The maize genome comprises 150,000–250,000 long terminal repeat (LTR)-retrotransposons, mostly in nested clusters, intermingled with other transpos-able elements and, more rarely, genes. All told, the genomic landscape of maize is 50–80% retrotransposons. Myriad families exist but >80% of maize retrotransposons belong to the five largest: Opie-Ji, Cinful-Zeon, Huck, Prem1 and Grande. Closely related to animal retroviruses, retrotransposons utilize an RNA intermediate to initiate their transposition. Despite extensive proliferation they are nevertheless suppressed by a variety of mechanisms, including DNA methylation, conversion to heterochromatin and various types of recombinational deletion. Retrotransposons play a large role in the size, structure, gene function and haplotype variation of the maize genome.
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References
Ananiev, E. V., R. L. Phillips and H. W. Rines (1998a) Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA 95: 13073–13078.
Ananiev, E. V., R. L. Phillips and H. W. Rines (1998b) Complex structure of knob DNA on maize chromosome 9: Retrotransposon invasion into heterochromatin. Genetics 149: 2025–2037.
Arumuganathan, K. and E. Earle (1991) Nuclear DNA content of some important plant species.Plant Molecular Biology Reporter 9: 208–218.
Asami, Y., D. W. Jia, K. Tatebayashi, K. Yamagata, M. Tanokura and H. Ikeda (2002) Effect of the DNA topoisomerase II inhibitor VP-16 on illegitimate recombination in yeast chromosomes. Gene 291: 251–257.
Avramova, Z., P. SanMiguel, E. Georgieva and J. L. Bennetzen (1995) Matrix Attachment Regions and Transcribed Sequences within a Long Chromosomal Continuum Containing Maize Adh1.Plant Cell 7: 1667–1680.
Bender, J. (2004) DNA methylation and epigenetics. Annu Rev Plant Biol 55: 41–68.
Bennetzen, J. L., K. Schrick, P. S. Springer, W. E. Brown and P. SanMiguel (1994) Active Maize Genes Are Unmodified and Flanked by Diverse Classes of Modified, Highly Repetitive DNA.Genome 37: 565–576.
Brunner, S., K. Fengler, M. Morgante, S. Tingey and A. Rafalski (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17: 343–360.
Bureau, T. E., S. E. White and S. R. Wessler (1994) Transduction of a Cellular Gene by a Plant Retroelement. Cell 77: 479–480.
Coulondre, C., J. H. Miller, P. J. Farabaugh and W. Gilbert (1978) Molecular-Basis of Base Substitution Hotspots in Escherichia-Coli. Nature 274: 775–780.
Devos, K. M., J. K. M. Brown and J. L. Bennetzen (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12: 1075–1079.
Du, C. G., Z. Swigonova and J. Messing (2006) Retrotranspositions in orthologous regions of closely related grass species. BMC Evol Biol 6: 62.
Eichinger, D. J. and J. D. Boeke (1990) A Specific Terminal Structure Is Required for Ty1 Transposition. Gene Dev 4: 324–330.
Elrouby, N. and T. E. Bureau (2001) A novel hybrid open reading frame formed by multiple cellular gene transductions by a plant long terminal repeat retroelement. J Biol Chem 276: 41963–41968.
Emberton, J., J. X. Ma, Y. N. Yuan, P. SanMiguel and J. L. Bennetzen (2005) Gene enrichment in maize with hypomethylated partial restriction (HMPR) libraries. Genome Res 15:1441–1446.
Eyre-Walker, A., R. L. Gaut, H. Hilton, D. L. Feldman and B. S. Gaut (1998) Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci USA 95: 4441–4446.
Feng, Y.-X., S. P. Moore, D. J. Garfinkel and A. Rein (2000) The Genomic RNA in Ty1 Virus-Like Particles Is Dimeric. J Virol 74: 10819–10821.
Fu, H. H. and H. K. Dooner (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99: 9573–9578.
Fu, H. H., W. K. Park, X. H. Yan, Z. W. Zheng, B. Z. Shen and H. K. Dooner (2001) The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome. Proc Natl Acad Sci USA 98: 8903–8908.
Fu, H. H., Z. W. Zheng and H. K. Dooner (2002) Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc Natl Acad Sci USA 99: 1082–1087.
Garcia-Martinez, J. and J. A. Martinez-Izquierdo (2003) Study on the evolution of the Grande retrotransposon in the Zea genus. Mol Biol Evol 20: 831–841.
Garfinkel, D. J. (2005) Genome evolution mediated by Ty elements in Saccharomyces. Cytogenet Genome Res 110: 63–69.
Gaut, B. S., B. R. Morton, B. C. McCaig and M. T. Clegg (1996) Substitution rate comparisons between grasses and palms: Synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93: 10274–10279.
Haberer, G., S. Young, A. K. Bharti, H. Gundlach, C. Raymond, G. Fuks, E. Butler, R. A. Wing, S. Rounsley, B. Birren, C. Nusbaum, K. F. X. Mayer and J. Messing (2005) Structure and architecture of the maize genome. Plant Physiol 139: 1612–1624.
Hamilton, A., O. Voinnet, L. Chappell and D. Baulcombe (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21: 4671–4679.
Hu, W. M., O. P. Das and J. Messing (1995) Zeon-1, a Member of a New Maize Retrotransposon Family. Molecular & General Genetics 248: 471–480.
Huettel, B., T. Kanno, L. Daxinger, E. Bucher, J. van der Winden, A. J. M. Matzke and M. Matzke (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: A versatile pathway for transcriptional gene silencing in plants. Biochimica Et Biophysica Acta-Gene Structure and Expression 1769: 358–374.
Ilic, K., P. J. SanMiguel and J. L. Bennetzen (2003) A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes. Proc Natl Acad Sci USA 100: 12265–12270.
Jin, Y. K. and J. L. Bennetzen (1989) Structure and Coding Properties of Bs1, a Maize Retrovirus-Like Transposon. Proc Natl Acad Sci USA 86: 6235–6239.
Jin, Y. K. and J. L. Bennetzen (1994) Integration and Nonrandom Mutation of a Plasma-Membrane Proton Atpase Gene Fragment within the Bs1 Retroelement of Maize. Plant Cell 6: 1177–1186.
Kashkush, K., M. Feldman and A. A. Levy (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33: 102–106.
Kim, A., C. Terzian, P. Santamaria, A. Pelisson, N. Prudhomme and A. Bucheton (1994) Retroviruses in Invertebrates - the Gypsy Retrotransposon Is Apparently an Infectious Retrovirus of Drosophila-Melanogaster. Proc Natl Acad Sci USA 91: 1285–1289.
Kumar, A. and J. L. Bennetzen (1999) Plant retrotransposons. Annu Rev Genet 33: 479–532.
Lamb, J. C., J. M. Meyer, B. Corcoran, A. Kato, F. P. Han and J. A. Birchler (2007) Distinct chromosomal distributions of highly repetitive sequences in maize. Chromosome Research 15: 33–49.
Langham, R. J., J. Walsh, M. Dunn, C. Ko, S. A. Goff and M. Freeling (2004) Genomic duplication, fractionation and the origin of regulatory novelty. Genetics 166: 935–945.
Laten, H. M., A. Majumdar and E. A. Gaucher (1998) SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc Natl Acad Sci USA 95: 6897–6902.
Lim, J. K. and M. J. Simmons (1994) Gross Chromosome Rearrangements Mediated by Transposable Elements in Drosophila-Melanogaster. Bioessays 16: 269–275.
Lippman, Z., A. V. Gendrel, M. Black, M. W. Vaughn, N. Dedhia, W. R. McCombie, K. Lavine, V. Mittal, B. May, K. D. Kasschau, J. C. Carrington, R. W. Doerge, V. Colot and R. Martienssen (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471–476.
Liu, R., C. Vitte, J. Ma, A. A. Mahama, T. Dhliwayo, M. Lee and J. L. Bennetzen (2007) A GeneTrek analysis of the maize genome. Proc Natl Acad Sci USA 104: 11844–11849.
Ma, J. X. and J. L. Bennetzen (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101: 12404–12410.
Ma, J. X., K. M. Devos and J. L. Bennetzen (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14: 860–869.
Ma, J. X., P. SanMiguel, J. S. Lai, J. Messing and J. L. Bennetzen (2005) DNA rearrangement in orthologous Orp regions of the maize, rice and sorghum genomes. Genetics 170: 1209–1220.
Marillonnet, S. and S. R. Wessler (1997) Retrotransposon insertion into the maize waxy gene results in tissue-specific RNA processing. Plant Cell 9: 967–978.
Martienssen, R. (1998) Transposons, DNA methylation and gene control. Trends Genet 14: 263–264.
Matsuoka, Y., Y. Vigouroux, M. M. Goodman, G. J. Sanchez, E. Buckler and J. Doebley (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99: 6080–6084.
Matzke, M., T. Kanno, B. Huettel, L. Daxinger and A. J. M. Matzke (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10: 512–519.
McClintock, B., Y. T. A. Kato and A. Blumenshein (1981) In: Chromosome Constitution of Races of Maize. Colegio do Postgraduados, Chapingo, Mexico.
Messing, J., A. K. Bharti, W. M. Karlowski, H. Gundlach, H. R. Kim, Y. Yu, F. S. Wei, G. Fuks, C. A. Soderlund, K. F. X. Mayer and R. A. Wing (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101: 14349–14354.
Meyers, B. C., S. V. Tingley and M. Morgante (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11: 1660–1676.
Mieczkowski, P. A., F. J. Lemoine and T. D. Petes (2006) Recombination between retrotrans-posons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 5: 1010–1020.
Miller, J. T., F. G. Dong, S. A. Jackson, J. Song and J. M. Jiang (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150: 1615–1623.
Miller, W., J. McDonald and W. Pinsker (1997) Molecular domestication of mobile elements. Genetica 100: 261–270.
Monfort, A., C. M. Vicient, R. Raz, P. Puigdomenech and J. A. Martinez-Izquierdo (1995) Molecular Analysis of a Putative Transposable Retroelement from the Zea Genus with Internal Clusters of Tandem Repeats. DNA Res 2: 255–261.
Morgante, M., S. Brunner, G. Pea, K. Fengler, A. Zuccolo and A. Rafalski (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37: 997–1002.
Mroczek, R. J. and R. K. Dawe (2003) Distribution of retroelements in centromeres and neocen-tromeres of maize. Genetics 165: 809–819.
Palmer, L. E., P. D. Rabinowicz, A. L. O'Shaughnessy, V. S. Balija, L. U. Nascimento, S. Dike, M. De la Bastide, R. A. Martienssen and W. R. McCombie (2003) Maize genome sequencing by methylation filtration. Science 302: 2115–2117.
Palmgren, M. G. (1994) Capturing of Host DNA by a Plant Retroelement — Bs1 Encodes Plasma-Membrane H+ -Atpase Domains. Plant Mol Biol 25: 137–140.
Petrov, D. A., T. A. Sangster, J. S. Johnston, D. L. Hartl and K. L. Shaw (2000) Evidence for DNA loss as a determinant of genome size. Science 287: 1060–1062.
Presting, G. G., L. Malysheva, J. Fuchs and I. Z. Schubert (1998) A TY3/GYPSY retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J 16: 721–728.
Quayle, T. J. A., J. W. S. Brown and G. Feix (1989) Analysis of Distal Flanking Regions of Maize 19-Kda Zein Genes. Gene 80: 249–257.
Ramakrishna, W., J. Emberton, M. Ogden, P. SanMiguel and J. L. Bennetzen (2002a) Structural analysis of the maize Rp1 complex reveals numerous sites and unexpected mechanisms of local rearrangement. Plant Cell 14: 3213–3223.
Ramakrishna, W., J. Emberton, P. SanMiguel, M. Ogden, V. Llaca, J. Messing and J. L. Bennetzen (2002b) Comparative sequence analysis of the sorghum Rph region and the maize Rp1 resistance gene complex. Plant Physiol 130: 1728–1738.
Rayburn, A. L., H. J. Price, J. D. Smith and J. R. Gold (1985) C-Band Heterochromatin and DNA Content in Zea mays. Am J Bot 72: 1610–1617.
Roeder, G. S. and G. R. Fink (1980) DNA Rearrangements Associated with a Transposable Element in Yeast. Cell 21: 239–249.
SanMiguel, P. and J. L. Bennetzen (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82: 37–44.
SanMiguel, P., B. S. Gaut, A. Tikhonov, Y. Nakajima and J. L. Bennetzen (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20: 43–45.
SanMiguel, P., A. Tikhonov, Y. K. Jin, N. Motchoulskaia, D. Zakharov, A. MelakeBerhan, P. S. Springer, K. J. Edwards, M. Lee, Z. Avramova and J. L. Bennetzen (1996) Nested retrotrans-posons in the intergenic regions of the maize genome. Science 274: 765–768.
Sanz-Alferez, S., P. SanMiguel, Y. K. Jin, P. S. Springer and J. L. Bennetzen (2003) Structure and evolution of the Cinful retrotransposon family of maize. Genome 46: 745–752.
Song, R. T., V. Llaca, E. Linton and J. Messing (2001) Sequence, regulation, and evolution of the maize 22-kD alpha zein in gene family. Genome Res 11: 1817–1825.
Song, R. T. and J. Messing (2003) Gene expression of a gene family in maize based on noncol-linear haplotypes. Proc Natl Acad Sci USA 100: 9055–9060.
Song, S. U., T. Gerasimova, M. Kurkulos, J. D. Boeke and V. G. Corces (1994) An Env-Like Protein Encoded by a Drosophila Retroelement — Evidence That Gypsy Is an Infectious Retrovirus. Genes Dev 8: 2046–2057.
Springer, P. S., K. J. Edwards and J. L. Bennetzen (1994) DNA Class Organization on Maize Adh1 Yeast Artificial Chromosomes. Proc Natl Acad Sci USA 91: 863–867.
Swigonova, Z., J. L. Bennetzen and J. Messing (2005) Structure and evolution of the r/b chromosomal regions in rice, maize and sorghum. Genetics 169: 891–906.
Swigonova, Z., J. S. Lai, J. X. Ma, W. Ramakrishna, M. Llaca, J. L. Bennetzen and J. Messing (2004) On the tetraploid origin of the maize genome. Comp Funct Genomics 5: 281–284.
Tikhonov, A. P., P. J. SanMiguel, Y. Nakajima, N. M. Gorenstein, J. L. Bennetzen and Z. Avramova (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96: 7409–7414.
Turcich, M. P., A. Bokhari-Riza, D. A. Hamilton, C. P. He, W. Messier, C. B. Stewart and J. P. Mascarenhas (1996) PREM-2, a copia-type retroelement in maize is expressed preferentially in early microspores. Sexual Plant Reproduction 9: 65–74.
Turcich, M. P. and J. P. Mascarenhas (1994) PREM-1, a Putative Maize Retroelement Has LTR (Long Terminal Repeat) Sequences That Are Preferentially Transcribed in Pollen. Sexual Plant Reproduction 7: 2–11.
Vitte, C. and J. L. Bennetzen (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103: 17638–17643.
Vitte, C. and O. Panaud (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol Biol Evol 20: 528–540.
Vitte, C., O. Panaud and H. Quesneville (2007) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8: 218.
Wang, Q. H. and H. K. Dooner (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci USA 103: 17644–17649.
Wang, R. L., A. Stec, J. Hey, L. Lukens and J. Doebley (1999) The limits of selection during maize domestication. Nature 398: 236–239.
Wessler, S. R., T. E. Bureau and S. E. White (1995) LTR-Retrotransposons and Mites — Important Players in the Evolution of Plant Genomes. Curr Opin Genet Dev 5: 814–821.
White, S. E., L. F. Habera and S. R. Wessler (1994) Retrotransposons in the Flanking Regions of Normal Plant Genes — a Role for Copia-Like Elements in the Evolution of Gene Structure and Expression. Proc Natl Acad Sci USA 91: 11792–11796.
Whitelaw, C. A., W. B. Barbazuk, G. Pertea, A. P. Chan, F. Cheung, Y. Lee, L. Zheng, S. van Heeringen, S. Karamycheva, J. L. Bennetzen, P. SanMiguel, N. Lakey, J. Bedell, Y. Yuan, M. A. Budiman, A. Resnick, S. Van Aken, T. Utterback, S. Riedmuller, M. Williams, T. Feldblyum, K. Schubert, R. Beachy, C. M. Fraser and J. Quackenbush (2003) Enrichment of gene-coding sequences in maize by genome filtration. Science 302: 2118–2120.
Wicker, T., F. Sabot, A. Hua-Van, J. L. Bennetzen, P. Capy, B. Chalhoub, A. Flavell, P. Leroy, M. Morgante, O. Panaud, E. Paux, P. SanMiguel and A. H. Schulman (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973–982.
Wicker, T., N. Yahiaoui, R. Guyot, E. Schlagenhauf, Z. D. Liu, J. Dubcovsky and B. Keller (2003)Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and A(m) genomes of wheat. Plant Cell 15: 1186–1197.
Wright, D. A. and D. F. Voytas (1998) Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins.Genetics 149: 703–715.
Wright, D. A. and D. F. Voytas (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12: 122–131.
Xiong, Y. and T. H. Eickbush (1990) Origin and Evolution of Retroelements Based Upon Their Reverse-Transcriptase Sequences. EMBO J 9: 3353–3362.
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SanMiguel, P., Vitte, C. (2009). The LTR-Retrotransposons of Maize. In: Bennetzen, J.L., Hake, S. (eds) Handbook of Maize. Springer, New York, NY. https://doi.org/10.1007/978-0-387-77863-1_15
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