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Agrobacterium Rhizogenes rolB and rolD Genes: Regulation and Involvement in Plant Development

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Abstract

Rol genes belong to the T-DNA which is transferred by Agrobacterium rhizogenes into plant cells. Each of these genes affects plant development and is regulated by the host. In this review, after a brief historical background, the most intriguing aspects of past and current research on rolB and rolD genes are highlighted and discussed.

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References

  • Altamura MM (1996) Root histogenesis in herbaceous and woody explants cultured in vitro. A critical review. Agronomie 16: 589–602

    Google Scholar 

  • Altamura MM & Tomassi M (1998) Auxin, photoperiod and putrescine affect flower neoformation in normal and rolB-transformed tobacco thin cell layers. Plant Physiol. Biochem. 36: 441–448

    Article  CAS  Google Scholar 

  • Altamura MM, Archilletti T, Capone I & Costantino P (1991) Histological analysis of the expression of Agrobacterium rhizogenes rolB-GUS gene fusions in transgenic tobacco. New Phytol. 118: 69–78

    CAS  Google Scholar 

  • Altamura MM, Capitani F, Gazza L, Capone I & Costantino P (1994) The plant oncogene rolB stimulates the formation of flower and root meristemoids in tobacco thin cell layers. New Phytol. 126: 283–293

    CAS  Google Scholar 

  • Altamura MM, D'Angeli S & Capitani F (1998) The protein of rolB gene enhances shoot formation in tobacco leaf explants and thin cell layers from plants in different physiological stages. J. Exp. Bot. 49: 1139–1146

    Article  CAS  Google Scholar 

  • Aoki S, Kawaoka A, Sekine M, Ichikawa T, Fujita T, Shinmyo A & Syono K (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 × N. langsdorffii. Mol. Gen. Genet. 243: 706–710

    CAS  PubMed  Google Scholar 

  • Baron C & Zambryski C (1996) Plant transformation: a pilus in Agrobacterium T-DNA transfer. Curr. Biol. 6: 1567–1569

    Article  CAS  PubMed  Google Scholar 

  • Baumann K, De Paolis A, Costantino P & Gualberti G (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: 323–333

    Article  CAS  PubMed  Google Scholar 

  • Bellincampi D, Salvi G, De Lorenzo G, Cervone F, Marfà V, Eberhard S, Darvill A & Albersheim P (1993) Oligogalacturonides inhibit the formation of roots on tobacco explants. Plant J. 4: 207–213

    Article  CAS  Google Scholar 

  • Bellincampi D, Cardarelli M, Zaghi D, Serino G, Salvi G, Gatz C, Cervone F, Altamura MM, Costantino P & De Lorenzo G (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  Google Scholar 

  • Bellincampi D, Dipierro N, Salvi G, Cervone F & De Lorenzo G (2000) Extracellular H2O2 inducedBy 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  Google Scholar 

  • Binns AN & Constantino P (1988) The Agrobacterium Oncogones. In: Spink H, Kondorosi A & Hooykaas PJJ (eds) The Rhizobiaceae (pp. 251–266). Kluwer Academic Publishers, Dordrect

    Google Scholar 

  • Bouchez D & Camilleri C (1990) Identification of a putative rolB gene on the TR-DNA of the Agrobacterium rhizogenes A4 Riplasmid. Plant Mol. Biol. 14: 617-619

    Article  CAS  PubMed  Google Scholar 

  • Brevet J & Tempè J (1988) Homology mapping of T-DNA regions of three Agrobacterium rhizogenes Ri plasmids by electron microscope heteroduplex studies. Plasmid 19: 75–83

    Article  CAS  PubMed  Google Scholar 

  • Capone I, Cardarelli M, Trovato M & Costantino P (1989a) Upstream non-coding region which confers polar expression to Ri plasmid root inducing gene rolB. Mol. Gen. Genet. 216: 239–244

    Article  CAS  Google Scholar 

  • Capone I, Spanò L, Cardarelli M, Bellincampi D, Petit A & Costantino P (1989b) 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, Pomponi M, De Paolis A & Costantino P (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 & Cardarelli M(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, Spanò L, Capone I & Costantino P (1987) Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Mol. Gen. Genet. 209: 475–480

    Article  CAS  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 

  • Chilton MD, Drummond MH, Merlo DJ, Sciaky D, Montoya AL, Gordon MP & Nester EW(1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell11: 263–271

  • Chilton MD, Tepfer DA, Petit A, Casse-Delbart F & Tempè J (1982) Agrobacterium rhizogenes inserts T-DNA into the genome of host plant root cells. Nature 295: 432–434

    Article  CAS  Google Scholar 

  • Costantino P, Mauro ML, Micheli G, Risuleo G, Hooykaas PJJ & Schilperoort R (1981) Fingerprinting and sequence homology of plasmids from different virulent strains of Agrobacterium rhizogenes. Plasmid 5: 170–182

    Article  CAS  PubMed  Google Scholar 

  • Costantino P, Capone I, Cardarelli M, De Paolis A, Mauro ML & Trovato M(1994) Bacterial plant oncogenes: the rol genes' saga. Genetica 94: 203–211

    Article  CAS  PubMed  Google Scholar 

  • David C, Chilton MD & Tempè J (1984) Conservation of T-DNA in plants regenerated from hairy root cultures. Biotechnology 2: 73–76

    CAS  Google Scholar 

  • Dehio C & Schell J (1993) Stable expression of a single-copy rolA gene in transgenic Arabidopsis thaliana plants allows an exhaustive mutagenic analysis of the transgene associated phenotype. Mol. Gen. Genet. 241: 359–366

    Article  CAS  PubMed  Google Scholar 

  • Dehio C & Schell J (1994) Identification of plant genetic loci involved in a posttrascriptional mechanism for meiotically reversible transgene silencing. Proc. Natl. Acad. Sci. USA 91: 5538–5542

    CAS  PubMed  Google Scholar 

  • Dehio C, Grossmann K, Schell J & Schmulling T (1993) Phenotype and hormonal status of transgenic tobacco plants overexpressing the rolA gene of Agrobacterium rhizogenes T-DNA. Plant Mol. Biol. 23: 1199–1210

    Article  CAS  PubMed  Google Scholar 

  • Delbarre A, Muller P, Imhoff V, Barbier-Brygoo H, Maurel C & Guern J (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

    CAS  PubMed  Google Scholar 

  • De Paolis A, Mauro ML, Pomponi M, Cardarelli M, Spanò L & Costantino P (1985) Localization of agropine synthesizing functions in the TR region of the root inducing plasmid of Agrobacterium rhizogenes 1855. Plasmid 13: 1–7

    CAS  PubMed  Google Scholar 

  • De Paolis A, Sabatini S, De Pascalis L, Costantino P & Capone I (1996) A rolB regulatory factor belongs to a new class of single zinc finger plant proteins. Plant J. 10: 215–223

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Durand-Tardif M, Broglie R, Slightom J & Tepfer D (1985) Structure and expression of Ri T-DNA from Agrobacterium rhizogenes in Nicotiana tabacum organ and phenotypic specificity. J. Mol. Biol. 186: 557–564

    CAS  PubMed  Google Scholar 

  • Elmayan T & Tepfer M (1995) Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A, of the 35S promoter and the 35S2 promoter. Transgenic Res. 4: 388–396

    Article  CAS  PubMed  Google Scholar 

  • Estruch JJ, Chriqui D, Grossmann K, Schell J & Spena A (1991a) The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. EMBO J. 10: 2889–2895

    CAS  PubMed  Google Scholar 

  • Estruch JJ, Schell J & Spena A (1991b) The protein encoded by the rolB plant oncogene hydrolyses indole glycosides. EMBO J. 10: 3123–3128

    Google Scholar 

  • Falasca G, Tomassi M & Altamura MM (2000) Rhizogenesis from Arabidopsis thin cell layers: role of calcium and putrescine. The 4th International Symposium on In Vitro Culture and Horticultural Breeding, Tampere, Finland, 2–7 July 2000, Abstracts (p. 37)

  • Filetici P, Spanò L, Costantino P (1987) Conserved regions in the T-DNA of different Agrobacterium rhizogenes root-inducing plasmids. Plant Mol. Biol. 9: 19–26

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Filippini F, Rossi V, Marin O, Trovato M, Costantino P, Downey PM, Lo Schiavo F & Terzi M (1996) A plant oncogene as a phosphatase. Nature 379: 499–500

    Article  CAS  PubMed  Google Scholar 

  • Furner IJ, Huffman GA, Amasino RM, Garfinkel DJ, Gordon MP & Nester EW (1986) An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature 319: 422–427

    Article  CAS  Google Scholar 

  • Gualberti G, Papi M, Bellucci L, Ricci I, Bouchez D, Camilleri C, Costantino P & Vittorioso P (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14: 1253–1263

    Article  CAS  PubMed  Google Scholar 

  • Ichikawa T, Ozeki Y & Syono K (1990) Evidence for the expression of the rol genes of Nicotiana glauca in genetic tumors of N. glauca × N. langsdorffii. Mol. Gen. Genet. 220: 177–180

    Article  CAS  PubMed  Google Scholar 

  • Kisu Y, Ono T, Shimofurutani N, Suzuki M & Esaka M (1998) Characterization and expression of a new class of zinc finger protein that binds to silencer region of ascorbate oxidase gene. Plant Cell Physiol. 39: 1054–1064

    CAS  PubMed  Google Scholar 

  • Koltunow AM, Johnson SD, Lynch M, Yoshihara T & Costantino P (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

    CAS  PubMed  Google Scholar 

  • Leach F & Aoyagi K (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 Sci. 79: 69–76

    Article  CAS  Google Scholar 

  • Lemcke K & Schmulling 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 & Schmulling 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 

  • Marsilio S, Tornielli GB, Pomponi M, Pezzotti M, Costantino P & Cardarelli M (2001) Effect of rolB gene of Agrobacterium rhizogenes on gamete development and embryogenesis in model species. Second International Apomixis Conference APO2001. April 2001, Como, Italy, Abstract Book (p. 52)

  • Maurel C, Brevet J, Barbier-Brygoo H, Guern J & Tempè J (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, Tempè J & Guern J (1991) Single rol genes from the Agrobacterium rhizogenes TL-DNA alter some of the cellular responses to auxin in Nicotiana tabacum. Plant Physiol. 97: 212–216

    CAS  Google Scholar 

  • Maurel C, Leblanc N, Barbier-Brygoo H, Perrot-Rechenmann C, Bouvier-Durand M & Guern J (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  Google Scholar 

  • Mauro ML, Trovato M, De Paolis A, Gallelli A, Costantino P & Altamura MM (1996) The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Dev. Biol. 180: 693–700

    Article  CAS  PubMed  Google Scholar 

  • Mauro ML, De Lorenzo G, Costantino P & Bellincampi D (2002) Oligogalacturonides inhibit the induction of late but not of early auxin-responsive genes in tobacco. Planta 215: 494–501

    Article  CAS  PubMed  Google Scholar 

  • Mena M, Vicente-Carbajosa J, Schmidt R & Carbonero P (1998) An endosperm-specific Dof protein from barley, highly conserved in wheat, binds to and activates transcription from the prolamin-box of a native B-hordein promoter in barley endosperm. Plant J. 16: 53–62

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nagata N, Kosono S, Sekine M, Shinmyo A & Syono K (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

    CAS  PubMed  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

    CAS  Google Scholar 

  • Nilsson O, Crozier A, Schmulling T, Sandberg G & Olsson O (1993) 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, Tuominen H, Sundberg B & Olsson O (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

    CAS  Google Scholar 

  • Papi M, Sabatini S, Bouchez D, Camilleri C, Costantino P & Vittorioso P (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev. 14: 28–33

    CAS  PubMed  Google Scholar 

  • Papi M, Sabatini S, Altamura MM, Hennig L, Schafer E, Costantino P & Vittorioso P (2002) Inactivation of the phloem-specific Dof zinc finger gene DAG1 affects response to light and integrity of the testa of Arabidopsis seeds. Plant Physiol. 128: 411–417

    Article  CAS  PubMed  Google Scholar 

  • Rengel D, Kushnir S, Sparvoli S & Martin C (2001) DAG: a gene family involved in plastid development. Twelfth International Conference on Arabidopsis Research, 23–27 June 2001, University of Wisconsin-Madison, WI, Abstracts (p. 327)

  • Ricker AJ (1930) Studies on infectious hairy roots of nursery apple trees. J. Agric. Res. 41: 438–446

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schmulling 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

    Article  CAS  PubMed  Google Scholar 

  • Sheng J & Citovsky V (1996) Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8: 1699–1710

    Article  CAS  PubMed  Google Scholar 

  • Slightom JL, Durand-Tardif M, Jouanin L & Tepfer D (1986) Nucleotide sequence analysis of Agrobacterium rhizogenes agropine type plasmid: identification of open reading frames. J. Biol. Chem. 261: 108–121

    CAS  PubMed  Google Scholar 

  • Smulders MJM, Janssen GFE, Croes AF, Barendse GWM & Wullems GJ (1988) Auxin regulation of flower bud formation in tobacco explants. J. Exp. Bot. 39: 451–459

    CAS  Google Scholar 

  • Smulders MJM, Visser EJW, Croes AF & Wullems GJ (1990a) The dose of 1-naphthaleneacetic acid determines flower-bud regeneration in tobacco explants at a large range of concentrations. Planta 180: 410–415

    CAS  Google Scholar 

  • Smulders MJM, Visser EJW, Van der Krieken WM, Croes AF & Wullems GJ (1990b) Effects of the developmental state of the tissue on the competence for flower bud regeneration in pedicel explants of tobacco. Plant Physiol. 92: 582–586

    CAS  Google Scholar 

  • Tepfer D (1984) Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37: 959–967

    Article  CAS  PubMed  Google Scholar 

  • Tran Thanh Van M, Thi Dien NK & Chlyah A (1974) Regulation of organogenesis in small explants of superficial tissue of Nicotiana tabacum L. Planta 119: 149–159

    Article  CAS  Google Scholar 

  • Trovato M & Linhares F (1999) Recent advances on rol genes research: a tool to study plant differentiation. Current Topics Plant Biol. 1: 51–62

    CAS  Google Scholar 

  • Trovato M, Mauro ML, Costantino P & Altamura MM (1997) The rolD gene from Agrobacterium rhizogenes is developmentally regulated in transgenic tobacco. Protoplasma 197: 111–120

    Article  CAS  Google Scholar 

  • Trovato M, Maras B, Linhares F & Costantino P (2001) The plant oncogene rolD encodes a functional ornithine cyclodeaminase. PNAS 98(23): 13449–13453

    Article  CAS  PubMed  Google Scholar 

  • Van der Krieken WM, Croes AF, Barendse GWM & Wullems GJ (1988) Uptake and metabolism of benzyladenine in the early stage of flower bud development in vitro in tobacco. Physiol. Plant. 74: 113–118

    CAS  Google Scholar 

  • Venis MA, Napier RM, Barbier-Brygoo H, Maurel C, Perrot-Rechenmann C & Guern J (1992) Antibodies to a peptide from the maize auxin-binding protein have auxin agonist activity. Proc. Natl. Acad. Sci. USA 89: 7208–7212

    CAS  PubMed  Google Scholar 

  • Vicente-Carbajosa J, Moose S, Parsons RL & Schmidt R (1997) A maize zinc finger protein binds the prolamin box in zein gene promoters and interacts with basic leucine zipper transcriptional activator Opaque2. Proc. Natl. Acad. Sci. USA 94: 7685–7690

    Article  CAS  PubMed  Google Scholar 

  • White FF, Garfinkel DJ, Huffman G, Gordon MP & Nester EW (1983) Sequences homologous to Agrobacterium rhizogenes T-DNA in the genome of uninfected plants. Nature 301: 348–350

    Article  CAS  Google Scholar 

  • White FF, Taylor BH, Huffmann GA, Gordon MP & Nester EW (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J. Bacteriol. 164: 33–44

    CAS  PubMed  Google Scholar 

  • Zhang B, Chen W, Foley R, Buttner M & Singh K (1995) Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell 7: 2241–2252

    Article  CAS  PubMed  Google Scholar 

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  1. Dipartimento di Biologia Vegetale, Università 'La Sapienza', P.le A. Moro, 5, 00185, Rome, Italy

    Maria Maddalena Altamura

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Altamura, M.M. Agrobacterium Rhizogenes rolB and rolD Genes: Regulation and Involvement in Plant Development. Plant Cell, Tissue and Organ Culture 77, 89–101 (2004). https://doi.org/10.1023/B:TICU.0000016609.22655.33

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