On transposon silencing and DNA methylation
-
摘要: 转座子(transposable elements，TEs)在生物体基因组可以通过转座或逆转座移动，它拷贝数的大规模增加是基因组不稳定的重要因素，因此，维持TEs沉默是宿主进化的方向。DNA甲基化被认为是沉默TEs的可遗传表观遗传修饰方式，同时也在维持基因组稳定、基因印迹、调节基因表达中发挥作用。本研究综述了TEs对生物基因组进化和基因表达的影响，重点总结了以DNA甲基化为主的转座子沉默机制的最新研究进展，归纳了环境因素通过DNA去甲基化调控转座子跳跃的机理。图4参82Abstract: Transposable elements (TEs) can be moved by means of transposition or reverse transposition in the genome of an organism, whose copy number in large numbers is an important factor for genome instability. Therefore, it is the direction of host evolution to maintain TEs silence. DNA methylation, generally considered to be a heritable epigenetic modification method for silencing TEs, plays a role in the maintainance of genome stability, genetic imprinting and the regulation of gene expression. This study is aimed at an overview of the impact of TEs on the evolution of biological genome and gene expression, a summary of the latest research progress of transposon silencing mechanism dominated by DNA methylation, and an investigation of the mechanism of environmental factors that regulate transposon jumping via DNA demethylation. [Ch, 4 fig. 82 ref.]
-
Key words:
- botany /
- transposon /
- transposon silence /
- DNA methylation /
- stress
-
图 3 DNA甲基化与转座子作用机制
A. 水稻OsCMT3a发生突变，DNA甲基化的丧失导致Tos17、Tos19、mPing、Dasheng、Osr4、Osr13、DaiZ、LINE1-6_OS上调；OsMET1-2突变，DNA甲基化的丧失导致Tos17、Osr7、Ping/Pong、mPing上调[51－52]。B. RdDM途径沉默转座子MITEs、OsMIR156d和OsMIR156j基因失去活性，调控水稻表型变化[49]。C. KRAB-ZFPs通路涉及SETDB1、HP1元件，形成压制性染色质结构沉默TEs，TEs也能被DNMT1、DNMT3A/B维持的CG甲基化沉默，丧失CG甲基化后只有少部分TEs上调[53]。D. 去甲基化上调TEs，核酸内切酶Dicer切割dsRNA产生的小RNA与AGO2蛋白结合沉默TEs[56]
Figure 3 DNA methylation and transposon mechanism
-
[1] MITA P, BOEKE J D. How retrotransposons shape genome regulation [J]. Curr Opin Genet Dev, 2016, 37: 90 − 100. doi: 10.1016/j.gde.2016.01.001 [2] FINNEGAN D J. Eukaryotic transposable elements and genome evolution [J]. Trends Genet, 1989, 5(4): 103 − 107. [3] WICKER T, SABOT F, HUA-VAN A, et al. A unified classification system for eukaryotic transposable elements [J]. Nat Rev Genet, 2007, 8(12): 973 − 982. doi: 10.1038/nrg2165 [4] SCHULMAN A H. Retrotransposon replication in plants [J]. Curr Opin Virol, 2013, 3(6): 604 − 614. doi: 10.1016/j.coviro.2013.08.009 [5] OROZCO-ARIAS S, ISAZA G, GUYOT R. Retrotransposons in plant genomes: structure, identification, and classification through bioinformatics and machine learning [J]. Int J Mol Sci, 2019, 20(15): 1 − 31. [6] GONZALEZ J, PETROV D A. Evolution of genome content: population dynamics of transposable elements in flies and humans[C]//ANISIMOVA M. Evolutionary Genomics. Methods in Molecular Biology (Methods and Protocols), vol 855. Totowa: Humana Press, 2012: 361 − 383. [7] de KONING A P J, GU Wanjun, CASTOE T A, et al. Repetitive elements may comprise over two-thirds of the human genome[J]. PLoS Genet, 2011, 7(12): e1002384. doi: 10.1371/journal.pgen.1002384. [8] SAVAGE A L, SCHUMANN G G, BREEN G, et al. Retrotransposons in the development and progression of amyotrophic lateral sclerosis [J]. J Neurol Neurosurg Psychiatry, 2019, 90(3): 284 − 293. doi: 10.1136/jnnp-2018-319210 [9] LANDER E S, LINTON L M, BIRREN B, et al. Initial sequencing and analysis of the human genome [J]. Nature, 2001, 409(6822): 860 − 921. doi: 10.1038/35057062 [10] YANG Fang, WANG P J. Multiple LINEs of retrotransposon silencing mechanisms in the mammalian germline [J]. Semin Cell Dev Biol, 2016, 59: 118 − 125. doi: 10.1016/j.semcdb.2016.03.001 [11] CHOULET F, WICKER T, RUSTENHOLZ C, et al. Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces [J]. Plant Cell, 2010, 22(6): 1686 − 1701. doi: 10.1105/tpc.110.074187 [12] SONG Xianwei, CAO Xiaofeng. Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice [J]. Curr Opin Plant Biol, 2017, 36: 111 − 118. doi: 10.1016/j.pbi.2017.02.004 [13] SASAKI T. The map-based sequence of the rice genome [J]. Nature, 2005, 436(7052): 793 − 800. doi: 10.1038/nature03895 [14] JIAO Yinping, PELUSO P, SHI Jinghua, et al. Improved maize reference genome with single-molecule technologies [J]. Nature, 2017, 546(7659): 524 − 527. doi: 10.1038/nature22971 [15] SCHNABLE P S, WARE D, FULTON R S, et al. The B73 maize genome: complexity, diversity, and dynamics [J]. Science, 2009, 326(5956): 1112 − 1115. doi: 10.1126/science.1178534 [16] ENNOS R A, CLEGG M T. Flower color variation in the morning glory, Ipomoea purpurea [J]. J Hered, 1983, 74(4): 247 − 250. doi: 10.1093/oxfordjournals.jhered.a109778 [17] BUTELLI E, LICCIARDELLO C, ZHANG Yang, et al. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges [J]. Plant Cell, 2012, 24(3): 1242 − 1255. doi: 10.1105/tpc.111.095232 [18] LISCH D. How important are transposons for plant evolution? [J]. Nat Rev Genet, 2013, 14(1): 49 − 61. [19] BENOIT M, DROST H G, CATONI M, et al. Environmental and epigenetic regulation of Rider retrotransposons in tomato[J]. PLoS Genet, 2019, 15(9): e1008370. doi: 10.1371/journal.pgen.1008370. [20] SANCHEZ D H, GAUBERT H, YANG Weibing. Evidence of developmental escape from transcriptional gene silencing in MESSI retrotransposons [J]. New Phytol, 2019, 223(2): 950 − 964. doi: 10.1111/nph.15896 [21] KUBOTA S, ISHIKAWA T, KAWATA K, et al. Retrotransposons manipulating mammalian skeletal development in chondrocytes[J]. Int J Mol Sci, 2020, 21(5): 1564. doi: 10.3390/ijms21051564. [22] BUNDO M, TOYOSHIMA M, OKADA Y, et al. Increased l1 retrotransposition in the neuronal genome in schizophrenia [J]. Neuron, 2014, 81(2): 306 − 313. doi: 10.1016/j.neuron.2013.10.053 [23] 陈文充, 贾宁, 董昂, 等. 山核桃甲基化敏感扩增多态体系的建立与甲基化初步分析[J]. 浙江农林大学学报, 2019, 36(3): 468 − 478. doi: 10.11833/j.issn.2095-0756.2019.03.006 CHEN Wenchong, JIA Ning, DONG Ang, et al. A protocol for methylation-sensitive amplified polymorphism markers and its application to a methylation analysis in Carya cathayensis [J]. J Zhejiang A&F Univ, 2019, 36(3): 468 − 478. doi: 10.11833/j.issn.2095-0756.2019.03.006 [24] HANCKS D C, KAZAZIAN H H. Roles for retrotransposon insertions in human disease[J]. Mob DNA, 2016, 7(1): 9. doi: 10.1186/s13100-016-0065-9. [25] SCOTT E C, GARDNER E J, MASOOD A, et al. A hot L1 retrotransposon evades somatic repression and initiates human colorectal cancer [J]. Genome Res, 2016, 26(6): 745 − 755. doi: 10.1101/gr.201814.115 [26] MAO Hude, WANG Hongwei, LIU Shengxue, et al. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings [J]. Nat Commun, 2015, 6(1): 1 − 13. [27] MOLARO A, MALIK H S. Hide and seek: how chromatin-based pathways silence retroelements in the mammalian germline [J]. Curr Opin Genet Dev, 2016, 37: 51 − 58. doi: 10.1016/j.gde.2015.12.001 [28] CHOI Y J, LIN C P, RISSO D, et al. Deficiency of microRNA miR-34a expands cell fate potential in pluripotent stem cells [J]. Science, 2017, 355(6325): eaag1927. doi: 10.1126/science.aag1927. [29] HUTCHISON C A, MERRYMAN C, SUN Lijie, et al. Polar effects of transposon insertion into a minimal bacterial genome [J]. J Bacteriol, 2019, 201(19): e00185-19. doi: 10.1128/JB.00185-19. [30] FURNER I J, MATZKE M. Methylation and demethylation of the Arabidopsis genome [J]. Curr Opin Plant Biol, 2011, 14(2): 137 − 141. doi: 10.1016/j.pbi.2010.11.004 [31] DENIZ Ö, FROST J M, BRANCO M R. Author correction: regulation of transposable elements by DNA modifications [J]. Nat Rev Genet, 2019, 20(7): 432 − 432. doi: 10.1038/s41576-019-0117-3 [32] CHAN S W L, HENDERSON I R, JACOBSEN S E. Gardening the genome: DNA methylation in Arabidopsis thaliana [J]. Nat Rev Genet, 2005, 6(5): 351 − 360. doi: 10.1038/nrg1601 [33] GIRARD A, HANNON G J. Conserved themes in small-RNA-mediated transposon control [J]. Trends Cell Biol, 2008, 18(3): 136 − 148. doi: 10.1016/j.tcb.2008.01.004 [34] LI Qing, GENT J I, ZYNDA G, et al. RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome [J]. Proc Natl Acad Sci, 2015, 112(47): 14728 − 14733. doi: 10.1073/pnas.1514680112 [35] JÖNSSON M E, BRATTÅS P L, GUSTAFSSON C, et al. Activation of neuronal genes via LINE-1 elements upon global DNA demethylation in human neural progenitors [J]. Nat Commun, 2019, 10: 3182. doi: 10.1038/s41467-019-11150-8. [36] LIU Nian, LEE C H, SWIGUT T, et al. Selective silencing of euchromatic L1s revealed by genome-wide screens for L1 regulators [J]. Nature, 2018, 553(7687): 228 − 232. doi: 10.1038/nature25179 [37] CUI Xiekui, JIN Ping, CUI Xia, et al. Control of transposon activity by a histone H3K4 demethylase in rice [J]. Proc Natl Acad Sci, 2013, 110(5): 1953 − 1958. doi: 10.1073/pnas.1217020110 [38] WANG Dafang, ZHANG Jianbo, ZUO Tao, et al. Small RNA-mediated De Novo silencing of Ac/Ds transposons is initiated by alternative transposition in maize [J]. Genetics, 2020, 215(2): 393 − 406. doi: 10.1534/genetics.120.303264 [39] CAPPUCCI U, NORO F, CASALE A M, et al. The Hsp70 chaperone is a major player in stress-induced transposable element activation [J]. Proc Natl Acad Sci, 2019, 116(36): 17943 − 17950. doi: 10.1073/pnas.1903936116 [40] BARTHOLOMEW B. Regulating the chromatin landscape: structural and mechanistic perspectives [J]. Annu Rev Biochem, 2014, 83: 671 − 696. doi: 10.1146/annurev-biochem-051810-093157 [41] HORVÁTH V, MERENCIANO M, GONZÁLEZ J. Revisiting the relationship between transposable elements and the eukaryotic stress response [J]. Trends Genet, 2017, 33(11): 832 − 841. doi: 10.1016/j.tig.2017.08.007 [42] JIE Yang, YUAN Lianyu, YEN M R, et al. SWI3B and HDA6 interact and are required for transposon silencing in Arabidopsis [J]. Plant J, 2019, 102(4): 809 − 822. [43] 陈昂. 毛竹微型反向重复转座子(MITEs)鉴定及对宿主基因表达的影响[D]. 杭州: 浙江农林大学, 2016. CHEN Ang. Identification of Miniature Inverted Repeat Transposable Elements (MITEs) from Phyllostachys edulis and Their Effects on Host Gene Expression[D]. Hangzhou: Zhejiang A&F University, 2016. [44] ZHOU Mingbing, LIANG Linlin, HÄNNINEN H. A transposition-active Phyllostachys edulis long terminal repeat (LTR) retrotransposon [J]. J Plant Res, 2018, 131(2): 203 − 210. doi: 10.1007/s10265-017-0983-8 [45] WANG Zhengming, BAULCOMBE D C. Transposon age and non-CG methylation [J]. Nat Commun, 2020, 11(1): 1 − 9. doi: 10.1038/s41467-019-13993-7 [46] ZHANG Huiming, LANG Zhaobo, ZHU Jiankang. Dynamics and function of DNA methylation in plants [J]. Nat Rev Mol Cell Biol, 2018, 19(8): 489 − 506. doi: 10.1038/s41580-018-0016-z [47] KIM M Y, ZILBERMAN D. DNA methylation as a system of plant genomic immunity [J]. Trends Plant Sci, 2014, 19(5): 320 − 326. doi: 10.1016/j.tplants.2014.01.014 [48] CZECH B, HANNON G J. One loop to rule them all: the ping-pong cycle and piRNA-guided silencing [J]. Trends Biochem Sci, 2016, 41(4): 324 − 337. doi: 10.1016/j.tibs.2015.12.008 [49] XU Le, YUAN Kun, YUAN Meng, et al. Regulation of rice tillering by RNA-Directed DNA methylation at miniature inverted-repeat transposable elements [J]. Mol Plant, 2020, 13(6): 851 − 863. doi: 10.1016/j.molp.2020.02.009 [50] MIROUZE M, REINDERS J, BUCHER E, et al. Selective epigenetic control of retrotransposition in Arabidopsis [J]. Nature, 2009, 461(7262): 427 − 430. doi: 10.1038/nature08328 [51] CHENG Chaoyang, TARUTANI Y, MIYAO A, et al. Loss of function mutations in the rice chromomethylase Os CMT 3a cause a burst of transposition [J]. Plant J, 2015, 83(6): 1069 − 1081. doi: 10.1111/tpj.12952 [52] HU Lanjuan, LI Ning, ZHANG Zhibin, et al. CG hypomethylation leads to complex changes in DNA methylation and transpositional burst of diverse transposable elements in callus cultures of rice [J]. Plant J, 2020, 101(1): 188 − 203. doi: 10.1111/tpj.14531 [53] ROWE H M, JAKOBSSON J, MESNARD D, et al. KAP1 controls endogenous retroviruses in embryonic stem cells [J]. Nature, 2010, 463(7278): 237 − 240. doi: 10.1038/nature08674 [54] MATSUI T, LEUNG D, MIYASHITA H, et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET [J]. Nature, 2010, 464(7290): 927 − 931. doi: 10.1038/nature08858 [55] IMBEAULT M, HELLEBOID P Y, TRONO D. KRAB zinc-finger proteins contribute to the evolution of gene regulatory networks [J]. Nature, 2017, 543(7646): 550 − 554. doi: 10.1038/nature21683 [56] BERRENS R V, ANDREWS S, SPENSBERGER D, et al. An endosiRNA-based repression mechanism counteracts transposon activation during global DNA demethylation in embryonic stem cells [J]. Cell Stem Cell, 2017, 21(5): 694 − 703. doi: 10.1016/j.stem.2017.10.004 [57] NOUROZ F, NOREEN S, HESLOP-HARRISON J S. Identification and evolutionary dynamics of CACTA DNA transposons in brassica [J]. Pak J Bot, 2017, 49(2): 789 − 798. [58] WANG Qingbiao, WANG Yanping, SUN Honghe, et al. Transposon-induced methylation of the RsMYB1 promoter disturbs anthocyanin accumulation in red-fleshed radish [J]. J Exp Bot, 2020, 71(9): 2537 − 2550. doi: 10.1093/jxb/eraa010 [59] KONG Yu, ROSE C M, CASS A A, et al. Transposable element expression in tumors is associated with immune infiltration and increased antigenicity [J]. Nat Commun, 2019, 10: 5228. doi: 10.1038/s41467-019-13035-2. [60] LA Honggui, DING Bo, MISHRA G P, et al. A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice [J]. Proc Natl Acad Sci, 2011, 108(37): 15498 − 15503. doi: 10.1073/pnas.1112704108 [61] KASHINO-FUJII M, YOKOSHO K, YAMAJI N, et al. Retrotransposon insertion and DNA methylation regulate aluminum tolerance in European barley accessions [J]. Plant Physiol, 2018, 178(2): 716 − 727. doi: 10.1104/pp.18.00651 [62] CHOI J Y, PURUGGANAN M D. Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice [J]. Mol Biol Evol, 2018, 35(2): 365 − 382. doi: 10.1093/molbev/msx284 [63] WALSH C P, CHAILLET J R, BESTOR T H. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation [J]. Nat Genet, 1998, 20(2): 116 − 117. doi: 10.1038/2413 [64] ZHOU Y, CAMBARERI E, KINSEY J. DNA methylation inhibits expression and transposition of the neurospora tad retrotransposon [J]. Mol Genet Genomics, 2001, 265(4): 748 − 754. doi: 10.1007/s004380100472 [65] CHERNYAVSKAYA Y, MUDBHARY R, ZHANG Chi, et al. Loss of DNA methylation in zebrafish embryos activates retrotransposons to trigger antiviral signaling [J]. Development, 2017, 144(16): 2925 − 2939. doi: 10.1242/dev.147629 [66] HOSAKA A, SAITO R, TAKASHIMA K, et al. Evolution of sequence-specific anti-silencing systems in Arabidopsis [J]. Nat Commun, 2017, 8(1): 1 − 10. doi: 10.1038/s41467-016-0009-6 [67] FU Yu, KAWABE A, ETCHEVERRY M, et al. Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor [J]. EMBO J, 2013, 32(17): 2407 − 2417. doi: 10.1038/emboj.2013.169 [68] CUI Hongchang, FEDOROFF N V. Inducible DNA demethylation mediated by the maize suppressor-mutator transposon-encoded TnpA protein [J]. Plant Cell, 2002, 14(11): 2883 − 2899. doi: 10.1105/tpc.006163 [69] DUAN Chengguo, WANG Xingang, XIE Shaojun, et al. A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation [J]. Cell Res, 2017, 27(2): 226 − 240. doi: 10.1038/cr.2016.147 [70] QIAN Weiqiang, MIKI D, ZHANG Heng, et al. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis [J]. Science, 2012, 336(6087): 1445 − 1448. doi: 10.1126/science.1219416 [71] CHEN Xiaochao, SCHÖNBERGER B, MENZ J, et al. Plasticity of DNA methylation and gene expression under zinc deficiency in Arabidopsis roots [J]. Plant Cell Physiol, 2018, 59(9): 1790 − 1802. doi: 10.1093/pcp/pcy100 [72] MAGER S, LUDEWIG U. Massive loss of DNA methylation in nitrogen-, but not in phosphorus-deficient Zea mays roots is poorly correlated with gene expression differences [J]. Front Plant Sci, 2018, 9: 497. doi: 10.3389/fpls.2018.00497. [73] FERREIRA L J, AZEVEDO V, MAROCO J, et al. Salt tolerant and sensitive rice varieties display differential methylome flexibility under salt stress [J]. PLoS One, 2015, 10(5): e0124060. doi: 10.1371/journal.pone.0124060. [74] RODRÍGUEZ-NEGRETE E, LOZANO-DURÁN R, PIEDRA-AGUILERA A, et al. Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing [J]. New Phytol, 2013, 199(2): 464 − 475. doi: 10.1111/nph.12286 [75] LIANG Xiong, HOU Xue, LI Jianying, et al. High-resolution DNA methylome reveals that demethylation enhances adaptability to continuous cropping comprehensive stress in soybean [J]. BMC Plant Biol, 2019, 19(1): 79. doi: 10.1186/s12870-019-1670-9. [76] YU A, LEPÈRE G, JAY F, et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense [J]. Proc Natl Acad Sci, 2013, 110(6): 2389 − 2394. doi: 10.1073/pnas.1211757110 [77] ZHANG Meng, ZHANG Xuexian, GUO Liping, et al. Single-base resolution methylomes of cotton CMS system reveal epigenomic changes in response to high-temperature stress during anther development [J]. J Exp Bot, 2019, 71(3): 951 − 969. [78] HE S, VICKERS M, ZHANG J, et al. Natural depletion of histone H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation [J]. eLife, 2019, 8: e42530. doi: 10.7554/eLife.42530.002. [79] NISHIMURA H, HIMI E, EUN C H, et al. Transgenerational activation of an autonomous DNA transposon, Dart1-24, by 5-azaC treatment in rice [J]. Theor Appl Genet, 2019, 132(12): 3347 − 3355. doi: 10.1007/s00122-019-03429-7 [80] SECCO D, WANG Chuang, SHOU Huixia, et al. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements [J]. eLife, 2015, 4: e09343. doi: 10.7554/eLife.09343.001. [81] KOFLER R. Dynamics of transposable element invasions with piRNA clusters [J]. Mol Biol Evol, 2019, 36(7): 1457 − 1472. doi: 10.1093/molbev/msz079 [82] GRAY Y H M. It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements [J]. Trends Genet, 2000, 16(10): 461 − 468. doi: 10.1016/S0168-9525(00)02104-1 -
-
链接本文:
http://zlxb.zafu.edu.cn/article/doi/10.11833/j.issn.2095-0756.20200338
下载:
点击查看大图
计量
- 文章访问数: 71
- 被引次数: 0
