The Agrobacterium Phenotypic Plasticity (Plast) Genes

  • Léon OttenEmail author
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 418)


The transfer of T-DNA sequences from Agrobacterium to plant cells is a well-understood process of natural genetic engineering. The expression of T-DNA genes in plants leads to tumors, hairy roots, or transgenic plants. The transformed cells multiply and synthesize small molecules, called opines, used by Agrobacteria for their growth. Several T-DNA genes stimulate or influence plant growth. Among these, iaaH and iaaM encode proteins involved in auxin synthesis, whereas ipt encodes a protein involved in cytokinin synthesis. Growth can also be induced or modified by other T-DNA genes, collectively called plast genes (for phenotypic plasticity). The plast genes are defined by their common ancestry and are mostly found on T-DNAs. They can influence plant growth in different ways, but the molecular basis of their morphogenetic activity remains largely unclear. Only some plast genes, such as 6b, rolB, rolC, and orf13, have been studied in detail. Plast genes have a significant potential for applied research and may be used to modify the growth of crop plants. In this review, I summarize the most important findings and models from 30 years of plast gene research and propose some outlooks for the future.


  1. Adams EC, Gurley WB (1994) Nuclear protein 780BP from cauliflower binds an element in the 780 gene promoter of T-DNA. Plant Mol Biol 26:377–392PubMedGoogle Scholar
  2. Altabella T, Angel E, Biondi S et al (1995) Effect of the rol genes from Agrobacterium rhizogenes on polyamine metabolism in tobacco roots. Physiol Plant 95:479–485Google Scholar
  3. Altamura MM, Archilletti T, Capone I et al (1991) Histological analysis of the expression of Agrobacterium rhizogenes rolB-GUS gene fusion in transgenic tobacco. New Phytol 118:69–78Google Scholar
  4. Altamura MM, Capitani F, Gazza L et al (1994) The plant oncogene rolB stimulates the formation of flower and root meristemoids in tobacco thin cell layers. New Phytol 126:283–293Google Scholar
  5. Alvarez JP, Furumizu C, Efroni I et al (2016) Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife 5:e15023Google Scholar
  6. Aoki S (2004) Resurrection of an ancestral gene: functional and evolutionary analyses of the Ngrol genes transferred from Agrobacterium to Nicotiana. J Plant Res 117:329–337PubMedGoogle Scholar
  7. Aoki S, Syono K (1999a) Function of Ngrol genes in the evolution of Nicotiana glauca: conservation of the function of NgORF13 and NgORF14 after ancient infection by an Agrobacterium rhizogenes-like ancestor. Plant Cell Physiol 40:222–230Google Scholar
  8. Aoki S, Syono K (1999b) Synergistic function of rolB, rolC, ORF13, and ORF14 of TL-DNA of Agrobacterium rhizogenes in hairy root induction in Nicotiana tabacum. Plant Cell Physiol 40:252–256Google Scholar
  9. Aoki S, Syono K (1999c) Horizontal gene transfer and mutation: Ngrol genes in the genome of Nicotiana glauca. Proc Natl Acad Sci USA 96:13229–13234PubMedGoogle Scholar
  10. Aoki S, Syono K (2000) The roles of Rirol and Ngrol genes in hairy root induction in Nicotiana debneyi. Plant Sci 159:183–189PubMedGoogle Scholar
  11. Aoki S, Kawaoka A, Sekine M et al (1994) Sequence of the cellular T-DNA in the untransformed genome of Nicotiana glauca that is homologous to ORFs 13 and 14 of the Ri plasmid and analysis of its expression in genetic tumors of N. glauca x N. langsdorffii. Mol Gen Genet 243:706–710PubMedPubMedCentralGoogle Scholar
  12. Arshad W, Haq I, Waheed MT et al (2014) Agrobacterium-mediated transformation of tomato with rolB gene results in enhancement of fruit quality and foliar resistance against fungal pathogens. PLoS ONE 9:e96979PubMedPubMedCentralGoogle Scholar
  13. Bagyan IL, Revenkova EV, Kraev AS et al (1994) Functional analysis of the 5’-flanking region of gene 6b from TL-DNA pTiBo542 in transgenic tobacco. Mol Biol 28:487–492Google Scholar
  14. Bagyan IL, Revenkova EV, Pozmogova GE et al (1995) 5′-regulatory region of Agrobacterium tumefaciens T-DNA gene 6b directs organ-specific, wound-inducible and auxin-inducible expression in transgenic tobacco. Plant Mol Biol 29:1299–1304PubMedGoogle Scholar
  15. Barbier-Brygoo H, Maurel C, Shen WH et al (1990) Use of mutants and transformed plants to study the action of auxins. Symp Soc Exp Biol 44:67–77PubMedGoogle Scholar
  16. Baumann K, De Paolis A, Costantino P et al (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11:323–334PubMedPubMedCentralGoogle Scholar
  17. Bellincampi D, Cardarelli M, Zaghi D et al (1996) Oligogalacturonides prevent rhizogenesis in rolB-transformed tobacco explants by inhibiting auxin-induced expression of the rolB gene. Plant Cell 8:477–487PubMedPubMedCentralGoogle Scholar
  18. Bellincampi D, Dipierro N, Salvi G et al (2000) Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol 122:1379–1385PubMedPubMedCentralGoogle Scholar
  19. Bettini P, Baraldi R, Rapparini F et al (2010) The insertion of the Agrobacterium rhizogenes rolC gene in tomato (Solanum lycopersicum L.) affects plant architecture and endogenous auxin and abscisic acid levels. Sci Hortic 123:323–328Google Scholar
  20. Bettini P, Marvasi M, Fabiola F et al (2016) Agrobacterium rhizogenes rolB gene affects photosynthesis and chlorophyll content in transgenic tomato (Solanum lycopersicum L.) plants. J Plant Physiol 204:27–35PubMedGoogle Scholar
  21. Bonnard G, Tinland B, Paulus F et al (1989) Nucleotide sequence, evolutionary origin and biological role of a rearranged cytokinin gene isolated from a wide host range biotype III Agrobacterium strain. Mol Gen Genet 216:428–438PubMedGoogle Scholar
  22. Bouchez D, Camilleri C (1990) Identification of a putative rolB gene on the TR-DNA of the Agrobacterium rhizogenes A4 Ri plasmid. Plant Mol Biol 14:617–619PubMedGoogle Scholar
  23. Bouzar H, Jones JB (2001) Agrobacterium larrymoorei sp. nov., a pathogen isolated from aerial tumours of Ficus benjamina. Int J Syst Evol Microbiol 51:1023–1026PubMedGoogle Scholar
  24. Bresso EG, Chorostecki U, Rodriguez RE et al (2017) Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol. Epub ahead of printGoogle Scholar
  25. Broer I, Dröge-Laser W, Barker RF et al (1995) Identification of the Agrobacterium tumefaciens C58 T-DNA genes e and f and their impact on crown gall tumour formation. Plant Mol Biol 27:41–57PubMedGoogle Scholar
  26. Bruce W, Gurley WB (1987) Functional domains of a T-DNA promoter active in Crown Gall tumors. Mol Cell Biol 7:59–67PubMedPubMedCentralGoogle Scholar
  27. Bruce W, Gurley WB (1988) An enhancer-like element present in the promoter of a T-DNA gene from the Ti plasmid of Agrobacterium tumefaciens. Proc Natl Acad Sci USA 85:4310–4314PubMedGoogle Scholar
  28. Bulgakov VP, Khodakovskaya MV, Labetskaya NV et al (1998) The impact of rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochem 49:1929–1934Google Scholar
  29. Bulgakov VP, Tchernoded GK, Mischenko NP et al (2002) Effect of salicylic acid, methyl jasmonate, ethephon and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with the rolB and rolC genes. J Biotech 97:213–221Google Scholar
  30. Bulgakov VP, Veselova MV, Tchernoded GK et al (2005) Inhibitory effect of the Agrobacterium rhizogenes rolC gene on rabdosiin and rosmarinic acid production in Eritrichium sericeum and Lithospermum erythrorhizon transformed cell cultures. Planta 221:471–478PubMedGoogle Scholar
  31. Bulgakov VP, Kiselev KV, Yakovlev KV et al (2006) Agrobacterium mediated transformation of sea urchin embryos. Biotech J 1:454–461Google Scholar
  32. Bulgakov VP, Shkryl YN, Veremeichik GN et al (2013) Recent advances in the understanding of Agrobacterium rhizogenes-derived genes and their effects on stress resistance and plant metabolism. Adv Biochem Eng Biotech 134:1–22Google Scholar
  33. Bulgakov VP, Veremeichik G, Grigorchuk VP et al (2016) The rolB gene activates secondary metabolism in Arabidopsis calli via selective activation of genes encoding MYB and bHLH transcription factors. Plant Physiol Biochem 102:70–79PubMedGoogle Scholar
  34. Capone I, Spano L, Cardarelli M et al (1989) Induction and growth properties of carrot roots with different complements of Agrobacterium rhizogenes T-DNA. Plant Mol Biol 13:43–52PubMedGoogle Scholar
  35. Capone I, Cardarelli M, Mariotti D et al (1991) Different promoter regions control level and tissue specificity of expression of Agrobacterium rhizogenes rolB gene in plants. Plant Mol Biol 16:427–436PubMedGoogle Scholar
  36. Capone I, Frugis G, Costantino P et al (1994) Expression in different populations of cells of the root meristem is controlled by different domains of the rolB promoter. Plant Mol Biol 25:681–691PubMedGoogle Scholar
  37. Cardarelli M, Mariotti D, Pomponi M et al (1987) Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Mol Gen Genet 210:111–115Google Scholar
  38. Carmi N, Salts Y, Dedicova D et al (2003) Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta 217:726–735PubMedGoogle Scholar
  39. Casanova E, Valdés AE, Zuker A et al (2004) rolC-transgenic carnation plants: adventitious organogenesis and levels of endogenous auxin and cytokinins. Plant Sci 167:551–560Google Scholar
  40. Casanova E, Trillas MI, Moysset L et al (2005) Influence of rol genes in floriculture. Biotech Adv 23:3–39Google Scholar
  41. Cecchetti V, Pomponi M, Altamura MM et al (2004) Expression of rolB in tobacco flowers affects the coordinated processes of anther dehiscence and style elongation. Plant J 38:512–525PubMedGoogle Scholar
  42. Chen K (2016) Sequencing and functional analysis of cT-DNAs in Nicotiana. Thesis, University of StrasbourgGoogle Scholar
  43. Chen K, Otten L (2015) Morphological analysis of the 6b oncogene-induced enation syndrome. Planta 243:131–148PubMedGoogle Scholar
  44. Chen K, Otten L (2017) Natural Agrobacterium transformants: recent results and some theoretical considerations. Front Plant Sci 8:1600PubMedPubMedCentralGoogle Scholar
  45. Chen K, Dorlhac de Borne F, Szegedi E et al (2014) Deep sequencing of the ancestral tobacco species Nicotiana tomentosiformis reveals multiple T-DNA inserts and a complex evolutionary history of natural transformation in the genus Nicotiana. Plant J 80:669–682PubMedGoogle Scholar
  46. Chen K, Dorlhac de Borne F, Julio E et al (2016) Root-specific expression of opine genes and opine accumulation in some cultivars of the naturally occurring GMO Nicotiana tabacum. Plant J 87:258–269PubMedGoogle Scholar
  47. Chen K, Dorlhac de Borne F, Sierro N et al (2018) Organization of the TC and TE cT-DNA regions in Nicotiana otophora and functional analysis of three diverged TE-6b genes. Plant J (in press)Google Scholar
  48. Chichiriccò G, Costantino P, Spanò L (1992) Expression of the rolB oncogene from Agrobacterium rhizogenes during zygotic embryogenesis in tobacco. Plant Cell Physiol 33:827–832Google Scholar
  49. Clément B, Pollmann S, Weiler E et al (2006) The Agrobacterium vitis T-6b oncoprotein induces auxin-independent cell expansion in tobacco. Plant J 45:1017–1027PubMedGoogle Scholar
  50. Clément B, Perot J, Geoffroy P et al (2007) Abnormal accumulation of sugars and phenolics in tobacco roots expressing the Agrobacterium T-6b oncogene and the role of these compounds in 6b-induced growth. Mol Plant-Microbe Interact 20:53–62PubMedGoogle Scholar
  51. Comai L, Kosuge T (1982) Cloning and characterization of iaaM, a virulence determinant of Pseudomonas savastanoi. J Bacteriol 143:950–957Google Scholar
  52. de Groot MJA, Bundock P, Hooykaas PJJ et al (1998) Agrobacterium tumefaciens mediated transformation of filamentous fungi. Nat Biotechnol 16:839–842PubMedGoogle Scholar
  53. De Paolis A, Sabatini S, De Pascalis L et al (1996) A rolB regulatory factor belongs to a new class of single zinc finger plant proteins. Plant J 10:215–223PubMedGoogle Scholar
  54. Dehio C, Schell J (1994) Identification of plant genetic loci involved in a posttranscriptional mechanism for meiotically reversible transgene silencing. Proc Natl Acad Sci USA 91:5538–5542PubMedGoogle Scholar
  55. Delbarre A, Muller P, Imhoff V et al (1994) The rolB gene of Agrobacterium rhizogenes does not increase the auxin sensitivity of tobacco protoplasts by modifying the intracellular auxin concentration. Plant Physiol 105:563–569PubMedPubMedCentralGoogle Scholar
  56. Di Cola A, Poma A, Spano L (1997) rolB expression pattern in the early stages of carrot somatic embryogenesis. Cell Biol Int 21:595–600PubMedGoogle Scholar
  57. Drevet C, Brasileiro AC, Jouanin L (1994) Oncogene arrangement in a shooty strain of Agrobacterium tumefaciens. Plant Mol Biol 25:83–90PubMedGoogle Scholar
  58. Estruch JJ, Parets-Soler A, Schmülling T et al (1991a) Cytosolic localization in transgenic plants of the rolC peptide from Agrobacterium rhizogenes. Plant Mol Biol 17:547–550PubMedGoogle Scholar
  59. Estruch JJ, Chriqui D, Grossmann K et al (1991b) The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. EMBO J 10:2889–2895PubMedPubMedCentralGoogle Scholar
  60. Estruch JJ, Schell J, Spena A (1991c) The protein encoded by the rolB plant oncogene hydrolyses indole glucosides. EMBO J 10:3125–3128PubMedPubMedCentralGoogle Scholar
  61. Faiss M, Strnad M, Redig P et al (1996) Chemically induced expression of the rolC encoded β-glucosidase in transgenic tobacco plants and analysis of cytokinin metabolism: rolC does not hydrolyze endogenous cytokinin glucosides in planta. Plant J 10:33–46Google Scholar
  62. Filippini F, Lo Schiavo F, Terzi M (1994) The plant oncogene rolB alters binding of auxin to plant cell membranes. Plant Cell Physiol 35:767–771Google Scholar
  63. Filippini F, Rossi V, Marin O et al (1996) A plant oncogene as a phosphatase. Nature 379:499–500PubMedGoogle Scholar
  64. Fladung M (1990) Transformation of diploid and tetraploid potato clones with the rolC gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breeding 104:295–304Google Scholar
  65. Fladung M, Ahuja M (1997) Excision of the maize transposable element Ac in periclinal chimeric leaves of 35S-Ac-rolC transgenic aspen-Populus. Plant Mol Biol 33:1097–2003PubMedGoogle Scholar
  66. Fladung M, Gieffers W (1993) Resistance reactions of leaves and tubers of rolC transgenic tetraploid potato to bacterial and fungal pathogenes. Correlations with sugar, starch and chlorophyll content. Phys Mol Plant Physiol 42:123–132Google Scholar
  67. Fladung M, Ballvora A, Schmülling T (1993) Constitutive or light-regulated expression of the rolC gene in transgenic potato plants has different effects on yield attributes and tuber carbohydrate composition. Plant Mol Biol 23:749–757PubMedGoogle Scholar
  68. Fründt C, Meyer AD, Ichikawa T et al (1998) A tobacco homologue of the Ri-plasmid orf13 gene causes cell proliferation in carrot root discs. Mol Gen Genet 259:559–568PubMedGoogle Scholar
  69. Fujii N (1997) Pattern of DNA binding of nuclear proteins to the proximal Agrobacterium rhizogenes rolC promoter is altered during somatic embryogenesis of carrot. Gene 201:55–62PubMedGoogle Scholar
  70. Fujii N, Uchimiya H (1991) Conditions favorable for the somatic embryogenesis in carrot cell culture enhance expression of the rolC promoter-GUS fusion gene. Plant Physiol 95:238–241PubMedPubMedCentralGoogle Scholar
  71. Fujii N, Yokoyama R, Uchimiya H (1994) Analysis of the rolC promoter region involved in somatic embryogenesis-related activation in carrot cell cultures. Plant Physiol 104:1151–1157PubMedPubMedCentralGoogle Scholar
  72. Gális I, Simek P, Macas J et al (1999) The Agrobacterium tumefaciens C58-6b gene confers resistance to N(6)-benzyladenine without modifying cytokinin metabolism in tobacco seedlings. Planta 209:453–461PubMedGoogle Scholar
  73. Gális I, Simek P, Van Onckelen HA et al (2002) Resistance of transgenic tobacco seedlings expressing the Agrobacterium tumefaciens C58-6b gene to growth-inhibitory levels of cytokinin is associated with elevated IAA levels and activation of phenylpropanoid metabolism. Plant Cell Physiol 43:939–950PubMedGoogle Scholar
  74. Gális I, Kakiuchi Y, Simek P et al (2004) Agrobacterium tumefaciens AK-6b gene modulates phenolic compound metabolism in tobacco. Phytochem 65:169–179Google Scholar
  75. Gardner N, Melberg T, George M et al (2006) Differential expression of rolC results in unique plant phenotypes. J Am Soc Hortic Sci 131:82–88Google Scholar
  76. Garfinkel DJ, Simpson RB, Ream LW et al (1981) Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27:143–153PubMedGoogle Scholar
  77. Gelvin SB (2012) Traversing the cell: Agrobacterium T-DNA’s journey to the host genome. Front Plant Sci 26:3–52Google Scholar
  78. Gidoni D, Bar M, Gilboa N (2001) FLP/FRT-mediated restoration of normal phenotypes and clonal sectors formation in rolC transgenic tobacco. Transgenic Res 10:317–328PubMedGoogle Scholar
  79. Gorpenchenko TY, Kiselev KV, Bulgakov VP et al (2006) The Agrobacterium rhizogenes rolC-gene-induced somatic embryogenesis and shoot organogenesis in Panax ginseng transformed calluses. Planta 223:457–467PubMedGoogle Scholar
  80. Graham MW, Craig S, Waterhouse PM (1997) Expression patterns of vascular-specific promoters RolC and Sh in transgenic potatoes and their use in engineering PLRV-resistant plants. Plant Mol Biol 33:729–735PubMedGoogle Scholar
  81. Grémillon L, Helfer A, Clément B et al (2004) New plant growth-modifying properties of the Agrobacterium T-6b oncogene revealed by the use of a dexamethasone-inducible promoter. Plant J 37:218–228PubMedGoogle Scholar
  82. Guivarc’h A, Carneiro M, Vilaine F et al (1996) Tissue-specific expression of the rolA gene mediates morphological changes in transgenic tobacco. Plant Mol Biol 30:125–134PubMedGoogle Scholar
  83. Hack E, Kemp JD (1980) Purification and characterization of the crown gall-specific enzyme, octopine synthase. Plant Physiol 65:949–955PubMedPubMedCentralGoogle Scholar
  84. Hansen G, Larribe M, Vaubert D et al (1991) Agrobacterium rhizogenes pRi8196 T-DNA: mapping and DNA sequence of functions involved in mannopine synthesis and hairy root differentiation. Proc Natl Acad Sci USA 88:7763–7767PubMedGoogle Scholar
  85. Hansen G, Vaubert D, Heron JH et al (1993) Phenotypic effects of overexpression of Agrobacterium rhizogenes T-DNA ORF13 in transgenic tobacco plants are mediated by diffusible factor(s). Plant J 4:581–585Google Scholar
  86. Hansen G, Vaubert D, Clérot D et al (1997) Wound-inducible and organ-specific expression of ORF13 from Agrobacterium rhizogenes 8196 T-DNA in transgenic tobacco plants. Mol Gen Genet 254:337–343PubMedGoogle Scholar
  87. Helfer A, Pien S, Otten L (2002) Functional diversity and mutational analysis of Agrobacterium 6B oncoproteins. Mol Gen Genom 267:577–586Google Scholar
  88. Helfer A, Clément B, Michler P et al (2003) The Agrobacterium oncogene AB-6b causes a graft-transmissible enation syndrome in tobacco. Plant Mol Biol 52:483–493PubMedGoogle Scholar
  89. Hildebrand EM (1940) Cane gall of brambles caused by Phytomonas rubi n. sp. J Agric Res 61:685–696Google Scholar
  90. Hooykaas PJJ, Den Dulk-Ras H, Schilperoort RA (1988) The Agrobacterium tumefaciens T-DNA gene 6b is an oncogene. Plant Mol Biol 11:791–794PubMedGoogle Scholar
  91. Hu Y, Chen B, Ni T et al (2003) Promoter of the rolC gene of Agrobacterium rhizogenes can be strongly regulated in glandular cell of transgenic tobacco. Mol Biotech 24:121–126Google Scholar
  92. Ichikawa T, Ozeki Y, Syono K (1990) Evidence for the expression of rol genes of Nicotiana glauca in genetic tumors of N. glauca X N. langsdorfii. Mol Gen Genet 220:177–180PubMedGoogle Scholar
  93. Intrieri MC, Buiatti M (2001) The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Mol Phylogenet Evol 20:100–110PubMedPubMedCentralGoogle Scholar
  94. Inzé D, Follin A, Van Lijsebettens M et al (1984) Genetic analysis of the individual T-DNA genes of Agrobacterium tumefaciens: further evidence that two genes are involved in indole-3-acetic acid synthesis. Mol Gen Genet 194:265–274Google Scholar
  95. Ishibashi N, Kitakura S, Terakura S et al (2014) Protein encoded by oncogene 6b from Agrobacterium tumefaciens has a reprogramming potential and histone chaperone-like activity. Front Plant Sci 5:1–7Google Scholar
  96. Ito M, Machida Y (2015) Reprogramming of plant cells induced by 6b oncoproteins from the plant pathogen Agrobacterium. J Plant Res 128:423–435PubMedGoogle Scholar
  97. Jin Y, Hu J, Liu X et al (2017) T-6b allocates more assimilation product for oil synthesis and less for polysaccharide synthesis during the seed development of Arabidopsis thaliana. Biotechnol Biofuels 10:19PubMedPubMedCentralGoogle Scholar
  98. Joos H, Inzé D, Caplan A et al (1983) Genetic analysis of T-DNA transcripts in nopaline crown galls. Cell 32:1057–1067PubMedPubMedCentralGoogle Scholar
  99. Kado CI (2014) Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front Microbiol 5:340PubMedPubMedCentralGoogle Scholar
  100. Kakiuchi Y, Gális I, Tamogami S et al (2006) Reduction of polar auxin transport in tobacco by the tumorigenic Agrobacterium tumefaciens AK-6b gene. Planta 223:237–247PubMedGoogle Scholar
  101. Kakiuchi Y, Takahashi S, Wabiko H (2007) Modulation of the venation pattern of cotyledons of transgenic tobacco for the tumorigenic 6b gene of Agrobacterium tumefaciens AKE10. J Plant Res 120:259–268PubMedGoogle Scholar
  102. Kares C, Prinsen E, Van Onckelen H et al (1990) IAA synthesis and root induction with iaa genes under heat shock promoter control. Plant Mol Biol 15:225–236PubMedGoogle Scholar
  103. Kerr A, Panagopoulos CG (1977) Biotypes of Agrobacterium radiobacter var. tumefaciens and their biological control. Phytopath Z 90:172–179Google Scholar
  104. Kiselev KV, Kusaykin MI, Dubrovina AS et al (2006) The rolC gene induces expression of a pathogenesis-related beta-1,3-glucanase in transformed ginseng cells. Phytochemistry 67:2225–2231PubMedGoogle Scholar
  105. Kiselev KV, Dubrovina AS, Veselova MV et al (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692PubMedGoogle Scholar
  106. Kitakura S, Fujita T, Ueno Y et al (2002) The protein encoded by oncogene 6b from Agrobacterium tumefaciens interacts with a nuclear protein of tobacco. Plant Cell 14:451–463PubMedPubMedCentralGoogle Scholar
  107. Kitakura S, Terakura S, Yoshioka Y et al (2008) Interaction between Agrobacterium tumefaciens oncoprotein 6b and a tobacco nucleolar protein that is homologous to TNP1 encoded by a transposable element of Antirrhinum majus. J Plant Res 121:425–433PubMedGoogle Scholar
  108. Kiyokawa S, Kobayashi K, Kikuchi Y (1994) Root-inducing region of mikimopine type Ri plasmid pRi1724. Plant Physiol 104:801–802PubMedPubMedCentralGoogle Scholar
  109. Klee H, Horsch R, Hinchee MA et al (1987) The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic Petunia plants. Genes Dev 1:86–96Google Scholar
  110. Kodahl N, Müller R, Lütken H (2016) The Agrobacterium rhizogenes oncogenes rolB and ORF13 increase formation of generative shoots and induce dwarfism in Arabidopsis thaliana (L.) Heynh. Plant Sci 252:22–29PubMedGoogle Scholar
  111. Koltunow AM, Johnson SD, Lynch M et al (2001) Expression of rolB in apomictic Hieracium piloselloides Vill. causes ectopic meristems in planta and changes in ovule formation, where apomixis initiates at higher frequency. Planta 214:196–205PubMedGoogle Scholar
  112. Komari T (1990) Genetic characterization of a double-flowered tobacco plant obtained by a transformation experiment. Theor Appl Genet 80:167–171PubMedGoogle Scholar
  113. Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396Google Scholar
  114. Körber H, Strizhov H, Staiger D et al (1991) T-DNA gene 5 of Agrobacterium modulates auxin response by autoregulated synthesis of a growth hormone antagonist in plants. EMBO J 10:3983–3991PubMedPubMedCentralGoogle Scholar
  115. Kyndt T, Quispe D, Zhai H et al (2015) The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: an example of a naturally transgenic food crop. Proc Natl Acad Sci USA 112:5844–5849PubMedPubMedCentralGoogle Scholar
  116. Leach F (1991) Promoter analysis of the highly expressed rolC and rolD root-inducing genes of Agrobacterium rhizogenes: enhancer and tissue-specific DNA determinants are dissociated. Plant Sc 79:69–76Google Scholar
  117. Leemans J, Hernalsteens JP, Deblaere R et al (1983) Genetic analysis of T-DNA and regeneration of transformed plants. In: Molecular genetics of the bacteria-plant interaction. Proc Life Sci 322–330Google Scholar
  118. Legué V, Driss-Ecole D, Maldiney R et al (1996) The response to auxin of rapeseed (Brassica napus L.) roots displaying reduced gravitropism due to transformation by Agrobacterium rhizogenes. Planta 200:119–124PubMedGoogle Scholar
  119. Lemcke K, Schmülling T (1998a) Gain of function assays identify non-rol genes from Agrobacterium rhizogenes TL-DNA that alter plant morphogenesis or hormone sensitivity. Plant J 15:423–433PubMedGoogle Scholar
  120. Lemcke K, Schmülling T (1998b) A putative rolB gene homologue of the Agrobacterium rhizogenes TR-DNA has different morphogenetic activity in tobacco than rolB. Plant Mol Biol 36:803–808PubMedGoogle Scholar
  121. Lemcke K, Prinsen E, Van Onckelen H et al (2000) The ORF8 gene product of Agrobacterium rhizogenes TL-DNA has tryptophan 2-monooxygenase activity. Mol Plant-Microbe Interact 13:787–790PubMedGoogle Scholar
  122. Levesque H, Delepelaire P, Rouzé P et al (1988) Common evolutionary origin of the central portion of the Ri TL-DNA of Agrobacterium rhizogenes and the Ti T-DNAs of Agrobacterium tumefaciens. Plant Mol Biol 11:731–744PubMedGoogle Scholar
  123. Lütken H, Clarke JL, Müller R (2012) Genetic engineering and sustainable production of ornamentals: current status and future directions. Plant Cell Rep 31:1141–1157PubMedGoogle Scholar
  124. Marchler-Bauer A, Bo Y, Han L et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. NAR 45:D200–D203PubMedGoogle Scholar
  125. Matsuki R, Uchimiya H (1994) A 43-kDa nuclear tobacco protein interacts with a specific single-stranded DNA sequence from the 5′-upstream region of the Agrobacterium rhizogenes rolC gene. Gene 140:201–205Google Scholar
  126. Matsuki R, Onodera H, Yamaguchi T (1989) Tissue-specific expression of the rolC promoter of the Ri plasmid in transgenic rice plants. Mol Gen Genet 220:12–16Google Scholar
  127. Matveeva TV, Bogomaz DI, Pavlova OA et al (2012) Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. Mol Plant-Microbe Interact 25:1542–1551PubMedPubMedCentralGoogle Scholar
  128. Maurel C, Brevet J, Barbier-Brygoo H et al (1990) Auxin regulates the promoter of the root-inducing rolB gene of Agrobacterium rhizogenes in transgenic tobacco. Mol Gen Genet 223:58–64PubMedGoogle Scholar
  129. Maurel C, Barbier-Brygoo H, Spena A et al (1991) Single rol genes from the Agrobacterium rhizogenes T(L)-DNA alter some of the cellular responses to auxin in Nicotiana tabacum. Plant Physiol 97:212–216PubMedPubMedCentralGoogle Scholar
  130. Maurel C, Leblanc N, Barbier-Brygoo H et al (1994) Alterations of auxin perception in rolB-transformed tobacco protoplasts. Time course of rolB mRNA expression and increase in auxin sensitivity reveal multiple control by auxin. Plant Physiol 105:1209–1215PubMedPubMedCentralGoogle Scholar
  131. Messens E, Lenaerts A, Van Montagu M et al (1985) Genetic basis for opine secretion from crown gall tumor cells. Mol Gen Genet 199:344–348Google Scholar
  132. Meyer AD, Ichikawa T, Meins F (1995) Horizontal gene transfer: regulated expression of tobacco homologue of the Agrobacterium rhizogenes rolC gene. Mol Gen Genet 249:265–273PubMedGoogle Scholar
  133. Meyer A, Tempé J, Costantino P (2000) Hairy root: a molecular overview. Functional analysis of Agrobacterium rhizogenes T-DNA genes. In: Stacey G, Keen NT (eds) Plant-Microbe Interact, vol 5. American Phytopathological Society Press, St Paul, pp 93–139Google Scholar
  134. Mohajjel-Shoja H (2010) Contribution to the study of the Agrobacterium rhizogenes plast genes rolB and rolC, and their homologs in Nicotiana tabacum. Thesis, University of StrasbourgGoogle Scholar
  135. Mohajjel-Shoja H, Clément B, Perot J et al (2011) Biological activity of the Agrobacterium rhizogenes-derived trolC gene of Nicotiana tabacum and its functional relationship to other plast genes. Mol Plant-Microbe Interact 24:44–53PubMedGoogle Scholar
  136. Moriuchi H, Okamoto C, Nishihama R et al (2004) Nuclear localization and interaction of RolB with plant 14-3-3 proteins correlates with induction of adventitious roots by the oncogene rolB. Plant J 38:260–275PubMedGoogle Scholar
  137. Nagata N, Kosono S, Sekine M et al (1995) The regulatory functions of the rolB and rolC genes of Agrobacterium rhizogenes are conserved in the homologous genes (Ngrol) of Nicotiana glauca in tobacco genetic tumors. Plant Cell Physiol 36:1003–1012PubMedGoogle Scholar
  138. Nagata N, Kosono S, Sekine M et al (1996) Different expression patterns of the promoters of the NgrolB and NgrolC genes during the development of tobacco genetic tumors. Plant Cell Physiol 37:489–498Google Scholar
  139. Nath U, Crawford BCW, Carpenter R et al (2003) Genetic control of surface curvature. Science 299:1404–1407PubMedGoogle Scholar
  140. Nester EW (2015) Agrobacterium: nature’s genetic engineer. Front Plant Sci 5, article 730Google Scholar
  141. Nilsson O, Olsson O (1997) Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiol Plant 100:463–473Google Scholar
  142. Nilsson O, Moritz T, Imbault N et al (1993a) Hormonal characterization of transgenic tobacco plants expressing the rolC gene of Agrobacterium rhizogenes TL-DNA. Plant Physiol 102:363–371PubMedPubMedCentralGoogle Scholar
  143. Nilsson O, Crozier A, Schmülling T et al (1993b) Indole-3-acetic acid homeostasis in transgenic tobacco plants expressing the Agrobacterium rhizogenes rolB gene. Plant J 3:681–689Google Scholar
  144. Nilsson O, Moritz T, Sundberg B et al (1996a) Expression of the Agrobacterium rhizogenes rolC gene in a deciduous forest tree alters growth and development and leads to stem fasciation. Plant Physiol 112:493–502PubMedPubMedCentralGoogle Scholar
  145. Nilsson O, Little CH, Sandberg G et al (1996b) Expression of two heterologous promoters, Agrobacterium rhizogenes rolC and cauliflower mosaic virus 35S, in the stem of transgenic hybrid aspen plants during the annual cycle of growth and dormancy. Plant Mol Biol 31:887–895PubMedGoogle Scholar
  146. Nilsson O, Tuominen H, Sundberg B et al (1997) The Agrobacterium rhizogenes rolB and rolC promoters are expressed in pericycle cells competent to serve as root initials in transgenic hybrid aspen. Physiol Plant 100:456–462Google Scholar
  147. O’Grady K, Gurley WB (1995) Site-directed mutagenesis of the enhancer region of the 780 gene promoter of T-DNA. Plant Mol Biol 29:99–108PubMedGoogle Scholar
  148. Oono Y, Handa T, Kanaya K et al (1987) The TL-DNA of Ri plasmids responsable for dwarfness of tobacco plants. Jpn J Genet 62:501–505Google Scholar
  149. Oono Y, Kanaya K, Uchimiya H (1990) Early flowering in transgenic tobacco plants possessing the rolC gene of Agrobacterium rhizogenes Ri plasmid. Jpn J Genet 65:7–16Google Scholar
  150. Oono Y, Satomi T, Uchimiya H (1991) Agrobacterium rhizogenes lacZ-rolC gene expression in Escherichia coli: detection of the product in transgenic plants using RolC-specific antibodies. Gene 104:95–98PubMedGoogle Scholar
  151. Oono Y, Suzuki T, Toki S et al (1993) Effects of the over-expression of the rolC gene on leaf development in transgenic periclinal chimeric plants. Plant Cell Physiol 34:745–752Google Scholar
  152. Ophel K, Kerr A (1990) Agrobacterium vitis-new species for strains of Agrobacterium biovar 3 from grapevine. Int J Syst Bacteriol 40:236–241Google Scholar
  153. Otten L, De Ruffray P (1994) Agrobacterium vitis nopaline Ti plasmid pTiAB4: relationship to other Ti plasmids and T-DNA structure. Mol Gen Genet 245:493–505PubMedPubMedCentralGoogle Scholar
  154. Otten L, Helfer A (2001) Biological activity of the rolB-like 5′ end of the A4-orf8 gene from the Agrobacterium rhizogenes TL-DNA. Mol Plant-Microbe Interact 14:405–411PubMedGoogle Scholar
  155. Otten L, Schmidt JA (1998) T-DNA from the Agrobacterium limited-host range strain AB2/73 contains a single oncogene. Mol Plant-Microbe Interact 11:335–342PubMedGoogle Scholar
  156. Otten L, Szegedi E (1985) Crown galls induced by octopine-degrading biotype 3 strains of Agrobacterium tumefaciens contain a new form of lysopine dehydrogenase. Plant Sci 40:81–85Google Scholar
  157. Otten L, Vreugdenhil D, Schilperoort RA (1977) Properties of d(+)-lysopine dehydrogenase from crown gall tumour tissue. Biochim Biophys Acta 485:268–277PubMedGoogle Scholar
  158. Otten L, Salomone JY, Helfer A et al (1999) Sequence and functional analysis of the left-hand part of the T-region from the nopaline-type Ti plasmid, pTiC58. Plant Mol Biol 41:765–776PubMedGoogle Scholar
  159. Palatnik JF, Allen E, Wu X, Schommer C et al (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedGoogle Scholar
  160. Palazon J, Cusido RM, Roig C et al (1998) Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Rep 17:384–390Google Scholar
  161. Pasternak T, Haser T, Falk T et al (2017) A 3D digital atlas of the Nicotiana tabacum root tip and its use to investigate changes in the root apical meristem induced by the Agrobacterium 6b oncogene. Plant J 92:31–42PubMedGoogle Scholar
  162. Ream LW, Gordon MP, Nester EW (1983) Multiple mutations in the T region of the Agrobacterium tumefaciens tumor-inducing plasmid. Proc Natl Acad Sci USA 80:1660–1664PubMedPubMedCentralGoogle Scholar
  163. Reddy S, Dasgupta S, Rymarquis L et al (2003) Analysis of the Agrobacterium tumefaciens pTiChry5 6b promoter. J Plant Biochem Biotech 12:87–91Google Scholar
  164. Riker AJ (1930) Studies on infectious hairy root of nursery apple trees. J Agric Res 41:507–540Google Scholar
  165. Röder FT, Schmülling T, Gatz C (1994) Efficiency of the tetracycline-dependent gene expression system: complete suppression and efficient induction of the rolB phenotype in transgenic plants. Mol Gen Genet 243:32–38PubMedGoogle Scholar
  166. Saha P, Chakraborti D, Sarkar A et al (2007) Characterization of vascular-specific RSs1 and rolC promoters for their utilization in engineering plants to develop resistance against hemipteran insect pests. Planta 226:429–442PubMedGoogle Scholar
  167. Salomon F, Deblaere R, Leemans J et al (1984) Genetic identification of functions of TR-DNA transcripts in octopine crown galls. EMBO J 3:141–146PubMedPubMedCentralGoogle Scholar
  168. Satuti NSN, Moriuchi H, Yamakawa M et al (2005) Characterization of the rolB promoter on mikimopine-type pRi1724 T-DNA. Plant Sci 108:1353–1364Google Scholar
  169. Satuti NSN, Tanaka N, Yoshida K et al (2007) Phenotype of transgenic tobacco plants (Nicotiana tabacum cv. Petit Havana SR-1) expressing 1724orf13 gene of Agrobacterium rhizogenes strain MAFF301724. Indonesian J Biotechnol 12:980–987Google Scholar
  170. Schell J, Van Montagu M, De Beuckeleer M et al (1979) Interactions and DNA transfer between Agrobacterium tumefaciens, the Ti-plasmid and the plant host. Proc R Soc Lond B Biol Sci 204:251–266PubMedPubMedCentralGoogle Scholar
  171. Schmidt J (1999) Etude d’un oncogène de la souche AB2/73 d’Agrobacterium tumefaciens. Thesis, Louis Pasteur University of StrasbourgGoogle Scholar
  172. Schmülling T, Schell J (1993) Transgenic tobacco plants regenerated from leaf disks can be periclinal chimeras. Plant Mol Biol 21:705–708PubMedGoogle Scholar
  173. Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629PubMedPubMedCentralGoogle Scholar
  174. Schmülling T, Schell J, Spena A (1989) Promoters of the rolA, B, and C genes of Agrobacterium rhizogenes are differentially regulated in transgenic plants. Plant Cell 1:665–670PubMedPubMedCentralGoogle Scholar
  175. Schmülling T, Fladung M, Grossmann K et al (1993) Hormonal content and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA. Plant J 3:371–382Google Scholar
  176. Schröder G, Waffenschmidt S, Weiler W et al (1984) The T-region of Ti plasmid codes for an enzyme synthesizing indole-3-acetic acid. Eur J Biochem 138:387–391PubMedGoogle Scholar
  177. Scorza R, Zimmerman TW, Cordts JM et al (1994) Horticultural characteristics of transgenic tobacco expressing the rolC gene from Agrobacterium rhizogenes. J Am Soc Hortic Sci 119:1091–1098Google Scholar
  178. Serino G, Clérot D, Brevet J et al (1994) rol genes of Agrobacterium rhizogenes cucumopine strain: sequence, effects and pattern of expression. Plant Mol Biol 26:415–422PubMedGoogle Scholar
  179. Shabtai S, Salts Y, Kaluzky G et al (2007) Improved yielding and reduced puffiness under extreme temperatures induced by fruit-specific expression of rolB in processing tomatoes. Theor Appl Genet 114:1203–1209PubMedGoogle Scholar
  180. Shen WH, Petit A, Guern J et al (1988) Hairy roots are more sensitive to auxin than normal roots. Proc Natl Acad Sci USA 85:3417–3421PubMedGoogle Scholar
  181. Shen WH, Davioud E, David C et al (1990) High sensitivity to auxin is a common feature of hairy root. Plant Physiol 94:554–560PubMedPubMedCentralGoogle Scholar
  182. Shkryl YN, Veremeichik GN, Bulgakov VP et al (2008) Individual and combined effects of the rolA, B, and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnol Bioeng 100:118–125PubMedGoogle Scholar
  183. Sinkar VP, Pythoud F, White FF et al (1988) rolA locus of the Ri plasmid directs developmental abnormalities in transgenic tobacco plants. Genes Dev 2:688–697PubMedGoogle Scholar
  184. Sitbon F, Hennion S, Sundberg B et al (1992) Transgenic tobacco plants coexpressing the Agrobacterium tumefaciens iaaM and iaaH genes display altered growth and indoleacetic acid metabolism. Plant Physiol 99:1062–1069PubMedPubMedCentralGoogle Scholar
  185. Spanier K, Schell J, Schreier PH (1989) A functional analysis of T-DNA gene 6b: the fine-tuning of cytokinin effects on shoot development. Mol Gen Genet 219:209–216PubMedGoogle Scholar
  186. Spano L, Mariotti D, Cardarelli M et al (1988) Morphogenesis and auxin sensitivity of transgenic tobacco with different complements of Ri T-DNA. Plant Physiol 87:479–483PubMedPubMedCentralGoogle Scholar
  187. Spena A, Schmülling T, Koncz C et al (1987) Independent and synergistic activity of rolA, B and C loci in stimulating abnormal growth in plants. EMBO J 6:3891–3899PubMedPubMedCentralGoogle Scholar
  188. Spena A, Aalen RB, Schulze SC (1989) Cell-autonomous behavior of the rolC gene of Agrobacterium rhizogenes during leaf development: a visual assay for transposon excision in transgenic plants. Plant Cell 1:1157–1164PubMedPubMedCentralGoogle Scholar
  189. Stieger PA, Meyer AD, Kathmann P et al (2004) The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells. Plant Physiol 135:1798–1808PubMedPubMedCentralGoogle Scholar
  190. Studholme DJ, Downie JA, Preston GM (2005) Protein domains and architectural innovation in plant-associated Proteobacteria. BMC Genomics 16:6–17Google Scholar
  191. Sugaya S, Uchimiya H (1992) Deletion analysis of the 5′-upstream region of the Agrobacterium rhizogenes Ri plasmid rolC gene required for tissue-specific expression. Plant Physiol 99:464–467PubMedPubMedCentralGoogle Scholar
  192. Sugaya S, Hayakawa K, Handa T et al (1989) Cell-specific expression of the rolC gene of the TL-DNA of Ri plasmid in transgenic tobacco plants. Plant Cell Physiol 30:649–653Google Scholar
  193. Suzuki A, Kato A, Uchimiya H (1992) Single-stranded DNA of 5′-upstream region of the rolC gene interacts with nuclear proteins of carrot cell cultures. Biochem Biophys Res Commun 188:727–733PubMedGoogle Scholar
  194. Suzuki K, Yamashita I, Tanaka N (2002) Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution. Plant J 32:775–787PubMedPubMedCentralGoogle Scholar
  195. Takahashi S, Sato R, Takahashi M et al (2013) Ectopic localization of auxin and cytokinin in tobacco seedlings by the plant-oncogenic AK-6b gene of Agrobacterium tumefaciens AKE10. Planta 238:753–770PubMedGoogle Scholar
  196. Tanaka N, Ikeda T, Oka A (1994) Nucleotide sequence of the rol region of the mikimopine-type root-inducing plasmid pRi1724. Biosci Biotechnol Biochem 58:548–551PubMedGoogle Scholar
  197. Terakura S, Kitakura S, Ishikawa M et al (2006) Oncogene 6b from Agrobacterium tumefaciens induces abaxial cell division at late stages of leaf development and modifies vascular development in petioles. Plant Cell Physiol 47:664–672PubMedGoogle Scholar
  198. Terakura S, Ueno Y, Tagami H et al (2007) An oncoprotein from the plant pathogen Agrobacterium has histone chaperone-like activity. Plant Cell 19:2855–2865PubMedPubMedCentralGoogle Scholar
  199. Thomashow LS, Reeves S, Thomashow MF (1984) Crown gall oncogenesis: evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyzes synthesis of indoleacetic acid. Proc Nat Acad Sci USA 81:5071–5075PubMedGoogle Scholar
  200. Thomashow MF, Hugly S, Buchholz WG et al (1986) Molecular basis for the auxin-independent phenotype of crown gall tumor tissue. Science 231:616–618PubMedGoogle Scholar
  201. Tinland B, Huss B, Paulus F et al (1989) Agrobacterium tumefaciens 6b genes are strain-specific and affect the activity of auxin as well as cytokinin genes. Mol Gen Genet 219:217–224Google Scholar
  202. Tinland B, Rohfritsch O, Michler P et al (1990) Agrobacterium tumefaciens T-DNA gene 6b stimulates rol-induced root formation, permits growth at high auxin concentrations and increases root size. Mol Gen Genet 223:1–10PubMedGoogle Scholar
  203. Tinland B, Fournier P, Heckel T et al (1992) Expression of a chimaeric heat-shock-inducible Agrobacterium 6b oncogene in Nicotiana rustica. Plant Mol Biol 18:921–930PubMedGoogle Scholar
  204. Udagawa M, Aoki S, Syono K (2004) Expression analysis of the NgORF13 promoter during the development of tobacco genetic tumors. Plant Cell Physiol 45:1023–1031PubMedGoogle Scholar
  205. Umber M, Voll L, Weber A et al (2002) The rolB-like part of the Agrobacterium rhizogenes orf8 gene inhibits sucrose export in tobacco. Mol Plant-Microbe Interact 15:956–962PubMedGoogle Scholar
  206. Umber M, Clément B, Otten L (2005) The T-DNA oncogene A4-orf8 from Agrobacterium rhizogenes A4 induces abnormal growth in tobacco. Mol Plant-Microbe Interact 18:205–211PubMedGoogle Scholar
  207. van Altvorst AC, Bino RJ, van Dijk AJ et al (1992) Effects of the introduction of Agrobacterium rhizogenes rol genes on tomato plant and flower development. Plant Sci 83:77–85Google Scholar
  208. Van Onckelen H, Rüdelsheim P, Inzé D et al (1985) Tobacco plants transformed with the Agrobacterium T-DNA gene 1 contain high amounts of indole-3-acetamide. FEBS Lett 181:373–376Google Scholar
  209. Van Onckelen H, Prinsen E, Inzé D et al (1986) Agrobacterium T-DNA gene 1 codes for tryptophan monooxygenase activity in tobacco crown gall cells. FEBS Lett 198:357–360Google Scholar
  210. Veremeichik GN, Shkryl YN, Bulgakov VP et al (2012) Molecular cloning and characterization of seven class III peroxidases induced by overexpression of the agrobacterial rolB gene in Rubia cordifolia transgenic callus cultures. Plant Cell Rep 31:1009–1019PubMedGoogle Scholar
  211. Wabiko H, Minemura M (1996) Exogenous phytohormone-independent growth and regeneration of tobacco plants transgenic for the 6b gene of Agrobacterium tumefaciens AKE10. Plant Physiol 112:939–951PubMedPubMedCentralGoogle Scholar
  212. Wang M, Soyano T, Machida S et al (2011) Molecular insights into plant cell proliferation disturbance by Agrobacterium protein 6b. Genes Dev 25:64–76PubMedPubMedCentralGoogle Scholar
  213. Wasserman LA, Sergeev AI, Vasil’ev VG et al (2015) Thermodynamic and structural properties of tuber starches from transgenic potato plants grown in vitro and in vivo. Carbohydr Polym 125:214–223PubMedGoogle Scholar
  214. White FF, Garfinkel DJ, Huffman GA et al (1983) Sequence homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature 301:348–350Google Scholar
  215. White FF, Taylor BH, Huffman GA et al (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164:33–44PubMedPubMedCentralGoogle Scholar
  216. Winefield C, Lewis D, Arathoon S et al (1999) Alteration in Petunia plant form through the introduction of the rolC gene from Agrobacterium rhizogenes. Mol Breeding 5:543–551Google Scholar
  217. Yokoyama R, Hirose T, Fujii N et al (1994) The rolC promoter of Agrobacterium rhizogenes Ri plasmid is activated by sucrose in transgenic tobacco plants. Mol Gen Genet 244:15–22PubMedGoogle Scholar
  218. Zhang M, Pereira e Silva Mde C, Chaib De Mares M et al (2014) The mycosphere constitutes an arena for horizontal gene transfer with strong evolutionary implications for bacterial-fungal interactions. FEMS Microbiol Ecol 89:516–526PubMedGoogle Scholar
  219. Zhu L, Holefors A, Ahlman A et al (2001) Transformation of the apple rootstock M.9/29 with the rolB gene and its influence on rooting and growth. Plant Sc 160:433–439Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.IBMPStrasbourgFrance

Personalised recommendations