Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Autoři: Nino A. Espinas aff001;  Le Ngoc Tu aff001;  Leonardo Furci aff001;  Yasuka Shimajiri aff001;  Yoshiko Harukawa aff001;  Saori Miura aff001;  Shohei Takuno aff004;  Hidetoshi Saze aff001
Působiště autorů: Plant Epigenetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, Japan aff001;  Plant Immunity Research Group, RIKEN Center for Sustainable Resource Science (CSRS), Yokohama city, Kanagawa, Japan aff002;  EditForce, Fukuoka, Japan aff003;  Department of Evolutionary Studies of Biosystems, SOKENDAI (The Graduate University for Advanced Studies), Hayama, Kanagawa, Japan aff004
Vyšlo v časopise: Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008637
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008637


Intronic regions of eukaryotic genomes accumulate many Transposable Elements (TEs). Intronic TEs often trigger the formation of transcriptionally repressive heterochromatin, even within transcription-permissive chromatin environments. Although TE-bearing introns are widely observed in eukaryotic genomes, their epigenetic states, impacts on gene regulation and function, and their contributions to genetic diversity and evolution, remain poorly understood. In this study, we investigated the genome-wide distribution of intronic TEs and their epigenetic states in the Oryza sativa genome, where TEs comprise 35% of the genome. We found that over 10% of rice genes contain intronic heterochromatin, most of which are associated with TEs and repetitive sequences. These heterochromatic introns are longer and highly enriched in promoter-proximal positions. On the other hand, introns also accumulate hypomethylated short TEs. Genes with heterochromatic introns are implicated in various biological functions. Transcription of genes bearing intronic heterochromatin is regulated by an epigenetic mechanism involving the conserved factor OsIBM2, mutation of which results in severe developmental and reproductive defects. Furthermore, we found that heterochromatic introns evolve rapidly compared to non-heterochromatic introns. Our study demonstrates that heterochromatin is a common epigenetic feature associated with actively transcribed genes in the rice genome.

Klíčová slova:

Arabidopsis thaliana – DNA methylation – Gene expression – Genetic loci – Heterochromatin – Introns – Plant genomics – Rice


1. Kazazian HH Jr. Mobile elements: drivers of genome evolution. Science. 2004;303(5664):1626–32. Epub 2004/03/16. doi: 10.1126/science.1089670 15016989.

2. Bennetzen JL, Wang H. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol. 2014;65:505–30. Epub 2014/03/04. doi: 10.1146/annurev-arplant-050213-035811 24579996.

3. Tenaillon MI, Hollister JD, Gaut BS. A triptych of the evolution of plant transposable elements. Trends Plant Sci. 2010;15(8):471–8. Epub 2010/06/15. doi: 10.1016/j.tplants.2010.05.003 20541961.

4. Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009;19(8):1419–28. Epub 2009/05/30. doi: 10.1101/gr.091678.109 19478138; PubMed Central PMCID: PMC2720190.

5. Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, et al. Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet. 2015;11(1):e1004915. Epub 2015/01/09. doi: 10.1371/journal.pgen.1004915 25569788; PubMed Central PMCID: PMC4287451.

6. Galindo-Gonzalez L, Mhiri C, Deyholos MK, Grandbastien MA. LTR-retrotransposons in plants: Engines of evolution. Gene. 2017;626:14–25. Epub 2017/05/10. doi: 10.1016/j.gene.2017.04.051 28476688.

7. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature. 2009;461(7267):1130–4. Epub 2009/10/23. doi: 10.1038/nature08479 19847266.

8. Lisch D. How important are transposons for plant evolution? Nat Rev Genet. 2013;14(1):49–61. Epub 2012/12/19. doi: 10.1038/nrg3374 23247435.

9. Quadrana L, Colot V. Plant Transgenerational Epigenetics. Annu Rev Genet. 2016;50:467–91. Epub 2016/10/13. doi: 10.1146/annurev-genet-120215-035254 27732791.

10. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8(4):272–85. Epub 2007/03/17. doi: 10.1038/nrg2072 17363976.

11. Saze H, Mittelsten Scheid O, Paszkowski J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet. 2003;34(1):65–9. Epub 2003/04/02. doi: 10.1038/ng1138 12669067.

12. Hu LJ, Li N, Xu CM, Zhong SL, Lin XY, Yang JJ, et al. Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Proc Natl Acad Sci USA. 2014;111(29):10642–7. doi: 10.1073/pnas.1410761111 WOS:000339310700060. 25002488

13. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, et al. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics. 2003;163(3):1109–22. WOS:000182046900023. 12663548

14. Yamauchi T, Johzuka-Hisatomi Y, Terada R, Nakamura I, Iida S. The MET1b gene encoding a maintenance DNA methyltransferase is indispensable for normal development in rice. Plant Mol Biol. 2014;85(3):219–32. doi: 10.1007/s11103-014-0178-9 WOS:000336030800002. 24535433

15. Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014;15(6):394–408. Epub 2014/05/09. doi: 10.1038/nrg3683 24805120.

16. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11(3):204–20. Epub 2010/02/10. doi: 10.1038/nrg2719 20142834; PubMed Central PMCID: PMC3034103.

17. Wendte JM, Schmitz RJ. Specifications of Targeting Heterochromatin Modifications in Plants. Mol Plant. 2018;11(3):381–7. doi: 10.1016/j.molp.2017.10.002 WOS:000426964100005. 29032247

18. Martienssen R, Moazed D. RNAi and heterochromatin assembly. Cold Spring Harb Perspect Biol. 2015;7(8):a019323. Epub 2015/08/05. doi: 10.1101/cshperspect.a019323 26238358; PubMed Central PMCID: PMC4526745.

19. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013;153(1):193–205. Epub 2013/04/02. doi: 10.1016/j.cell.2013.02.033 23540698; PubMed Central PMCID: PMC4035305.

20. Tan F, Zhou C, Zhou QW, Zhou SL, Yang WJ, Zhao Y, et al. Analysis of Chromatin Regulators Reveals Specific Features of Rice DNA Methylation Pathways. Plant Physiol. 2016;171(3):2041–54. doi: 10.1104/pp.16.00393 WOS:000381303300043. 27208249

21. Numa H, Yamaguchi K, Shigenobu S, Habu Y. Gene Body CG and CHG Methylation and Suppression of Centromeric CHH Methylation are Mediated by DECREASE IN DNA METHYLATION1 in Rice. Mol Plant. 2015;8(10):1560–2. Epub 2015/08/19. doi: 10.1016/j.molp.2015.08.002 26277261.

22. Hirsch CD, Springer NM. Transposable element influences on gene expression in plants. Biochim Biophys Acta. 2017;1860(1):157–65. Epub 2016/05/29. doi: 10.1016/j.bbagrm.2016.05.010 27235540.

23. Mirouze M, Vitte C. Transposable elements, a treasure trove to decipher epigenetic variation: insights from Arabidopsis and crop epigenomes. J Exp Bot. 2014;65(10):2801–12. doi: 10.1093/jxb/eru120 WOS:000338005600021. 24744427

24. Henderson IR, Jacobsen SE. Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Gene Dev. 2008;22(12):1597–606. doi: 10.1101/gad.1667808 WOS:000256797300006. 18559476

25. Soppe WJJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell. 2000;6(4):791–802. doi: 10.1016/s1097-2765(05)00090-0 WOS:000090136700004. 11090618

26. Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet. 2006;38(8):948–52. doi: 10.1038/ng1841 WOS:000239325700027. 16832354

27. Gehring M, Bubb KL, Henikoff S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science. 2009;324(5933):1447–51. Epub 2009/06/13. doi: 10.1126/science.1171609 19520961; PubMed Central PMCID: PMC2886585.

28. Le TN, Miyazaki Y, Takuno S, Saze H. Epigenetic regulation of intragenic transposable elements impacts gene transcription in Arabidopsis thaliana. Nucleic Acids Res. 2015;43(8):3911–21. Epub 2015/03/31. doi: 10.1093/nar/gkv258 25813042; PubMed Central PMCID: PMC4417168.

29. Seymour DK, Koenig D, Hagmann J, Becker C, Weigel D. Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLoS Genet. 2014;10(11):e1004785. Epub 2014/11/14. doi: 10.1371/journal.pgen.1004785 25393550; PubMed Central PMCID: PMC4230842.

30. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, et al. The Norway spruce genome sequence and conifer genome evolution. Nature. 2013;497(7451):579–84. Epub 2013/05/24. doi: 10.1038/nature12211 23698360.

31. West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, et al. Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One. 2014;9(8):e105267. Epub 2014/08/15. doi: 10.1371/journal.pone.0105267 25122127; PubMed Central PMCID: PMC4133378.

32. To TK, Saze H, Kakutani T. DNA Methylation within Transcribed Regions. Plant Physiol. 2015;168(4):1219–25. Epub 2015/07/06. doi: 10.1104/pp.15.00543 26143255; PubMed Central PMCID: PMC4528756.

33. Duan CG, Wang X, Zhang L, Xiong X, Zhang Z, Tang K, et al. A protein complex regulates RNA processing of intronic heterochromatin-containing genes in Arabidopsis. Proc Natl Acad Sci U S A. 2017;114(35):E7377–E84. Epub 2017/08/16. doi: 10.1073/pnas.1710683114 28808009; PubMed Central PMCID: PMC5584460.

34. Saze H, Kitayama J, Takashima K, Miura S, Harukawa Y, Ito T, et al. Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin. Nat Commun. 2013;4:2301. Epub 2013/08/13. doi: 10.1038/ncomms3301 23934508.

35. Coustham V, Vlad D, Deremetz A, Gy I, Cubillos FA, Kerdaffrec E, et al. SHOOT GROWTH1 maintains Arabidopsis epigenomes by regulating IBM1. PLoS One. 2014;9(1):e84687. Epub 2014/01/10. doi: 10.1371/journal.pone.0084687 24404182; PubMed Central PMCID: PMC3880313.

36. Wang X, Duan CG, Tang K, Wang B, Zhang H, Lei M, et al. RNA-binding protein regulates plant DNA methylation by controlling mRNA processing at the intronic heterochromatin-containing gene IBM1. Proc Natl Acad Sci U S A. 2013;110(38):15467–72. Epub 2013/09/05. doi: 10.1073/pnas.1315399110 24003136; PubMed Central PMCID: PMC3780877.

37. Saze H. Epigenetic regulation of intragenic transposable elements: a two-edged sword. J Biochem. 2018;164(5):323–8. doi: 10.1093/jb/mvy060 WOS:000449471000001. 30010918

38. Wei L, Gu L, Song X, Cui X, Lu Z, Zhou M, et al. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci U S A. 2014;111(10):3877–82. Epub 2014/02/21. doi: 10.1073/pnas.1318131111 24554078; PubMed Central PMCID: PMC3956178.

39. Liu N, Lee CH, Swigut T, Grow E, Gu B, Bassik MC, et al. Selective silencing of euchromatic L1s revealed by genome-wide screens for L1 regulators. Nature. 2018;553(7687):228–32. Epub 2017/12/07. doi: 10.1038/nature25179 29211708; PubMed Central PMCID: PMC5774979.

40. Lorincz MC, Dickerson DR, Schmitt M, Groudine M. Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol. 2004;11(11):1068–75. Epub 2004/10/07. doi: 10.1038/nsmb840 15467727.

41. Liu J, He Y, Amasino R, Chen X. siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev. 2004;18(23):2873–8. Epub 2004/11/17. doi: 10.1101/gad.1217304 15545622; PubMed Central PMCID: PMC534648.

42. Kum R, Tsukiyama T, Inagaki H, Saito H, Teraishi M, Okumoto Y, et al. The active miniature inverted-repeat transposable element mPing posttranscriptionally produces new transcriptional variants in the rice genome. Mol Breeding. 2015;35(8). ARTN 159 doi: 10.1007/s11032-015-0353-y WOS:000360005100010.

43. Khan AR, Enjalbert J, Marsollier AC, Rousselet A, Goldringer I, Vitte C. Vernalization treatment induces site-specific DNA hypermethylation at the VERNALIZATION-A1 (VRN-A1) locus in hexaploid winter wheat. BMC Plant Biol. 2013;13:209. Epub 2013/12/18. doi: 10.1186/1471-2229-13-209 24330651; PubMed Central PMCID: PMC3890506.

44. Osabe K, Harukawa Y, Miura S, Saze H. Epigenetic Regulation of Intronic Transgenes in Arabidopsis. Sci Rep. 2017;7:45166. Epub 2017/03/25. doi: 10.1038/srep45166 28338020; PubMed Central PMCID: PMC5364540.

45. Tsuchiya T, Eulgem T. An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proc Natl Acad Sci U S A. 2013;110(37):E3535–43. Epub 2013/08/14. doi: 10.1073/pnas.1312545110 23940361; PubMed Central PMCID: PMC3773791.

46. Ong-Abdullah M, Ordway JM, Jiang N, Ooi SE, Kok SY, Sarpan N, et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature. 2015;525(7570):533–7. Epub 2015/09/10. doi: 10.1038/nature15365 26352475; PubMed Central PMCID: PMC4857894.

47. Xie Y, Zhang Y, Han J, Luo J, Li G, Huang J, et al. The Intronic cis Element SE1 Recruits trans-Acting Repressor Complexes to Repress the Expression of ELONGATED UPPERMOST INTERNODE1 in Rice. Mol Plant. 2018;11(5):720–35. Epub 2018/03/11. doi: 10.1016/j.molp.2018.03.001 29524649.

48. Questa JI, Song J, Geraldo N, An HL, Dean C. Arabidopsis transcriptional repressor VAL1 triggers Polycomb silencing at FLC during vernalization. Science. 2016;353(6298):485–8. doi: 10.1126/science.aaf7354 WOS:000380583600040. 27471304

49. Yuan WY, Luo X, Li ZC, Yang WN, Wang YZ, Liu R, et al. A cis cold memory element and a trans epigenome reader mediate Polycomb silencing of FLC by vernalization in Arabidopsis. Nat Genet. 2016;48(12):1527–34. doi: 10.1038/ng.3712 WOS:000389011100013. 27819666

50. Hong RL, Hamaguchi L, Busch MA, Weigel D. Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell. 2003;15(6):1296–309. doi: 10.1105/tpc.009548 WOS:000185078300004. 12782724

51. Song X, Cao X. Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice. Curr Opin Plant Biol. 2017;36:111–8. Epub 2017/03/09. doi: 10.1016/j.pbi.2017.02.004 28273484.

52. Feschotte C, Jiang N, Wessler SR. Plant transposable elements: Where genetics meets genomics. Nat Rev Genet. 2002;3(5):329–41. doi: 10.1038/nrg793 WOS:000175350000011. 11988759

53. Matsumoto T, Wu JZ, Kanamori H, Katayose Y, Fujisawa M, Namiki N, et al. The map-based sequence of the rice genome. Nature. 2005;436(7052):793–800. doi: 10.1038/nature03895 WOS:000231116500034. 16100779

54. Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell. 2012;151(1):167–80. Epub 2012/10/02. doi: 10.1016/j.cell.2012.07.034 23021223; PubMed Central PMCID: PMC3471781.

55. Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, Cortijo S, et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 2011;30(10):1928–38. doi: 10.1038/emboj.2011.103 WOS:000291645400009. 21487388

56. Bradnam KR, Korf I. Longer First Introns Are a General Property of Eukaryotic Gene Structure. Plos One. 2008;3(8). ARTN e3093 doi: 10.1371/journal.pone.0003093 WOS:000264796800003. 18769727

57. Oki N, Yano K, Okumoto Y, Tsukiyama T, Teraishi M, Tanisaka T. A genome-wide view of miniature inverted-repeat transposable elements (MITEs) in rice, Oryza sativa ssp japonica. Genes Genet Syst. 2008;83(4):321–9. doi: 10.1266/ggs.83.321 WOS:000261872300004. 18931457

58. Lu C, Chen J, Zhang Y, Hu Q, Su W, Kuang H. Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol. 2012;29(3):1005–17. Epub 2011/11/19. doi: 10.1093/molbev/msr282 22096216; PubMed Central PMCID: PMC3278479.

59. Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, et al. The Arabidopsis thaliana mobilome and its impact at the species level. Elife. 2016;5. Epub 2016/06/04. doi: 10.7554/eLife.15716 27258693; PubMed Central PMCID: PMC4917339.

60. Choi JY, Purugganan MD. Evolutionary Epigenomics of Retrotransposon-Mediated Methylation Spreading in Rice. Mol Biol Evol. 2018;35(2):365–82. Epub 2017/11/11. doi: 10.1093/molbev/msx284 29126199; PubMed Central PMCID: PMC5850837.

61. Chen J, Hu Q, Zhang Y, Lu C, Kuang H. P-MITE: a database for plant miniature inverted-repeat transposable elements. Nucleic Acids Res. 2014;42(Database issue):D1176–81. Epub 2013/11/01. doi: 10.1093/nar/gkt1000 24174541; PubMed Central PMCID: PMC3964958.

62. Sato Y, Takehisa H, Kamatsuki K, Minami H, Namiki N, Ikawa H, et al. RiceXPro Version 3.0: expanding the informatics resource for rice transcriptome. Nuc Acids Res. 2013;41(D1):D1206–D13. doi: 10.1093/nar/gks1125 WOS:000312893300171. 23180765

63. Kawahara Y, Oono Y, Wakimoto H, Ogata J, Kanamori H, Sasaki H, et al. TENOR: Database for Comprehensive mRNA-Seq Experiments in Rice. Plant Cell Physiol. 2016;57(1):e7. Epub 2015/11/19. doi: 10.1093/pcp/pcv179 26578693.

64. Schug J, Schuller WP, Kappen C, Salbaum JM, Bucan M, Stoeckert CJ. Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biol. 2005;6(4). ARTN R33 doi: 10.1186/gb-2005-6-4-r33 WOS:000228436000010. 15833120

65. Fawcett JA, Kado T, Sasaki E, Takuno S, Yoshida K, Sugino RP, et al. QTL map meets population genomics: an application to rice. PLoS One. 2013;8(12):e83720. Epub 2014/01/01. doi: 10.1371/journal.pone.0083720 24376738; PubMed Central PMCID: PMC3871663.

66. Wasternack C, Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot-London. 2013;111(6):1021–58. doi: 10.1093/aob/mct067 WOS:000319433300002. 23558912

67. Mansueto L, Fuentes RR, Borja FN, Detras J, Abriol-Santos JM, Chebotarov D, et al. Rice SNP-seek database update: new SNPs, indels, and queries. Nucleic Acids Res. 2017;45(D1):D1075–D81. Epub 2016/12/03. doi: 10.1093/nar/gkw1135 27899667; PubMed Central PMCID: PMC5210592.

68. Mei CS, Qi M, Sheng GY, Yang YN. Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe In. 2006;19(10):1127–37. doi: 10.1094/Mpmi-19-1127 WOS:000240692300009. 17022177

69. Ogawa S, Kawahara-Miki R, Miyamoto K, Yamane H, Nojiri H, Tsujii Y, et al. OsMYC2 mediates numerous defence-related transcriptional changes via jasmonic acid signalling in rice. Biochem Bioph Res Co. 2017;486(3):796–803. doi: 10.1016/j.bbrc.2017.03.125 WOS:000399966700030. 28347822

70. Le TN, Osabe K, Miyazaki Y, Saze H. Epigenetic regulation of intragenic repeats in plant genomes. Genes Genet Syst. 2016;91(6):317–. WOS:000405886000006. doi: 10.1266/ggs.91.317

71. Yang Q, Liang C, Zhuang W, Li J, Deng H, Deng Q, et al. Characterization and identification of the candidate gene of rice thermo-sensitive genic male sterile gene tms5 by mapping. Planta. 2007;225(2):321–30. Epub 2006/08/10. doi: 10.1007/s00425-006-0353-6 16896793.

72. Itabashi E, Iwata N, Fujii S, Kazama T, Toriyama K. The fertility restorer gene, Rf2, for Lead Rice-type cytoplasmic male sterility of rice encodes a mitochondrial glycine-rich protein. Plant J. 2011;65(3):359–67. Epub 2011/01/27. doi: 10.1111/j.1365-313X.2010.04427.x 21265890.

73. Kubo T, Takano-kai N, Yoshimura A. RFLP mapping of genes for long kernel and awn on chromosome 3 in rice. Rice Genet Newsl. 2001;18:26–8.

74. Kang HG, Park S, Matsuoka M, An G. White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J. 2005;42(6):901–11. Epub 2005/06/09. doi: 10.1111/j.1365-313X.2005.02423.x 15941402.

75. Hirano HY, Sano Y. Molecular Characterization of the Waxy Locus of Rice (Oryza-Sativa). Plant Cell Physiol. 1991;32(7):989–97. doi: 10.1093/oxfordjournals.pcp.a078186 WOS:A1991GN75000009.

76. Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F. Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant Journal. 2009;59(6):908–20. doi: 10.1111/j.1365-313X.2009.03925.x WOS:000269708400005. 19473328

77. Miura A, Nakamura M, Inagaki S, Kobayashi A, Saze H, Kakutani T. An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J. 2009;28(8):1078–86. Epub 2009/03/06. doi: 10.1038/emboj.2009.59 19262562; PubMed Central PMCID: PMC2653724.

78. Inagaki S, Miura-Kamio A, Nakamura Y, Lu F, Cui X, Cao X, et al. Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J. 2010;29(20):3496–506. Epub 2010/09/14. doi: 10.1038/emboj.2010.227 20834229; PubMed Central PMCID: PMC2964174.

79. Lu FL, Li GL, Cui X, Liu CY, Wang XJ, Cao XF. Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice. J Integr Plant Biol. 2008;50(7):886–96. doi: 10.1111/j.1744-7909.2008.00692.x WOS:000257708300014. 18713399

80. Zhang QJ, Zhu T, Xia EH, Shi C, Liu YL, Zhang Y, et al. Rapid diversification of five Oryza AA genomes associated with rice adaptation. Proc Natl Acad Sci USA. 2014;111(46):E4954–E62. doi: 10.1073/pnas.1418307111 WOS:000345153300010. 25368197

81. Cheng C, Tarutani Y, Miyao A, Ito T, Yamazaki M, Sakai H, et al. Loss of function mutations in the rice chromomethylase OsCMT3a cause a burst of transposition. Plant J. 2015;83(6):1069–81. Epub 2015/08/06. doi: 10.1111/tpj.12952 26243209.

82. Moritoh S, Eun CH, Ono A, Asao H, Okano Y, Yamaguchi K, et al. Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation. Plant Journal. 2012;71(1):85–98. doi: 10.1111/j.1365-313X.2012.04974.x WOS:000305407000008. 22380881

83. Higo H, Tahir M, Takashima K, Miura A, Watanabe K, Tagiri A, et al. DDM1 (Decrease in DNA Methylation) genes in rice (Oryza sativa). Molecular Genetics and Genomics. 2012;287(10):785–92. doi: 10.1007/s00438-012-0717-5 WOS:000309240500002. 22915302

84. Kakutani T, Jeddeloh JA, Flowers SK, Munakata K, Richards EJ. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci USA. 1996;93(22):12406–11. doi: 10.1073/pnas.93.22.12406 WOS:A1996VP93700065. 8901594

85. Bartee L, Malagnac F, Bender J. Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Gene Dev. 2001;15(14):1753–8. doi: 10.1101/gad.905701 WOS:000170020000002. 11459824

86. Lindroth AM, Cao XF, Jackson JP, Zilberman D, McCallum CM, Henikoff S, et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science. 2001;292(5524):2077–80. doi: 10.1126/science.1059745 WOS:000169284700048. 11349138

87. Cao XF, Jacobsen SE. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol. 2002;12(13):1138–44. Pii S0960-9822(02)00925-9 doi: 10.1016/s0960-9822(02)00925-9 WOS:000176916900026. 12121623

88. Wei LY, Gu LF, Song XW, Cui XK, Lu ZK, Zhou M, et al. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci USA. 2014;111(10):3877–82. doi: 10.1073/pnas.1318131111 WOS:000332564800056. 24554078

89. Niu XM, Xu YC, Li ZW, Bian YT, Hou XH, Chen JF, et al. Transposable elements drive rapid phenotypic variation in Capsella rubella. Proc Natl Acad Sci USA. 2019;116(14):6908–13. doi: 10.1073/pnas.1811498116 WOS:000463069900067. 30877258

90. Maumus F, Quesneville H. Ancestral repeats have shaped epigenome and genome composition for millions of years in Arabidopsis thaliana. Nat Commun. 2014;5. ARTN 4104 doi: 10.1038/ncomms5104 WOS:000338838200018. 24954583

91. Chamary JV, Hurst LD. Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: Evidence for selectively driven codon usage. Mol Biol Evol. 2004;21(6):1014–23. doi: 10.1093/molbev/msh087 WOS:000221599300006. 15014158

92. Keightley PD, Gaffney DJ. Functional constraints and frequency of deleterious mutations in noncoding DNA of rodents. Proc Natl Acad Sci USA. 2003;100(23):13402–6. doi: 10.1073/pnas.2233252100 WOS:000186573700053. 14597721

93. Parra G, Bradnam K, Rose AB, Korf I. Comparative and functional analysis of intron-mediated enhancement signals reveals conserved features among plants. Nuc Acids Res. 2011;39(13):5328–37. doi: 10.1093/nar/gkr043 WOS:000293020000009. 21427088

94. Jeon JS, Lee S, Jung KH, Jun SH, Kim C, An G. Tissue-preferential expression of a rice alpha-tubulin gene, OsTubA1, mediated by the first intron. Plant Physiol. 2000;123(3):1005–14. doi: 10.1104/pp.123.3.1005 WOS:000088213300023. 10889249

95. Morello L, Bardini M, Sala F, Breviario D. A long leader intron of the Ostub16 rice beta-tubulin gene is required for high-level gene expression and can autonomously promote transcription both in vivo and in vitro. Plant J. 2002;29(1):33–44. doi: 10.1046/j.0960-7412.2001.01192.x WOS:000173544800004. 12060225

96. Liu SZ, Yeh CT, Ji TM, Ying K, Wu HY, Tang HM, et al. Mu Transposon Insertion Sites and Meiotic Recombination Events Co-Localize with Epigenetic Marks for Open Chromatin across the Maize Genome. Plos Genet. 2009;5(11). ARTN e1000733 doi: 10.1371/journal.pgen.1000733 WOS:000272419500028. 19936291

97. Vollbrecht E, Duvick J, Schares JP, Ahern KR, Deewatthanawong P, Xu L, et al. Genome-Wide Distribution of Transposed Dissociation Elements in Maize. Plant Cell. 2010;22(6):1667–85. doi: 10.1105/tpc.109.073452 WOS:000280505300004. 20581308

98. Yang L, Gaut BS. Factors that Contribute to Variation in Evolutionary Rate among Arabidopsis Genes. Mol Biol Evol. 2011;28(8):2359–69. doi: 10.1093/molbev/msr058 WOS:000293304700017. 21389272

99. Turner BM. Epigenetic responses to environmental change and their evolutionary implications. Philos T R Soc B. 2009;364(1534):3403–18. doi: 10.1098/rstb.2009.0125 WOS:000270800800009. 19833651

100. Meyers BC, Kaushik S, Nandety RS. Evolving disease resistance genes. Curr Opin Plant Biol. 2005;8(2):129–34. Epub 2005/03/09. doi: 10.1016/j.pbi.2005.01.002 15752991.

101. Espinas NA, Saze H, Saijo Y. Epigenetic Control of Defense Signaling and Priming in Plants. Front Plant Sci. 2016;7. ARTN 1201 doi: 10.3389/fpls.2016.01201 WOS:000381206400001. 27563304

102. Hosaka A, Kakutani T. Transposable elements, genome evolution and transgenerational epigenetic variation. Curr Opin Plant Biol. 2018;49:43–8. doi: 10.1016/j.gde.2018.02.012 WOS:000433211500007. 29525544

103. Li X, Guo K, Zhu X, Chen P, Li Y, Xie G, et al. Domestication of rice has reduced the occurrence of transposable elements within gene coding regions. BMC Genomics. 2017;18(1):55. Epub 2017/01/11. doi: 10.1186/s12864-016-3454-z 28068923; PubMed Central PMCID: PMC5223533.

104. Parenteau J, Maignon L, Berthoumieux M, Catala M, Gagnon V, Abou Elela S. Introns are mediators of cell response to starvation. Nature. 2019;565(7741):612–7. Epub 2019/01/18. doi: 10.1038/s41586-018-0859-7 30651641.

105. Morgan JT, Fink GR, Bartel DP. Excised linear introns regulate growth in yeast. Nature. 2019;565(7741):606–11. Epub 2019/01/18. doi: 10.1038/s41586-018-0828-1 30651636.

106. Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, et al. Rice Annotation Project Database (RAP-DB): An Integrative and Interactive Database for Rice Genomics. Plant Cell Physiol. 2013;54(2):E6–+. doi: 10.1093/pcp/pcs183 WOS:000315218700006. 23299411

107. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110(1–4):462–7. doi: 10.1159/000084979 WOS:000231064600047. 16093699

108. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res. 2008;36(Web Server issue):W5–9. Epub 2008/04/29. doi: 10.1093/nar/gkn201 18440982; PubMed Central PMCID: PMC2447716.

109. Lu L, Chen JF, Robb SMC, Okumoto Y, Stajich JE, Wessler SR. Tracking the genome-wide outcomes of a transposable element burst over decades of amplification. Proc Natl Acad Sci USA. 2017;114(49):E10550–E9. doi: 10.1073/pnas.1716459114 WOS:000417339700009. 29158416

110. Miki D, Shimamoto K. Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 2004;45(4):490–5. doi: 10.1093/pcp/pch048 WOS:000221037200015. 15111724

111. Miura F, Enomoto Y, Dairiki R, Ito T. Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res. 2012;40(17):e136. Epub 2012/06/01. doi: 10.1093/nar/gks454 22649061; PubMed Central PMCID: PMC3458524.

112. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 WOS:000340049100004. 24695404

113. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–2. doi: 10.1093/bioinformatics/btr167 WOS:000291062400018. 21493656

114. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841–2. doi: 10.1093/bioinformatics/btq033 WOS:000275243500019. 20110278

115. Takuno S, Gaut BS. Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol. 2012;29(1):219–27. Epub 2011/08/05. doi: 10.1093/molbev/msr188 21813466.

116. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013;152(1–2):352–64. Epub 2013/01/15. doi: 10.1016/j.cell.2012.10.054 23313553; PubMed Central PMCID: PMC3597350.

117. Ramirez F, Dundar F, Diehl S, Gruning BA, Manke T. deepTools: a flexible platform for exploring deep-sequencing data. Nuc Acids Res. 2014;42(W1):W187–W91. doi: 10.1093/nar/gku365 WOS:000339715000031. 24799436

118. Tian T, Liu Y, Yan HY, You Q, Yi X, Du Z, et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nuc Acids Res. 2017;45(W1):W122–W9. doi: 10.1093/nar/gkx382 WOS:000404427000019. 28472432

119. Mi HY, Lazareva-Ulitsky B, Loo R, Kejariwal A, Vandergriff J, Rabkin S, et al. The PANTHER database of protein families, subfamilies, functions and pathways. Nuc Acids Res. 2005;33:D284–D8. doi: 10.1093/nar/gki078 WOS:000226524300058. 15608197

120. Sun JQ, Nishiyama T, Shimizu K, Kadota K. TCC: an R package for comparing tag count data with robust normalization strategies. BMC Bioinformatics. 2013;14. Artn 219 doi: 10.1186/1471-2105-14-219 WOS:000321835900001. 23837715

121. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–U54. doi: 10.1038/nmeth.1923 WOS:000302218500017. 22388286

122. Alexandrov N, Tai S, Wang W, Mansueto L, Palis K, Fuentes RR, et al. SNP-Seek database of SNPs derived from 3000 rice genomes. Nucleic Acids Res. 2015;43(Database issue):D1023–7. Epub 2014/11/29. doi: 10.1093/nar/gku1039 25429973; PubMed Central PMCID: PMC4383887.

123. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60. Epub 2015/03/10. doi: 10.1038/nmeth.3317 25751142; PubMed Central PMCID: PMC4655817.

124. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. Epub 2009/06/10. doi: 10.1093/bioinformatics/btp352 19505943; PubMed Central PMCID: PMC2723002.

125. Freese NH, Norris DC, Loraine AE. Integrated genome browser: visual analytics platform for genomics. Bioinformatics. 2016;32(14):2089–95. Epub 2016/05/07. doi: 10.1093/bioinformatics/btw069 27153568; PubMed Central PMCID: PMC4937187.

126. Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nuc Acids Res. 2013;41(10). ARTN e108 doi: 10.1093/nar/gkt214 WOS:000319806600005. 23558742

127. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12). ARTN 550 doi: 10.1186/s13059-014-0550-8 WOS:000346609500022. 25516281

128. Gremme G, Brendel V, Sparks ME, Kurtz S. Engineering a software tool for gene structure prediction in higher organisms. Inform Software Tech. 2005;47(15):965–78. doi: 10.1016/j.infsof.2005.09.005 WOS:000234322400003.

129. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and clustal X version 2.0. Bioinformatics. 2007;23(21):2947–8. doi: 10.1093/bioinformatics/btm404 WOS:000251197700021. 17846036

130. Nei M, Gojobori T. Simple Methods for Estimating the Numbers of Synonymous and Nonsynonymous Nucleotide Substitutions. Mol Biol Evol. 1986;3(5):418–26. WOS:A1986E136000004. doi: 10.1093/oxfordjournals.molbev.a040410 3444411

131. Thompson JD, Higgins DG, Gibson TJ. Clustal-W—Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice. Nuc Acids Res. 1994;22(22):4673–80. doi: 10.1093/nar/22.22.4673 WOS:A1994PU19900018. 7984417

132. Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nuc Acids Res. 2018;46(D1):D493–D6. doi: 10.1093/nar/gkx922 WOS:000419550700075. 29040681

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