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Generation of Tandem Direct Duplications by Reversed-Ends Transposition of Maize Elements


Tandem direct duplications are a common feature of the genomes of eukaryotes ranging from yeast to human, where they comprise a significant fraction of copy number variations. The prevailing model for the formation of tandem direct duplications is non-allelic homologous recombination (NAHR). Here we report the isolation of a series of duplications and reciprocal deletions isolated de novo from a maize allele containing two Class II Ac/Ds transposons. The duplication/deletion structures suggest that they were generated by alternative transposition reactions involving the termini of two nearby transposable elements. The deletion/duplication breakpoint junctions contain 8 bp target site duplications characteristic of Ac/Ds transposition events, confirming their formation directly by an alternative transposition mechanism. Tandem direct duplications and reciprocal deletions were generated at a relatively high frequency (∼0.5 to 1%) in the materials examined here in which transposons are positioned nearby each other in appropriate orientation; frequencies would likely be much lower in other genotypes. To test whether this mechanism may have contributed to maize genome evolution, we analyzed sequences flanking Ac/Ds and other hAT family transposons and identified three small tandem direct duplications with the structural features predicted by the alternative transposition mechanism. Together these results show that some class II transposons are capable of directly inducing tandem sequence duplications, and that this activity has contributed to the evolution of the maize genome.


Vyšlo v časopise: Generation of Tandem Direct Duplications by Reversed-Ends Transposition of Maize Elements. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003691
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003691

Souhrn

Tandem direct duplications are a common feature of the genomes of eukaryotes ranging from yeast to human, where they comprise a significant fraction of copy number variations. The prevailing model for the formation of tandem direct duplications is non-allelic homologous recombination (NAHR). Here we report the isolation of a series of duplications and reciprocal deletions isolated de novo from a maize allele containing two Class II Ac/Ds transposons. The duplication/deletion structures suggest that they were generated by alternative transposition reactions involving the termini of two nearby transposable elements. The deletion/duplication breakpoint junctions contain 8 bp target site duplications characteristic of Ac/Ds transposition events, confirming their formation directly by an alternative transposition mechanism. Tandem direct duplications and reciprocal deletions were generated at a relatively high frequency (∼0.5 to 1%) in the materials examined here in which transposons are positioned nearby each other in appropriate orientation; frequencies would likely be much lower in other genotypes. To test whether this mechanism may have contributed to maize genome evolution, we analyzed sequences flanking Ac/Ds and other hAT family transposons and identified three small tandem direct duplications with the structural features predicted by the alternative transposition mechanism. Together these results show that some class II transposons are capable of directly inducing tandem sequence duplications, and that this activity has contributed to the evolution of the maize genome.


Zdroje

1. Ohno S (1970) Evolution by Gene Duplication: Springer-Verlag.

2. ZhangF, GuW, HurlesME, LupskiJR (2009) Copy Number Variation in Human Health, Disease, and Evolution. Annual Review of Genomics and Human Genetics 10: 451–481.

3. BaileyJA, GuZ, ClarkRA, ReinertK, SamonteRV, et al. (2002) Recent segmental duplications in the human genome. Science (New York, NY) 297: 1003–1007.

4. SheX, ChengZ, ZollnerS, ChurchDM, EichlerEE (2008) Mouse segmental duplication and copy number variation. Nat Genet 40: 909–914.

5. LinH, ZhuW, SilvaJC, GuX, BuellCR (2006) Intron gain and loss in segmentally duplicated genes in rice. Genome Biol 7: R41.

6. VandepoeleK, SimillionC, Van de PeerY (2003) Evidence that rice and other cereals are ancient aneuploids. Plant Cell 15: 2192–2202.

7. WangX, ShiX, HaoB, GeS, LuoJ (2005) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165: 937–946.

8. PatersonAH, BowersJE, ChapmanBA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101: 9903–9908.

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

10. GautBS (2001) Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. Genome Res 11: 55–66.

11. AhnS, AndersonJA, SorrellsME, TanksleySD (1993) Homoeologous relationships of rice, wheat and maize chromosomes. Mol Gen Genet 241: 483–490.

12. OdlandW, BaumgartenA, PhillipsR (2006) Ancestral Rice Blocks Define Multiple Related Regions in the Maize Genome. Crop Science 46: S-41–S-48.

13. MooreG, DevosKM, WangZ, GaleMD (1995) Cereal genome evolution. Grasses, line up and form a circle. Curr Biol 5: 737–739.

14. SchnablePS, WareD, FultonRS, SteinJC, WeiF, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115.

15. SpringerNM, YingK, FuY, JiT, YehC-T, et al. (2009) Maize Inbreds Exhibit High Levels of Copy Number Variation (CNV) and Presence/Absence Variation (PAV) in Genome Content. PLoS Genet 5: e1000734.

16. DeBoltS (2010) Copy number variation shapes genome diversity in Arabidopsis over immediate family generational scales. Genome Biol Evol 2: 441–453.

17. CannonS, MitraA, BaumgartenA, YoungN, MayG (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology 4: 10.

18. HouY, LiuGE, BickhartDM, CardoneM, WangK, et al. (2011) Genomic characteristics of cattle copy number variations. BMC Genomics 12: 127.

19. HastingsPJ, LupskiJR, RosenbergSM, IraG (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10: 551–564.

20. ZhangF, GuW, HurlesME, LupskiJR (2009) Copy number variation in human health, disease, and evolution. Annu Rev Genomics Hum Genet 10: 451–481.

21. KrausE, LeungWY, HaberJE (2001) Break-induced replication: a review and an example in budding yeast. Proc Natl Acad Sci U S A 98: 8255–8262.

22. MorrowDM, ConnellyC, HieterP (1997) “Break Copy” Duplication: A Model for Chromosome Fragment Formation in Saccharomyces cerevisiae. Genetics 147: 371–382.

23. HastingsPJ, IraG, LupskiJR (2009) A Microhomology-Mediated Break-Induced Replication Model for the Origin of Human Copy Number Variation. PLoS Genet 5: e1000327.

24. LeeJA, CarvalhoCM, LupskiJR (2007) A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131: 1235–1247.

25. GrayYHM (2000) It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements. Trends in Genetics 16: 461–468.

26. GrayYH, TanakaMM, SvedJA (1996) P-element-induced recombination in Drosophila melanogaster: hybrid element insertion. Genetics 144: 1601–1610.

27. PrestonCR, SvedJA, EngelsWR (1996) Flanking duplications and deletions associated with P-induced male recombination in Drosophila. Genetics 144: 1623–1638.

28. WeilCF, WesslerSR (1993) Molecular evidence that chromosome breakage by Ds elements is caused by aberrant transposition. Plant Cell 5: 515–522.

29. YuC, ZhangJ, PulletikurtiV, WeberDF, PetersonT (2010) Spatial configuration of transposable element Ac termini affects their ability to induce chromosomal breakage in maize. Plant Cell 22: 744–754.

30. ZhangJ, PetersonT (1999) Genome rearrangements by nonlinear transposons in maize. Genetics 153: 1403–1410.

31. ZhangJ, PetersonT (2004) Transposition of reversed Ac element ends generates chromosome rearrangements in maize. Genetics 167: 1929–1937.

32. HuangJT, DoonerHK (2008) Macrotransposition and other complex chromosomal restructuring in maize by closely linked transposons in direct orientation. Plant Cell 20: 2019–2032.

33. XuanYH, PiaoHL, JeBI, ParkSJ, ParkSH, et al. (2011) Transposon Ac/Ds-induced chromosomal rearrangements at the rice OsRLG5 locus. Nucleic Acids Res 39: e149.

34. McClintockB (1948) Mutable loci in maize. Carnegie Inst Wash Year Book 47: 155–169.

35. McClintockB (1951) Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol 16: 13–47.

36. ZhangJ, YuC, PulletikurtiV, LambJ, DanilovaT, et al. (2009) Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize. Genes Dev 23: 755–765.

37. SinghM, LewisPE, HardemanK, BaiL, RoseJK, et al. (2003) Activator mutagenesis of the pink scutellum1/viviparous7 locus of maize. Plant Cell 15: 874–884.

38. RosF, KunzeR (2001) Regulation of activator/dissociation transposition by replication and DNA methylation. Genetics 157: 1723–1733.

39. Peterson T, Zhang J (2013) The Mechanism of Ac/Ds Transposition. In: Fedoroff NV, editor. Plant Transposons and Genome Dynamics in Evolution. Oxford, UK: Wiley-Blackwell. pp. 41–59.

40. LamK-WG, JeffreysAJ (2006) Processes of copy-number change in human DNA: The dynamics of α-globin gene deletion. Proceedings of the National Academy of Sciences 103: 8921–8927.

41. LamK-WG, JeffreysAJ (2007) Processes of de novo duplication of human α-globin genes. Proceedings of the National Academy of Sciences 104: 10950–10955.

42. TurnerDJ, MirettiM, RajanD, FieglerH, CarterNP, et al. (2008) Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nat Genet 40: 90–95.

43. MolinierJ, RiesG, BonhoefferS, HohnB (2004) Interchromatid and interhomolog recombination in Arabidopsis thaliana. Plant Cell 16: 342–352.

44. DuC, HoffmanA, HeL, CaronnaJ, DoonerHK (2011) The complete Ac/Ds transposon family of maize. BMC Genomics 12: 588.

45. MartinC, MackayS, CarpenterR (1988) Large-scale chromosomal restructuring is induced by the transposable element tam3 at the nivea locus of antirrhinum majus. Genetics 119: 171–184.

46. MartinC, ListerC (1989) Genome juggling by transposons: Tam3-induced rearrangements in Antirrhinum majus. Dev Genet 10: 438–451.

47. ListerC, JacksonD, MartinC (1993) Transposon-induced inversion in Antirrhinum modifies nivea gene expression to give a novel flower color pattern under the control of cycloidearadialis. Plant Cell 5: 1541–1553.

48. EmrichSJ, BarbazukWB, LiL, SchnablePS (2007) Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Res 17: 69–73.

49. PhillippyAM, SchatzMC, PopM (2008) Genome assembly forensics: finding the elusive mis-assembly. Genome Biol 9: R55.

50. PrithamEJ, PutliwalaT, FeschotteC (2007) Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene 390: 3–17.

51. FeschotteC, PrithamEJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41: 331–368.

52. YuC, ZhangJ, PetersonT (2011) Genome rearrangements in maize induced by alternative transposition of reversed Ac/Ds termini. Genetics 188: 59–67.

53. GoettelW, MessingJ (2010) Divergence of gene regulation through chromosomal rearrangements. BMC Genomics 11: 678.

54. PorebskiS, BaileyL, BaumB (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter 15: 8–15.

55. Sambrook J, Fritsch E, Maniatis T (1989) Molecular Cloning: A Laboratory Manual New York: Cold Spring Harbor Laboratory Press.

Štítky
Genetika Reprodukčná medicína

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PLOS Genetics


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