Advertisement

Maize Transposable Element Dynamics

  • Jeffrey L. BennetzenEmail author
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Transposable elements (TEs) are among the most important factors in the evolution of gene and genome structure/function in plants. All plant genomes contain mostly quiescent TEs that are activated, independently by family, in currently unpredictable timeframes by largely unknown phenomena. Different reawakened or horizontally transferred TE families can remain active for as little as a few years to as much as a few million years, and the reasons for these duration-of-activity differences are also not known. The maize lineage has seen extraordinary TE activity, and changes in TE activity, over the last few million years, and much of this dynamic continues to be ongoing. Hence, studies of TE biology have been particularly informative in maize, and will continue to be so. This review describes the history of TE activity over the last few million years in the maize lineage, briefly mentions the extensive literature regarding maize TE regulation, and suggests approaches for characterizing the processes that determine which TEs are active: where, when, how and why.

Notes

Acknowledgements

The author thanks Aye Htun for her assistance with figures. The writing of this manuscript was supported by the Giles Professorship Endowment at the University of Georgia.

References

  1. Baker B, Schell J, Lörz H, Fedoroff N (1986) Transposition of the maize controlling element “Activator” in tobacco. Proc Natl Acad Sci USA 83:4844–4848CrossRefGoogle Scholar
  2. Barghini E, Natali L, Giordani T et al (2015) LTR retrotransposon dynamics in the evolution of the olive (Olea europaea) genome. DNA Res 22:91–100CrossRefGoogle Scholar
  3. Baucom RS, Estill JC, Leebens-Mack J, Bennetzen JL (2009a) Natural selection on gene function drives the evolution of LTR retrotransposon families in the rice genome. Genome Res 19:243–254CrossRefGoogle Scholar
  4. Baucom RS, Estill JC, Upshaw N et al (2009b) Exceptional diversity, non-random distribution and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5:e1000732CrossRefGoogle Scholar
  5. Bennetzen JL (1985) The regulation of Mutator function and Mu1 transposition. UCLA Symp Mol Cell Biol 35:343–354Google Scholar
  6. Bennetzen JL (2009) Maize genome structure and evolution. In: Bennetzen JL, Hake S (eds) The maize handbook—volume II: genetics and genomics. Springer, New York, pp 179–200CrossRefGoogle Scholar
  7. Bennetzen JL, Freeling M (1993) Grasses as a single genetic system: genome composition, collinearity and complementarity. Trends Genet 9:259–261CrossRefGoogle Scholar
  8. Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132CrossRefGoogle Scholar
  9. Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function and evolution of plant genomes. Ann Rev Plant Biol 65:505–530CrossRefGoogle Scholar
  10. Bennetzen JL, Wang X (2018) Relationships between gene structure and genome instability in flowering plants. Mol Plant.  https://doi.org/10.1016/jmolp.2018.02.003CrossRefPubMedGoogle Scholar
  11. Bohr VA, Smith CA, Okumoto DS, Hanawalt PC (1985) DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40:359–369CrossRefGoogle Scholar
  12. Christin PA, Edwards EJ, Besnard G et al (2012) Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Curr Biol 22:445–449CrossRefGoogle Scholar
  13. Cossu RM, Casola C, Giacomello S et al (2017) LTR retrotransposons show low levels of unequal recombination and high rates of intraelement gene conversion in large plant genomes. Genome Biol Evol 9:3349–3462CrossRefGoogle Scholar
  14. Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079CrossRefGoogle Scholar
  15. Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:637–646CrossRefGoogle Scholar
  16. Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601CrossRefGoogle Scholar
  17. Diao X, Freeling M, Lisch D (2005) Horizontal transfer of a plant transposon. PLoS Biol 4:e5CrossRefGoogle Scholar
  18. Eichten SR, Ellis NA, Makarevitch I et al (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8:e1003127CrossRefGoogle Scholar
  19. El Baidouri M, Carpentier MC, Cooke R et al (2014) Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24:831–838CrossRefGoogle Scholar
  20. El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 5:954–965CrossRefGoogle Scholar
  21. Estep MC, DeBarry JD, Bennetzen JL (2013) The dynamics of LTR retrotransposon accumulation across 25 million years of panicoid grass evolution. Heredity 110:194–204CrossRefGoogle Scholar
  22. Gai XW, Voytas DF (1998) A single amino acid change in the yeast retrotransposon Ty5 abolishes targeting to silent chromatin. Mol Cell 1:1051–1055CrossRefGoogle Scholar
  23. Gilbert W (1978) Why genes in pieces? Nature 271:501CrossRefGoogle Scholar
  24. Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380CrossRefGoogle Scholar
  25. Hammond R, Teng C, Meyers BC (2018) Maize small RNAs as seeds of change and stability in gene expression and genome stability. In: The maize genome. Springer, this volumeGoogle Scholar
  26. Hirochika H, Sugimoto K, Otsuki Y et al (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93:7783–7788CrossRefGoogle Scholar
  27. Jiang N, Bao Z, Zhang X et al (2004a) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573CrossRefGoogle Scholar
  28. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004b) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573CrossRefGoogle Scholar
  29. Kelly LJ, Renny-Byfield S, Pellicer J et al (2015) Analysis of the giant genomes of Fritillaria (Lilliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytol 208:596–607CrossRefGoogle Scholar
  30. Kim S, Park J, Yeom SI et al (2017) New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biol 18:210CrossRefGoogle Scholar
  31. Lisch D, Bennetzen JL (2011) Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol 14:156–161CrossRefGoogle Scholar
  32. Lisch D, Chomet P, Freeling M (1995) Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics 139:1777–1796PubMedPubMedCentralGoogle Scholar
  33. Lucas H, Feuerbach F, Kunert K et al (1995) RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana. EMBO J 14:2364–2373CrossRefGoogle Scholar
  34. Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869CrossRefGoogle Scholar
  35. Mahelka V, Krak K, Kopecký D et al (2017) Multiple horizontal transfers of nuclear ribosomal genes between phylogenetically distinct grass lineages. Proc Natl Acad Sci USA 114:1726–1731CrossRefGoogle Scholar
  36. Martienssen RA (2010) Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytol 186:46–53CrossRefGoogle Scholar
  37. Masson P, Fedoroff N (1989) Mobility of the maize suppressor-mutator element in transgenic tobacco cells. Proc Natl Acad Sci USA 86:2219–2223CrossRefGoogle Scholar
  38. Matzke AJM, Matzke MA (1998) Position effects and epigenetic silencing of plant transgenes. Curr Opin Plant Biol 1:142–148CrossRefGoogle Scholar
  39. Maumus F, Quesneville H (2014) Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLoS One 9:e94101CrossRefGoogle Scholar
  40. McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harb Symp 16:13–47CrossRefGoogle Scholar
  41. McClintock B (1953) Induction of instability at selected loci in maize. Genetics 38:579–599PubMedPubMedCentralGoogle Scholar
  42. McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801CrossRefGoogle Scholar
  43. Morgante M, Brunner S, Pea G et al (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002CrossRefGoogle Scholar
  44. Naito K, Zhang F, Tsukiyama T et al (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134CrossRefGoogle Scholar
  45. Nystedt B, Street NR, Wetterbom A et al (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584CrossRefGoogle Scholar
  46. Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604CrossRefGoogle Scholar
  47. Parisod C, Alix K, Just J, Petit M, Sarilar V (2010) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186:37–45CrossRefGoogle Scholar
  48. Peschke VM, Phillips R, Gengenbach BG (1987) Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238:804–807CrossRefGoogle Scholar
  49. Peterson PA (1991) The transposable element-En-four decades after Bikini. Genetica 84:63–72CrossRefGoogle Scholar
  50. Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56:1–14CrossRefGoogle Scholar
  51. SanMiguel P, Tikhonov A, Jin Y-K et al (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768CrossRefGoogle Scholar
  52. SanMiguel P, Gaut BS, Tikhonov A et al (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45CrossRefGoogle Scholar
  53. Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546CrossRefGoogle Scholar
  54. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity and dynamics. Science 326:1112–1115CrossRefGoogle Scholar
  55. Sharma A, Schneider KL, Presting GG (2008) Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations. Proc Natl Acad Sci USA 105:15470–15474CrossRefGoogle Scholar
  56. Slotkin RK, Freeling M, Lisch D (2005) Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37:641–644CrossRefGoogle Scholar
  57. Tikhonov AP, SanMiguel PJ, Nakajima Y et al (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96:7409–7414CrossRefGoogle Scholar
  58. Vicient CM (2010) Transcriptional activity of transposable elements in maize. BMC Genom 11:601CrossRefGoogle Scholar
  59. Vicient CM, Casacuberta JM (2017) Impact of transposable elements on polyploid plant genomes. Ann Bot 120:195–207CrossRefGoogle Scholar
  60. Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643CrossRefGoogle Scholar
  61. Walbot V, Chandler C, Taylor L (1985) Alterations in the Mutator transposable element family of Zea mays. UCLA Symp Mol Cell Biol 35:333–342Google Scholar
  62. Wang Q, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci USA 103:17644–17649CrossRefGoogle Scholar
  63. Wicker T, Keller B (2007) Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res 17:1072–1081CrossRefGoogle Scholar
  64. Yang L, Bennetzen JL (2009) Distribution, diversity, evolution, and survival of Helitrons in the maize genome. Proc Natl Acad Sci USA 106:19922–19927CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of GeneticsUniversity of GeorgiaAthensUSA

Personalised recommendations