高粱Sorghum bicolor	SbSRT1	476	53.24	8.88	Chloroplast	[36]
高粱Sorghum bicolor	SbSRT2	484	53.66	9.17	Chloroplast	[36]
甜菜Beta vulgaris	BvSRT1	496	55.64	9.22	/	Unpublished data
甜菜Beta vulgaris	BvSRT2	389	43.37	8.89	/	Unpublished data

Fig. 1 Three-dimensional structure of SRTs in plants The three-dimensional structure of SIR2 domain in SRT1（A）and SRT2（B）proteins from Oryza sativa was predicted by homology modeling using SWISS-MODEL workspace[38]. The protein sequences of SRTs SIR2 domain were applied to search for a suitable template in the SWISS-MODEL Template Library（SMTL）and two crystal structures of SIR2（SRT1/2）from Homo sapiens（SMTL ID: 3k35.1 for SRT1）and Xenopus tropicalis（SMTL ID: 5oj7.1 for SRT2）were selected as the templates by the Global Model Quality Estimation（GMQE）values and the QMEANZ-scores[43-45]. Visualization and comparison of the SIR2 domains from SRT1 and SRT2 protein were performed through the Swiss PDB viewer and PyMOL program[46]

Fig. 2 Phylogenetic analysis of SRTs in different species SRTs基因的来源、名称及蛋白登录号如下: 拟南芥（Arabidopsis thaliana）AtSRT1（NP_200387.1）, AtSRT2（NP_001078550.1）；水稻（Oryza sativa）OsSRT1（XP_015636502.1）, OsSRT2（XP_015618411.1）；葡萄（Vitis riparia）VrSRT1（XP_034679101.1）, VrSRT2（XP_010652926.1）；番茄（Solanum lycopersicum）SlSRT1（XP_004244044.1）, SlSRT2（XP_004236824.1）；大豆（Glycine max）GmSRT1（XP_003522478.1）, GmSRT1（XP_003528059.2）, GmSRT3（KHN11152.1）, GmSRT4（XP_003551434.1）；地钱（Marchantia polymorpha）MpSIRT（PTQ32963.1）, MpSIRT5（PTQ31328.1）, MpSIRT6（PTQ40866.1）；玉米（Zea mays）ZmSRT1（NP_001105577.1）, ZmSRT2（XP_020400867.1）；白梨（Pyrus bretschneideri）PbSRT1（XP_009375070.1）, PbSRT2（XP_009375792.1）；大麻（Cannabis sativa）CsSRT1（XP_030478610.1）, CsSRT2（XP_030499415.1）；高粱（Sorghum bicolor）SbSRT1（XP_021318881.1）, SbSRT2（XP_002442918.2）；甜菜（Beta vulgaris）BvSRT1（XP_019104724.1）, BvSRT2（XP_010674411.1）；菠菜（Spinacia oleracea）SoSRT1（XP_021842668.1）, SoSRT2（XP_021835887.1）；油菜（Brassica napus）BnSRT1（XP_022570011.1）, BnSRT2（XP_013675778.1）；芜菁（Brassica rapa）BrSRT1（XP_009132354.1）, BrSRT2（XP_033140955.1）；荠菜（Capsella rubella）CrSRT1（XP_023641545.1）, CrSRT2（XP_023637530.1）；烟草（Nicotiana tabacum）NtSRT1（XP_016490271.1）, NtSRT2（XP_016482509.1）；小麦（Triticum aestivum）TaSRT1（XP_044455034.1）, TaSRT2（XP_044380222.1）；谷子（Setaria italica）SiSRT1（XP_004975166.1）, SiSRT2（XP_004977219.1）；狗尾草（Setaria viridis）SvSRT1（XP_034603198.1）, SvSRT2（XP_034606073.1）；花生（Arachis hypogaea）AhSRT1（XP_025626741.1）, AhSRT2（XP_025615786.1）；木豆（Cajanus cajan）CcSRT1（XP_020232854.1）, CcSRT2（XP_020234960.1）；鹰嘴豆（Cicer arietinum）CaSRT1（XP_004516096.2）, CaSRT2（XP_004502971.1）；大叶栎（Quercus lobata）QlSRT1（XP_030931433.1）, QlSRT2（XP_030940716.1）；番木瓜（Carica papaya）CpSRT1（XP_021906115.1）, CpSRT2（XP_021900464.1）；南瓜（Cucurbita moschata）CmSRT1（XP_022936498.1）, CmSRT2（XP_022948086.1）；蒺藜苜蓿（Medicago truncatula）MtSRT1（XP_013460060.1）, MtSRT2（XP_003602659.1）；豇豆（Vigna unguiculata）VuSRT1（XP_027930984.1）, VuSRT2（XP_027901777.1）；冬瓜（Benincasa hispida）BhSRT1（XP_038900035.1）, BhSRT1（XP_038902560.1）；盐芥（Eutrema salsugineum）EsSRT1（XP_006401417.1）, EsSRT2（XP_006399395.1）

Fig. 3 Diagram of histone acetylation/deacetylation modif-ication and dynamic regulation of gene transcription HAT：组蛋白乙酰转移酶 Histone acetyltransferase；HDACs：组蛋白去乙酰化酶 Histone deacetylases；Ac：乙酰基 Acetyl；TF：转录因子 Transcription factor

References 95

[1]	Luger K, Mäder AW, Richmond RK, et al. Crystal structure of the nucleosome core particle at 2.8 A resolution[J]. Nature, 1997, 389(6648): 251-260. doi: 10.1038/38444
[2]	Zhou KD, Gaullier G, Luger K. Nucleosome structure and dynamics are coming of age[J]. Nat Struct Mol Biol, 2019, 26(1): 3-13. doi: 10.1038/s41594-018-0166-x pmid: 30532059
[3]	Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications[J]. Cell Res, 2011, 21(3): 381-395. doi: 10.1038/cr.2011.22 pmid: 21321607
[4]	Kouzarides T. Chromatin modifications and their function[J]. Cell, 2007, 128(4): 693-705. doi: 10.1016/j.cell.2007.02.005 pmid: 17320507
[5]	Yang TT, Wang DY, Tian GM, et al. Chromatin remodeling complexes regulate genome architecture in Arabidopsis[J]. Plant Cell, 2022, 34(7): 2638-2651. doi: 10.1093/plcell/koac117 URL
[6]	Cavalli G, Heard E. Advances in epigenetics link genetics to the environment and disease[J]. Nature, 2019, 571(7766): 489-499. doi: 10.1038/s41586-019-1411-0
[7]	Ueda M, Seki M. Histone modifications form epigenetic regulatory networks to regulate abiotic stress response[J]. Plant Physiol, 2020, 182(1): 15-26. doi: 10.1104/pp.19.00988 pmid: 31685643
[8]	Brukhin V, Albertini E. Epigenetic modifications in plant development and reproduction[J]. Epigenomes, 2021, 5(4): 25. doi: 10.3390/epigenomes5040025 URL
[9]	Xia C, Tao Y, Li M, et al. Protein acetylation and deacetylation: an important regulatory modification in gene transcription(Review)[J]. Exp Ther Med, 2020, 20(4): 2923-2940.
[10]	Wu X, Oh MH, Schwarz EM, et al. Lysine acetylation is a widespread protein modification for diverse proteins in Arabidop-sis[J]. Plant Physiol, 2011, 155(4): 1769-1778. doi: 10.1104/pp.110.165852 URL
[11]	Ma XJ, Lv SB, Zhang C, et al. Histone deacetylases and their functions in plants[J]. Plant Cell Rep, 2013, 32(4): 465-478. doi: 10.1007/s00299-013-1393-6 pmid: 23408190
[12]	Chen XS, Ding AB, Zhong XH. Functions and mechanisms of plant histone deacetylases[J]. Sci China Life Sci, 2020, 63(2): 206-216. doi: 10.1007/s11427-019-1587-x pmid: 31879846
[13]	Marmorstein R, Roth SY. Histone acetyltransferases: function, structure, and catalysis[J]. Curr Opin Genet Dev, 2001, 11(2): 155-161. pmid: 11250138
[14]	Sadoul K, Boyault C, Pabion M, et al. Regulation of protein turnover by acetyltransferases and deacetylases[J]. Biochimie, 2008, 90(2): 306-312. pmid: 17681659
[15]	van Gennip AH, Caron HN, et al. Histone deacetylases(HDACs): characterization of the classical HDAC family[J]. Biochem J, 2003, 370(Pt 3): 737-749. doi: 10.1042/bj20021321 URL
[16]	Tahir MS, Tian LN. HD2-type histone deacetylases: unique regulators of plant development and stress responses[J]. Plant Cell Rep, 2021, 40(9): 1603-1615. doi: 10.1007/s00299-021-02688-3 pmid: 34041586
[17]	Hollender C, Liu ZC. Histone deacetylase genes in Arabidopsis development[J]. J Integr Plant Biol, 2008, 50(7): 875-885. doi: 10.1111/j.1744-7909.2008.00704.x
[18]	Yruela I, Moreno-Yruela C, Olsen CA. Zn²⁺-dependent histone deacetylases in plants: structure and evolution[J]. Trends Plant Sci, 2021, 26(7): 741-757. doi: 10.1016/j.tplants.2020.12.011 URL
[19]	Zheng WP. Review: the plant sirtuins[J]. Plant Sci, 2020, 293: 110434. doi: 10.1016/j.plantsci.2020.110434 URL
[20]	Brachmann CB, Sherman JM, Devine SE, et al. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability[J]. Genes Dev, 1995, 9(23): 2888-2902. doi: 10.1101/gad.9.23.2888 URL
[21]	Martínez-Redondo P, Vaquero A. The diversity of histone versus nonhistone sirtuin substrates[J]. Genes Cancer, 2013, 4(3/4): 148-163. doi: 10.1177/1947601913483767 URL
[22]	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[J]. Nucleic Acids Res, 2002, 30(23): 5036-5055. doi: 10.1093/nar/gkf660 pmid: 12466527
[23]	Fu WQ, Wu KQ, Duan J. Sequence and expression analysis of histone deacetylases in rice[J]. Biochem Biophys Res Commun, 2007, 356(4): 843-850. doi: 10.1016/j.bbrc.2007.03.010 URL
[24]	符稳群, 吴克强, 张美, 等. 水稻组蛋白脱乙酰化酶SIR2的功能注释分析[J]. 安徽农业大学学报, 2008, 35(1): 70-75.
	Fu WQ, Wu KQ, Zhang M, et al. Analysis of function notation of histone deacetylase SIR2 family in rice by bioinformatics strategy[J]. J Anhui Agric Univ, 2008, 35(1): 70-75.
[25]	Aquea F, Timmermann T, Arce-Johnson P. Analysis of histone acetyltransferase and deacetylase families of Vitis vinifera[J]. Plant Physiol Biochem, 2010, 48(2/3): 194-199. doi: 10.1016/j.plaphy.2009.12.009 URL
[26]	Aiese Cigliano R, Sanseverino W, Cremona G, et al. Genome-wide analysis of histone modifiers in tomato: Gaining an insight into their developmental roles[J]. BMC Genomics, 2013, 14: 57. doi: 10.1186/1471-2164-14-57 pmid: 23356725
[27]	Zhao LM, Lu JX, Zhang JX, et al. Identification and characterization of histone deacetylases in tomato(Solanum lycopersicum)[J]. Front Plant Sci, 2015, 5: 760.
[28]	Yang C, Shen WJ, Chen HF, et al. Characterization and subcellular localization of histone deacetylases and their roles in response to abiotic stresses in soybean[J]. BMC Plant Biol, 2018, 18(1): 226. doi: 10.1186/s12870-018-1454-7 pmid: 30305032
[29]	方淑梅, 冯乃杰, 梁喜龙. 大豆去乙酰化酶Sir2的生物信息学分析[J]. 贵州农业科学, 2015, 43(8): 34-37.
	Fang SM, Feng NJ, Liang XL. Bioinformatics analysis of deacetylase Sir2 in soybean[J]. Guizhou Agric Sci, 2015, 43(8): 34-37.
[30]	Chu JS, Chen Z. Molecular identification of histone acetyltransferases and deacetylases in lower plant Marchantia polymorpha[J]. Plant Physiol Biochem, 2018, 132: 612-622. doi: 10.1016/j.plaphy.2018.10.012 URL
[31]	Zhang K, Yu L, Pang X, et al. In silico analysis of maize HDACs with an emphasis on their response to biotic and abiotic stresses[J]. PeerJ, 2020, 8: e8539. doi: 10.7717/peerj.8539 URL
[32]	Yuan LY, Dai HW, Zheng ST, et al. Genome-wide identification of the HDAC family proteins and functional characterization of CsHD2C, a HD2-type histone deacetylase gene in tea plant(Camellia sinensis L. O. Kuntze)[J]. Plant Physiol Biochem, 2020, 155: 898-913. doi: 10.1016/j.plaphy.2020.07.047 URL
[33]	Zhang MZ, Teixeira da Silva JA, Yu ZM, et al. Identification of histone deacetylase genes in Dendrobium officinale and their expression profiles under phytohormone and abiotic stress treatments[J]. PeerJ, 2020, 8: e10482. doi: 10.7717/peerj.10482 URL
[34]	Vall-Llaura N, Torres R, Lindo-García V, et al. PbSRT1 and PbSRT2 regulate pear growth and ripening yet displaying a species-specific regulation in comparison to other Rosaceae spp[J]. Plant Sci, 2021, 308: 110925. doi: 10.1016/j.plantsci.2021.110925 URL
[35]	Yang L, Meng XX, Chen SL, et al. Identification of the histone deacetylases gene family in hemp reveals genes regulating cannabinoids synthesis[J]. Front Plant Sci, 2021, 12: 755494. doi: 10.3389/fpls.2021.755494 URL
[36]	Du QL, Fang YP, Jiang JM, et al. Characterization of histone deacetylases and their roles in response to abiotic and PAMPs stresses in Sorghum bicolor[J]. BMC Genomics, 2022, 23(1): 28. doi: 10.1186/s12864-021-08229-2
[37]	Blander G, Guarente L. The Sir2 family of protein deacetylases[J]. Annu Rev Biochem, 2004, 73: 417-435. pmid: 15189148
[38]	Bordoli L, Kiefer F, Arnold K, et al. Protein structure homology modeling using SWISS-MODEL workspace[J]. Nat Protoc, 2009, 4(1): 1-13. doi: 10.1038/nprot.2008.197 pmid: 19131951
[39]	Rossmann MG, Moras D, Olsen KW. Chemical and biological evolution of nucleotide-binding protein[J]. Nature, 1974, 250(463): 194-199. doi: 10.1038/250194a0
[40]	Brzezinski K. S-adenosyl-l-homocysteine hydrolase: a structural perspective on the enzyme with two rossmann-fold domains[J]. Biomolecules, 2020, 10(12): 1682. doi: 10.3390/biom10121682 URL
[41]	Bellamacina CR. The nicotinamide dinucleotide binding motif: a comparison of nucleotide binding proteins[J]. FASEB J, 1996, 10(11): 1257-1269. doi: 10.1096/fasebj.10.11.8836039 pmid: 8836039
[42]	Min J, Landry J, Sternglanz R, et al. Crystal structure of a SIR2 homolog-NAD complex[J]. Cell, 2001, 105(2): 269-279. pmid: 11336676
[43]	Pannek M, Simic Z, Fuszard M, et al. Crystal structures of the mitochondrial deacylase Sirtuin 4 reveal isoform-specific acyl recognition and regulation features[J]. Nat Commun, 2017, 8(1): 1513. doi: 10.1038/s41467-017-01701-2 pmid: 29138502
[44]	Jiménez-García B, Teixeira JMC, Trellet M, et al. PDB-tools web: a user-friendly interface for the manipulation of PDB files[J]. Proteins, 2021, 89(3): 330-335. doi: 10.1002/prot.v89.3 URL
[45]	Pan PW, Feldman JL, Devries MK, et al. Structure and biochemical functions of SIRT6[J]. J Biol Chem, 2011, 286(16): 14575-14587. doi: 10.1074/jbc.M111.218990 pmid: 21362626
[46]	Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling[J]. Electrophoresis, 1997, 18(15): 2714-2723. doi: 10.1002/elps.1150181505 pmid: 9504803
[47]	Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms[J]. Mol Biol Evol, 2018, 35(6): 1547-1549. doi: 10.1093/molbev/msy096 pmid: 29722887
[48]	Zhang H, Zhao Y, Zhou DX. Rice NAD⁺-dependent histone deacetylase OsSRT1 represses glycolysis and regulates the moonlighting function of GAPDH as a transcriptional activator of glycolytic genes[J]. Nucleic Acids Res, 2017, 45(21): 12241-12255. doi: 10.1093/nar/gkx825 pmid: 28981755
[49]	Liu XY, Wei W, Zhu WJ, et al. Histone deacetylase AtSRT1 links metabolic flux and stress response in Arabidopsis[J]. Mol Plant, 2017, 10(12): 1510-1522. doi: 10.1016/j.molp.2017.10.010 URL
[50]	König AC, Hartl M, Pham PA, et al. The Arabidopsis class II sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism[J]. Plant Physiol, 2014, 164(3): 1401-1414. doi: 10.1104/pp.113.232496 URL
[51]	Chen B, Zang WW, Wang J, et al. The chemical biology of sirtuins[J]. Chem Soc Rev, 2015, 44(15): 5246-5264. doi: 10.1039/c4cs00373j pmid: 25955411
[52]	Greiss S, Gartner A. Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation[J]. Mol Cells, 2009, 28(5): 407-415. doi: 10.1007/s10059-009-0169-x pmid: 19936627
[53]	Chung PJ, Kim YS, Park SH, et al. Subcellular localization of rice histone deacetylases in organelles[J]. FEBS Lett, 2009, 583(13): 2249-2254. doi: 10.1016/j.febslet.2009.06.003 pmid: 19505461
[54]	Borra MT, Langer MR, Slama JT, et al. Substrate specificity and kinetic mechanism of the Sir2 family of NAD⁺-dependent histone/protein deacetylases[J]. Biochemistry, 2004, 43(30): 9877-9887. pmid: 15274642
[55]	Bheda P, Jing H, Wolberger C, et al. The substrate specificity of sirtuins[J]. Annu Rev Biochem, 2016, 85: 405-429. doi: 10.1146/annurev-biochem-060815-014537 pmid: 27088879
[56]	Berger SL. The complex language of chromatin regulation during transcription[J]. Nature, 2007, 447(7143): 407-412. doi: 10.1038/nature05915
[57]	Liu XC, Yang SG, Zhao ML, et al. Transcriptional repression by histone deacetylases in plants[J]. Mol Plant, 2014, 7(5): 764-772. doi: 10.1093/mp/ssu033 pmid: 24658416
[58]	Imai S, Armstrong CM, Kaeberlein M, et al. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase[J]. Nature, 2000, 403(6771): 795-800. doi: 10.1038/35001622
[59]	Vaquero A, Scher MB, Lee DH, et al. SirT2 is a histone deacetylase with preference for histone H4 Lys 16 during mitosis[J]. Genes Dev, 2006, 20(10): 1256-1261. doi: 10.1101/gad.1412706 URL
[60]	North BJ, Verdin E. Sirtuins: Sir2-related NAD-dependent protein deacetylases[J]. Genome Biol, 2004, 5(5): 224. pmid: 15128440
[61]	Marmorstein R. Structure and chemistry of the Sir2 family of NAD⁺-dependent histone/protein deactylases[J]. Biochem Soc Trans, 2004, 32(Pt 6): 904-909. doi: 10.1042/BST0320904 URL
[62]	Avalos JL, Boeke JD, Wolberger C. Structural basis for the mechanism and regulation of Sir2 enzymes[J]. Mol Cell, 2004, 13(5): 639-648. pmid: 15023335
[63]	Seto E, Yoshida M. Erasers of histone acetylation: the histone deacetylase enzymes[J]. Cold Spring Harb Perspect Biol, 2014, 6(4): a018713. doi: 10.1101/cshperspect.a018713 URL
[64]	Sauve AA, Celic I, Avalos J, et al. Chemistry of gene silencing: the mechanism of NAD⁺-dependent deacetylation reactions[J]. Biochemistry, 2001, 40(51): 15456-15463. pmid: 11747420
[65]	Hawse WF, Wolberger C. Structure-based mechanism of ADP-ribosylation by sirtuins[J]. J Biol Chem, 2009, 284(48): 33654-33661. doi: 10.1074/jbc.M109.024521 pmid: 19801667
[66]	Fahie K, Hu P, Swatkoski S, et al. Side chain specificity of ADP-ribosylation by a sirtuin[J]. FEBS J, 2009, 276(23): 7159-7176. doi: 10.1111/j.1742-4658.2009.07427.x pmid: 19895577
[67]	Wu LW, Ren DY, Hu SK, et al. Down-regulation of a nicotinate phosphoribosyltransferase gene, OsNaPRT1, leads to withered leaf tips[J]. Plant Physiol, 2016, 171(2): 1085-1098.
[68]	Li Y, You L, Huang WF, et al. A FRET-based assay for screening SIRT6 modulators[J]. Eur J Med Chem, 2015, 96: 245-249. doi: 10.1016/j.ejmech.2015.04.008 pmid: 25884115
[69]	Mautone N, Zwergel C, Mai A, et al. Sirtuin modulators: where are we now? A review of patents from 2015 to 2019[J]. Expert Opin Ther Pat, 2020, 30(6): 389-407. doi: 10.1080/13543776.2020.1749264 pmid: 32228181
[70]	Alcaín FJ, Villalba JM. Sirtuin inhibitors[J]. Expert Opin Ther Pat, 2009, 19(3): 283-294. doi: 10.1517/13543770902755111 pmid: 19441904
[71]	Bitterman KJ, Anderson RM, Cohen HY, et al. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1[J]. J Biol Chem, 2002, 277(47): 45099-45107. doi: 10.1074/jbc.M205670200 pmid: 12297502
[72]	Bogan KL, Brenner C. Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD⁺ precursor vitamins in human nutrition[J]. Annu Rev Nutr, 2008, 28: 115-130. doi: 10.1146/nutr.2008.28.issue-1 URL
[73]	Grubisha O, Smith BC, Denu JM. Small molecule regulation of Sir2 protein deacetylases[J]. FEBS J, 2005, 272(18): 4607-4616. pmid: 16156783
[74]	Avalos JL, Celic I, Muhammad S, et al. Structure of a Sir2 enzyme bound to an acetylated p53 peptide[J]. Mol Cell, 2002, 10(3): 523-535. pmid: 12408821
[75]	Singh S, Singh A, Yadav S, et al. Sirtinol, a Sir2 protein inhibitor, affects stem cell maintenance and root development in Arabidopsis thaliana by modulating auxin-cytokinin signaling components[J]. Sci Rep, 2017, 7: 42450. doi: 10.1038/srep42450
[76]	Alcaín FJ, Villalba JM. Sirtuin activators[J]. Expert Opin Ther Pat, 2009, 19(4): 403-414. doi: 10.1517/13543770902762893 pmid: 19441923
[77]	Sauve AA, Moir RD, Schramm VL, et al. Chemical activation of Sir2-dependent silencing by relief of nicotinamide inhibition[J]. Mol Cell, 2005, 17(4): 595-601. pmid: 15721262
[78]	Kulkarni SS, Cantó C. The molecular targets of resveratrol[J]. Biochim Biophys Acta, 2015, 1852(6): 1114-1123. doi: 10.1016/j.bbadis.2014.10.005 pmid: 25315298
[79]	Shakibaei M, Shayan P, Busch F, et al. Resveratrol mediated modulation of Sirt-1/Runx2 promotes osteogenic differentiation of mesenchymal stem cells: potential role of Runx2 deacetylation[J]. PLoS One, 2012, 7(4): e35712. doi: 10.1371/journal.pone.0035712 URL
[80]	Zhang F, Wang LK, Ko EE, et al. Histone deacetylases SRT1 and SRT2 interact with ENAP1 to mediate ethylene-induced transcriptional repression[J]. Plant Cell, 2018, 30(1): 153-166. doi: 10.1105/tpc.17.00671 URL
[81]	Fernie AR, Carrari F, Sweetlove LJ. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport[J]. Curr Opin Plant Biol, 2004, 7(3): 254-261. doi: 10.1016/j.pbi.2004.03.007 pmid: 15134745
[82]	Finkemeier I, Laxa M, Miguet L, et al. Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis[J]. Plant Physiol, 2011, 155(4): 1779-1790. doi: 10.1104/pp.110.171595 pmid: 21311031
[83]	Cucurachi M, Busconi M, Morreale G, et al. Characterization and differential expression analysis of complete coding sequences of Vitis vinifera L. sirtuin genes[J]. Plant Physiol Biochem, 2012, 54: 123-132. doi: 10.1016/j.plaphy.2012.02.017 URL
[84]	Bond DM, Dennis ES, Pogson BJ, et al. Histone acetylation, vernalization insensitive 3, flowering locus c, and the vernalization response[J]. Mol Plant, 2009, 2(4): 724-737. doi: S1674-2052(14)60755-3 pmid: 19825652
[85]	Zhang H, Lu Y, Zhao Y, et al. OsSRT1 is involved in rice seed development through regulation of starch metabolism gene expression[J]. Plant Sci, 2016, 248: 28-36. doi: 10.1016/j.plantsci.2016.04.004 pmid: 27181944
[86]	Lee K, Park OS, Jung SJ, et al. Histone deacetylation-mediated cellular dedifferentiation in Arabidopsis[J]. J Plant Physiol, 2016, 191: 95-100. doi: 10.1016/j.jplph.2015.12.006 URL
[87]	Huang LM, Sun QW, Qin FJ, et al. Down-regulation of a silent information regulator2-related histone deacetylase gene, ossrt1, induces DNA fragmentation and cell death in rice[J]. Plant Physiol, 2007, 144(3): 1508-1519. pmid: 17468215
[88]	Fang CY, Zhang H, Wan J, et al. Control of leaf senescence by an MeOH-jasmonates cascade that is epigenetically regulated by OsSRT1 in rice[J]. Mol Plant, 2016, 9(10): 1366-1378. doi: 10.1016/j.molp.2016.07.007 URL
[89]	Tang WS, Zhong L, Ding QQ, et al. Histone deacetylase AtSRT2 regulates salt tolerance during seed germination via repression of vesicle-associated membrane protein 714(VAMP714)in Arabidopsis[J]. New Phytol, 2022, 234(4): 1278-1293. doi: 10.1111/nph.v234.4 URL
[90]	Imran M, Shafiq S, Naeem MK, et al. Histone deacetylase(HDAC)gene family in allotetraploid cotton and its diploid progenitors: in silico identification, molecular characterization, and gene expression analysis under multiple abiotic stresses, DNA damage and phytohormone treatments[J]. Int J Mol Sci, 2020, 21(1): 321. doi: 10.3390/ijms21010321 URL
[91]	Wang CZ, Gao F, Wu JG, et al. Arabidopsis putative deacetylase AtSRT2 regulates basal defense by suppressing PAD4, EDS5 and SID2 expression[J]. Plant Cell Physiol, 2010, 51(8): 1291-1299. doi: 10.1093/pcp/pcq087 URL
[92]	Zhang F, Wang LK, Qi B, et al. EIN2 mediates direct regulation of histone acetylation in the ethylene response[J]. Proc Natl Acad Sci USA, 2017, 114(38): 10274-10279. doi: 10.1073/pnas.1707937114 pmid: 28874528
[93]	Zhao H, Yin CC, Ma B, et al. Ethylene signaling in rice and Arabidopsis: new regulators and mechanisms[J]. J Integr Plant Biol, 2021, 63(1): 102-125. doi: 10.1111/jipb.v63.1 URL
[94]	Huang CRL, Burns KH, Boeke JD. Active transposition in genomes[J]. Annu Rev Genet, 2012, 46: 651-675. doi: 10.1146/annurev-genet-110711-155616 pmid: 23145912
[95]	Zhong XC, Zhang H, Zhao Y, et al. The rice NAD⁺-dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements[J]. PLoS One, 2013, 8(6): e66807. doi: 10.1371/journal.pone.0066807 URL