Abstract
Three subfamilies of the En/Spm-type transposable element of carrot, Tdc A, B, and C, were characterized. It was supposed that the Tdc A subfamily may include autonomous elements which can produce transposases. Tdc B elements are defective, but still generate transcripts containing mutant open reading frame (ORF) sequences for transposases. The single member of the Tdc C group recovered seems to be a pseudogene. The sequences of the transposase ORFs of Tdc A and Tdc B elements are more highly conserved than those of the 5´ and 3´ untranslated regions and introns, as is found in other structural genes that are subject to selection. These observations indicate that the mutations in the nucleotide sequences of the Tdc elements occurred in the host genome. However, the mutations in the 5´ and 3´ untranslated regions and introns, which may not be sufficient to prevent transposition, accumulated in autonomous elements, which could transpose and produce copies. When the reproduction rate and the rate of disabling mutations reached an equilibrium, that is, when the birth rate of the transposable elements in the genome equalled the death rate, the population of elements achieved a stationary state in the genome, and could thus survive.
Similar content being viewed by others
References
Britten RJ (1996) Cases of ancient mobile element DNA insertions that now affect gene regulation. Mol Phylogenet Evol 5:13–17
Chandler VL, Hardeman KJ (1992) The Mu elements of Zea mays. Adv Genet 30:77–122
Chen J, Greenblatt IM, Dellaporta SL (1987) Transposition of Ac from the P locus of maize into unreplicated chromosomal sites. Genetics 117:109–116
Chen J, Greenblatt IM, Dellaporta SL (1992) Molecular analysis of Ac transposition and DNA replication. Genetics 130:665–676
Dash S, Peterson PA (1994) Frequent loss of the En transposable element after excision and its relation to chromosome replication in maize (Zea mays L.). Genetics 136:653–671
Dayhoff MO (1978) Atlas of protein sequence and structure. National Biochemical Research Foundation, Washington, D.C.
Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603
Fedoroff NV (1989) About maize transposable elements and development. Cell 56:181–191
Fedoroff NV (1999) The Suppressor-mutator element and the evolutionary riddle of transposons. Genes Cells 4:11–19
Fedoroff N, Schlappi M, Raina R (1995) Epigenetic regulation of the maize Spm transposon. Bioessays 17:291–297
Finnegan DJ (1997) Transposable elements: how non-LTR retrotransposons do it. Curr Biol 7:R245–248
Flavell A J, Pearce SR, Kumar A. (1994) Plant transposable elements and the genome. Curr Opin Genet Dev 4:838–844
Frey M, Reinecke J, Grant S, Saedler H, Gierl A (1990) Excision of the En/Spm transposable element of Zea mays requires two element-encoded proteins. EMBO J 9:4037–4044
Gierl A, Lütticke S, Saedler H (1988) TnpA product encoded by the transposable element En-1of Zea mays is a DNA binding protein. EMBO J 7:4045–4053
Gierl A, Saedler H, Peterson PA (1989) Maize transposable elements. Annu Rev Genet 23:71–85
Grandbastien MA (1992) Retroelements in higher plants. Trends Genet 8:103–108
Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1mutation. Plant Cell 12:357–369
International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Kunze R, Saedler H, Lönnig WE (1997) Plant transposable elements. Adv Bot Res 27:331–470
Le QH, Wright S, Yu Z, Bureau T (2000) Transposon diversity in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:7376–7381
Masson P, Fedoroff NV (1989) Mobility of the maize Suppressor-mutator element in transgenic tobacco cells. Proc Natl Acad Sci USA 86:2219–2223
Masson P, Surosky R, Kingsbury JA, Fedoroff NV (1987) Genetic and molecular analysis of the Spm -dependent a-m2alleles of the maize a locus. Genetics 117:117–137
Masson P, Rutherford G, Banks JA, Fedoroff N (1989) Essential large transcripts of the maize Spm transposable element are generated by alternative splicing. Cell 58:755–765
Masson P, Strem M, Fedoroff N (1991) The tnpA and tnpD gene products of the Spm element are required for transposition in tobacco. Plant Cell 3:73–85
McClintock B (1946) Maize genetics. Carnegie Inst Wash Ybk 45:176–186
McClintock B (1971) The contribution of one component of a control system to versatility of gene expression. Carnegie Inst Wash Ybk 70:5–17
McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801
Nacken WK, Piotrowiak R, Saedler H, Sommer H (1991) The transposable element Tam1from Antirrhinum majus shows structural homology to the maize transposon En/Spm and has no sequence specificity of insertion. Mol Gen Genet 228:201–208
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607
Ozeki Y, Matsui K, Sakuta M, Matsuoka M, Ohashi Y, Kano-Murakami Y, Yamamoto N, Tanaka Y (1990) Differential regulation of phenylalanine ammonia-lyase genes during anthocyanin synthesis and by transfer effect in carrot cell suspension cultures. Physiol Planta 80:379–387
Ozeki Y, Davies E, Takeda J (1997) Plant cell culture variation during long-term subculturing caused by insertion of a transposable element in a phenylalanine ammonia-lyase (PAL) gene. Mol Gen Genet 254:407–416
Pereira A, Saedler H (1989) Transpositional behavior of the maize En/Spm element in transgenic tobacco. EMBO J 8:1315–1321
Pereira A, Cuyoers H, Gierl A, Schwarz-Sommer Z, Saedler H (1986) Molecular analysis of the En/Spm element system of Zea mays. EMBO J 5:835–841
Peschke VM, Phillips RL, Gengenbach BG (1987) Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238:804–807
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenic trees. Mol Biol Evol 4:406–425
SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
Schiefelbein JW, Raboy V, Fedoroff NV, Nelson OEJr. (1985) Deletions within a defective Suppressor-mutator element in maize affect the frequency and developmental timing of its excision from the bronze locus. Proc Natl Acad Sci USA 82:4783–4787
Snowden KC, Napoli CA (1998) Psl: a novel Spm -like transposable element from Petunia hybrida. Plant J 14:43–54
Stewart WN, Rothwell GW (1993) Paleobotany and the evolution of plants (2nd ed). Cambridge University Press, Cambridge, UK
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680
Wessler SR, Bureau TE, White SE (1995) LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 5:814–821
Yan X, Martinez-Ferez IM, Kavchok S, Dooner HK (1999) Origination of Ds elements from Ac elements in maize: evidence for rare repair synthesis at the site of Ac excision. Genetics 152:1733–1740
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166
Acknowledgements
This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. P. Georgiev
Rights and permissions
About this article
Cite this article
Itoh, Y., Hasebe, M., Davies, E. et al. Survival of Tdc transposable elements of the En/Spm superfamily in the carrot genome. Mol Gen Genomics 269, 49–59 (2003). https://doi.org/10.1007/s00438-002-0798-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-002-0798-7