Mechanisms of T-DNA integration

  • Alicja Ziemienowicz
  • Tzvi Tzfira
  • Barbara Hohn

T-DNA integration is the final step of the transformation process. During this step, the T-DNA, which traveled as a single-stranded DNA molecule from the bacterial cell through the host-cell cytoplasm into the nucleus, must covalently attach itself to the host cell’s double-stranded genomic DNA. To fulfil its destiny, the T-DNA needs to be directed to its point of integration in the host genome, to be stripped of some, if not all, of its bacterial and host escorting proteins, and to interact with and co-opt the host's DNA-repair proteins and machinery for its complementation into a double-stranded DNA molecule during its integration into the host genome. In the following chapter, we describe the current knowledge on the functions performed by the bacterial and host proteins, and the role that the host genome may play, during the integration process. We also present the dominant models used today to explain the complex mechanism of T-DNA integration in plant cells.


Host Genome Chromatin Assembly Factor ssDNA Molecule VirD2 Protein Human Immunodeficiency Virus Integrase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

8 References

  1. Abu-Arish A, Frenkiel-Krispin D, Fricke T, Tzfira T, Citovsky V, Grayer Wolf S, Elbaum M (2004) Three-dimensional reconstruction of Agrobacterium VirE2 protein with single-stranded DNA. J Biol Chem 279: 25359-25363PubMedCrossRefGoogle Scholar
  2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657PubMedCrossRefGoogle Scholar
  3. Ambros PF, Matzke AJ, Matzke MA (1986) Localization of Agrobacterium rhizogenes T-DNA in plant chromosomes by in situ hybridization. EMBO J 5: 2073-2077PubMedGoogle Scholar
  4. An S, Park S, Jeong DH, Lee DY, Kang HG, Yu JH, Hur J, Kim SR, Kim YH, Lee M, Han S, Kim SJ, Yang J, Kim E, Wi SJ, Chung HS, Hong JP, Choe V, Lee HK, Choi JH, Nam J, Park PB, Park KY, Kim WT, Choe S, Lee CB, An G (2003) Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol 133: 2040-2047PubMedCrossRefGoogle Scholar
  5. Anand A, Krichevsky A, Schornack S, Lahaye T, Tzfira T, Tang Y, Citovsky V, Mysore KS (2007) Arabidopsis VirE2 interacting protein2 is required for Agrobacterium T-DNA Integration in Plants. Plant Cell 19: 1695-1708PubMedCrossRefGoogle Scholar
  6. Babiychuk E, Cottrill PB, Storozhenko S, Fuangthong M, Chen Y, O’Farrell MK, Van Montagu M, Inze D, Kushnir S (1998) Higher plants possess two struc-turally different poly(ADP-ribose) polymerases. Plant J 15: 635-645PubMedCrossRefGoogle Scholar
  7. Bakkeren G, Koukolikova-Nicola Z, Grimsley N, Hohn B (1989) Recovery of Agrobacterium tumefaciens T-DNA molecules from whole plants early after transfer. Cell 57: 847-857PubMedCrossRefGoogle Scholar
  8. Bako L, Umeda M, Tiburcio AF, Schell J, Koncz C (2003) The VirD2 pilot protein of Agrobacterium-transferred DNA interacts with the TATA box-binding protein and a nuclear protein kinase in plants. Proc Natl Acad Sci USA 100: 10108-10113PubMedCrossRefGoogle Scholar
  9. Ballas N, Citovsky V (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc Natl Acad Sci USA 94: 10723-10728PubMedCrossRefGoogle Scholar
  10. Bebenek K, Kunkel TA (2004) Functions of DNA polymerases. Adv Protein Chem 69: 137-165PubMedCrossRefGoogle Scholar
  11. Blobel G (1985) Gene gating: a hypothesis. Proc Natl Acad Sci USA 82: 8527-8529PubMedCrossRefGoogle Scholar
  12. Boulton SJ, Jackson SP (1998) Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J 17: 1819-1828PubMedCrossRefGoogle Scholar
  13. Bray CM, West CE (2005) DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity. New Phytol 168: 511-528PubMedCrossRefGoogle Scholar
  14. Brunaud V, Balzergue S, Dubreucq B, Aubourg S, Samson F, Chauvin S, Bechtold N, Cruaud C, DeRose R, Pelletier G, Lepiniec L, Caboche M, Lecharny A (2002) T-DNA integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep 3: 1152-1157PubMedCrossRefGoogle Scholar
  15. Bundock P, den Dulk-Ras A, Beijersbergen A, Hooykaas PJJ (1995) Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14: 3206-3214PubMedGoogle Scholar
  16. Bundock P, Hooykaas PJJ (1996) Integration of Agrobacterium tumefaciens T-DNA in the Saccharomyces cerevisiae genome by illegitimate recombination. Proc Natl Acad Sci USA 93: 15272-15275PubMedCrossRefGoogle Scholar
  17. Bundock P, van Attikum H, den Dulk-Ras A, Hooykaas PJ (2002) Insertional mutagenesis in yeasts using T-DNA from Agrobacterium tumefaciens. Yeast 19: 529-536PubMedCrossRefGoogle Scholar
  18. Butaye KM, Goderis IJ, Wouters PF, Pues JM, Delaure SL, Broekaert WF, Depicker A, Cammue BP, De Bolle MF (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J 39: 440-449PubMedCrossRefGoogle Scholar
  19. Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin JC, Hurt EC, Nehrbass U (2006) SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441: 770-773PubMedCrossRefGoogle Scholar
  20. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA (2004) Genome-wide localization of the nuclear transport machinery couples trans-criptional status and nuclear organization. Cell 117: 427-439PubMedCrossRefGoogle Scholar
  21. Chen S, Jin W, Wang M, Zhang F, Zhou J, Jia Q, Wu Y, Liu F, Wu P (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J 36: 105-113PubMedCrossRefGoogle Scholar
  22. Chilton M-D, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133: 956-965PubMedCrossRefGoogle Scholar
  23. Chyi YS, Jorgensen RA, Goldstein D, Tanksley SD, Loaiza-Figueroa F (1986) Locations and stability of Agrobacterium-mediated T-DNA insertions in the Lycopersicon genome. Mol Gen Genet 204: 64-69CrossRefGoogle Scholar
  24. Citovsky V, Guralnick B, Simon MN, Wall JS (1997) The molecular structure of Agrobacterium VirE2-single stranded DNA complexes involved in nuclear import. J Mol Biol 271: 718-727PubMedCrossRefGoogle Scholar
  25. Citovsky V, Kozlovsky SV, Lacroix B, Zaltsman A, Dafny-Yelin M, Vyas S, Tovkach A, Tzfira T (2007) Biological systems of the host cell involved in Agrobacterium infection. Cell Microbiol 9: 9-20PubMedCrossRefGoogle Scholar
  26. Ciuffi A, Llano M, Poeschla E, Hoffmann C, Leipzig J, Shinn P, Ecker JR, Bushman F (2005) A role for LEDGF/p75 in targeting HIV DNA integration. Nat Med 11: 1287-1289PubMedCrossRefGoogle Scholar
  27. Daniel PP, Bryant JA (1985) DNA ligase in pea (Pisum sativum L.) seedlings: changes in activity during germination and effects of deoxyribonucleotides. J Exp Bot 39: 481-486CrossRefGoogle Scholar
  28. De Bolle MF, Butaye KM, Goderis IJ, Wouters PF, Jacobs A, Delaure SL, Depicker A, Cammue BP (2006) The influence of matrix attachment regions on transgene expression in Arabidopsis thaliana wild type and gene silencing mutants. Plant Mol Biol 63: 533-543CrossRefGoogle Scholar
  29. De Buck S, Jacobs A, Van Montagu M, Depicker A (1999) The DNA sequences of T-DNA junctions suggest that complex T-DNA loci are formed by a recombination process resembling T-DNA integration. Plant J 20: 295-304PubMedCrossRefGoogle Scholar
  30. De Neve M, De Buck S, Jacobs A, Van Montagu M, Depicker A (1997) T-DNA integration patterns in co-transformed plant cells suggest that T-DNA repeats originate from co-integration of separate T-DNAs. Plant J 11: 15-29PubMedCrossRefGoogle Scholar
  31. Deng W, Chen L, Wood DW, Metcalfe T, Liang X, Gordon MP, Comai L, Nester EW (1998) Agrobacterium VirD2 protein interacts with plant host cyclophilins. Proc Natl Acad Sci USA 95: 7040-7045PubMedCrossRefGoogle Scholar
  32. Dominguez A, Fagoaga C, Navarro L, Moreno P, Pena L (2002) Regeneration of transgenic citrus plants under non selective conditions results in high-frequency recovery of plants with silenced transgenes. Mol Genet Genomics 267: 544-556PubMedCrossRefGoogle Scholar
  33. Dunoyer P, Himber C, Voinnet O (2006) Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections. Nat Genet 38: 258-263PubMedCrossRefGoogle Scholar
  34. Elmayan T, Balzergue S, Beon F, Bourdon V, Daubremet J, Guenet Y, Mourrain P, Palauqui JC, Vernhettes S, Vialle T, Wostrikoff K, Vaucheret H (1998) Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747-1758PubMedCrossRefGoogle Scholar
  35. Endo M, Ishikawa Y, Osakabe K, Nakayama S, Kaya H, Araki T, Shibahara K, Abe K, Ichikawa H, Valentine L, Hohn B, Toki S (2006) Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO J 25: 5579-5590PubMedCrossRefGoogle Scholar
  36. Ferreira PC, Hemerly AS, Engler JD, van Montagu M, Engler G, Inze D (1994) Developmental expression of the Arabidopsis cyclin gene cyc1At. Plant Cell 6: 1763-1774PubMedCrossRefGoogle Scholar
  37. Forsbach A, Schubert D, Lechtenberg B, Gils M, Schmidt R (2003) A comprehensive characterization of single-copy T-DNA insertions in the Arabidopsis thaliana genome. Plant Mol Biol 52: 161-176PubMedCrossRefGoogle Scholar
  38. Francis KE, Spiker S (2005) Identification of Arabidopsis thaliana transformants without selection reveals a high occurrence of silenced T-DNA integrations. Plant J 41: 464-477PubMedCrossRefGoogle Scholar
  39. Friesner J, Britt AB (2003) Ku80- and DNA ligase IV-deficient plants are sensitive to ionizing radiation and defective in T-DNA integration. Plant J 34: 427-440PubMedCrossRefGoogle Scholar
  40. Fritsch O, Benvenuto G, Bowler C, Molinier J, Hohn B (2004) The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol Cell 16: 479-485PubMedCrossRefGoogle Scholar
  41. Gallego ME, Bleuyard JY, Daoudal-Cotterell S, Jallut N, White CI (2003) Ku80 plays a role in non-homologous recombination but is not required for T-DNA integration in Arabidopsis. Plant J 35: 557-565PubMedCrossRefGoogle Scholar
  42. Garcia-Rodriguez FM, Schrammeijer B, Hooykaas PJ (2006) The Agrobacterium VirE3 effector protein: a potential plant transcriptional activator. Nucleic Acids Res 34: 6496-6504PubMedCrossRefGoogle Scholar
  43. Gelvin SB (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51: 223-256PubMedCrossRefGoogle Scholar
  44. Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67: 16-37PubMedCrossRefGoogle Scholar
  45. Gelvin SB, Kim SI (2007) Effect of chromatin upon Agrobacterium T-DNA integration and transgene expression. Biochim Biophys Acta 1769: 409-420Google Scholar
  46. Gheysen G, Villarroel R, Van Montagu M (1991) Illegitimate recombination in plants: a model for T-DNA integration. Genes Dev 5: 287-297PubMedCrossRefGoogle Scholar
  47. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92-100PubMedCrossRefGoogle Scholar
  48. Gorbunova V, Levy AA (1997) Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. Nucleic Acids Res 25: 4650-4657PubMedCrossRefGoogle Scholar
  49. Haber JE (2000) Lucky breaks: analysis of recombination in Saccharomyces. Mutat Res 451: 53-69PubMedGoogle Scholar
  50. Herman L, Jacobs A, Van Montagu M, Depicker A (1990) Plant chromosome/ marker gene fusion assay for study of normal and truncated T-DNA integration events. Mol Gen Genet 224: 248-256PubMedCrossRefGoogle Scholar
  51. Jacque JM, Stevenson M (2006) The inner-nuclear-envelope protein emerin regulates HIV-1 infectivity. Nature 441: 641-645PubMedCrossRefGoogle Scholar
  52. Journin L, Bouchezs D, Drong RF, Tepfer D, Slightom JL (1989) Analysis of TR-DNA/plant junctions in the genome of Convolvulus arvensis clone transformed by Agrobacterium rhizogenes strain A4. Plant Mol Biol 12: 72-85Google Scholar
  53. Kalpana GV, Marmon S, Wang W, Crabtree GR, Goff SP (1994) Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266: 2002-2006PubMedCrossRefGoogle Scholar
  54. Kato M, Takashima K, Kakutani T (2004) Epigenetic control of CACTA transposon mobility in Arabidopsis thaliana. Genetics 168: 961-969PubMedCrossRefGoogle Scholar
  55. Kertbundit S, De Greve H, Deboeck F, Van Montagu M, Hernalsteens JP (1991) In vivo random beta-glucuronidase gene fusions in Arabidopsis thaliana. Proc Natl Acad Sci USA 88: 5212-5216PubMedCrossRefGoogle Scholar
  56. Kim S-I, Veena, Gelvin SB (2007) Genome-wide analysis of Agrobacterium T-DNA integration sites in the Arabidopsis genome generated under non-selective conditions. Plant J 51: 779-791PubMedCrossRefGoogle Scholar
  57. Kirik A, Pecinka A, Wendeler E, Reiss B (2006) The chromatin assembly factor subunit FASCIATA1 is involved in homologous recombination in plants. Plant Cell 18: 2431-2442PubMedCrossRefGoogle Scholar
  58. Kohler F, Cardon G, Pohlman M, Gill R, Schieder O (1989) Enhancement of transformation rates in higher plants by low-dose irradiation: are DNA repair systems involved in the incorporation of exogenous DNA into the plant genome? Plant Mol Biol 12: 189-199CrossRefGoogle Scholar
  59. Koncz C, Martini N, Mayerhofer R, Koncz-Kalman Z, Korber H, Redei GP, Schell J (1989) High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci USA 86: 8467-8471PubMedCrossRefGoogle Scholar
  60. Krizkova L, Hrouda M (1998) Direct repeats of T-DNA integrated in tobacco chromosome: characterization of junction regions. Plant J 16: 673-680PubMedCrossRefGoogle Scholar
  61. Kumar S, Fladung M (2002) Transgene integration in aspen: structures of integration sites and mechanism of T-DNA integration. Plant J 31: 543-551PubMedCrossRefGoogle Scholar
  62. Lacroix B, Tzfira T, Vainstein A, Citovsky V (2006) A case of promiscuity: Agrobacterium’s endless hunt for new partners. Trends Genet 22: 29-37PubMedCrossRefGoogle Scholar
  63. Leskov KS, Criswell T, Antonio S, Li J, Yang CR, Kinsella TJ, Boothman DA (2001) When X-ray-inducible proteins meet DNA double strand break repair. Semin Radiat Oncol 11: 352-372PubMedCrossRefGoogle Scholar
  64. Lewinski MK, Yamashita M, Emerman M, Ciuffi A, Marshall H, Crawford G, Collins F, Shinn P, Leipzig J, Hannenhalli S, Berry CC, Ecker JR, Bushman FD (2006) Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog 2: e60PubMedCrossRefGoogle Scholar
  65. Lewis LK, Resnick MA (2000) Tying up loose ends: nonhomologous end-joining in Saccharomyces cerevisiae. Mutat Res 451: 71-89PubMedGoogle Scholar
  66. Li J, Krichevsky A, Vaidya M, Tzfira T, Citovsky V (2005a) Uncoupling of the functions of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc Natl Acad Sci USA 102: 5733-5738PubMedCrossRefGoogle Scholar
  67. Li J, Vaidya M, White C, Vainstein A, Citovsky V, Tzfira T (2005b) Involvement of KU80 in T-DNA integration in plant cells. Proc Natl Acad Sci USA 102: 19231-19236PubMedCrossRefGoogle Scholar
  68. Li Y, Rosso MG, Ulker B, Weisshaar B (2006) Analysis of T-DNA insertion site distribution patterns in Arabidopsis thaliana reveals special features of genes without insertions. Genomics 87: 645-652PubMedCrossRefGoogle Scholar
  69. Loyter A, Rosenbluh J, Zakai N, Li J, Kozlovsky SV, Tzfira T, Citovsky V (2005) The plant VirE2 interacting protein 1. A molecular link between the Agrobacterium T-complex and the host cell chromatin? Plant Physiol 138: 1318-1321PubMedCrossRefGoogle Scholar
  70. Luthra R, Kerr SC, Harreman MT, Apponi LH, Fasken MB, Ramineni S, Chaurasia S, Valentini SR, Corbett AH (2007) Actively transcribed GAL genes can be physically linked to the nuclear pore by the SAGA chromatin modifying complex. J Biol Chem 282: 3042-3049PubMedCrossRefGoogle Scholar
  71. Makarevitch I, Somers DA (2006) Association of Arabidopsis topoisomerase IIA cleavage sites with functional genomic elements and T-DNA loci. Plant J 48: 697-709PubMedCrossRefGoogle Scholar
  72. Martinez JJ, Seveau S, Veiga E, Matsuyama S, Cossart P (2005) Ku70, a component of DNA-dependent protein kinase, is a mammalian receptor for Rickettsia conorii. Cell 123: 1013-1023PubMedCrossRefGoogle Scholar
  73. Mayerhofer R, Koncz-Kalman Z, Nawrath C, Bakkeren G, Crameri A, Angelis K, Redei GP, Schell J, Hohn B, Koncz C (1991) T-DNA integration: a mode of illegitimate recombination in plants. EMBO J 10: 697-704PubMedGoogle Scholar
  74. Michielse CB, Hooykaas PJ, van den Hondel CA, Ram AF (2005) Agrobacterium-mediated transformation as a tool for functional genomics in fungi. Curr Genet 48: 1-17PubMedCrossRefGoogle Scholar
  75. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, Ecker JR, Bushman FD (2004) Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2: E234PubMedCrossRefGoogle Scholar
  76. Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retro-transposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15: 1771-1780PubMedCrossRefGoogle Scholar
  77. Montague JW, Hughes FM, Jr., Cidlowski JA (1997) Native recombinant cyclophilins A, B, and C degrade DNA independently of peptidylprolyl cistrans-isomerase activity. Potential roles of cyclophilins in apoptosis. J Biol Chem 272: 6677-6684PubMedCrossRefGoogle Scholar
  78. Muller AE, Atkinson RG, Sandoval RB, Jorgensen RA (2007) Microhomologies between T-DNA ends and target sites often occur in inverted orientation and may be responsible for the high frequency of T-DNA-associated inversions. Plant Cell Rep 26: 617-630PubMedCrossRefGoogle Scholar
  79. Mysore KS, Kumar CTR, Gelvin SB (2000a) Arabidopsis ecotypes and mutants that are recalcitrant to Agrobacterium root transformation are susceptible to germ-line transformation. Plant J 21: 9-16PubMedCrossRefGoogle Scholar
  80. Mysore KS, Nam J, Gelvin SB (2000b) An Arabidopsis histone H2A mutant is deficient in Agrobacterium T-DNA integration. Proc Natl Acad Sci USA 97: 948-953PubMedCrossRefGoogle Scholar
  81. Nam J, Matthysse AG, Gelvin SB (1997) Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. Plant Cell 9: 317-333PubMedCrossRefGoogle Scholar
  82. Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436: 1053-1057PubMedCrossRefGoogle Scholar
  83. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313: 848-851PubMedCrossRefGoogle Scholar
  84. Offringa R, de Groot MJA, Haagsman HJ, Does MP, van den Elzen PJM, Hooykaas PJJ (1990) Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium mediated transformation. EMBO J 9: 3077-3084PubMedGoogle Scholar
  85. Pansegrau W, Schoumacher F, Hohn B, Lanka E (1993) Site-specific cleavage and joining of single-stranded DNA by VirD2 protein of Agrobacterium tumefaciens Ti plasmids: analogy to bacterial conjugation. Proc Natl Acad Sci USA 90: 11538-11542PubMedCrossRefGoogle Scholar
  86. Paszkowski J, Baur M, Bogucki A, Potrykus I (1988) Gene targeting in plants. EMBO J 7: 4021-4026PubMedGoogle Scholar
  87. Pelczar P, Kalck V, Gomez D, Hohn B (2004) Agrobacterium proteins VirD2 and VirE2 mediate precise integration of synthetic T-DNA complexes in mammalian cells. EMBO Rep 5: 632-637PubMedCrossRefGoogle Scholar
  88. Riha K, Watson JM, Parkey J, Shippen DE (2002) Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J 21: 2819-2826PubMedCrossRefGoogle Scholar
  89. Rodenburg KW, de Groot MJ, Schilperoort RA, Hooykaas PJ (1989) Single-stranded DNA used as an efficient new vehicle for transformation of plant protoplasts. Plant Mol Biol 13: 711-719PubMedCrossRefGoogle Scholar
  90. Rodriguez-Navarro S, Fischer T, Luo MJ, Antunez O, Brettschneider S, Lechner J, Perez-Ortin JE, Reed R, Hurt E (2004) Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116: 75-86PubMedCrossRefGoogle Scholar
  91. Rossi L, Hohn B, Tinland B (1996) Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc Natl Acad Sci USA 93: 126-130PubMedCrossRefGoogle Scholar
  92. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53: 247-259PubMedCrossRefGoogle Scholar
  93. Sallaud C, Gay C, Larmande P, Bes M, Piffanelli P, Piegu B, Droc G, Regad F, Bourgeois E, Meynard D, Perin C, Sabau X, Ghesquiere A, Glaszmann JC, Delseny M, Guiderdoni E (2004) High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. Plant J 39: 450-464PubMedCrossRefGoogle Scholar
  94. Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17: 6086-6095PubMedCrossRefGoogle Scholar
  95. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85PubMedCrossRefGoogle Scholar
  96. Schmid M, Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli UK (2006) Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol Cell 21: 379-391PubMedCrossRefGoogle Scholar
  97. Schneeberger RG, Zhang K, Tatarinova T, Troukhan M, Kwok SF, Drais J, Klinger K, Orejudos F, Macy K, Bhakta A, Burns J, Subramanian G, Donson J, Flavell R, Feldmann KA (2005) Agrobacterium T-DNA integration in Arabidopsis is correlated with DNA sequence compositions that occur frequently in gene promoter regions. Funct Integr Genomics 5: 240-253PubMedCrossRefGoogle Scholar
  98. Schubert D, Lechtenberg B, Forsbach A, Gils M, Bahadur S, Schmidt R (2004) Silencing in Arabidopsis T-DNA transformants: the predominant role of a gene-specific RNA sensing mechanism versus position effects. Plant Cell 16: 2561-2572PubMedCrossRefGoogle Scholar
  99. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, Clarke JD, Cotton D, Bullis D, Snell J, Miguel T, Hutchison D, Kimmerly B, Mitzel T, Katagiri F, Glazebrook J, Law M, Goff SA (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994PubMedCrossRefGoogle Scholar
  100. Sha Y, Li S, Pei Z, Luo L, Tian Y, He C (2004) Generation and flanking sequence analysis of a rice T-DNA tagged population. Theor Appl Genet 108: 306-314PubMedCrossRefGoogle Scholar
  101. Szabados L, Kovacs I, Oberschall A, Abraham E, Kerekes I, Zsigmond L, Nagy R, Alvarado M, Krasovskaja I, Gal M, Berente A, Redei GP, Haim AB, Koncz C (2002) Distribution of 1000 sequenced T-DNA tags in the Arabidopsis genome. Plant J 32: 233-242PubMedCrossRefGoogle Scholar
  102. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser SM (2006) Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441: 774-778PubMedCrossRefGoogle Scholar
  103. Teo SH, Jackson SP (1997) Identification of Saccharomyces cerevisiae DNA ligase IV: involvement in DNA double-strand break repair. EMBO J 16: 4788-4795PubMedCrossRefGoogle Scholar
  104. Timson DJ, Singleton MR, Wigley DB (2000) DNA ligases in the repair and rep-lication of DNA. Mutat Res 460: 301-318PubMedGoogle Scholar
  105. Tinland B (1996) The integration of T-DNA into plant genomes. Trends Plant Sci 1: 178-184CrossRefGoogle Scholar
  106. Tinland B, Hohn B (1995) Recombination between prokaryotic and eukaryotic DNA: integration of Agrobacterium tumefaciens T-DNA into the plant genome. Genet Eng 17: 209-229Google Scholar
  107. Tinland B, Schoumacher F, Gloeckler V, Bravo-Angel AM, Hohn B (1995) The Agrobacterium tumefaciens virulence D2 protein is responsible for precise integration of T-DNA into the plant genome. EMBO J 14: 3585-3595PubMedGoogle Scholar
  108. Tsukamoto Y, Ikeda H (1998) Double-strand break repair mediated by DNA end-joining. Genes Cells 3: 135-144PubMedCrossRefGoogle Scholar
  109. Tzfira T, Citovsky V (2002) Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol 12: 121-129PubMedCrossRefGoogle Scholar
  110. Tzfira T, Frankman LR, Vaidya M, Citovsky V (2003) Site-specific integration of Agrobacterium tumefaciens T-DNA via double-stranded intermediates. Plant Physiol 133: 1011-1023PubMedCrossRefGoogle Scholar
  111. Tzfira T, Li J, Lacroix B, Citovsky V (2004a) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20: 375-383PubMedCrossRefGoogle Scholar
  112. Tzfira T, Vaidya M, Citovsky V (2004b) Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431: 87-92PubMedCrossRefGoogle Scholar
  113. van Attikum H, Bundock P, Hooykaas PJJ (2001) Non-homologous end-joining proteins are required for Agrobacterium T-DNA integration. EMBO J 20: 6550-6558PubMedCrossRefGoogle Scholar
  114. van Attikum H, Bundock P, Overmeer RM, Lee LY, Gelvin SB, Hooykaas PJJ (2003) The Arabidopsis AtLIG4 gene is required for the repair of DNA damage, but not for the integration of Agrobacterium T-DNA. Nucleic Acids Res 31: 4247-4255PubMedCrossRefGoogle Scholar
  115. van Attikum H, Hooykaas PJJ (2003) Genetic requirements for the targeted integration of Agrobacterium T-DNA in Saccharomyces cerevisiae. Nucleic Acids Res 31: 826-832PubMedCrossRefGoogle Scholar
  116. Volokhina I, Chumakov M (2007) Study of the VirE2-ssT-DNA complex formation by scanning probe microscopy and gel electrophoresis- T-complex visualization. Microsc Microanal 13: 51-54PubMedCrossRefGoogle Scholar
  117. Wallroth M, Gerats AGM, Rogers SG, Fraley RT, Horsch RB (1986) Chromosomal localization of foreign genes in Petunia hybrida. Mol Gen Genet 202: 6-15CrossRefGoogle Scholar
  118. West CE, Waterworth WM, Story GW, Sunderland PA, Jiang Q, Bray CM (2002) Disruption of the Arabidopsis AtKu80 gene demonstrates an essential role for AtKu80 protein in efficient repair of DNA double-strand breaks in vivo. Plant J 31: 517-528PubMedCrossRefGoogle Scholar
  119. Weterings E, van Gent DC (2004) The mechanism of non-homologous end-joining: a synopsis of synapsis. DNA Repair (Amst) 3: 1425-1435CrossRefGoogle Scholar
  120. Wu Y-Q (2002) Protein-protein interaction between VirD2 and DNA ligase: an essential step of Agrobacterium tumefaciens T-DNA integration. Ph.D. thesis. University of BaselGoogle Scholar
  121. Wu Y-Q, Hohn B (2003) Cellular transfer and Chromosomal integration of T-DNA during Agrobacterium tumefaciens-mediated plant transformation. In G Stacey, NT Keen, eds, Plant-Microbe Interactions Vol 6, pp 1-18Google Scholar
  122. Yi H, Mysore KS, Gelvin SB (2002) Expression of the Arabidopsis histone H2A-1 gene correlates with susceptibility to Agrobacterium transformation. Plant J 32: 285-298PubMedCrossRefGoogle Scholar
  123. Yi H, Sardesai N, Fujinuma T, Chan CW, Veena, Gelvin SB (2006) Constitutive expression exposes functional redundancy between the Arabidopsis histone H2A gene HTA1 and other H2A gene family members. Plant Cell 18: 1575-1589PubMedCrossRefGoogle Scholar
  124. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Li J, Liu Z, Qi Q, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Zhao W, Li P, Chen W, Zhang Y, Hu J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Tao M, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79-92PubMedCrossRefGoogle Scholar
  125. Zambryski PC (1992) Chronicles from the Agrobacterium-plant cell DNA transfer story. Annu Rev Plant Physiol Plant Mol Biol 43: 465-490CrossRefGoogle Scholar
  126. Zhang J, Guo D, Chang Y, You C, Li X, Dai X, Weng Q, Chen G, Liu H, Han B, Zhang Q, Wu C (2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13 804 T-DNA flanking sequences from an enhancer-trap mutant library. Plant J 49: 947-959PubMedCrossRefGoogle Scholar
  127. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201PubMedCrossRefGoogle Scholar
  128. Zhu Y, Nam J, Humara JM, Mysore KS, Lee LY, Cao H, Valentine L, Li J, Kaiser AD, Kopecky AL, Hwang HH, Bhattacharjee S, Rao PK, Tzfira T, Rajagopal J, Yi H, Veena, Yadav BS, Crane YM, Lin K, Larcher Y, Gelvin MJ, Knue M, Ramos C, Zhao X, Davis SJ, Kim SI, Ranjith-Kumar CT, Choi YJ, Hallan VK, Chattopadhyay S, Sui X, Ziemienowicz A, Matthysse AG, Citovsky V, Hohn B, Gelvin SB (2003) Identification of Arabidopsis rat mutants. Plant Physiol 132: 494-505PubMedCrossRefGoogle Scholar
  129. Ziemienowicz A, Merkle T, Schoumacher F, Hohn B, Rossi L (2001) Import of Agrobacterium T-DNA into plant nuclei: Two distinct functions of VirD2 and VirE2 proteins. Plant Cell 13: 369-384PubMedCrossRefGoogle Scholar
  130. Ziemienowicz A, Tinland B, Bryant J, Gloeckler V, Hohn B (2000) Plant enzymes but not Agrobacterium VirD2 mediate T-DNA ligation in vitro. Mol Cell Biol 20: 6317-6322PubMedCrossRefGoogle Scholar
  131. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdepen-dence between methylation and transcription. Nat Genet 39: 61-69PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Alicja Ziemienowicz
    • 1
  • Tzvi Tzfira
    • 2
  • Barbara Hohn
    • 3
  1. 1.Department of Molecular Genetics, Faculty of Biochemistry, Biophysics and BiotechnologyJagiellonian UniversityKrakowPoland
  2. 2.Department of Molecular, Cellular and Developmental BiologyThe University of MichiganAnn ArborUSA
  3. 3.FMI for Biomedical ResearchBaselSwitzerland

Personalised recommendations