非生物胁迫下植物DNA甲基化研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2020-0330

摘要/Abstract

摘要：

非生物胁迫,包括高温、干旱、寒冷、洪涝和盐碱化等,通常不利于植物生长发育。在植物长期的自然选择和进化过程中,植物已经形成了一套完整的体系,以应对外界不断变化的环境。在真核细胞中,蛋白质编码基因的表达在很大程度上受到染色质状态的影响。表观遗传修饰,主要包括DNA甲基化,组蛋白修饰,组蛋白变体和一些非编码RNA（Non-coding RNA,ncRNA）的变化,会影响染色质的结构和可及性,进而改变基因表达的活性。近年来研究表明,表观遗传修饰广泛参与植物非生物胁迫响应,对植物适应不断变化的环境十分重要。作为最重要的表观遗传修饰之一,DNA甲基化在调控非生物胁迫响应中的作用引起了人们的广泛关注。主要综述植物DNA甲基化和非生物胁迫下DNA甲基化动态性研究的最新进展,以期为利用表观遗传变异提高植物的抗胁迫能力提供参考。

关键词: DNA甲基化, 非生物胁迫, 胁迫应答

Abstract:

Abiotic stress,including high temperatures,droughts,colds,floods,and salinization,is usually not conducive to plant growth and development. In the long-term natural selection and evolution of plants,plants have formed a complete system to cope with the constantly changing environment. In eukaryotic cells,the expression of protein-coding genes is largely influenced by the state of chromatin. Epigenetic modifications,mainly including DNA methylation,histone modifications,histone variants,and some non-coding RNA（ncRNA）changes,will affect the structure and accessibility of chromatin,thereby altering the activity of gene expression. Recent studies have shown that epigenetic modification is widely involved in plant abiotic stress response and is important for plants to adapt to changing environments. As one of the most important epigenetic modifications,the role of DNA methylation in regulating abiotic stress responses has attracted widespread attention. This paper reviews the recent advances in plant DNA methylation and abiotic stress under DNA stress,with a view to providing a reference for using epigenetic variation to improve plant resistance to stress.

Key words: DNA methylation, abiotic stress, stress response

刘治民, 杨芷怡, 冀凤丹, 梅志超, 于佳慧, 解莉楠. 非生物胁迫下植物DNA甲基化研究进展[J]. 生物技术通报, 2020, 36(11): 122-132.

LIU Zhi-min, YANG Zhi-yi, JI Feng-dan, MEI Zhi-chao, YU Jia-hui, XIE Li-nan. Research Progress of Plant DNA Methylation Under Abiotic Stress[J]. Biotechnology Bulletin, 2020, 36(11): 122-132.

图/表 3

参考文献 80

[1]	Zhu J. Abiotic stress signaling and responses in plants[J]. Cell, 2016,167(2):313-324. doi: 10.1016/j.cell.2016.08.029 URL pmid: 27716505
[2]	Fedoroff NV, Battisti DS, Beachy RN, et al. Radically rethinking agriculture for the 21st century[J]. Science, 2010,327(5967):833-834. URL pmid: 20150494
[3]	Boyko A, Kovalchuk I. Epigenetic control of plant stress response[J]. Environmental and Molecular Mutagenesis, 2008,49(1):61-72. doi: 10.1002/em.20347 URL pmid: 17948278
[4]	Sun X, Zheng H, Sui N. Regulation mechanism of long non-coding RNA in plant response to stress[J]. Biochemical and Biophysical Research Communications, 2018,503(2):402-407. URL pmid: 30055799
[5]	Golldack D, Lüking I, Yang O. Plant tolerance to drought and salinity:stress regulating transcription factors and their functional significance in the cellular transcriptional network[J]. Plant Cell Reports, 2011,30(8):1383-1391. doi: 10.1007/s00299-011-1068-0 URL pmid: 21476089
[6]	Wang L, Wu J, Chang W, et al. Arabidopsis HIT4 encodes a novel chromocentre-localized protein involved in the heat reactivation of transcriptionally silent loci and is essential for heat tolerance in plants[J]. Journal of Experimental Botany, 2013,64(6):1689-1701. doi: 10.1093/jxb/ert030 URL pmid: 23408827
[7]	Wang H, Wang H, Shao H, et al. Recent advances in uilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology[J]. Frontiers in Plant Science, 2016,7:67. doi: 10.3389/fpls.2016.00067 URL pmid: 26904044
[8]	Deinlein U, Stephan AB, Horie T, et al. Plant salt-tolerance mechanisms[J]. Trends Plant Sci, 2014,19(6):371-379. doi: 10.1016/j.tplants.2014.02.001 URL pmid: 24630845
[9]	Tang X, Mu X, Shao H, et al. Global plant-responding mechanisms to salt stress:physiological and molecular levels and implications in biotechnology[J]. Crit Rev Biotechnol, 2015,35(4):425-437. doi: 10.3109/07388551.2014.889080 URL pmid: 24738851
[10]	Miura K, Furumoto T. Cold signaling and cold response in plants[J]. International Journal of Molecular Sciences, 2013,14(3):5312-5337. URL pmid: 23466881
[11]	Saidi Y, Finka A, Goloubinoff P. Heat perception and signalling in plants:a tortuous path to thermotolerance[J]. New Phytol, 2011,190(3):556-565. doi: 10.1111/j.1469-8137.2010.03571.x URL pmid: 21138439
[12]	Duan CG, Zhu JK, Cao X. Retrospective and perspective of plant epigenetics in China[J]. J Genet Genomics, 2018,45(11):621-638. doi: 10.1016/j.jgg.2018.09.004 URL pmid: 30455036
[13]	Popova OV, Dinh HQ, Aufsatz W, et al. The RdDM pathway is required for basal heat tolerance in Arabidopsis[J]. Molecular Plant, 2013,6(2):396-410. doi: 10.1093/mp/sst023 URL
[14]	Xu R, Wang Y, Zheng H, et al. Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis[J]. Journal of Experimental Botany, 2015,66(19):5997-6008. doi: 10.1093/jxb/erv312 URL pmid: 26139822
[15]	Zhang H, Lang Z, Zhu J. Dynamics and function of DNA methylation in plants[J]. Nature reviews. Molecular Cell Biology, 2018,19(8):489-506. doi: 10.1038/s41580-018-0016-z URL pmid: 29784956
[16]	Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals[J]. Nature Reviews Genetics, 2010,11(3):204-220. doi: 10.1038/nrg2719 URL pmid: 20142834
[17]	He XJ, Ma ZY, Liu ZW. Non-coding RNA transcription and RNA-directed DNA methylation in Arabidopsis[J]. Mol Plant, 2014,7(9):1406-1414. doi: 10.1093/mp/ssu075 URL pmid: 24966349
[18]	Matzke MA, Mosher RA. RNA-directed DNA methylation:an epigenetic pathway of increasing complexity[J]. Nat Rev Genet, 2014,15(6):394-408. doi: 10.1038/nrg3683 URL pmid: 24805120
[19]	Zhang H, Zhu JK. RNA-directed DNA methylation[J]. Curr Opin Plant Biol, 2011,14(2):142-147. doi: 10.1016/j.pbi.2011.02.003 URL pmid: 21420348
[20]	Pikaard CS, Haag JR, Pontes OM, et al. A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation[J]. Cold Spring Harb Symp Quant Biol, 2012,77:205-212. URL pmid: 23567894
[21]	Zhong X, Du J, Hale CJ, et al. Molecular mechanism of action of pant DRM de novo DNA methyltransferases[J]. Cell, 2014,157(5):1050-1060. doi: 10.1016/j.cell.2014.03.056 URL pmid: 24855943
[22]	Law JA, Du J, Hale CJ, et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1[J]. Nature, 2013,498(7454):385-389. doi: 10.1038/nature12178 URL pmid: 23636332
[23]	Smith LM, Pontes O, Searle I, et al. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis[J]. The Plant Cell, 2007,19(5):1507-1521. doi: 10.1105/tpc.107.051540 URL pmid: 17526749
[24]	Zhang H, Ma Z, Zeng L, et al. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013,110(20):8290-8295. URL pmid: 23637343
[25]	Johnson LM, Du J, Hale CJ, et al. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation[J]. Nature, 2014,507(7490):124-128. doi: 10.1038/nature12931 URL pmid: 24463519
[26]	Zhang H, Tang K, Qian W, et al. An Rrp6-like protein positively regulates non-coding RNA levels and DNA methylation in Arabidopsis[J]. Molecular Cell, 2014,54(3):418-430. doi: 10.1016/j.molcel.2014.03.019 URL pmid: 24726328
[27]	Zhang C, Ning Y, Zhang S, et al. IDN2 and its paralogs form a complex required for RNA-directed DNA methylation[J]. PLoS Genetics, 2012,8(5):e1002693. doi: 10.1371/journal.pgen.1002693 URL
[28]	Zhu Y, Rowley MJ, Böhmdorfer G, et al. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing[J]. Molecular Cell, 2013,49(2):298-309. doi: 10.1016/j.molcel.2012.11.011 URL
[29]	Nuthikattu S, Mccue AD, Panda K, et al. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs1[W][OA][J]. Plant Physiology, 2013,162(1):116-131. doi: 10.1104/pp.113.216481 URL
[30]	Mccue AD, Panda K, Nuthikattu S, et al. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation[J]. The EMBO Journal, 2015,34(1):20-35. doi: 10.15252/embj.201489499 URL pmid: 25388951
[31]	Marí-Ordóñez A, Marchais A, Etcheverry M, et al. Reconstructing de novo silencing of an active plant retrotransposon[J]. Nature Genetics, 2013,45(9):1029-1039. doi: 10.1038/ng.2703 URL pmid: 23852169
[32]	Ye R, Chen Z, Lian B, et al. A dicer-independent route for biogen-esis of siRNAs that direct DNA methylation in Arabidopsis[J]. Molecular Cell, 2016,61(2):222-235. URL pmid: 26711010
[33]	Kankel MW, Ramsey DE, Stokes TL, et al. Arabidopsis MET1 cytosine methyltransferase mutants[J]. Genetics, 2003,163(3):1109-1122. URL pmid: 12663548
[34]	Stroud H, Do T, Du J, et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis[J]. Nature Structural & Molecular Biology, 2014,21(1):64-72. doi: 10.1038/nsmb.2735 URL pmid: 24336224
[35]	Lindroth AM, Cao X, Jackson JP, et al. Requirement of chromomethylase3 for maintenance of CpXpG methylation[J]. Science, 2001,292(5524):2077-2080. doi: 10.1126/science.1059745 URL pmid: 11349138
[36]	Du J, Zhong X, Bernatavichute YV, et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants[J]. Cell, 2012,151(1):167-180. URL pmid: 23021223
[37]	Du J, Johnson LM, Groth M, et al. Mechanism of DNA methylation-directed histone methylation by KRYPTONITE[J]. Molecular Cell, 2014,55(3):495-504. doi: 10.1016/j.molcel.2014.06.009 URL pmid: 25018018
[38]	Liu ZW, Shao CR, Zhang CJ, et al. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci[J]. PLoS Genet, 2014,10(1):e1003948. URL pmid: 24465213
[39]	Zemach A, Kim M Y, Hsieh P, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin[J]. Cell, 2013,153(1):193-205. doi: 10.1016/j.cell.2013.02.033 URL pmid: 23540698
[40]	Liu R, Lang Z. The mechanism and function of active DNA demethylation in plants[J]. Journal of Integrative Plant Biology, 2020,62(1):148-159. URL pmid: 31628716
[41]	Gong Z, Morales-Ruiz T, Ariza RR, et al. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase[J]. Cell, 2002,111(6):803-814. doi: 10.1016/s0092-8674(02)01133-9 URL pmid: 12526807
[42]	Gehring M, Huh JH, Hsieh T, et al. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation[J]. Cell, 2006,124(3):495-506. doi: 10.1016/j.cell.2005.12.034 URL pmid: 16469697
[43]	Ortega-Galisteo AP, Morales-Ruiz T, Ariza RR, et al. Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks[J]. Plant Molecular Biology, 2008,67(6):671-681. doi: 10.1007/s11103-008-9346-0 URL pmid: 18493721
[44]	Qian W, Miki D, Zhang H, et al. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis[J]. Science, 2012,336(6087):1445-1448. doi: 10.1126/science.1219416 URL pmid: 22700931
[45]	Li Y, Cordoba-Canero D, Qian W, et al. An AP endonuclease functions in active DNA dimethylation and gene imprinting in Arabidopsis[J]. PLoS Genet, 2015,11(1):e1004905. URL pmid: 25569774
[46]	Martinez-Macias MI, Qian W, Miki D, et al. A DNA 3' phosphatase functions in active DNA demethylation in Arabidopsis[J]. Mol Cell, 2012,45(3):357-370. doi: 10.1016/j.molcel.2011.11.034 URL pmid: 22325353
[47]	Li Y, Duan C, Zhu X, et al. A DNA ligase required for active DNA demethylation and genomic imprinting in Arabidopsis[J]. Cell Research, 2015,25(6):757-760. doi: 10.1038/cr.2015.45 URL pmid: 25906993
[48]	Rus A, Yokoi S, Sharkhuu A, et al. AtHKT1 is a salt tolerance determinant that controls Na⁺ entry into plant roots[J]. Proceedings of the National Academy of Sciences of the United States of America, 2001,98(24):14150-14155. doi: 10.1073/pnas.241501798 URL pmid: 11698666
[49]	Baek D, Jiang J, Chung J, et al. Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance[J]. Plant & Cell Physiology, 2011,52(1):149-161. doi: 10.1093/pcp/pcq182 URL pmid: 21097475
[50]	Kumar S, Beena AS, Awana M, et al. Salt-induced tissue-specific cytosine methylation downregulates expression of HKT genes in contrasting wheat(Triticum aestivum L.)genotypes[J]. DNA and Cell Biology, 2017,36(4):283-294. URL pmid: 28384069
[51]	Song Y, Ji D, Li S, et al. The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean[J]. PLoS One, 2012,7(7):e41274. doi: 10.1371/journal.pone.0041274 URL pmid: 22815985
[52]	Huang W, Xian Z, Hu G, et al. SlAGO4A, a core factor of RNA-directed DNA methylation(RdDM)pathway, plays an important role under salt and drought stress in tomato[J]. Molecular Breeding, 2016,36(3):28.
[53]	Liang D, Zhang Z, Wu H, et al. Single-base-resolution methylomes of Populus trichocarpa reveal the association between DNA methylation and drought stress[J]. BMC Genetics, 2014,15(Suppl 1):S9.
[54]	Komivi D, Marie AM, Rong Z, et al. The contrasting response to drought and waterlogging is underpinned by divergent DNA methylation programs associated with transcript accumulation in sesame[J]. Plant Science, 2018,277:207-217. doi: 10.1016/j.plantsci.2018.09.012 URL pmid: 30466587
[55]	Sharma R, Vishal P, Kaul S, et al. Epiallelic changes in known stress-responsive genes under extreme drought conditions in Brassica juncea(L.)Czern.[J]. Plant Cell Reports, 2017,36(1):203-217. doi: 10.1007/s00299-016-2072-1 URL pmid: 27844102
[56]	Moglia A, Gianoglio S, Acquadro A, et al. Identification of DNA methyltransferases and demethylases in Solanum melongena L. , and their transcription dynamics during fruit development and after salt and drought stresses[J]. PLoS One, 2019,14(10):e0223581. URL pmid: 31596886
[57]	Sanghera GS, Wani SH, Hussain W, et al. Engineering cold stress tolerance in crop plants[J]. Current Genomics, 2011,12(1):30-43. URL pmid: 21886453
[58]	Guo H, Wu T, Li S, et al. The methylation patterns and transcriptional responses to chilling stress at the seedling stage in rice[J]. International Journal of Molecular Sciences, 2019,20(20):5089.
[59]	Kumar G, Rattan UK, Singh AK. Chilling-mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple(Malus x domestica Borkh. )[J]. PLoS One, 2016,11(2):e149934.
[60]	Song Y, Liu L, Li G, et al. Trichostatin A and 5-aza-2’-deoxycytidine influence the expression of cold-induced genes in Arabidopsis[J]. Plant Signal Behav, 2017,12(11):e1389828. doi: 10.1080/15592324.2017.1389828 URL pmid: 29027833
[61]	Chan Z, Wang Y, Cao M, et al. RDM4 modulates cold stress resistance in Arabidopsis partially through the CBF-mediated pathway[J]. New Phytol, 2016,209(4):1527-1539. doi: 10.1111/nph.13727 URL pmid: 26522658
[62]	Zhu C, Zhang S, Zhou C, et al. Genome-wide investigation and transcriptional analysis of cytosine-5 DNA methyltransferase and DNA demethylase gene families in tea plant(Camellia sinensis)under abiotic stress and withering processing[J]. PeerJ, 2020,8:e8432. doi: 10.7717/peerj.8432 URL pmid: 31976183
[63]	Ohama N, Sato H, Shinozaki K, et al. Transcriptional regulatory network of plant heat stress response[J]. Trends in Plant Science, 2017,22(1):53-65. doi: 10.1016/j.tplants.2016.08.015 URL pmid: 27666516
[64]	Qian Y, Hu W, Liao J, et al. The Dynamics of DNA methylation in the maize(Zea mays L.)inbred line B73 response to heat stress at the seedling stage[J]. Biochemical and Biophysical Research Communications, 2019,512(4):742-749. doi: 10.1016/j.bbrc.2019.03.150 URL pmid: 30926168
[65]	Sanchez DH, Paszkowski J. Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene[J]. PLoS Genet, 2014,10(11):e1004806. doi: 10.1371/journal.pgen.1004806 URL pmid: 25411840
[66]	Naydenov M, Baev V, Apostolova E, et al. High-temperature effect on genes engaged in DNA methylation and affected by DNA methylation in Arabidopsis[J]. Plant Physiology and Biochemistry, 2015,87:102-108. doi: 10.1016/j.plaphy.2014.12.022 URL pmid: 25576840
[67]	Fan S, Liu H, Liu J, et al. Systematic analysis of the DNA methylase and demethylase gene families in rapeseed(Brassica napus L.)and their expression variations after salt and heat stresses[J]. International Journal of Molecular Sciences, 2020,21(3):953.
[68]	Chang YN, Zhu C, Jiang J, et al. Epigenetic regulation in plant abiotic stress responses[J]. Journal of Integrative Plant Biology, 2019. URL pmid: 32970364
[69]	Yong-Villalobos L, González-Morales SI, Wrobel K, et al. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2015,112(52):E7293-E7302. URL pmid: 26668375
[70]	Kou HP, Li Y, Song XX, et al. Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice(Oryza sativa L.)[J]. Journal of Plant Physiology, 2011,168(14):1685-1693. doi: 10.1016/j.jplph.2011.03.017 URL pmid: 21665325
[71]	Chen X, Schoenberger B, Menz J, et al. Plasticity of DNA methylation and gene expression under zinc deficiency in Arabidopsis roots[J]. Plant and Cell Physiology, 2018,59(9):1790-1802. doi: 10.1093/pcp/pcy100 URL pmid: 29800330
[72]	Huang X, Chao D, Koprivova A, et al. Nuclear localised MORE SULPHUR ACCUMULATION1 epigenetically regulates sulphur homeostasis in Arabidopsis thaliana[J]. PLoS Genetics, 2016,12(9):e1006298. doi: 10.1371/journal.pgen.1006298 URL pmid: 27622452
[73]	Kim J, Lim JY, Shin H, et al. ROS1-dependent DNA demethylation is required for ABA-inducible NIC3 expression[J]. Plant Physiology, 2019,179(4):1810-1821. URL pmid: 30692220
[74]	Shi D, Zhuang K, Xia Y, et al. Hydrilla verticillata employs two different ways to affect DNA methylation under excess copper stress[J]. Aquatic Toxicology, 2017,193:97-104. URL pmid: 29053963
[75]	Shafiq S, Zeb Q, Ali A, et al. Lead, cadmium and zinc phytotoxicity alter DNA methylation levels to confer heavy metal tolerance in wheat[J]. International Journal of Molecular Sciences, 2019,20(19):4676.
[76]	Sudan J, Raina M, Singh R. Plant epigenetic mechanisms:role in abiotic stress and their generational heritability[J]. 3 Biotech, 2018,8(3):172. doi: 10.1007/s13205-018-1202-6 URL pmid: 29556426
[77]	Feng QZ, Yang CW, Lin XY, et al. Salt and alkaline stress induced transgenerational alteration in DNA methylation of rice(Oryza sativa)[J]. Australian Journal of Crop Science, 2012,6(5):877-883.
[78]	Molinier J, Ries G, Zipfel C, et al. Transgeneration memory of stress in plants[J]. Nature, 2006,442(7106):1046-1049. URL pmid: 16892047
[79]	Cong W, Miao Y, Xu L, et al. Transgenerational memory of gene expression changes induced by heavy metal stress in rice(Oryza sativa L.)[J]. BMC Plant Biology, 2019,19(1):282. doi: 10.1186/s12870-019-1887-7 URL pmid: 31248374
[80]	Verhoeven KJ, Jansen JJ, van Dijk PJ, et al. Stress-induced DNA methylation changes and their heritability in asexual dandelions[J]. New Phytol, 2010,185(4):1108-1118. doi: 10.1111/j.1469-8137.2009.03121.x URL pmid: 20003072