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Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture

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Summary

Previous experiments have revealed that the maize transposable element Activator (Ac) may become active during tissue culture. The objective of the present study was to determine whether a second transposable element, Suppressor-mutator (Spm), could also be activated in tissue culture and detected in regenerated maize plants. Approximately 500 R1 progeny of 143 regenerated plants (derived from 49 embryo cell lines) were crossed as males onto an Spm-responsive tester stock. Spm activity was observed in two R1 progeny of a single regenerated plant. This plant had been regenerated from Type II (friable embryogenic) callus of an A188 × B73 genetic background after 8 months in culture; the absence of Spm activity in four other plants regenerated from this same callus demonstrates that Spm activity was not present before culturing. Approximately 20 Spm-homologous DNA sequences were detected in each of the inbreds used to initiate the tissue cultures; it is presumed that one of these became active to give rise to Spm activity.

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References

  • Armstrong CL (1986) Genetic and cytogenetic stability of maize tissue cultures: a comparative study of organogenic and embryogenic cultures. PhD thesis, University of Minnesota-St. Paul

  • Armstrong CL, Phillips RL (1988) Genetic and cytogenetic variation in plants regenerated from organogenic and friable, embryogenic tissue cultures of maize. Crop Sci 28:363–369

    Google Scholar 

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

    Google Scholar 

  • Benner MS, Phillips RL, Kirihara JA, Messing JW (1989) Genetic analysis of methionine-rich storage protein genes in maize. Theor Appl Genet 78:761–767

    Google Scholar 

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

    Google Scholar 

  • Benzion G (1984) Genetic and cytogenetic analysis of maize tissue cultures: a cell line pedigree analysis. PhD thesis, University of Minnesota-St. Paul

  • Benzion G, Phillips RL (1988) Cytogenetic stability of maize tissue cultures: a cell line pedigree analysis. Genome 30:318–325

    Google Scholar 

  • Bianchi MW, Viotti A (1988) DNA methylation and tissue-specific transcription of the storage protein genes of maize. Plant Mol Biol 11:203–214

    Google Scholar 

  • Bianchi A, Salamini F, Parlavecchio R (1969) On the origin of controlling elements in maize. Genet Agrar 22:335–344

    Google Scholar 

  • Bingham ET, Groose RW, Ray IM (1988) Activation of a mutable allele in alfalfa tissue culture. In: Nelson OE (ed) Plant transposable elements. Plenum Press, New York, pp 325–338

    Google Scholar 

  • Brettell RIS, Thomas E, Ingram DS (1980) Reversion of Texas male-sterile cytoplasm maize in culture to give fertile, T-toxin resistant plants. Theor Appl Genet 58:55–58

    Google Scholar 

  • Brettell RIS, Dennis ES, Scowcroft WR, Peacock WJ (1986) Molecular analysis of a somaclonal mutant of maize alcohol dehydrogenase. Mol Gen Genet 202:235–239

    Google Scholar 

  • Brown PTH (1989) DNA methylation in plants and its role in tissue culture. Genome 31:717–729

    Google Scholar 

  • Brown PTH, Lorz H (1986) Molecular changes and possible origins of somaclonal variation. In: Semal J (ed) Somaclonal variation and crop improvement. Martinus Nijhoff, Dordrecht, The Netherlands, pp 148–159

    Google Scholar 

  • Burr B, Burr F (1981) Transposable elements and genetic instabilities in crop plants. Stadler Genet Symp 13:115–128

    Google Scholar 

  • Burr B, Burr FA (1988) Activation of silent transposable elements. In: Nelson OE (ed) Plant transposable elements. Plenum Press, New York, pp 317–324

    Google Scholar 

  • Catcheside DG (1939) A position effect in Oenothera. J Genet 38:345–352

    Google Scholar 

  • Chandler VL, Walbot V (1986) DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci USA 83:1767–1771

    Google Scholar 

  • Chandler VL, Talbert LE, Raymond F (1988) Sequence, genomic distribution, and DNA modification of a Mu1 element from non-mutator maize stocks. Genetics 119:951–958

    Google Scholar 

  • Chen CH, Freeling ML, Merckelbach A (1986) Enzymatic and morphological consequences of Ds excisions from maize Adh1. Maydica 31:93–108

    Google Scholar 

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

    Google Scholar 

  • Cone KC, Burr FA, Burr B (1986) Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci USA 83:9631–9635

    Google Scholar 

  • Culley DE (1986) Evidence for the activation of a cryptic transposable element Ac in maize endosperm cultures. 6th Int Congr Plant Tiss Cell Cult, Minneapolis/MN. Abstracts, p 220

  • Dennis ES, Brettell RIS (1990) DNA methylation of maize transposable elements is correlated with activity. Philos Trans R Soc Lond Ser B 326:217–229

    Google Scholar 

  • Dennis ES, Brettell RIS, Peacock WJ (1987) A tissue-culture-induced Adh1 null mutant of maize results from a single base change. Mol Gen Genet 210:181–183

    Google Scholar 

  • Doerschug EB (1973) Studies of Dotted, a regulatory element in maize. 1. Induction of Dotted by chromosome breaks. 2. Phase variation of Dotted. Theor Appl Genet 43:182–189

    Google Scholar 

  • Dooner HK (1980) Regulation of the enzyme UFGT by the controlling element Ds in bz-m4, an unstable mutant in maize. Cold Spring Harbor Symp Quant Biol 45:457–462

    Google Scholar 

  • Dooner HK, Nelson OE Jr (1977) Controlling element-induced alterations in UDP glucose: flavonoid glucosyltransferase, the enzyme specified by the bronze locus in maize. Proc Natl Acad Sci USA 74:5623–5627

    Google Scholar 

  • Dooner HK, Nelson OE Jr (1979) Heterogeneous flavonoid glucosyltransferases in purple derivatives from a controlling element-suppressed bronze mutant in maize. Proc Natl Acad Sci USA 76:2369–2371

    Google Scholar 

  • Dooner HK, Ralston E, English J (1988) Deletions and breaks involving the borders of the Ac element in the bz-m2(Ac) allele of maize In: Nelson OE (ed) Plant transposable elements. Plenum Press, New York, pp 213–226

    Google Scholar 

  • Echt CS, Schwartz D (1981) Evidence for the inclusion of controlling elements within the structural gene at the waxy locus in maize. Genetics 99:275–284

    Google Scholar 

  • Edallo S, Zucchinali C, Perenzin M, Salamini F (1981) Chromosome variation and frequency of spontaneous mutation associated with in vitro culture and plant regeneration in maize. Maydica 26:39–56

    Google Scholar 

  • Evola SV, Burr FA, Burr B (1984) The nature of tissue-culture-induced mutations in maize. 11 th Annu Aharon Katzir-Katchalsky Conf, 8–3 January, 1984, Jerusalem. Abstract

  • Evola SV, Tuttle A, Burr F, Burr B (1985) Tissue-culture-associated variability in maize: molecular and genetic studies. 1st Int Congr Plant Mol Biol, Savannah/GA. Abstracts, p 10

  • Fedoroff NV (1989) About maize transposable elements and development. Cell 56:181–191

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fedoroff N, Shure M, Kelley S, Johns M, Furtek D, Schiefelbein J, Nelson O (1984) Isolation of Spm controlling elements from maize. Cold Spring Harbor Symp Quant Biol 49:339–345

    Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    CAS  PubMed  Google Scholar 

  • Gierl A, Saedler H (1989) The En/Spm transposable element of Zea mays. Plant Mol Biol 13:261–266

    Google Scholar 

  • Grafstrom RH, Hamilton DL, Yuan R (1984) DNA methylation: DNA replication and repair. In: Razin A, Cedar H, Riggs AD (eds) DNA methylation: biochemistry and biological significance. Springer, New York, pp 111–126

    Google Scholar 

  • Groose RW, Bingham ET (1986) An unstable anthocyanin mutation recovered from tissue culture of alfalfa (Medicago sativa). 1. High frequency of reversion upon reculture. 2. Stable nonrevertants derived from reculture. Plant Cell Rep 5:104–110

    Google Scholar 

  • Hare JT, Taylor JH (1985) One role for DNA methylation in vertebrate cells is strand discrimination in mismatch repair. Proc Natl Acad Sci USA 82:7350–7354

    Google Scholar 

  • Hepburn AG, Clark LE, Pearson L, White J (1983) The role of cytosine methylation in the control of nopaline synthase gene expression in a plant tumor. J Mol Appl Genet 2:315–329

    Google Scholar 

  • James MG, Stadier J (1989) Molecular characterization of Mutator systems in maize embryogenic callus cultures indicates Mu activity in vitro. Theor Appl Genet 77:383–393

    Google Scholar 

  • Johns MA, Mottinger J, Freeling M (1985) A low copy number, copia-like transposon in maize. EMBO J 4:1093–1102

    Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation — a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214

    Google Scholar 

  • Lee M, Phillips RL (1987a) Genomic rearrangements in maize induced by tissue culture. Genome 29:122–128

    Google Scholar 

  • Lee M, Phillips RL (1987b) Genetic variants in progeny of regenerated maize plants. Genome 29:834–838

    Google Scholar 

  • Lee M, Geadelmann JL, Phillips RL (1988) Agronomic evaluation of inbred lines derived from tissue cultures of maize. Theor Appl Genet 75:841–849

    Google Scholar 

  • 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

    Google Scholar 

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

    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 Wash Yearbk 50:174–181

    Google Scholar 

  • McClintock B (1954) Mutations in maize and chromosomal aberrations in Neurospora. Carnegie Inst Wash Yearbk 53:254–260

    Google Scholar 

  • McClintock B (1978) Mechanisms that rapidly reorganize the genome. Stadler Genet Symp 10:25–47

    Google Scholar 

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

    Google Scholar 

  • Neuffer MG (1966) Stability of the suppressor element in two mutator systems of the A1 locus in maize. Genetics 53:541–549

    Google Scholar 

  • Nick H, Bowen B, Ferl RJ, Gilbert W (1986) Detection of cytosine methylation in the maize alcohol dehydrogenase gene by genomic sequencing. Nature 319:243–246

    Google Scholar 

  • Peacock WJ, Dennis ES, Gerlach WL, Sachs MM, Schwartz D (1984) Insertion and excision of Ds controlling elements in maize. Cold Spring Harbor Symp Quant Biol 49:347–354

    Google Scholar 

  • Pereira A, Cuypers H, Gierl A, Schwarz-Sommer Zs, Saedler H (1986) Molecular analysis of the En/Spm transposable element system of Zea mays. EMBO J 5:835–841

    Google Scholar 

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

    Google Scholar 

  • Peschke VM, Phillips RL, Gengenbach BG. Genetic and molecular analysis of tissue culture-derived Ac elements. Theor Appl Genet, in press

  • Peterson PA (1953) A mutable pale-green locus in maize. Genetics 38:682–683

    Google Scholar 

  • Peterson PA (1965) A relationship between the Spm and En control systems in maize. Am Nat 99:391–398

    Google Scholar 

  • Peterson PA (1986) Mobile elements in maize. Plant Breed Rev 4:81–122

    Google Scholar 

  • Phillips RL, Block LG, Peschke VM, Burnham CR (1986) A suppressor-mutator transposable element system of independent origin. Maize Genet Coop Lett 60:115–117

    Google Scholar 

  • Phillips RL, Kaeppler SM, Peschke VM (1990) Do we understand somaclonal variation? In: Nijkamp HJJ, Van Der Plas LHW, Van Aartrijk J (eds) Progress in Plant Cellular and Molecular Biology: Proceedings, 7th International Congress on Plant Tissue and Cell Culture. Kluwer Acad Publ, Dordrecht, The Netherlands, pp 131–141

    Google Scholar 

  • Planckaert F, Walbot V (1989) Molecular and genetic characterization of Mu transposable elements in Zea mays: behavior in callus culture and regenerated plants. Genetics 123:567–578

    Google Scholar 

  • Reed KC, Mann DA (1985) Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res 13:7207–7221

    Google Scholar 

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

    Google Scholar 

  • Rhodes CA, Phillips RL, Green CE (1986) Cytogenetic stability of aneuploid maize tissue cultures. Can J Genet Cytol 28:374–384

    Google Scholar 

  • Robertson DS, Stinard PS (1987) Genetic evidence of Mutator-induced deletions in the short arm of chromosome nine of maize. Genetics 115:353–361

    Google Scholar 

  • Sachs MM, Peacock WJ, Dennis ES, Gerlach WL (1983) Maize Ac/Ds controlling elements — a molecular viewpoint. Maydica 28:289–301

    Google Scholar 

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

    Google Scholar 

  • Schwartz D (1989) Gene-controlled cytosine demethylation in the promoter region of the Ac transposable element in maize. Proc Natl Acad Sci USA 86:2789–2793

    Google Scholar 

  • Schwartz D, Dennis E (1986) Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Mol Gen Genet 205:476–482

    Google Scholar 

  • Shure M, Wessler S, Fedoroff N (1983) Molecular identification and isolation of the waxy locus in maize. Cell 35:225–233

    Article  CAS  PubMed  Google Scholar 

  • Stadier LJ (1941) The comparison of ultraviolet and X-ray effects on mutation. Cold Spring Harbor Symp Quant Biol 9:168–178

    Google Scholar 

  • Sturtevant AH (1925) The effects of unequal crossing-over at the Bar locus in Drosophila. Genetics 10:117–147

    Google Scholar 

  • Taylor LP, Walbot V (1985) A deletion adjacent to the maize transposable element Mu1 accompanies loss of Adh1 expression. EMBO 14:869–876

    Google Scholar 

  • Umbeck P, Gengenbach BG (1983) Reversion of male-sterile T-cytoplasm to male fertility in tissue culture. Crop Sci 23:584–588

    Google Scholar 

  • Walbot V (1988) Reactivation of the Mutator transposable element system following gamma irradiation of seed. Mol Gen Genet 212:259–264

    Google Scholar 

  • Woodman JC, Kramer DA (1986) The recovery of somaclonal variants from tissue cultures of B73, an elite enbred line of maize. 6th Int Congr Plant Tiss Cell Cult, Minneapolis/MN. Abstracts, p 215

  • Zehr BE, Williams ME, Duncan DR, Widholm JM (1987) Somaclonal variation in the progeny of plants regenerated from callus cultures of seven inbred lines of maize. Can J Bot 65:491–499

    Google Scholar 

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  1. V. M. Peschke

    Present address: Department of Biology, Washington University, 63130, St. Louis, MO, USA

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  1. Department of Agronomy and Plant Genetics and the Plant Molecular Genetics Institute, University of Minnesota, 55108, St. Paul, MN, USA

    V. M. Peschke & R. L. Phillips

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  1. V. M. Peschke
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  2. R. L. Phillips
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Communicated by F. Salamini

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Peschke, V.M., Phillips, R.L. Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture. Theoret. Appl. Genetics 81, 90–97 (1991). https://doi.org/10.1007/BF00226117

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