Skip to main content

Maize Transposable Element Dynamics

  • Chapter
  • First Online:

Part of the book series: Compendium of Plant Genomes ((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.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Baker B, Schell J, Lörz H, Fedoroff N (1986) Transposition of the maize controlling element “Activator” in tobacco. Proc Natl Acad Sci USA 83:4844–4848

    Article  CAS  Google Scholar 

  • Barghini E, Natali L, Giordani T et al (2015) LTR retrotransposon dynamics in the evolution of the olive (Olea europaea) genome. DNA Res 22:91–100

    Article  CAS  Google Scholar 

  • 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 19:243–254

    Article  CAS  Google Scholar 

  • 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:e1000732

    Article  Google Scholar 

  • Bennetzen JL (1985) The regulation of Mutator function and Mu1 transposition. UCLA Symp Mol Cell Biol 35:343–354

    CAS  Google Scholar 

  • 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 179–200

    Chapter  Google Scholar 

  • Bennetzen JL, Freeling M (1993) Grasses as a single genetic system: genome composition, collinearity and complementarity. Trends Genet 9:259–261

    Article  CAS  Google Scholar 

  • Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132

    Article  CAS  Google Scholar 

  • Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function and evolution of plant genomes. Ann Rev Plant Biol 65:505–530

    Article  CAS  Google Scholar 

  • Bennetzen JL, Wang X (2018) Relationships between gene structure and genome instability in flowering plants. Mol Plant. https://doi.org/10.1016/jmolp.2018.02.003

    Article  PubMed  Google Scholar 

  • 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 40:359–369

    Article  CAS  Google Scholar 

  • Christin PA, Edwards EJ, Besnard G et al (2012) Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Curr Biol 22:445–449

    Article  CAS  Google Scholar 

  • 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 9:3349–3462

    Article  Google Scholar 

  • Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  CAS  Google Scholar 

  • Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:637–646

    Article  CAS  Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601

    Article  CAS  Google Scholar 

  • Diao X, Freeling M, Lisch D (2005) Horizontal transfer of a plant transposon. PLoS Biol 4:e5

    Article  Google Scholar 

  • Eichten SR, Ellis NA, Makarevitch I et al (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8:e1003127

    Article  CAS  Google Scholar 

  • El Baidouri M, Carpentier MC, Cooke R et al (2014) Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24:831–838

    Article  Google Scholar 

  • El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 5:954–965

    Article  Google Scholar 

  • Estep MC, DeBarry JD, Bennetzen JL (2013) The dynamics of LTR retrotransposon accumulation across 25 million years of panicoid grass evolution. Heredity 110:194–204

    Article  CAS  Google Scholar 

  • Gai XW, Voytas DF (1998) A single amino acid change in the yeast retrotransposon Ty5 abolishes targeting to silent chromatin. Mol Cell 1:1051–1055

    Article  CAS  Google Scholar 

  • Gilbert W (1978) Why genes in pieces? Nature 271:501

    Article  CAS  Google Scholar 

  • Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380

    Article  CAS  Google Scholar 

  • 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 volume

    Google Scholar 

  • Hirochika H, Sugimoto K, Otsuki Y et al (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93:7783–7788

    Article  CAS  Google Scholar 

  • Jiang N, Bao Z, Zhang X et al (2004a) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573

    Article  CAS  Google Scholar 

  • Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004b) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573

    Article  CAS  Google Scholar 

  • 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 208:596–607

    Article  CAS  Google Scholar 

  • 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 18:210

    Article  Google Scholar 

  • Lisch D, Bennetzen JL (2011) Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol 14:156–161

    Article  CAS  Google Scholar 

  • 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 139:1777–1796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lucas H, Feuerbach F, Kunert K et al (1995) RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana. EMBO J 14:2364–2373

    Article  CAS  Google Scholar 

  • Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869

    Article  CAS  Google Scholar 

  • 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 114:1726–1731

    Article  CAS  Google Scholar 

  • Martienssen RA (2010) Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytol 186:46–53

    Article  CAS  Google Scholar 

  • Masson P, Fedoroff N (1989) Mobility of the maize suppressor-mutator element in transgenic tobacco cells. Proc Natl Acad Sci USA 86:2219–2223

    Article  CAS  Google Scholar 

  • Matzke AJM, Matzke MA (1998) Position effects and epigenetic silencing of plant transgenes. Curr Opin Plant Biol 1:142–148

    Article  CAS  Google Scholar 

  • 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:e94101

    Article  Google Scholar 

  • McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harb Symp 16:13–47

    Article  CAS  Google Scholar 

  • McClintock B (1953) Induction of instability at selected loci in maize. Genetics 38:579–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  CAS  Google Scholar 

  • 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 37:997–1002

    Article  CAS  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T et al (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    Article  CAS  Google Scholar 

  • Nystedt B, Street NR, Wetterbom A et al (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584

    Google Scholar 

  • Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604

    Article  CAS  Google Scholar 

  • 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 186:37–45

    Article  CAS  Google Scholar 

  • Peschke VM, Phillips R, Gengenbach BG (1987) Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238:804–807

    Article  CAS  Google Scholar 

  • Peterson PA (1991) The transposable element-En-four decades after Bikini. Genetica 84:63–72

    Article  CAS  Google Scholar 

  • Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56:1–14

    Article  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin Y-K et al (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

    Article  CAS  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A et al (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  CAS  Google Scholar 

  • Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546

    Article  Google Scholar 

  • Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity and dynamics. Science 326:1112–1115

    Article  CAS  Google Scholar 

  • Sharma A, Schneider KL, Presting GG (2008) Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations. Proc Natl Acad Sci USA 105:15470–15474

    Article  CAS  Google Scholar 

  • Slotkin RK, Freeling M, Lisch D (2005) Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37:641–644

    Article  CAS  Google Scholar 

  • 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 96:7409–7414

    Article  CAS  Google Scholar 

  • Vicient CM (2010) Transcriptional activity of transposable elements in maize. BMC Genom 11:601

    Article  Google Scholar 

  • Vicient CM, Casacuberta JM (2017) Impact of transposable elements on polyploid plant genomes. Ann Bot 120:195–207

    Article  Google Scholar 

  • Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643

    Article  CAS  Google Scholar 

  • Walbot V, Chandler C, Taylor L (1985) Alterations in the Mutator transposable element family of Zea mays. UCLA Symp Mol Cell Biol 35:333–342

    CAS  Google Scholar 

  • Wang Q, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci USA 103:17644–17649

    Article  CAS  Google Scholar 

  • 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 17:1072–1081

    Article  CAS  Google Scholar 

  • Yang L, Bennetzen JL (2009) Distribution, diversity, evolution, and survival of Helitrons in the maize genome. Proc Natl Acad Sci USA 106:19922–19927

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey L. Bennetzen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bennetzen, J.L. (2018). Maize Transposable Element Dynamics. In: Bennetzen, J., Flint-Garcia, S., Hirsch, C., Tuberosa, R. (eds) The Maize Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-97427-9_4

Download citation

Publish with us

Policies and ethics