Abstract
Analysis of published sequences for Ri TL-DNA (root-inducing left-hand transferred DNA) of Agrobacterium rhizogenes revealed several unsuspected structural features. First, Ri TL-DNA genes are redundant. Using redundancy as a criterion, three regions (left, middle and right) were discerned. The left one, ORFs (open reading frames) 1–7, contains no detectable redundancy. In the middle region a highly diverged gene family was detected in ORFs 8, 11, 12, 13 and 14. The right region contains an apparently recent duplication (ORF 15 =18+17). We interpret the phenomenon of redundancy, particularly in the central region that encodes the transformed phenotype, to be an adaptation that ensures function in a variety of host species. Comparison of Ri TL-DNA and Ti T-DNAs from Agrobacterium tumefaciens revealed common structures, unpredicted by previous nucleic acid hybridization studies. Ri TL-DNA ORF 8 is a diverged Ti T-DNA tms1. Both Agrobacterium genes consist of a member of the diverged gene family detected in the central part of the Ri TL-DNA, but fused to a sequence similar to iaaM of Pseudomonas savastonoi. Other members of this gene family were found scattered throughout Ti T-DNA. We argue that the central region of Ri and the part of Ti T-DNA including ORFs 5–10 evolved from a common ancestor. We present the hypothesis that the gene family encodes functions that alter developmental plasticity in higher plants.
Similar content being viewed by others
References
Akiyoshi DE, Klee H, Amasino RM, Nester EW, Gordon MP: T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci USA 81: 5994–5998 (1984).
Barker RF, Idler KB, Thompson DV, Kemp JD: Nucleotide sequence of the T-DNA region from Agrobacterium tumefaciens octopine Ti plasmid pTi15955. Plant Mol Biol 2: 335–350 (1983).
Barry GF, Rogers SG, Fraley RT, Brand: Identification of a cloned cytokinin biosynthesis gene. Proc Natl Acad Sci USA 81: 4776–4780 (1984).
Birot AM, Bouchez D, Casse-Delbart F, Durand-Tardif M, Jouanin L, Pautot V, Robaglia C, Tepfer D, Tepfer M, Tourmeur J, Vilaine F: Studies and uses of the Ri plasmids of Agrobacterium rhizogenes. Plant Physiol Biochem 25: 1–13 (1987).
Buchmann I, Marner FJ, Schroeder G, Waffenschmidt S, Schroeder J: Tumor genes in plants: T-DNA encoded cytokinin biosynthesis. EMBO J 4: 853–850 (1985).
Cardarelli M, Spano L, DePaolis A, Mauro ML, Vitali G, Costantino P: Identification of the genetic locus responsible for non-polar root induction by Agrobacterium rhizogenes 1855. Plant Mol Biol 5: 385–391 (1985).
Cardarelli M, Mariotti D, Pomponi M, Spano L, Capone I, Costantino P: Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Mol Gen Genet 209: 475–480 (1987).
Davey M, Gartland K, Mulligan B: Transformation of the genomic expression of plant cells. In: Jennings DH, Trewavas AJ (ed) Plasticity in plants, pp. 85–120. The Company of Biologists, Cambridge (1986).
Durand-Tardif M, Broglie R, Slightom J, Tepfer D: Structure and expression of Ri T-DNA from Agrobacterium rhizogenes in Nicotiana tabacum. Organ and phenotypic specificity. J Mol Biol 186: 557–564 (1985).
Engler G, Depicker A, Maenhaut R, Villarroel R, VanMontagu M, Schell J: Physical mapping of DNA base sequence homologies between an octopine and a nopaline Ti plasmid of Agrobacterium tumefaciens. J Mol Biol 152: 183–208 (1981).
Follin A, Inze D, Budar F, Genetello C, VanMontagu M, Schell J: Genetic evidence that the tryptophan 3-mono-oxygenase gene of Pseudomonas savastanoi is functionally equivalent to one of the T-DNA genes involved in plant tumour formation by Agrobacterium tumefaciens T-DNA. Mol Gen Genet 201: 178–185 (1985).
Furner IJ, Huffman GA, Amasino RM, Garfinkel DJ, Gordon MP, Nester EW: An Agrobacterium transformation in the evolution of the genus nicotiana. Nature 319: 422–427 (1986).
Garfinkel DJ, Simpson RB, Ream LW, White FF, Gordon MP, Nester EW: Genetic analysis of crown-gall: Fine structure map of the T-DNA by site-directed mutagenesis. Cell 27: 143–153 (1981).
Gielen J, DeBeuckeleer M, Seurick J, Deboek F, DeGreve H, Lemmers M, VanMontagu M, Schell J: The complete nucleotide sequence of the TL-DNA of the Agrobacterium tumefaciens plasmid pTiAch5. EMBO J 3: 835–846 (1984).
Hoekema A, Hooykaas PJJ, Schilperoort RA: Transfer of the octopine T-DNA segment to plant cells mediated by different types of Agrobacterium tumor or root-inducing plasmids: Generality of virulence systems. J Bact 158: 383–385 (1984).
Huffman GA, White FF, Gordon MP, Nester EW: Hairy root inducing plasmid: Physical map and homology to tumor-inducing plasmids. J Bact 157: 269–276 (1984).
Jouanin L: Restriction map of an agropine-type Ri plasmid and its homologies with Ti plasmids. Plasmid 12: 91–102 (1984).
Jouanin L, Guerche P, Pamboukdjian N, Tourmeur C, Casse-Delbart F, Tourneur J: Structure of T-DNA in plants regenerated from roots transformed by Agrobacterium rhizogenes strain A4. Mol Gen Genet 206: 387–392 (1987).
Kemper E, Waffenschmidt S, Weiler EW, Rausch T, Schroeder J: T-DNA-encoded auxin formation in crown-gall cells. Planta 163: 257–262 (1985).
Klee H, Horsch R, Hinchee M, Hein M, Hoffmann N: The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes & Dev 1: 86–96 (1987).
Koncz C, Schell J: 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 (1986).
Lahners K, Byrne MC, Chilton MD: T-DNA fragments of hairy root plasmid pRi8196 are distantly related to octopine and nopaline Ti plasmid T-DNA. Plasmid 11: 130–140 (1984).
Leach F: Etude de la région TL du plasmide Ri d'Agrobacterium rhizogenes souche A4. Thèse Doct. 3e Cycle, Université de Paris-Sud (1983).
MacDonald E, Powell G, Regier D, Glass L, Roberto F, Kosuge T, Morris R: Secretion of zeatin, ribosylzeatin and ribosyl-1′-Methylzeatin by Pseudomonas savastanoi. Plant Physiol 82: 742–747 (1986).
Messens E, Lenaerts A, VanMontagu M, Hedges RW: Genetic basis for opine secretion from crown gall tumour cells. Mol Gen Genet 199: 344–348 (1985).
Morris R: Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Ann Rev Plant Physiol 37: 509–538 (1986).
Offringa IA, Melchers LS, Regensburg-Tuink AJG, Costantino P, Schilperoort RA, Hooykaas PJJ: Complementation of Agrobacterium tumefaciens tumor-inducing aux mutants by genes from the TR-region of the Ri plasmid of Agrobacterium rhizogenes. Proc Natl Acad Sci USA 83: 6935–6939 (1986).
Ooms G, Hooykaas PJJ, Moolenaar G, Schilperoort RA: Crown gall plant tumors of abnormal morphology, induced by Agrobacterium tumefaciens carrying mutated octopine Ti plasmids; analysis of T-DNA functions. Gene 14: 33–50 (1981).
Ooms G, Twell D, Bossen ME, Harry C, Hoge C, Burrell MM: Developmental regulation of Ri TL-DNA gene expression in roots, shoots and tubers of transformed potato (Solanum tuberosum cv. Désirée). Plant Mol Biol 6: 321–330 (1986).
Oono Y, Handa T, Kanaya K, Uchimiya H: The TL-DNA gene of Ri plasmids responsible for dwarfness of tobacco plants. Jpn J Genet 62: 501–505 (1987).
Quattrochio F, Benvenuto E, Tavazza R, Cuozzo L, Ancora G: A study on the possible role of auxin in potato ‘hairy root’ tissues. J Plant Physiol 123: 143–150 (1986).
Ream W, Gordon MP, Nester EW: Multiple mutations in the T-region of the Agrobacterium tumefaciens tumor-inducing plasmid. Proc Natl Acad Sci USA 80: 1660–1664 (1983).
Renalier M-H, Batut J, Ghai Y, Terghazi B, Gherardi M, David M, Garnerone A-M, Vasse J, Truchet G, Huguet T, Boistard P: A new symbiotic cluster on the pSym mega plasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J. Bact. 169: 2231–2238 (1987).
Ryder M, Tate M, Kerr A: Virulence properties of strains of Agrobacterium on the apical and basal surfaces of carrot root discs. Plant Physiol 77: 215–221 (1985).
Schmulling T, Schell J, Spena A: Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7: 2621–2629 (1988).
Shen WH, Petit A, Guern J, Tempé J: Hairy roots are more sensitive to auxin than normal roots. Proc Natl Acad Sci USA 85: 3417–3421 (1988).
Sinkar VP, White FF, Furner IJ, Abrahamsen M, Pythoud F, Gordon MP: Reversion of aberrant plants transformed with Agrobacterium rhizogenes is associated with the transcriptional inactivation of the TL-DNA genes. Plant Physiol 86: 584–590 (1988).
Sinkar VP, Pythoud F, White FF, Nester EW, Gordon MP: Rol A locus of the Ri plasmid directs developmental abnormalities in transgenic tobacco plants. Genes & Dev 2: 688–697 (1988).
Spena A, Schmulling T, Koncz C, Schell JS: Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants. EMBO J 6: 3891–3899 (1987).
Slightom JL, Jouanin L, Leach F, Drong RF, Tepfer D: Isolation and identification of TL-DNA/plant junctions in Convolvulus arvensis transformed by Agrobacterium rhizogenes strain A4. EMBO J 4: 3069–3077 (1985).
Slightom JL, Durand-Tardif M, Jouanin L, Tepfer D: Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid: identification of open-reading frames. J Biol Chem 261: 108–121 (1986).
Staden R: An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10: 2951–2961 (1982).
Taylor BH, White FF, Nester EW, Gordon MP: Transcription of Agrobacterium rhizogenes A4 T-DNA. Mol Gen Genet 201: 546–553 (1985).
Tepfer D, Tempé J: Production d'agropine par des racines formées sous l'action d'Agrobacterium rhizogenes, souche A4. C R Acad Sci, série III 292: 153–156 (1981).
Tepfer D: La transformation génétique de plantes supérieures par Agrobacterium rhizogenes. In 2e Colloque sur les Recherches Fruitières, CTIFL-INRA, Bordeaux, Paris, pp. 47–59 (1982).
Tepfer D: The biology of genetic transformation of higher plants by Agrobacterium rhizogenes. In: Puhler A (ed) Molecular Genetics of the Bacteria Plant Interaction. pp. 248–258. Springer Verlag, Berlin, (1983).
Tepfer D: Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37: 959–967 (1984).
Tepfer D: Ri T-DNA from Agrobacterium rhizogenes, a semiochemical that alters morphological plasticity. In: vonWettstein D, Chua N-H (eds) Plant Molecular Biology. pp. 565–571. Plenum Press, New York (1987).
Tepfer D: Ri T-DNA from Agrobacterium rhizogenes: a source of genes having applications in rhizosphere biology and plant development, ecology and evolution. In: Kosuge T, Nester E (eds), Plant-Microorganism Interactions. McGraw-Hill, in press (1989).
Thomashow LS, Reeves S, Thomashow MF: Crown gall oncogenesis: Evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyses synthesis of indoleacetic acid. Proc Natl Acad Sci USA 81: 5071–5075 (1984).
Trewavas AJ: Resource allocation under poor growth conditions. A major role for growth substances in developmental plasticity. In: Jennings DH, Trewavas AJ (eds) Plasticity in Plants. pp. 31–76. The Company of Biologists, Cambridge (1986).
Vanderleyden J, Desair J, DeMeirsman C, Michiels K, VanGool A, Jen G, Chilton MD: Nucleotide sequence of the T-DNA region encoding transcripts 6a and 6b of the pTiT37 nopaline Ti plasmid. Plant Mol Biol 7: 33–41 (1986).
Vilaine F, Casse-Delbart F: Independant induction of transformed roots by the TL- and TR-regions of the Ri plasmid of agropine type Agrobacterium rhizogenes. Mol Gen Genet 206: 17–23 (1987).
Vilaine F, Charbonnier C, Casse-Delbart F: Further insight concerning the TL region of the Ri plasmid of Agrobacterium rhizogenes strain A4: Transfer of a 1.9 kb fragment is sufficient to induce transformed roots on tobacco leaf fragments. Mol Gen Genet 210: 111–115 (1987).
White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW: Sequences homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature 301: 348–350 (1983).
White FF, Taylor BH, Huffman GA, Gordon MP, Nester EW: Molecular and genetic analysis of the transferred DNA regions of the root inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164: 33–44 (1985).
Yamada T, Palm C, Brooks B, Kosuge T: Nucleotide sequences of the Pseudomonas savastanoi indoleacetic acid genes show homology with Agrobacterium tumefaciens T-DNA. Proc Natl Acad Sci USA 82: 6522–6526 (1985).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Levesque, H., Delepelaire, P., Rouzé, P. et al. Common evolutionary origin of the central portions of the Ri TL-DNA of Agrobacterium rhizogenes and the Ti T-DNAs of Agrobacterium tumefaciens . Plant Mol Biol 11, 731–744 (1988). https://doi.org/10.1007/BF00019514
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00019514