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Evolution of Ac and Dsl elements in select grasses (Poaceae)

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Abstract

We present data on evolution of the Ac/Ds family of transposable elements in select grasses (Poaceae). An Ac-like element was cloned from a DNA library of the grass Pennisetum glaucum (pearl millet) and 2387 bp of it have been sequenced. When the pearl millet Ac-like sequence is aligned with the corresponding region of the maize Ac sequence, it is found that all sequences corresponding to intron II in maize Ac are absent in pearl millet Ac. Kimura's evolutionary distance between maize and pearl millet Ac sequences is estimated to be 0.429±0.020 nucleotide substitutions per site. This value is not significantly different from the average number of synonymous substitutions for coding regions of the Adh1 gene between maize and pearl millet, which is 0.395±0.051 nucleotide substitutions per site. If we can assume Ac and Adh1 divergence times are equivalent between maize and pearl millet, then the above calculations suggest Ac-like sequences have probably not been strongly constrained by natural selection. The level of DNA sequence divergence between maize and pearl millet Ac sequences, the estimated date when maize and pearl millet diverged (25–40 million years ago), coupled with their reproductive isolation/lack of current genetic exchange, all support the theory that Ac-like sequences have not been recently introduced into pearl millet from maize. Instead, Ac-like sequences were probably present in the progenitor of maize and pearl millet, and have thus existed in the grasses for at least 25 million years. Ac-like sequences may be widely distributed among the grasses. We also present the first 2 Dsl controlling element sequences from teosinte species: Zea luxurians and Zea perennis. A total of 10 Dsl elements had previously been sequenced from maize and a distant maize relative, Tripsacum. When a maximum likelihood network of genetic relationships is constructed for all 12 sequenced Dsl elements, the 2 teosinte Dsl elements are as distant from most maize Dsl elements and from each other, as the maize Dsl elements are from one another. Our new teosinte sequence data support the previous conclusion that Dsl elements have been accumulating mutations independently since maize and Tripsacum diverged. We present a scenario for the origin of Dsl elements.

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References

  • Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith & K. Struhl, 1989. Current Protocols in Molecular Biology. Wiley and Sons, New York.

    Google Scholar 

  • Banks, J. A., P. Masson & N. Fedoroff, 1988. Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev. 2: 1364–1380.

    Google Scholar 

  • Behrens, U., N. V. Fedoroff, A. Laird, M. Muller-Neumann, P. Starlinger & J. Yoder, 1984. Cloning of the Zea mays controlling element Ac from the wx-m7 allele. Mol. Gen. Genet. 194: 346–347.

    Google Scholar 

  • Bennetzen, J. L., 1987. Covalent DNA modification and the regulation of Mutator element transposition in maize. Mol. Gen. Genet. 208: 45–51.

    Google Scholar 

  • Bhattacharyya, M. K., A. M. Smith, T. H. N. Ellis, C. Hedley & C. Martin, 1990. The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme Cell 60: 115–122.

    Google Scholar 

  • Brink, R. A. & R. A. Nilan, 1952. The relation between light variegated and medium variegated pericarp in maize. Genetics 37: 519–544.

    Google Scholar 

  • Calvi, B. R., T. J. Hong, S. D. Findley & W. M. Gelbart, 1991. Evidence for a Chandler, V. L. and V. Walbot, 1986. DNA modification of a maize transposable element correlated with loss of activity. Proc. Natl. Acad. Sci. USA 83: 1767–1771.

    Google Scholar 

  • Chen, J., I. M. Greenblatt & S. L. Dellaporta 1987. Transposition of Ac from the P locus of maize into unreplicated chromosomal sites. Genetics 117: 109–116.

    Google Scholar 

  • Chomet, P. S., S. Wessler & S. L. Dellaporta, 1987. Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. EMBO J. 6: 295–302.

    Google Scholar 

  • Courage-Tebbe, U., H.-P. Doring, N. V. Fedoroff & P. Starlinger, 1983. The controlling element Ds at the Shrunken locus in Zea mays: structure of the unstable sh-m5933 allele and several revertants. Cell 34: 383–393.

    Google Scholar 

  • Dennis, E. S., W. L. Gerlach, A. J. Pryor, J. L. Bennetzen, A. Inglis, D. Llewellyn, M. M. Sachs, R. J. Ferl & W. J. Peacock, 1984. Molecular analysis of the alcohol dehydrogenase (Adhl) gene of maize. Nuc. Acids Research 12: 3983–4000.

    Google Scholar 

  • Devereux, J., P. Haerberli & O. Smithies, 1984. A comprehensive set of sequence analysis programs for the VAX. Nuc. Acids. Res. 12: 387–395.

    Google Scholar 

  • Doebley, J., 1989. Molecular evidence for a missing wild relative of maize and the introgression of its chloroplast genome into Zea perennis. Evolution 43: 1555–1559.

    Google Scholar 

  • Doebley, J., M. Durbin, E. M. Golenberg, M. T. Clegg & D.-P. Ma, 1990. Evolutionary analysis of the large subunit of carboxylase (rbcL) nucleotide sequence among the grasses (Gramineae). Evolution 44: 1097–1108.

    Google Scholar 

  • Doring, H.-P., M. Freeling, S. Hake, M. A. Johns & R. Kunze, 1984a. A Ds mutation of the Adhl gene in Zea mays. L. Mol. Gen. Genet. 193: 199–204.

    Google Scholar 

  • Doring, H.-P., E. Tillmann & P. Starlinger, 1984b. DNA sequence of the maize transposable element Dissociation. Nature 307: 127–130.

    Google Scholar 

  • Fedoroff, N. V., 1989. About maize transposable elements and development. Cell 56: 181–191.

    Google Scholar 

  • Fedoroff, N. V., 1989b. The heritable activation of cryptic Suppressor-mutator elements by an active element. Genetics 121: 591–608.

    Google Scholar 

  • Fedoroff, N. V., D. B. Furtek & O. E. Nelson, 1984. Cloning of the bronze locus in maize by a simple and generalizable procedure using the transposable controlling element Activator (Ac). Proc. Natl. Acad. Sci. USA 81: 3825–3829.

    Google Scholar 

  • Fedoroff, N. V., S. Wessler & M. Shure, 1983. Isolation of the transposable maize controlling elements Ac and Ds. Cell 35: 235–242.

    Google Scholar 

  • Felsenstein, J., 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17: 368–376.

    Google Scholar 

  • Felsenstein, J., 1983. Inferring evolutionary trees from DNA sequences, pp. 133–150 in Statistical analysis of DNA sequence data, edited by B. S. Weir. Marcel Dekker, New York.

    Google Scholar 

  • Finnegan, E. J., B. H. Taylor, E. S. Dennis & W. J. Peacock, 1988. Transcription of the maize transposable element Ac in maize seedlings and in transgenic tobacco. Mol. Gen. Genet. 212: 505–509.

    Google Scholar 

  • Gaut, B. S. & M. T. Clegg, 1991. Molecular evolution of alcohol dehydrogenase 1 in members of the grass family. Proc. Natl. Acad. Sci. USA 88: 2060–2064.

    Google Scholar 

  • Gerlach, W. L., E. S. Dennis, W. J. Peacock & M. T. Clegg, 1987. The Dsl controlling element family in maize and Tripsacum. J. Mol. Evol. 26: 329–334.

    Google Scholar 

  • Greenblatt, I. M., 1966. Transposition and replication of Modulator in maize. Genetics 53: 361–369.

    Google Scholar 

  • Greenblatt, I. M., 1968. The mechanism of Modulator transposition in maize. Genetics 58: 585–597.

    Google Scholar 

  • Greenblatt, I. M.: 1974a. Proximal-distal polarity of Modulator transpositions upon leaving the P locus. Maize Genet. Coop. News Lett. 48: 188–189.

    Google Scholar 

  • Greenblatt, I. M., 1974b. Modulator: a modifier of crossing over. Maize Genet. Coop. News Lett. 48: 189–191.

    Google Scholar 

  • Greenblatt, I. M., 1974c. Movement of Modulator in maize: a test of an hypothesis. Genetics 77: 671–678.

    Google Scholar 

  • Greenblatt, I. M., 1984. A chromosomal replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, Modulator, in maize. Genetics 108: 471–485.

    Google Scholar 

  • Greenblatt, I. M. & R. A. Brink, 1962. Twin mutations in medium variegated pericarp maize. Genetics 47: 489–501.

    Google Scholar 

  • Greenblatt, I. M. & R. A. Brink, 1963. Transposition of Modulator in maize into divided and undivided chromosome segments. Nature 197: 412–413.

    Google Scholar 

  • Herrmann, A., W. Schulz & K. Hahlbrock, 1988. Two alleles of the single-copy chalcone synthase gene in parsley differ by a transposon-like element. Mol. Gen. Genet. 212: 93–98.

    Google Scholar 

  • Howard, E. A. & E. S. Dennis, 1984. Transposable elements in maize-the Activator-Dissociation (Ac-Ds) system. Aust. J. Biol. Sci. 37: 307–314.

    Google Scholar 

  • Johns, M. A., 1990. Sequences related to the maize transposable element Ac in the Genus Zea. J. Mol. Evol. 30: 493–499.

    Google Scholar 

  • Kimura, M., Estimation of evolutionary distances between homologous nucleotide sequences. Proc. Natl. Acad. Sci. USA 78: 454–458.

  • Kunze, R. & P. Starlinger, 1989. The putative transposase of transposable element Ac from Zea mays L. interacts with subterminal sequences of Ac. EMBO J. 8: 3177–3185.

    Google Scholar 

  • Kunze, R., U. Stochaj, J. Laufs & P. Starlinger, 1987. Transcription of transposable element Activator (Ac) of Zea mays. L. EMBO J. 6: 1555–1563.

    Google Scholar 

  • MacRae, A. F., G. H. Learn, M. Karjala & M. T. Clegg, 1990. Presence of an Activator (Ac)-like sequence in Pennisetum glaucum (pearl millet). Plant Mol. Biol. 15: 177–179.

    Google Scholar 

  • Maniatis, T., E. F. Fritsch & J. Sambrook, 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Martin, C., A. Prescott, C. Lister & S. MacKay, 1989. Activity of the transposon Tam3 in Antirrhinum and tobacco: possible role of DNA methylation. EMBO J. 8: 997–1004.

    Google Scholar 

  • McClintock, B., 1945. Cytogenic studies of maize and Neurospora. Carnegie Inst. Washington Year Book 44: 108–112.

    Google Scholar 

  • McClintock, B., 1946. Maize genetics. Carnegie Inst. Washington Year Book 45: 176–186.

    Google Scholar 

  • McClintock, B., 1947. Cytogenetic studies of maize and Neurospora. Carnegie Inst. Wash. Year Book 46: 146–151.

    Google Scholar 

  • McClintock, B., 1948. Mutable loci in maize. Carnegie Inst. Washington Year Book 47: 155–169.

    Google Scholar 

  • McClintock, B., 1950a. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 36: 344–355.

    Google Scholar 

  • McClintock, B., 1950b. Mutable loci in maize. Carnegie Inst. Washington Year Book 49: 157–167.

    Google Scholar 

  • McClintock, B., 1951a. Chromosome organization and genic expression. Cold Spring Harbor Symp. Quant. Biol. 16: 13–47.

    Google Scholar 

  • McClintock, B., 1951b. Mutable loci in maize. Carnegie Inst. Washington Year Book 50: 174–181.

    Google Scholar 

  • McClintock, B., 1956. Controlling elements and the gene. Cold Spring Harbor Symp. Quant. Biol. 21: 197–216.

    Google Scholar 

  • McClintock, B., 1961. Further studies of the Suppressor-mutator system of control of gene action in maize. Carnegie Inst. Washington Year Book 60: 469–576.

    Google Scholar 

  • Merckelbach, A., H.-P. Doring & P. Starlinger, 1986. The aberrant Ds element in the Adh1–2F11::Ds allele. Maydica 31: 109–122.

    Google Scholar 

  • Muller-Neumann, M., J. Yoder & P. Starlinger, 1984. The DNA sequence of the transposable element Ac of Zea mays. Mol. Gen. Genet. 198: 19–24.

    Google Scholar 

  • Nevers, P., N. Shepherd & H. Saedler, 1986. Plant transposable elements. Adv. Bot. Res. 12: 102–203.

    Google Scholar 

  • Osterman, J. C. & E. S. Dennis, 1989. Molecular analysis of the Adh1-C mallele of maize. Plant Mol. Biol. 13: 203–212.

    Google Scholar 

  • Peacock, W. J., E. S. Dennis, W. L. Gerlach, D. Llewellyn & H. Lorz et al., 1983. Gene transfer in maize: Controlling elements and the alcohol dehydrogenase genes, pp. 311–326 in Proc. 15th Miami Winter Symp., edited by K. Downry, R. W. Vollmy, F. Ahmad and J. Schultz. Academic, New York.

    Google Scholar 

  • Peschke, V., R. L. Phillips & B. G. Gengenbach, 1985. Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238: 804–806.

    Google Scholar 

  • Pohlman, R. F., N. V. Fedoroff & J. Messing, 1984a. The nucleotide sequence of the maize controlling element Activator. Cell 37: 635–643.

    Google Scholar 

  • Rhoades, M. M. & E. Dempsey, 1982. The induction of mutable systems in plants with the high-loss mechanism. Maize Genet. Coop. Newsl. 56: 21–26.

    Google Scholar 

  • Ritland, K. & M. T. Clegg, 1987. Evolutionary analysis of plant DNA sequences. Am. Nat. 130: S74-S100.

    Google Scholar 

  • Sachs, M. M., E. S. Dennis, W. L. Gerlach & W. J. Peacock, 1986. Two alleles of maize alcohol dehydrogenase 1 have 3′ structural and poly (A) addition polymorphisms. Genetics 113: 449–467.

    Google Scholar 

  • Saedler, H. & P. Nevers, 1985. Transposition in plants: a molecular model. EMBO J. 4: 585–590.

    Google Scholar 

  • Sanger, F., S. Nicklen & A. R. Coulson, 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.

    Google Scholar 

  • Schiefelbein, J. W., D. B. Furtek, V. Raboy, J. A. Banks, N. V. Fedoroff & O. E. Nelson, 1985a. Exploiting transposable elements to study the expression of a maize gene pp. 445–459 in Plant Genetics, edited by M. Freeling. Alan R. Liss, New York.

    Google Scholar 

  • Sommer, H., R. Carpenter, B. J. Harrison & H. Saedler, 1985. The transposable element Tam3 of Antirrhinum majus generates a novel type of sequence alteration upon excision. Mol. Gen. Genet. 199: 225–231.

    Google Scholar 

  • Sommer, H., R. Hehl, E. Krebbers, R. Piotrowiak, W.-E. Lonnig & H. Saedler, 1988. Transposable elements of Antirrhinum majus, pp. 227–235 in Plant Transposable Elements, edited by O. Nelson. Plenum Press, New York and London.

    Google Scholar 

  • Streck, R. D., J. E. MacGaffey & S. K. Beckendorf, 1986. The structure of hobo transposable elements and their insertion sites. EMBO J. 5: 3615–3623.

    Google Scholar 

  • Sutton, W. D., W. L. Gerlach, D. Schwartz & W. J. Peacock, 1984. Molecular analysis of Ds controlling element mutations at the Adh1 locus of maize. Science 223: 1265–1268.

    Google Scholar 

  • Vershinin, A. V., E. A. Salina, S. K. Svitashev & V. K. Shumny, 1987. The occurrence of Ds-like sequences in cereal genomes. Theor. Appl. Genet. 73: 428–432.

    Google Scholar 

  • Weck, E., U. Courage, H.-P. Doring, N. V. Fedoroff & P. Starlinger, 1984. Analysis of sh-m6233, a mutation induced by the transposable element Ds in the sucrose synthase gene of Zea mays. EMBO J. 3: 1713–1716.

    Google Scholar 

  • Wessler, S. R., G. Baran, M. Varagona & S. L. Dellaporta, 1986. Excision of the Ds element produces waxy proteins with a range of enzymatic activities. EMBO J. 5: 2427–2432.

    Google Scholar 

  • Wolfe, K. H., W.-H. Li & P. M. Sharp, 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chlorolplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84: 9054–9058.

    Google Scholar 

  • Yanisch-Perron, C., J. Vieira & J. Messing, 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103–119.

    Google Scholar 

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  1. A. F. MacRae

    Present address: Division of Biological Sciences, University of Missouri, Tucker Hall, 65211, Columbia, MO, USA

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  1. Department of Botany and Plant Sciences, University of California, 92521, Riverside, CA, USA

    A. F. MacRae & M. T. Clegg

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MacRae, A.F., Clegg, M.T. Evolution of Ac and Dsl elements in select grasses (Poaceae). Genetica 86, 55–66 (1992). https://doi.org/10.1007/BF00133711

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