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Proc Natl Acad Sci U S A. 1994 Dec 6; 91(25): 11792–11796.

Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression.


The wx-K mutation results from the insertion of a copia-like retrotransposon into exon 12 of the maize waxy gene. This retrotransposon, named Hopscotch, has one long open reading frame encoding all of the domains required for transposition. Computer-assisted database searches using Hopscotch and other plant copia-like retroelements as query sequences have revealed that ancient, degenerate retrotransposon insertions are found in close proximity to 21 previously sequenced plant genes. The data suggest that these elements may be involved in gene duplication and the regulation of gene expression. Similar searches using the Drosophila retrotransposon copia did not reveal any retrotransposon-like sequences in the flanking regions of animal genes. These results, together with the recent finding that reverse-transcriptase sequences characteristic of copia-like elements are ubiquitous and diverse in plants, suggest that copia-like retrotransposons are an ancient component of plant genomes.

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  • Hull R, Will H. Molecular biology of viral and nonviral retroelements. Trends Genet. 1989 Nov;5(11):357–359. [PubMed]
  • Boeke JD, Corces VG. Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol. 1989;43:403–434. [PubMed]
  • Flavell AJ, Smith DB. A Ty1-copia group retrotransposon sequence in a vertebrate. Mol Gen Genet. 1992 May;233(1-2):322–326. [PubMed]
  • Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A. Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res. 1992 Jul 25;20(14):3639–3644. [PMC free article] [PubMed]
  • Voytas DF, Cummings MP, Koniczny A, Ausubel FM, Rodermel SR. copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7124–7128. [PMC free article] [PubMed]
  • Hirochika H, Hirochika R. Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Jpn J Genet. 1993 Feb;68(1):35–46. [PubMed]
  • Flavell AJ, Smith DB, Kumar A. Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet. 1992 Jan;231(2):233–242. [PubMed]
  • Johns MA, Mottinger J, Freeling M. A low copy number, copia-like transposon in maize. EMBO J. 1985 May;4(5):1093–1101. [PMC free article] [PubMed]
  • Grandbastien MA, Spielmann A, Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989 Jan 26;337(6205):376–380. [PubMed]
  • Varagona MJ, Purugganan M, Wessler SR. Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell. 1992 Jul;4(7):811–820. [PMC free article] [PubMed]
  • Wessler SR, Varagona MJ. Molecular basis of mutations at the waxy locus of maize: correlation with the fine structure genetic map. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4177–4181. [PMC free article] [PubMed]
  • Voytas DF, Ausubel FM. A copia-like transposable element family in Arabidopsis thaliana. Nature. 1988 Nov 17;336(6196):242–244. [PubMed]
  • Lee DL, Ellis TH, Turner L, Hellens RP, Cleary WG. A copia-like element in Pisum demonstrates the uses of dispersed repeated sequences in genetic analysis. Plant Mol Biol. 1990 Nov;15(5):707–722. [PubMed]
  • Camirand A, Brisson N. The complete nucleotide sequence of the Tst1 retrotransposon of potato. Nucleic Acids Res. 1990 Aug 25;18(16):4929–4929. [PMC free article] [PubMed]
  • Emori Y, Shiba T, Kanaya S, Inouye S, Yuki S, Saigo K. The nucleotide sequences of copia and copia-related RNA in Drosophila virus-like particles. Nature. 315(6022):773–776. [PubMed]
  • Manninen I, Schulman AH. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol Biol. 1993 Aug;22(5):829–846. [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Rutledge RG, Quellet T, Hattori J, Miki BL. Molecular characterization and genetic origin of the Brassica napus acetohydroxyacid synthase multigene family. Mol Gen Genet. 1991 Sep;229(1):31–40. [PubMed]
  • Galau GA, Wang HY, Hughes DW. Sequence of the Gossypium hirsutum D-Genome Alloallele of Legumin A and Its mRNA. Plant Physiol. 1991 Nov;97(3):1268–1270. [PMC free article] [PubMed]
  • Galau GA, Wang HY, Hughes DW. Cotton Lea4 (D19) and LeaA2 (D132) Group 1 Lea Genes Encoding Water Stress-Related Proteins Containing a 20-Amino Acid Motif. Plant Physiol. 1992 Jun;99(2):783–788. [PMC free article] [PubMed]
  • Galau GA, Wang HY, Hughes DW. Cotton Mat5-A (C164) Gene and Mat5-D cDNAs Encoding Methionine-Rich 2S Albumin Storage Proteins. Plant Physiol. 1992 Jun;99(2):779–782. [PMC free article] [PubMed]
  • Huang PL, Parks JE, Rottmann WH, Theologis A. Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucurbita pepo) are clustered and similar but differentially regulated. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7021–7025. [PMC free article] [PubMed]
  • Akada S, Kung SD, Dube SK. The nucleotide sequence of gene 1 of the soybean chalcone synthase multigene family. Plant Mol Biol. 1991 Apr;16(4):751–752. [PubMed]
  • Franssen HJ, Thompson DV, Idler K, Kormelink R, van Kammen A, Bisseling T. Nucleotide sequence of two soybean ENOD2 early nodulin genes encoding Ngm-75. Plant Mol Biol. 1990 Jan;14(1):103–106. [PubMed]
  • Quigley F, Martin WF, Cerff R. Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2672–2676. [PMC free article] [PubMed]
  • Anthony JL, Haar RA, Hall TC. Nucleotide Sequence of a Genomic Clone Encoding Arcelin, a Lectin-Like Seed Protein from Phaseolus vulgaris. Plant Physiol. 1991 Oct;97(2):839–840. [PMC free article] [PubMed]
  • An C, Ichinose Y, Yamada T, Tanaka Y, Shiraishi T, Oku H. Organization of the genes encoding chalcone synthase in Pisum sativum. Plant Mol Biol. 1993 Mar;21(5):789–803. [PubMed]
  • Coruzzi G, Broglie R, Edwards C, Chua NH. Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J. 1984 Aug;3(8):1671–1679. [PMC free article] [PubMed]
  • Suzuki T, Kazama S, Hirai A, Akihama T, Kadowaki K. The rice mitochondrial nad3 gene has an extended reading frame at its 5' end: nucleotide sequence analysis of rice trnS, nad3, and rps12 genes. Curr Genet. 1991 Sep;20(4):331–337. [PubMed]
  • Lane BG, Bernier F, Dratewka-Kos E, Shafai R, Kennedy TD, Pyne C, Munro JR, Vaughan T, Walters D, Altomare F. Homologies between members of the germin gene family in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J Biol Chem. 1991 Jun 5;266(16):10461–10469. [PubMed]
  • Rohde W, Dörr S, Salamini F, Becker D. Structure of a chalcone synthase gene from Hordeum vulgare. Plant Mol Biol. 1991 Jun;16(6):1103–1106. [PubMed]
  • Allen RL, Lonsdale DM. Molecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development. Plant J. 1993 Feb;3(2):261–271. [PubMed]
  • Quayle TJ, Brown JW, Feix G. Analysis of distal flanking regions of maize 19-kDa zein genes. Gene. 1989 Aug 15;80(2):249–258. [PubMed]
  • Barakate A, Martin W, Quigley F, Mache R. Characterization of a multigene family encoding an exopolygalacturonase in maize. J Mol Biol. 1993 Feb 5;229(3):797–801. [PubMed]
  • Liaud MF, Zhang DX, Cerff R. Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8918–8922. [PMC free article] [PubMed]
  • Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S. Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev. 1991 Mar;5(3):496–507. [PubMed]
  • Bureau TE, Wessler SR. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell. 1992 Oct;4(10):1283–1294. [PMC free article] [PubMed]
  • Bureau TE, Wessler SR. Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1411–1415. [PMC free article] [PubMed]
  • Bureau TE, Wessler SR. Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell. 1994 Jun;6(6):907–916. [PMC free article] [PubMed]
  • Stavenhagen JB, Robins DM. An ancient provirus has imposed androgen regulation on the adjacent mouse sex-limited protein gene. Cell. 1988 Oct 21;55(2):247–254. [PubMed]
  • Ting CN, Rosenberg MP, Snow CM, Samuelson LC, Meisler MH. Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes Dev. 1992 Aug;6(8):1457–1465. [PubMed]
  • Banville D, Boie Y. Retroviral long terminal repeat is the promoter of the gene encoding the tumor-associated calcium-binding protein oncomodulin in the rat. J Mol Biol. 1989 Jun 5;207(3):481–490. [PubMed]
  • Chang-Yeh A, Mold DE, Huang RC. Identification of a novel murine IAP-promoted placenta-expressed gene. Nucleic Acids Res. 1991 Jul 11;19(13):3667–3672. [PMC free article] [PubMed]
  • Fluhr Robert, Moses Phyllis, Morelli Giorgio, Coruzzi Gloria, Chua Nam-Hai. Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J. 1986 Sep;5(9):2063–2071. [PMC free article] [PubMed]
  • Pedersen K, Devereux J, Wilson DR, Sheldon E, Larkins BA. Cloning and sequence analysis reveal structural variation among related zein genes in maize. Cell. 1982 Jul;29(3):1015–1026. [PubMed]
  • Spena A, Viotti A, Pirrotta V. Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction pattern. J Mol Biol. 1983 Oct 5;169(4):799–811. [PubMed]
  • Kriz AL, Boston RS, Larkins BA. Structural and transcriptional analysis of DNA sequences flanking genes that encode 19 kilodalton zeins. Mol Gen Genet. 1987 Apr;207(1):90–98. [PubMed]
  • Soave C, Reggiani R, Di Fonzo N, Salamini F. Clustering of genes for 20 kd zein subunits in the short arm of maize chromosome 7. Genetics. 1981 Feb;97(2):363–377. [PMC free article] [PubMed]
  • Mount SM, Rubin GM. Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol. 1985 Jul;5(7):1630–1638. [PMC free article] [PubMed]
  • Konieczny A, Voytas DF, Cummings MP, Ausubel FM. A superfamily of Arabidopsis thaliana retrotransposons. Genetics. 1991 Apr;127(4):801–809. [PMC free article] [PubMed]

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