Abstract
Defined mutant alleles with resident transposons display characteristic patterns of germinal and somatic reversion, and heritable changes in the timing and frequency of reversions, which have been termed “change of state” by McClintock, constantly arise. Several mechanisms were proposed to account for these changes. They may be ascribed to the structure and composition of the elements themselves (composition hypothesis) or to their location (position hypothesis). In the current study, insertion positions were determined for three autonomous En-controlled mutable alleles of the A2 locus in maize that show different somatic reversion patterns. A relationship was observed between En insertion positions in the single coding region of the intronless A2 gene and anthocyanin variegation patterns in the aleurone. An insertion in the 5′ region of the coding sequence produced a very late somatic variegation pattern, whereas two early variegation patterns were caused by En insertions in the 3′ region of the coding sequence.
Similar content being viewed by others
References
Alleman M, Kermicle JL (1993) Somatic variegation and germinal mutability reflect the position of transposable element Dissociation within the maize R gene. Genetics 135:189–203
Athma P, Grotewold E, Peterson T (1992) Insertional mutagenesis of the maize P gene by intragenic transposition of Ac. Genetics 131:199–209
Bennetzen JL (1987) Covalent DNA modification and the regulation of Mutator element transposition in maize. Mol Gen Genet 208:45–51
Brink RA, Williams E (1973) Mutable R-Navajo alleles of cyclic origin in maize. Genetics 73:273–296
Bunkers G, Nelson OE Jr, Raboy V (1993) Maize Bronze 1: dSpm insertion mutations that are not fully suppressed by an active Spm. Genetics 134:1211–1220
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
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
Dellaporta SL (1994) Plant DNA mini-prep and micro-prep: versions 2 and 3. In: Freeling M, Walbot V (eds) The maize handbook. Springer, Berlin Heidelberg New York, pp 522–525
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, Lutticke S, Saedler H (1988) TnpA product encoded by the transposable element En-1 of Zea mays is a DNA binding protein. EMBO J 7:4045–4053
Heinlein M (1995) Variegation patterns caused by excision of the maize transposable element Dissociation (Ds) are autonomously regulated by allele-specific Activator (Ac) elements and are not due to trans-acting modifier genes. Mol Gen Genet 246:1–9
Holton TA, Cornish E (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083
Kuduvalli PN, Rao JE, Craig NL (2001) Target DNA structure plays a critical role in Tn 7 transposition. EMBO J 20:924–932
Masson P, Surosky R, Kingsbury JA, Fedoroff NV (1987) Genetic and molecular analysis of the Spam-dependent a-m2 alleles of the maize a locus. Genetics 177:117–137
McClintock B (1946) Maize genetics. Carnegie Inst Wash Year Book 45:176–186
McClintock B (1947) Cytogenetic studies of maize and Neurospora. Carnegie Inst Wash Year Book 46:146–152
McClintock B (1948) Mutable loci in maize. Carnegie Inst Wash Year Book 47:155–169
McClintock B (1949) Mutable loci in maize. Carnegie Inst Wash Year Book 48:142–154
McClintock B (1954) Mutations in maize and chromosome aberrations in Neurospora. Carnegie Inst Wash Year Book 53:254–260
McClintock B (1962) Topographical relations between elements of control systems in maize. Carnegie Inst Wash Year Book 61:448–461
Menssen A, Höhmann S, Martin M, Schnable PS, Peterson PA, Saedler H, Gierl A (1990) The En/Spm transposable element of Zea mays contains splice sites at the termini generating a novel intron from a dSpm element in the A2 gene. EMBO J 9:3051–3057
Moreno MA, Chen J, Greenblatt I, Dellaporta SL (1992) Reconstitutional mutagenesis of the maize P gene by short-range Ac transpositions. Genetics 131:939–956
Müller-Neumann M, Yoder JI, Starlinger P (1984) The DNA sequence of the transposable element Ac of Zea mays L. Mol Gen Genet 198:19–24
Nelson OE, Klein AS (1984) Characterization of a Spm-controlled bronze-mutable allele in maize. Genetics 106:769–779
Pereira A, Cuypers H, Gierl A, Schwartz-Sommer Z, Saedler H (1986) Molecular analysis of the En/Spm transposable element system of Zea mays. EMBO J 5:835–841
Peterson PA (1953) A mutable pale green locus in maize. Genetics 38:682–683
Peterson PA (1965) A relationship between the Spm and En control systems in maize. Am Nat 99:391–398
Peterson PA (1976) Basis for the diversity of states of controlling elements in maize. Mol Gen Genet 149:15–21
Peterson PA (1977) The position hypothesis for controlling elements in maize. In: Bukhari AJ, Shapiro JA, Adhya SL (eds) DNA insertion elements, plasmids, and episomes. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 429–435
Peterson PA (1978) Controlling elements: the induction of mutability at the A2 and C loci in maize. In: Walden DB (ed) Maize breeding and genetics. Wiley Interscience, New York
Peterson T (1990) Intragenic transposition of Ac generates a new allele of the maize P gene. Genetics 126:469–476
Peterson PA (1995) Genetic analysis of the functions of the transpsable element En in Zea mays: Limited transposase elicits a differential response on reporter alleles. Genetics 141:1135–1145
Pohlman RF, Fedoroff NV, Messing J (1984) The nucleotide sequence of the maize controlling element Activator. Cell 37:635–643
Raboy V, Kim H-Y, Schiefelbein JW, Nelson Jr OE (1989) Deletions in a dSpm insert in a maize bronze-1 allele alter RNA processing and gene expression. Genetics 122:695–703
Raina R, Schlappi M, Karunanandaa B, Elhofy A, Fedoroff N (1998) Concerted formation of macromolecular Suppressor-mutator transposition complexes. Proc Natl Acad Sci USA 95:8526–8531
Robertson DS (1978) Characterization of a mutator system in maize. Mutat Res 51:21–28
Schiefelbein JW, Raboy V, Fedoroff NV, Nelson Jr OE (1985) Deletions within a defective Suppressor-mutator element in maize affect the frequency and development timing of its excision from the bronze locus. Proc Natl Acad Sci USA 82:4783–4787
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
Schwarz-Sommer Z, Gierl A, Berndtgen R, Saedler H (1985) Sequence comparison of “states” of a1-m1 suggests a model of Spm (En) action. EMBO J 4:2439–2443
Schwarz-Sommer Z, Shepherd N, Tacke E, Gierl A, Rhode W, Leclercq L, Mattes M, Berndtgen R, Peterson PA, Saedler H (1987) Influence of transposable elements on the structure and function of the A1 gene of Zea mays. EMBO J 6:287–294
Tacke E, Schwarz-Sommer Z, Peterson PA, Saedler H (1986) Molecular analysis of states of the A1 locus of Zea mays . Maydica 31:83–91
Weil CF, Marillonnet S, Burr B, Wessler SR (1992) Changes in state of the wx-m5 allele of maize are due to intragenic transposition of Ds. Genetics 130:175–185
Acknowledgements
The authors would like to thank Karen Price, Dr. Xiang-Gan Li, Jian-Bo Zhang, Pei-Fen Zhang, Yong-Li Xiao, Dr. Lyuda Sidorenko, Chen-Wen Zhu, Joann Dieter, and Dr. Brian Scheffler for their technical help and discussions. The authors are grateful to Dr. Tom Peterson for use of his laboratory in the early stages of this study. Special thanks are given to Dr. Alfons Gierl for kindly providing the A2 probe. Journal paper# J-17333 of Iowa Agriculture and Home Economics Experiment Station, Ames, Iowa 50011, USA, Project 3176.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.-A. Grandbastien
Rights and permissions
About this article
Cite this article
Chang, RY., Chopra, S. & Peterson, P.A. Differential excision patterns of the En-transposable element at the A2 locus in maize relate to the insertion site. Mol Genet Genomics 274, 189–195 (2005). https://doi.org/10.1007/s00438-005-0009-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-005-0009-4