Skip to main content

The Agrobacterium Phenotypic Plasticity (Plast) Genes

  • Chapter
  • First Online:
Agrobacterium Biology

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 418))

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adams EC, Gurley WB (1994) Nuclear protein 780BP from cauliflower binds an element in the 780 gene promoter of T-DNA. Plant Mol Biol 26:377–392

    Article  CAS  PubMed  Google Scholar 

  • 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 95:479–485

    Article  CAS  Google Scholar 

  • 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 118:69–78

    Article  CAS  Google Scholar 

  • 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 126:283–293

    Article  CAS  Google Scholar 

  • Alvarez JP, Furumizu C, Efroni I et al (2016) Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife 5:e15023

    Google Scholar 

  • Aoki S (2004) Resurrection of an ancestral gene: functional and evolutionary analyses of the Ngrol genes transferred from Agrobacterium to Nicotiana. J Plant Res 117:329–337

    CAS  PubMed  Google Scholar 

  • 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 40:222–230

    Article  CAS  Google Scholar 

  • 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 40:252–256

    Article  CAS  Google Scholar 

  • Aoki S, Syono K (1999c) Horizontal gene transfer and mutation: Ngrol genes in the genome of Nicotiana glauca. Proc Natl Acad Sci USA 96:13229–13234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aoki S, Syono K (2000) The roles of Rirol and Ngrol genes in hairy root induction in Nicotiana debneyi. Plant Sci 159:183–189

    Article  CAS  PubMed  Google Scholar 

  • 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 243:706–710

    Article  CAS  PubMed  Google Scholar 

  • 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:e96979

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 28:487–492

    Google Scholar 

  • 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 29:1299–1304

    Article  CAS  PubMed  Google Scholar 

  • 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 44:67–77

    CAS  PubMed  Google Scholar 

  • 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 11:323–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:477–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 122:1379–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 123:323–328

    Article  CAS  Google Scholar 

  • 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 204:27–35

    Article  CAS  PubMed  Google Scholar 

  • 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 216:428–438

    Article  CAS  PubMed  Google Scholar 

  • 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 14:617–619

    Article  CAS  PubMed  Google Scholar 

  • Bouzar H, Jones JB (2001) Agrobacterium larrymoorei sp. nov., a pathogen isolated from aerial tumours of Ficus benjamina. Int J Syst Evol Microbiol 51:1023–1026

    Article  CAS  PubMed  Google Scholar 

  • 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 print

    Google Scholar 

  • 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 27:41–57

    Article  CAS  PubMed  Google Scholar 

  • Bruce W, Gurley WB (1987) Functional domains of a T-DNA promoter active in Crown Gall tumors. Mol Cell Biol 7:59–67

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 85:4310–4314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulgakov VP, Khodakovskaya MV, Labetskaya NV et al (1998) The impact of rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochem 49:1929–1934

    Article  CAS  Google Scholar 

  • 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 97:213–221

    Article  CAS  Google Scholar 

  • 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 221:471–478

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP, Kiselev KV, Yakovlev KV et al (2006) Agrobacterium mediated transformation of sea urchin embryos. Biotech J 1:454–461

    Article  CAS  Google Scholar 

  • 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 134:1–22

    CAS  Google Scholar 

  • 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 102:70–79

    Article  CAS  PubMed  Google Scholar 

  • 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 13:43–52

    Article  CAS  PubMed  Google Scholar 

  • 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 16:427–436

    Article  CAS  PubMed  Google Scholar 

  • 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 25:681–691

    Article  CAS  PubMed  Google Scholar 

  • Cardarelli M, Mariotti D, Pomponi M et al (1987) Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Mol Gen Genet 210:111–115

    Article  Google Scholar 

  • 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 217:726–735

    Article  CAS  PubMed  Google Scholar 

  • Casanova E, Valdés AE, Zuker A et al (2004) rolC-transgenic carnation plants: adventitious organogenesis and levels of endogenous auxin and cytokinins. Plant Sci 167:551–560

    Article  CAS  Google Scholar 

  • Casanova E, Trillas MI, Moysset L et al (2005) Influence of rol genes in floriculture. Biotech Adv 23:3–39

    Article  CAS  Google Scholar 

  • 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 38:512–525

    Article  CAS  PubMed  Google Scholar 

  • Chen K (2016) Sequencing and functional analysis of cT-DNAs in Nicotiana. Thesis, University of Strasbourg

    Google Scholar 

  • Chen K, Otten L (2015) Morphological analysis of the 6b oncogene-induced enation syndrome. Planta 243:131–148

    Article  PubMed  CAS  Google Scholar 

  • Chen K, Otten L (2017) Natural Agrobacterium transformants: recent results and some theoretical considerations. Front Plant Sci 8:1600

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 80:669–682

    Article  CAS  PubMed  Google Scholar 

  • 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 87:258–269

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Chichiriccò G, Costantino P, Spanò L (1992) Expression of the rolB oncogene from Agrobacterium rhizogenes during zygotic embryogenesis in tobacco. Plant Cell Physiol 33:827–832

    Google Scholar 

  • Clément B, Pollmann S, Weiler E et al (2006) The Agrobacterium vitis T-6b oncoprotein induces auxin-independent cell expansion in tobacco. Plant J 45:1017–1027

    Article  PubMed  CAS  Google Scholar 

  • 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 20:53–62

    Article  PubMed  CAS  Google Scholar 

  • Comai L, Kosuge T (1982) Cloning and characterization of iaaM, a virulence determinant of Pseudomonas savastanoi. J Bacteriol 143:950–957

    Article  Google Scholar 

  • de Groot MJA, Bundock P, Hooykaas PJJ et al (1998) Agrobacterium tumefaciens mediated transformation of filamentous fungi. Nat Biotechnol 16:839–842

    Article  PubMed  Google Scholar 

  • 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 10:215–223

    Article  PubMed  Google Scholar 

  • 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 91:5538–5542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:563–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Cola A, Poma A, Spano L (1997) rolB expression pattern in the early stages of carrot somatic embryogenesis. Cell Biol Int 21:595–600

    Article  PubMed  Google Scholar 

  • Drevet C, Brasileiro AC, Jouanin L (1994) Oncogene arrangement in a shooty strain of Agrobacterium tumefaciens. Plant Mol Biol 25:83–90

    Article  CAS  PubMed  Google Scholar 

  • 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 17:547–550

    Article  CAS  PubMed  Google Scholar 

  • 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 10:2889–2895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estruch JJ, Schell J, Spena A (1991c) The protein encoded by the rolB plant oncogene hydrolyses indole glucosides. EMBO J 10:3125–3128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:33–46

    Article  CAS  Google Scholar 

  • Filippini F, Lo Schiavo F, Terzi M (1994) The plant oncogene rolB alters binding of auxin to plant cell membranes. Plant Cell Physiol 35:767–771

    Article  CAS  Google Scholar 

  • Filippini F, Rossi V, Marin O et al (1996) A plant oncogene as a phosphatase. Nature 379:499–500

    Article  CAS  PubMed  Google Scholar 

  • Fladung M (1990) Transformation of diploid and tetraploid potato clones with the rolC gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breeding 104:295–304

    Article  Google Scholar 

  • 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 33:1097–2003

    Article  CAS  PubMed  Google Scholar 

  • 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 42:123–132

    Article  CAS  Google Scholar 

  • 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 23:749–757

    Article  CAS  PubMed  Google Scholar 

  • 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 259:559–568

    Article  PubMed  Google Scholar 

  • 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 201:55–62

    Article  CAS  PubMed  Google Scholar 

  • 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 95:238–241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 104:1151–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 209:453–461

    Article  PubMed  Google Scholar 

  • 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 43:939–950

    Article  PubMed  Google Scholar 

  • Gális I, Kakiuchi Y, Simek P et al (2004) Agrobacterium tumefaciens AK-6b gene modulates phenolic compound metabolism in tobacco. Phytochem 65:169–179

    Article  CAS  Google Scholar 

  • Gardner N, Melberg T, George M et al (2006) Differential expression of rolC results in unique plant phenotypes. J Am Soc Hortic Sci 131:82–88

    Article  CAS  Google Scholar 

  • 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 27:143–153

    Article  CAS  PubMed  Google Scholar 

  • Gelvin SB (2012) Traversing the cell: Agrobacterium T-DNA’s journey to the host genome. Front Plant Sci 26:3–52

    Google Scholar 

  • Gidoni D, Bar M, Gilboa N (2001) FLP/FRT-mediated restoration of normal phenotypes and clonal sectors formation in rolC transgenic tobacco. Transgenic Res 10:317–328

    Article  CAS  PubMed  Google Scholar 

  • 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 223:457–467

    Article  CAS  PubMed  Google Scholar 

  • 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 33:729–735

    Article  CAS  PubMed  Google Scholar 

  • 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 37:218–228

    Article  PubMed  CAS  Google Scholar 

  • 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 30:125–134

    Article  PubMed  Google Scholar 

  • Hack E, Kemp JD (1980) Purification and characterization of the crown gall-specific enzyme, octopine synthase. Plant Physiol 65:949–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 88:7763–7767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:581–585

    Article  CAS  Google Scholar 

  • 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 254:337–343

    Article  CAS  PubMed  Google Scholar 

  • Helfer A, Pien S, Otten L (2002) Functional diversity and mutational analysis of Agrobacterium 6B oncoproteins. Mol Gen Genom 267:577–586

    Article  CAS  Google Scholar 

  • 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 52:483–493

    Article  CAS  PubMed  Google Scholar 

  • Hildebrand EM (1940) Cane gall of brambles caused by Phytomonas rubi n. sp. J Agric Res 61:685–696

    Google Scholar 

  • Hooykaas PJJ, Den Dulk-Ras H, Schilperoort RA (1988) The Agrobacterium tumefaciens T-DNA gene 6b is an oncogene. Plant Mol Biol 11:791–794

    Article  CAS  PubMed  Google Scholar 

  • 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 24:121–126

    Article  CAS  Google Scholar 

  • 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 220:177–180

    Article  CAS  PubMed  Google Scholar 

  • Intrieri MC, Buiatti M (2001) The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Mol Phylogenet Evol 20:100–110

    Article  CAS  PubMed  Google Scholar 

  • 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 194:265–274

    Article  Google Scholar 

  • 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 5:1–7

    Article  Google Scholar 

  • Ito M, Machida Y (2015) Reprogramming of plant cells induced by 6b oncoproteins from the plant pathogen Agrobacterium. J Plant Res 128:423–435

    Article  CAS  PubMed  Google Scholar 

  • 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 10:19

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joos H, Inzé D, Caplan A et al (1983) Genetic analysis of T-DNA transcripts in nopaline crown galls. Cell 32:1057–1067

    Article  CAS  PubMed  Google Scholar 

  • Kado CI (2014) Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front Microbiol 5:340

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 223:237–247

    Article  CAS  PubMed  Google Scholar 

  • 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 120:259–268

    Article  CAS  PubMed  Google Scholar 

  • 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 15:225–236

    Article  CAS  PubMed  Google Scholar 

  • Kerr A, Panagopoulos CG (1977) Biotypes of Agrobacterium radiobacter var. tumefaciens and their biological control. Phytopath Z 90:172–179

    Article  Google Scholar 

  • 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 67:2225–2231

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Veselova MV et al (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692

    Article  CAS  PubMed  Google Scholar 

  • 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 14:451–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121:425–433

    Article  CAS  PubMed  Google Scholar 

  • Kiyokawa S, Kobayashi K, Kikuchi Y (1994) Root-inducing region of mikimopine type Ri plasmid pRi1724. Plant Physiol 104:801–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:86–96

    Article  CAS  Google Scholar 

  • 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 252:22–29

    Article  CAS  PubMed  Google Scholar 

  • 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 214:196–205

    Article  CAS  PubMed  Google Scholar 

  • Komari T (1990) Genetic characterization of a double-flowered tobacco plant obtained by a transformation experiment. Theor Appl Genet 80:167–171

    Article  CAS  PubMed  Google Scholar 

  • 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 204:383–396

    Article  CAS  Google Scholar 

  • 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 10:3983–3991

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 112:5844–5849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 79:69–76

    Article  CAS  Google Scholar 

  • 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 322–330

    Google Scholar 

  • 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 200:119–124

    Article  PubMed  Google Scholar 

  • 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 15:423–433

    Article  CAS  PubMed  Google Scholar 

  • 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 36:803–808

    Article  CAS  PubMed  Google Scholar 

  • 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 13:787–790

    Article  CAS  PubMed  Google Scholar 

  • 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 11:731–744

    Article  CAS  PubMed  Google Scholar 

  • Lütken H, Clarke JL, Müller R (2012) Genetic engineering and sustainable production of ornamentals: current status and future directions. Plant Cell Rep 31:1141–1157

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Bo Y, Han L et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. NAR 45:D200–D203

    Article  CAS  PubMed  Google Scholar 

  • 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 140:201–205

    Google Scholar 

  • 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 220:12–16

    Article  CAS  Google Scholar 

  • 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 25:1542–1551

    Article  CAS  PubMed  Google Scholar 

  • 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 223:58–64

    Article  CAS  PubMed  Google Scholar 

  • 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 97:212–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:1209–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messens E, Lenaerts A, Van Montagu M et al (1985) Genetic basis for opine secretion from crown gall tumor cells. Mol Gen Genet 199:344–348

    Article  CAS  Google Scholar 

  • Meyer AD, Ichikawa T, Meins F (1995) Horizontal gene transfer: regulated expression of tobacco homologue of the Agrobacterium rhizogenes rolC gene. Mol Gen Genet 249:265–273

    Article  CAS  PubMed  Google Scholar 

  • 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 93–139

    Google Scholar 

  • 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 Strasbourg

    Google Scholar 

  • 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 24:44–53

    Article  CAS  PubMed  Google Scholar 

  • 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 38:260–275

    Article  CAS  PubMed  Google Scholar 

  • 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 36:1003–1012

    Article  CAS  PubMed  Google Scholar 

  • 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 37:489–498

    Article  CAS  Google Scholar 

  • Nath U, Crawford BCW, Carpenter R et al (2003) Genetic control of surface curvature. Science 299:1404–1407

    Article  CAS  PubMed  Google Scholar 

  • Nester EW (2015) Agrobacterium: nature’s genetic engineer. Front Plant Sci 5, article 730

    Google Scholar 

  • 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 100:463–473

    Article  CAS  Google Scholar 

  • 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 102:363–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:681–689

    Article  CAS  Google Scholar 

  • 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 112:493–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 31:887–895

    Article  CAS  PubMed  Google Scholar 

  • 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 100:456–462

    Article  CAS  Google Scholar 

  • O’Grady K, Gurley WB (1995) Site-directed mutagenesis of the enhancer region of the 780 gene promoter of T-DNA. Plant Mol Biol 29:99–108

    Article  PubMed  Google Scholar 

  • Oono Y, Handa T, Kanaya K et al (1987) The TL-DNA of Ri plasmids responsable for dwarfness of tobacco plants. Jpn J Genet 62:501–505

    Article  Google Scholar 

  • 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 65:7–16

    Article  CAS  Google Scholar 

  • 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 104:95–98

    Article  CAS  PubMed  Google Scholar 

  • 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 34:745–752

    Article  CAS  Google Scholar 

  • Ophel K, Kerr A (1990) Agrobacterium vitis-new species for strains of Agrobacterium biovar 3 from grapevine. Int J Syst Bacteriol 40:236–241

    Article  CAS  Google Scholar 

  • Otten L, De Ruffray P (1994) Agrobacterium vitis nopaline Ti plasmid pTiAB4: relationship to other Ti plasmids and T-DNA structure. Mol Gen Genet 245:493–505

    Article  CAS  PubMed  Google Scholar 

  • 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 14:405–411

    Article  CAS  PubMed  Google Scholar 

  • Otten L, Schmidt JA (1998) T-DNA from the Agrobacterium limited-host range strain AB2/73 contains a single oncogene. Mol Plant-Microbe Interact 11:335–342

    Article  CAS  PubMed  Google Scholar 

  • 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 40:81–85

    Article  CAS  Google Scholar 

  • Otten L, Vreugdenhil D, Schilperoort RA (1977) Properties of d(+)-lysopine dehydrogenase from crown gall tumour tissue. Biochim Biophys Acta 485:268–277

    Article  CAS  PubMed  Google Scholar 

  • 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 41:765–776

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C et al (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  PubMed  Google Scholar 

  • 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 17:384–390

    Article  CAS  PubMed  Google Scholar 

  • 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 92:31–42

    Article  CAS  PubMed  Google Scholar 

  • 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 80:1660–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy S, Dasgupta S, Rymarquis L et al (2003) Analysis of the Agrobacterium tumefaciens pTiChry5 6b promoter. J Plant Biochem Biotech 12:87–91

    Article  CAS  Google Scholar 

  • Riker AJ (1930) Studies on infectious hairy root of nursery apple trees. J Agric Res 41:507–540

    Google Scholar 

  • 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 243:32–38

    Article  PubMed  Google Scholar 

  • 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 226:429–442

    Article  CAS  PubMed  Google Scholar 

  • Salomon F, Deblaere R, Leemans J et al (1984) Genetic identification of functions of TR-DNA transcripts in octopine crown galls. EMBO J 3:141–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satuti NSN, Moriuchi H, Yamakawa M et al (2005) Characterization of the rolB promoter on mikimopine-type pRi1724 T-DNA. Plant Sci 108:1353–1364

    Google Scholar 

  • 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 12:980–987

    Google Scholar 

  • 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 204:251–266

    Article  CAS  PubMed  Google Scholar 

  • Schmidt J (1999) Etude d’un oncogène de la souche AB2/73 d’Agrobacterium tumefaciens. Thesis, Louis Pasteur University of Strasbourg

    Google Scholar 

  • Schmülling T, Schell J (1993) Transgenic tobacco plants regenerated from leaf disks can be periclinal chimeras. Plant Mol Biol 21:705–708

    Article  PubMed  Google Scholar 

  • Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 1:665–670

    PubMed  PubMed Central  Google Scholar 

  • 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 3:371–382

    Article  Google Scholar 

  • 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 138:387–391

    Article  PubMed  Google Scholar 

  • 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 119:1091–1098

    Article  CAS  Google Scholar 

  • 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 26:415–422

    Article  CAS  PubMed  Google Scholar 

  • 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 114:1203–1209

    Article  CAS  PubMed  Google Scholar 

  • Shen WH, Petit A, Guern J et al (1988) Hairy roots are more sensitive to auxin than normal roots. Proc Natl Acad Sci USA 85:3417–3421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen WH, Davioud E, David C et al (1990) High sensitivity to auxin is a common feature of hairy root. Plant Physiol 94:554–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 100:118–125

    Article  CAS  PubMed  Google Scholar 

  • Sinkar VP, Pythoud F, White FF et al (1988) rolA locus of the Ri plasmid directs developmental abnormalities in transgenic tobacco plants. Genes Dev 2:688–697

    Article  CAS  PubMed  Google Scholar 

  • 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 99:1062–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 219:209–216

    Article  CAS  PubMed  Google Scholar 

  • 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 87:479–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:3891–3899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:1157–1164

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 135:1798–1808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Studholme DJ, Downie JA, Preston GM (2005) Protein domains and architectural innovation in plant-associated Proteobacteria. BMC Genomics 16:6–17

    Google Scholar 

  • 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 99:464–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:649–653

    CAS  Google Scholar 

  • 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 188:727–733

    Article  CAS  PubMed  Google Scholar 

  • Suzuki K, Yamashita I, Tanaka N (2002) Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution. Plant J 32:775–787

    Article  CAS  PubMed  Google Scholar 

  • 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 238:753–770

    Article  CAS  PubMed  Google Scholar 

  • Tanaka N, Ikeda T, Oka A (1994) Nucleotide sequence of the rol region of the mikimopine-type root-inducing plasmid pRi1724. Biosci Biotechnol Biochem 58:548–551

    Article  CAS  PubMed  Google Scholar 

  • 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 47:664–672

    Article  CAS  PubMed  Google Scholar 

  • Terakura S, Ueno Y, Tagami H et al (2007) An oncoprotein from the plant pathogen Agrobacterium has histone chaperone-like activity. Plant Cell 19:2855–2865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:5071–5075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomashow MF, Hugly S, Buchholz WG et al (1986) Molecular basis for the auxin-independent phenotype of crown gall tumor tissue. Science 231:616–618

    Article  CAS  PubMed  Google Scholar 

  • 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 219:217–224

    Article  CAS  Google Scholar 

  • 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 223:1–10

    Article  CAS  PubMed  Google Scholar 

  • 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 18:921–930

    Article  CAS  PubMed  Google Scholar 

  • Udagawa M, Aoki S, Syono K (2004) Expression analysis of the NgORF13 promoter during the development of tobacco genetic tumors. Plant Cell Physiol 45:1023–1031

    Article  CAS  PubMed  Google Scholar 

  • 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 15:956–962

    Article  CAS  PubMed  Google Scholar 

  • 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 18:205–211

    Article  CAS  PubMed  Google Scholar 

  • 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 83:77–85

    Article  Google Scholar 

  • 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 181:373–376

    Article  Google Scholar 

  • 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 198:357–360

    Article  Google Scholar 

  • 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 31:1009–1019

    Article  CAS  PubMed  Google Scholar 

  • 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 112:939–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Soyano T, Machida S et al (2011) Molecular insights into plant cell proliferation disturbance by Agrobacterium protein 6b. Genes Dev 25:64–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 125:214–223

    Article  CAS  PubMed  Google Scholar 

  • White FF, Garfinkel DJ, Huffman GA et al (1983) Sequence homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature 301:348–350

    Article  CAS  Google Scholar 

  • 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 164:33–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5:543–551

    Article  CAS  Google Scholar 

  • 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 244:15–22

    Article  CAS  PubMed  Google Scholar 

  • 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 89:516–526

    Article  CAS  PubMed  Google Scholar 

  • 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 160:433–439

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Léon Otten .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Otten, L. (2018). The Agrobacterium Phenotypic Plasticity (Plast) Genes. In: Gelvin, S. (eds) Agrobacterium Biology. Current Topics in Microbiology and Immunology, vol 418. Springer, Cham. https://doi.org/10.1007/82_2018_93

Download citation

Publish with us

Policies and ethics