Somatic and Germinal Mobility of the RescueMu Transposon in Transgenic Maize

RescueMu, a Mu1 element containing a bacterial plasmid, is mobilized by MuDR in transgenic maize. Somatic excision from a cell-autonomous marker gene yields >90% single cell sectors; empty donor sites often have deletions and insertions, including up to 210 bp of RescueMu/Mu1 terminal DNA. Late somatic insertions are contemporaneous with excisions, suggesting that “cut-and-paste” transposition occurs in the soma. During reproduction, RescueMu transposes infrequently from the initial transgene array, but once transposed, RescueMu is suitable for high throughput gene mutation and cloning. As with MuDR/Mu elements, heritable RescueMu insertions are not associated with excisions. Both somatic and germinal RescueMu insertions occur preferentially into genes and gene-like sequences, but they exhibit weak target site preferences. New insights into Mu behaviors are discussed with reference to two models proposed to explain the alternative outcomes of somatic and germinal events: a switch from somatic cut-and-paste to germinal replicative transposition or to host-mediated gap repair from sister chromatids.

[1]  D. Robertson.  Characterization of a mutator system in maize , 1978 .

[2]  L. Hirth,et al.  Nucleotide sequence of cauliflower mosaic virus DNA , 1980, Cell.

[3]  D. Robertson.  Mutator Activity in Maize: Timing of Its Activation in Ontogeny , 1981, Science.

[4]  J. Bennetzen,et al.  Nucleotide sequence of the maize transposable element Mul. , 1984, Nucleic acids research.

[5]  V. Walbot,et al.  A deletion adjacent to the maize transposable element Mu‐1 accompanies loss of Adh1 expression. , 1985, The EMBO journal.

[6]  H. Saedler,et al.  Plant transposable elements generate the DNA sequence diversity needed in evolution , 1985, The EMBO journal.

[7]  M. Freeling,et al.  The Mu transposable elements of maize: evidence for transposition and copy number regulation during development. , 1986, Genetics.

[8]  M. Freeling,et al.  An extrachromosomal form of the Mu transposons of maize. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Hildebrand,et al.  Design and construction of a versatile system for the expression of foreign genes in plants. , 1987, Gene.

[10]  V. Walbot,et al.  Cloning of a mutable bz2 allele of maize by transposon tagging and differential hybridization. , 1987, Genetics.

[11]  D. Robertson,et al.  Molecular Analysis of viviparous-1: An Abscisic Acid-Insensitive Mutant of Maize. , 1989, The Plant cell.

[12]  S. Wessler,et al.  Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[13]  V. Walbot,et al.  Insertion of Mu1 elements in the first intron of the Adh1-S gene of maize results in novel RNA processing events. , 1990, The Plant cell.

[14]  V. Walbot,et al.  Regulation of the timing of transposable element excision during maize development. , 1990, Science.

[15]  S. Wessler,et al.  A Regulatory Gene as a Novel Visible Marker for Maize Transformation , 1990, Science.

[16]  P. Lemaux,et al.  Transformation of Maize Cells and Regeneration of Fertile Transgenic Plants. , 1990, The Plant cell.

[17]  J. Vieira,et al.  New pUC-derived cloning vectors with different selectable markers and DNA replication origins. , 1991, Gene.

[18]  D. Robertson,et al.  Cloning of the Mutator transposable element MuA2, a putative regulator of somatic mutability of the a1-Mum2 allele in maize. , 1991, Genetics.

[19]  A. Barkan,et al.  Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[20]  V. Walbot,et al.  Mutator activity in maize correlates with the presence and expression of the Mu transposable element Mu9. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Freeling,et al.  Identification of a regulatory transposon that controls the Mutator transposable element system in maize. , 1991, Genetics.

[22]  Vieira Jeffrey,et al.  New pUC-derived cloning vectors with different selectable markers and DNA replication origins. , 1991 .

[23]  A. Doseff,et al.  Somatic excision of the Mu1 transposable element of maize. , 1991, Nucleic acids research.

[24]  V. Walbot.  The Mutator transposable element family of maize. , 1991, Genetic engineering.

[25]  S. Hake,et al.  Active Mutator elements suppress the knotted phenotype and increase recombination at the Kn1-O tandem duplication. , 1992, Genetics.

[26]  V. Chandler,et al.  The Mu elements of Zea mays. , 1992, Advances in genetics.

[27]  J. Bennetzen,et al.  Specificity and regulation of the Mutator transposable element system in maize , 1993 .

[28]  M. Freeling,et al.  Loss of mutator activity in a minimal line , 1994 .

[29]  R. Martienssen,et al.  Coordinate suppression of mutations caused by Robertson's mutator transposons in maize. , 1994, Genetics.

[30]  S. Dellaporta.  Plant DNA Miniprep and Microprep: Versions 2.1–2.3 , 1994 .

[31]  C. A. Warren,et al.  Southern Blots of Maize Genomic DNA , 1994 .

[32]  C. Armstrong.  Regeneration of Plants from Somatic Cell Cultures: Applications for in vitro Genetic Manipulation , 1994 .

[33]  V. Walbot,et al.  Characterization of the major transcripts encoded by the regulatory MuDR transposable element of maize. , 1995, Genetics.

[34]  N. Craig.  Unity in Transposition Reactions , 1995, Science.

[35]  M. Freeling,et al.  Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. , 1995, Genetics.

[36]  M. Freeling,et al.  Tissue-specific accumulation of MURB, a protein encoded by MuDR, the autonomous regulator of the Mutator transposable element family. , 1995, The Plant cell.

[37]  R. Martienssen,et al.  Site-selected transposon mutagenesis at the hcf106 locus in maize. , 1995, The Plant cell.

[38]  D. Weaver,et al.  What to do at an end: DNA double-strand-break repair. , 1995, Trends in genetics : TIG.

[39]  J. Bennetzen,et al.  Mu1-related transposable elements of maize preferentially insert into low copy number DNA. , 1995, Genetics.

[40]  S. Krimigis,et al.  Electron Beams and Ion Composition Measured at Io and in Its Torus , 1996, Science.

[41]  D. Rio,et al.  Drosophila IRBP/Ku p70 corresponds to the mutagen-sensitive mus309 gene and is involved in P-element excision in vivo. , 1996, Genes & development.

[42]  N. Craig,et al.  Switching from Cut-and-Paste to Replicative Tn7 Transposition , 1996, Science.

[43]  C. Weil,et al.  Adjacent sequences influence DNA repair accompanying transposon excision in maize. , 1996, Genetics.

[44]  J. Bennetzen.  The Mutator transposable element system of maize. , 1996, Current topics in microbiology and immunology.

[45]  P. Schnable,et al.  DNA sequence analyses support the role of interrupted gap repair in the origin of internal deletions of the maize transposon, MuDR. , 1996, Genetics.

[46]  J. Bennetzen,et al.  Nested Retrotransposons in the Intergenic Regions of the Maize Genome , 1996, Science.

[47]  H. Dooner,et al.  Germinal excisions of the maize transposon activator do not stimulate meiotic recombination or homology-dependent repair at the bz locus. , 1997, Genetics.

[48]  D. Rio,et al.  Drosophila P-element transposase is a novel site-specific endonuclease. , 1997, Genes & development.

[49]  V. Gorbunova,et al.  Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. , 1997, Nucleic acids research.

[50]  V. Walbot,et al.  Characterization of the maize Mutator transposable element MURA transposase as a DNA-binding protein , 1997, Molecular and cellular biology.

[51]  S. Briggs,et al.  A Porphyrin Pathway Impairment Is Responsible for the Phenotype of a Dominant Disease Lesion Mimic Mutant of Maize , 1998, Plant Cell.

[52]  W. Stiekema,et al.  A Two-Component Enhancer-Inhibitor Transposon Mutagenesis System for Functional Analysis of the Arabidopsis Genome , 1999, Plant Cell.

[53]  V. Sundaresan,et al.  Analysis of Flanking Sequences from Dissociation Insertion Lines: A Database for Reverse Genetics in Arabidopsis , 1999, Plant Cell.

[54]  H. Dooner,et al.  Origination of Ds elements from Ac elements in maize: evidence for rare repair synthesis at the site of Ac excision. , 1999, Genetics.

[55]  L. Girard,et al.  Functional analysis of deletion derivatives of the maize transposon MuDR delineates roles for the MURA and MURB proteins. , 1999, Genetics.

[56]  V. Walbot,et al.  The Late Developmental Pattern of Mu Transposon Excision Is Conferred by a Cauliflower Mosaic Virus 35S–Driven MURA cDNA in Transgenic Maize , 2000, Plant Cell.

[57]  J. Haber.  Partners and pathwaysrepairing a double-strand break. , 2000, Trends in genetics : TIG.

[58]  K. Edwards,et al.  Identification of transposon-tagged genes by the random sequencing of Mutator-tagged DNA fragments from Zea mays. , 2000, The Plant journal : for cell and molecular biology.

[59]  A. Levy,et al.  Analysis of extrachromosomal Ac/Ds transposable elements. , 2000, Genetics.

[60]  G. Bernardi,et al.  Two classes of genes in plants. , 2000, Genetics.

[61]  A maize MuDR transposon promoter shows limited autoregulation , 2001, Molecular Genetics and Genomics.

[62]  V. Walbot,et al.  Expression and Post-Transcriptional Regulation of Maize Transposable Element MuDR and Its Derivatives , 2001, Plant Cell.

[63]  V. Walbot,et al.  The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs. , 2008, The Plant journal : for cell and molecular biology.