Early Embryogenesis-Specific Expression of the Rice Transposon Enhances Amplification of the MITE

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Transposable elements are major components of eukaryotic genomes, comprising a large portion of the genome in some species. Miniature inverted-repeat transposable elements (MITEs), which belong to the class II DNA transposable elements, are abundant in gene-rich regions, and their copy numbers are very high; therefore, they have been considered to contribute to genome evolution. Because MITEs are short and have no coding capacity, they cannot transpose their positions without the aid of transposase, provided in trans by their autonomous element(s). It has been unknown how MITEs amplify themselves to high copy numbers in the genome. Our results demonstrate that the rice active MITE mPing is mobilized in the embryo by the developmental stage-specific up-regulation of an autonomous element, Ping, and thereby successfully amplifies itself to a high copy number in the genome. The short-term expression of Ping is thought to be a strategy of the mPing family for amplifying mPing by escaping the silencing mechanism of the host genome.

Vyšlo v časopise: Early Embryogenesis-Specific Expression of the Rice Transposon Enhances Amplification of the MITE. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004396
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004396

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1. SchnablePS, WareD, FultonRS, SteinJC, WeiF, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115 doi: 10.1126/science.1178534

2. WickerT, ZimmermannW, PerovicD, PatersonAH, GanalM, et al. (2005) A detailed look at 7 million years of genome evolution in a 439 kb contiguous sequence at the barley Hv-eIF4E locus: recombination, rearrangements and repeats. Plant J 41: 184–194 doi: 10.1111/j.1365-313X.2004.02285.x

3. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436: 793–800 doi: 10.1038/nature03895

4. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815 doi: 10.1038/35048692

5. FedoroffNV (2012) Transposable Elements, Epigenetics, and Genome Evolution. Science 338: 758–767 doi: 10.1126/science.338.6108.758

6. CowleyM, OakeyRJ (2013) Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet 9: e1003234 doi: 10.1371/journal.pgen.1003234

7. BureauTE, WesslerSR (1992) Tourist: A Large Family of Small Inverted Repeat Elements Frequently Associated with Maize Genes. Plant Cell 4: 1283–1294.

8. BureauTE, WesslerSR (1994) Stowaway: A New Family of Inverted Repeat Elements Associated with the Genes of both Monocotyledonous and Dicotyledonous Plants. Plant Cell 6: 907–916 doi: 10.1105/tpc.6.6.907

9. WesslerSR, BureauTE, WhiteSE (1995) LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 5: 814–821 doi:10.1016/0959-437x(95)80016-x

10. OkiN, YanoK, OkumotoY, TsukiyamaT, TeraishiM, et al. (2008) A genome-wide view of miniature inverted-repeat transposable elements (MITEs) in rice, Oryza sativa ssp. japonica. Genes Genet Syst 83: 321–329 doi: 10.1266/ggs.83.321

11. ChenJ, LuC, ZhangY, KuangH (2012) Miniature inverted-repeat transposable elements (MITEs) in rice were originated and amplified predominantly after the divergence of Oryza and Brachypodium and contributed considerable diversity to the species. Mob Genet Elements 2: 127–132 doi: 10.4161/mge.20773

12. HanY, QinS, WesslerSR (2013) Comparison of class 2 transposable elements at superfamily resolution reveals conserved and distinct features in cereal grass genomes. BMC Genomics 14: 71 doi:10.1186/1471-2164-14-71

13. NaitoK, ZhangF, TsukiyamaT, SaitoH, HancockCN, et al. (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461: 1130–1134 doi:10.1038/nature08479

14. JiangN, BaoZ, ZhangX, HirochikaH, EddySR, et al. (2003) An active DNA transposon family in rice. Nature 421: 163–167 doi:10.1038/nature01214

15. KikuchiK, TerauchiK, WadaM, HiranoH-Y (2003) The plant MITE mPing is mobilized in anther culture. Nature 421: 167–170 doi:10.1038/nature01218

16. NakazakiT, OkumotoY, HoribataA, YamahiraS, TeraishiM, et al. (2003) Mobilization of a transposon in the rice genome. Nature 421: 170–172 doi:10.1038/nature01219

17. LinX, LongL, ShanX, ZhangS, ShenS, et al. (2006) In planta mobilization of mPing and its putative autonomous element Pong in rice by hydrostatic pressurization. J Exp Bot 57: 2313–2323 doi: 10.1093/jxb/erj203

18. YangX, YuY, JiangL, LinX, ZhangC, et al. (2012) Changes in DNA methylation and transgenerational mobilization of a transposable element (mPing) by the Topoisomerase II inhibitor, Etoposide, in rice. BMC Plant Biol 12: 48 doi:10.1186/1471-2229-12-48

19. ShanX, LiuZ, DongZ, WangY, ChenY, et al. (2005) Mobilization of the Active MITE Transposons mPing and Pong in Rice by Introgression from Wild Rice (Zizania latifolia Griseb.). Mol Biol Evol 22: 976–990 doi:10.1093/molbev/msi082

20. YasudaK, TsukiyamaT, KarkiS, OkumotoY, TeraishiM, et al. (2012) Mobilization of the active transposon mPing in interspecific hybrid rice between Oryza sativa and O. glaberrima. Euphytica 192: 17–24 doi: 10.1007/s10681-012-0810-1

21. NaitoK, ChoE, YangG, CampbellMA, YanoK, et al. (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 103: 17620–17625 doi: 10.1073/pnas.0605421103

22. YangG, ZhangF, HancockCN, WesslerSR (2007) Transposition of the rice miniature inverted repeat transposable element mPing in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 10962–10967 doi: 10.1073/pnas.0702080104

23. HancockCN, ZhangF, WesslerSR (2010) Transposition of the Tourist-MITE mPing in yeast: an assay that retains key features of catalysis by the class 2 PIF/Harbinger superfamily. Mob DNA 1: 5 doi:10.1186/1759-8753-1-5

24. HarenL, Ton-HoangB, ChandlerM (1999) INTEGRATING DNA: Transposases and Retroviral Integrases. Annu Rev Microbiol 53: 245–281 doi: 10.1146/annurev.micro.53.1.245

25. SinzelleL, KapitonovVV, GrzelaDP, JurschT, JurkaJ, et al. (2008) Transposition of a reconstructed Harbinger element in human cells and functional homology with two transposon-derived cellular genes. Proc Natl Acad Sci USA 105: 4715–4720 doi: 10.1073/pnas.0707746105

26. SlotkinRK, VaughnM, BorgesF, TanurdzićM, BeckerJD, et al. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461–472 doi: 10.1016/j.cell.2008.12.038

27. HamamuraY, SaitoC, AwaiC, KuriharaD, MiyawakiA, et al. (2011) Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr Biol 21: 497–502 doi: 10.1016/j.cub.2011.02.013

28. ItohJ-I, NonomuraK-I, IkedaK, YamakiS, InukaiY, et al. (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46: 23–47 doi: 10.1093/pcp/pci501

29. MondenY, NaitoK, OkumotoY, SaitoH, OkiN, et al. (2009) High potential of a transposon mPing as a marker system in japonica × japonica cross in rice. DNA Res 16: 131–140 doi: 10.1093/dnares/dsp004

30. TsukiyamaT, TeramotoS, YasudaK, HoribataA, MoriN, et al. (2013) Loss-of-Function of a Ubiquitin-Related Modifier Promotes the Mobilization of the Active MITE mPing. Mol Plant 6: 790–801 doi: 10.1093/mp/sst042

31. FukaiE, UmeharaY, SatoS, EndoM, KouchiH, et al. (2010) Derepression of the Plant Chromovirus LORE1 Induces Germline Transposition in Regenerated Plants. PLoS Genet 6 doi:10.1371/journal.pgen.1000868

32. LiuD, CrawfordNM (1998) Characterization of the germinal and somatic activity of the Arabidopsis transposable element Tag1. Genetics 148: 445–456.

33. LevyAA, BrittAB, LuehrsenKR, ChandlerVL, WarrenC, et al. (1989) Developmental and genetic aspects of Mutator excision in maize. Dev Genet 10: 520–531 doi: 10.1002/dvg.1020100611

34. LevyA, WalbotV (1990) Regulation of the timing of transposable element excision during maize development. Science 248: 1534–1537 doi: 10.1126/science.2163107

35. TsuganeK, MaekawaM, TakagiK, TakaharaH, QianQ, et al. (2006) An active DNA transposon nDart causing leaf variegation and mutable dwarfism and its related elements in rice. Plant J 45: 46–57 doi: 10.1111/j.1365-313X.2005.02600.x

36. KitamuraK, HashidaSN, MikamiT, KishimaY (2001) Position effect of the excision frequency of the Antirrhinum transposon Tam3: implications for the degree of position-dependent methylation in the ends of the element. Plant Mol Biol 47: 475–490 doi: 10.1023/A:1011892003996

37. TokuhiroS, YamadaR, ChangX, SuzukiA, KochiY, et al. (2003) An intronic SNP in a RUNX1 binding site of SLC22A4, encoding an organic cation transporter, is associated with rheumatoid arthritis. Nat Genet 35: 341–348 doi:10.1038/ng1267

38. AlberobelloAT, CongedoV, LiuH, CochranC, SkarulisMC, et al. (2011) An intronic SNP in the thyroid hormone receptor β gene is associated with pituitary cell-specific over-expression of a mutant thyroid hormone receptor β2 (R338W) in the index case of pituitary-selective resistance to thyroid hormone. J Transl Med 9: 144 doi: 10.1186/1479-5876-9-144

39. Guermonprez H, Henaff E, Cifuentes M, Casacuberta JM (2012) MITEs, Miniature Elements with a Major Role in Plant Genome Evolution. In: Grandbastien M-A, Casacuberta JM, editors. Plant Transposable Elements: Impact on Genome Structure and Function. Berlin, Heidelberg: Springer. pp. 113–124. doi: 10.1007/978-3-642-31842-9

40. KawaharaY, de la BastideM, HamiltonJP, KanamoriH, McCombieWR, et al. (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6: 4.

41. SakaiH, LeeSS, TanakaT, NumaH, KimJ, et al. (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54: e6 doi: 10.1093/pcp/pcs183

42. OkiN, OkumotoY, TsukiyamaT, NaitoK, NakazakiT, et al. (2007) A Novel Transposon Pyong in the japonica Rice Variety Gimbozu. J Crop Res 52: 39–43.

43. LivakKJ, SchmittgenTD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2–ΔΔCT Method. Methods 25: 402–408 doi: 10.1006/meth.2001.1262

44. KouchiH, HataS (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238: 106–119 doi: 10.1007/BF00279537

45. BaruchO, KashkushK (2012) Analysis of copy-number variation, insertional polymorphism, and methylation status of the tiniest class I (TRIM) and class II (MITE) transposable element families in various rice strains. Plant Cell Rep 31: 885–893 doi: 10.1007/s00299-011-1209-5s