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Natural Agrobacterium-Mediated Transformation in the Genus Nicotiana

  • Léon OttenEmail author
Chapter
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Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Agrobacterium can transfer genetic information to plants, transforming the plants naturally. An Agrobacterium plasmid fragment is transferred to the plant via bacterial infection and stably integrated into the plant’s nuclear DNA. This plasmid fragment (termed transferred DNA or T-DNA) contains several genes that are inserted into the plant’s chromosomes. Some natural plant species contain Agrobacterium T-DNA-like sequences, which have been shown to result from natural transformation. These sequences are called cellular T-DNAs or cT-DNAs. Multiple Nicotiana species have been shown to contain cT-DNA sequences and to express cT-DNA genes, qualifying these species as natural transformants. The composition and organization of the T-DNA sequences vary considerably. Sequencing the genome of the Tomentosae and Noctiflorae sections of the genus Nicotiana has identified seven cT-DNA sequences that are similar to sequences in A. rhizogenes, A. tumefaciens, and A. vitis. As some cT-DNA genes show strong growth effects when expressed in other species, they may influence the growth of the natural transformants as well. The precise mechanisms by which these genes alter growth patterns and their regulation by promoters and by plant transcription factors remain to be elucidated.

Keywords

Agrobacterium Nicotiana Sequencing cT-DNA 

References

  1. Aoki S, Syōno K (1999) 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.  https://doi.org/10.1093/oxfordjournals.pcp.a029531CrossRefGoogle Scholar
  2. Biemann K, Lioret C, Asselineau J, Lederer E, Polonsky J (1960) Sur la structure chimique de la lysopine nouvel acide aminé isolé de tissu de crown-gall. Bull Soc Chim Biol (Paris) 42:979–991Google Scholar
  3. Bouchez D, Tourneur J (1991) Organization of the agropine synthesis region of the T-DNA of the Ri plasmid from Agrobacterium rhizogenes. Plasmid 25:27–39CrossRefGoogle Scholar
  4. Burr TJ, Otten L (1999) Crown gall of grape: biology and disease management. Annu Rev Phytopathol 37:53–80.  https://doi.org/10.1146/annurev.phyto.37.1.53CrossRefPubMedGoogle Scholar
  5. Canaday J, Gérad JC, Crouzet P, Otten L (1992) Organization and functional analysis of three T-DNAs from the vitopine Ti plasmid pTiS4. Mol Gen Genet 235:292–303CrossRefGoogle Scholar
  6. Chen K (2016) Sequencing and functional analysis of cT-DNAs in Nicotiana. Doctoral dissertation, University of Strasbourg, FranceGoogle Scholar
  7. Chen K, Dorlhac de Borne F, Julio E, Obszynski J, Pale P, Otten L (2016) Root-specific expression of opine genes and opine accumulation in some cultivars of the naturally occurring genetically modified organism Nicotiana tabacum. Plant J 87:258–269.  https://doi.org/10.1111/tpj.13196CrossRefPubMedGoogle Scholar
  8. Chen K, Dorlhac de Borne F, Szegedi E, Otten L (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.  https://doi.org/10.1111/tpj.12661CrossRefPubMedGoogle Scholar
  9. Chen K, Otten L (2016) Morphological analysis of the 6b oncogene-induced enation syndrome. Planta 243:131–148.  https://doi.org/10.1007/s00425-015-2387-0CrossRefPubMedGoogle Scholar
  10. Chen K, Dorlhac de Borne F, Sierro N, Ivanov NV, Alouia M, Koechler S, Otten L (2018). Organization of the TC and TE cellular T-DNA regions in Nicotiana otophora and functional analysis of three diverged TE-6b genes. Plant J 94:274–287.  https://doi.org/10.1111/tpj.13853
  11. Chilton MD, Drummond MH, Merio 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. Cell 11:263–271CrossRefGoogle Scholar
  12. Christey MC (2001) Use of ri-mediated transformation for production of transgenic plants. Vitro Cell Dev Biol Plant 37:687–700.  https://doi.org/10.1007/s11627-001-0120-0CrossRefGoogle Scholar
  13. Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252.  https://doi.org/10.1111/j.1469-8137.2005.01480.xCrossRefPubMedGoogle Scholar
  14. De Cleene M, De Ley J (1981) The host range of infectious hairy-root. Bot Rev 47:147–194.  https://doi.org/10.1007/BF02868853CrossRefGoogle Scholar
  15. Dessaux Y, Petit A, Farrand SK, Murphy PJ (1998) Opines and opine-like molecules involved in plant-Rhizobiaceae interactions. In: Spaink HP, Kondorosi A, Hooykaas PJ (eds) The Rhizobiaceae: Molecular biology of model plant-associated bacteria. Springer, Berlin, pp 173–197CrossRefGoogle Scholar
  16. Fründt C, Meyer AD, Ichikawa T, Meins F (1998) A tobacco homologue of the Ri-plasmid orf13 gene causes cell proliferation in carrot root discs. Mol Gen Genet 259:559–568CrossRefGoogle Scholar
  17. 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.  https://doi.org/10.1038/319422a0CrossRefGoogle Scholar
  18. Gelvin SB (2012) Traversing the cell: Agrobacterium T-DNA’s journey to the host genome. Front Plant Sci.  https://doi.org/10.3389/fpls.2012.00052CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gordon JE, Christie PJ (2014) The Agrobacterium Ti plasmids. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PLAS-0010-2013CrossRefPubMedPubMedCentralGoogle Scholar
  20. Guyon P, Chilton MD, Petit A, Tempé J (1980) Agropine in “null-type” crown gall tumors: evidence for generality of the opine concept. Proc Natl Acad Sci U S A 77:2693–2697CrossRefGoogle Scholar
  21. Guyon P, Petit A, Tempé J, Dessaux Y (1993) Transformed plants producing opines specifically promote growth of opine-degrading Agrobacteria. Mol Plant Microbe Interact 6:92.  https://doi.org/10.1094/MPMI-6-092CrossRefGoogle Scholar
  22. Helfer A, Pien S, Otten L (2002) Functional diversity and mutational analysis of Agrobacterium 6B oncoproteins. Mol Genet Genomics 267:577–586.  https://doi.org/10.1007/s00438-002-0707-0CrossRefPubMedGoogle Scholar
  23. Hernalsteens J-P, Van Vliet F, De Beuckeleer M, Depicker A, Engler G, Lemmers M, Holsters M, Van Montagu M, Schell J (1980) The Agrobacterium tumefaciens Ti plasmid as a host vector system for introducing foreign DNA in plant cells. Nature 287:654–656CrossRefGoogle Scholar
  24. Hildebrand EM (1940) Cane gall of brambles caused by Phytomonas rubi n. sp. J Agric Res 61:685–696Google Scholar
  25. Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179–180.  https://doi.org/10.1038/303179a0CrossRefGoogle Scholar
  26. 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.  https://doi.org/10.1006/mpev.2001.0927CrossRefPubMedGoogle Scholar
  27. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405.  https://doi.org/10.1007/BF02667740CrossRefGoogle Scholar
  28. Kado CI (2014) Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front Microbiol.  https://doi.org/10.3389/fmicb.2014.00340CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kerr A (1969) Transfer of virulence between isolates of Agrobacterium. Nature 223:1175–1176.  https://doi.org/10.1038/2231175a0CrossRefGoogle Scholar
  30. Kerr A, Panagopoulos CG (1977) Biotypes of Agrobacterium radiobacter var. tumefaciens and their biological control. J Phytopathol 90:172–179.  https://doi.org/10.1111/j.1439-0434.1977.tb03233.xCrossRefGoogle Scholar
  31. Knapp S, Chase MW, Clarkson JJ (2004) nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73.  https://doi.org/10.2307/4135490CrossRefGoogle Scholar
  32. Kyndt T, Quispe D, Zhai H, Jarret R, Ghislain M, Liu Q, Gheysen G, Kreuze JF (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 U S A 112:5844–5849.  https://doi.org/10.1073/pnas.1419685112CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lemcke K, Schmülling T (1998) Gain of function assays identify non-rolgenes from Agrobacterium rhizogenes TL-DNA that alter plant morphogenesis or hormone sensitivity. Plant J 15:423–433.  https://doi.org/10.1046/j.1365-313X.1998.00223.xCrossRefPubMedGoogle Scholar
  34. Levesque H, Delepelaire P, Rouzé P, Slightom J, Tepfer D (1988) 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.  https://doi.org/10.1007/BF00019514CrossRefPubMedGoogle Scholar
  35. Lioret C (1956) Sur la mise en évidence d’un acide aminé non-identifié particulier aux tissus de crown-gall. Bull Société Fr Physiol Végétale 2:76Google Scholar
  36. Long N, Ren X, Xiang Z, Wan W, Dong Y (2016) Sequencing and characterization of leaf transcriptomes of six diploid Nicotiana species. J Biol Res Thessalon.  https://doi.org/10.1186/s40709-016-0048-5CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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.  https://doi.org/10.1007/s00299-012-1265-5CrossRefPubMedGoogle Scholar
  38. Matveeva T, Otten L (2019) Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Mol Biol 101:415-437. https://doi.org/10.1007/s11103-019-00913-y
  39. Matveeva TV, Bogomaz DI, Pavlova OA, Nester EW, Lutova LA (2012) Horizontal gene transfer from genus Agrobacterium to the Plant Linaria in nature. Mol Plant Microbe Interact 25:1542–1551.  https://doi.org/10.1094/MPMI-07-12-0169-RCrossRefPubMedGoogle Scholar
  40. Ménagé A, Morel G (1964) Sur la présence d’octopine dans les tissus de crown-gall cultivés in vitro. Comptes Rendus L’Académie Sci Paris 259:4795–4796Google Scholar
  41. Mohajjel Shoja H (2010) Contribution to the study of the Agrobacterium rhizogenes plast genes, rolB and rolC, and their homologs in Nicotiana tabacum. Doctoral dissertation, University of Strasbourg, FranceGoogle Scholar
  42. Mohajjel-Shoja H, Clément B, Perot J, Alioua M, Otten L (2011) Biological Activity of the Agrobacterium rhizogenes–derived trolC gene of Nicotiana tabacum and its functional relation to other plast genes. Mol Plant Microbe Interact 24:44–53.  https://doi.org/10.1094/MPMI-06-10-0139CrossRefPubMedGoogle Scholar
  43. Morris RO (1986) Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Annu Rev Plant Physiol 37:509–538CrossRefGoogle Scholar
  44. 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.  https://doi.org/10.1111/j.1399-3054.1997.tb03050.xCrossRefGoogle Scholar
  45. Ophel K, Kerr A (1990) Agrobacterium vitis sp. nov. for Strains of Agrobacterium biovar 3 from Grapevines. Int J Syst Bacteriol 40:236–241.  https://doi.org/10.1099/00207713-40-3-236CrossRefGoogle Scholar
  46. Petit A, Delhaye S, Tempé J, Morel G (1970) Recherches sur les guanidines des tissus de crown gall. mise en evidence d’une relation biochimique specifique entre le souches d’Agrobacterium tumefaciens et les tumeurs qu’elles induisent. Physiol Végétale 8:205–213Google Scholar
  47. Potuschak T, Palatnik J, Schommer C, Sierro N, Ivanov N, Kwon Y, Genschik P, Davière J-M, Otten L (2019) The Agrobacterium-derived TE-2-6b gene from the natural transformant Nicotiana otophora induces a jaw-D like phenotype and targets the CIN-like TCP transcription factors. The Plant J. https://doi.org/10.1111/tpj.14591
  48. Riker A, Banfield W, Wright W, Keitt G, Sagen HE et al (1930) Studies on infectious hairy root of nursery apple trees. J Agric Res 41:507–540Google Scholar
  49. 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.  https://doi.org/10.1007/BF00283873CrossRefPubMedGoogle Scholar
  50. Roullier C, Duputié A, Wennekes P, Benoit L, Fernández Bringas VM, Rossel G, Tay D, McKey D, Lebot V (2013) Disentangling the origins of cultivated Sweet Potato (Ipomoea batatas (L.) Lam.). PLoS One 8:e62707.  https://doi.org/10.1371/journal.pone.0062707
  51. Schell J, Montagu MV, Beuckeleer MD, Block MD, Depicker A, Wilde MD, Engler G, Genetello C, Hernalsteens JP, Holsters M, Seurinck J, Silva B, Vliet FV, Villarroel R (1979) Interactions and DNA transfer between Agrobacterium tumefaciens, the Ti-Plasmid and the plant host. Proc R Soc B Biol Sci 204:251–266.  https://doi.org/10.1098/rspb.1979.0026CrossRefGoogle Scholar
  52. Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629CrossRefGoogle Scholar
  53. Schröder G, Waffenschmidt S, Weiler EW, Schröder J (1984) The T-region of Ti plasmids codes for an enzyme synthesizing indole-3-acetic acid. Eur J Biochem 138:387–391.  https://doi.org/10.1111/j.1432-1033.1984.tb07927.xCrossRefPubMedGoogle Scholar
  54. Scott IM (1979) Opine content of unorganised and teratomatous tobacco crown gall tissues. Plant Sci Lett 16:239–248.  https://doi.org/10.1016/0304-4211(79)90034-8CrossRefGoogle Scholar
  55. Sierro N, Battey JND, Ouadi S, Bakaher N, Bovet L, Willig A, Goepfert S, Peitsch MC, Ivanov NV (2014) The tobacco genome sequence and its comparison with those of tomato and potato. Nat Commun.  https://doi.org/10.1038/ncomms4833CrossRefPubMedPubMedCentralGoogle Scholar
  56. Slightom JL, Durand-Tardif M, Jouanin L, Tepfer D (1986) Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid. Identification of open reading frames. J Biol Chem 261:108–121PubMedGoogle Scholar
  57. Smith EF, Townsend CO (1907) A plant-tumor of bacterial origin. Science 25:671–673.  https://doi.org/10.1126/science.25.643.671CrossRefPubMedGoogle Scholar
  58. Spena A, Schmülling T, Koncz C, Schell JS (1987) Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants. EMBO J 6:3891–3899CrossRefGoogle Scholar
  59. Suzuki K, Tanaka N, Kamada H, Yamashita I (2001) Mikimopine synthase (mis) gene on pRi1724. Gene 263:49–58.  https://doi.org/10.1016/S0378-1119(00)00578-3CrossRefPubMedGoogle Scholar
  60. Suzuki K, Yamashita I, Tanaka N (2002) Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution. Plant J 32:775–787.  https://doi.org/10.1046/j.1365-313X.2002.01468.xCrossRefPubMedGoogle Scholar
  61. Tepfer D (1990) Genetic transformation using Agrobacterium rhizogenes. Physiol Plant 79:140–146.  https://doi.org/10.1111/j.1399-3054.1990.tb05876.xCrossRefGoogle Scholar
  62. van Nuenen M, de Ruffray P, Otten L (1993) Rapid divergence of Agrobacterium vitis octopine-cucumopine Ti plasmids from a recent common ancestor. Mol Gen Genet (MGG) 240:49–57.  https://doi.org/10.1007/BF00276883CrossRefGoogle Scholar
  63. Wang K, Herrera-Estrella L, Van Montagu M, Zambryski P (1984) Right 25 by terminus sequence of the nopaline t-DNA is essential for and determines direction of DNA transfer from Agrobacterium to the plant genome. Cell 38:455–462.  https://doi.org/10.1016/0092-8674(84)90500-2CrossRefPubMedGoogle Scholar
  64. Ward SM, Fleischmann CE, Turner MF, Sing SE (2009) Hybridization between invasive populations of Dalmatian Toadflax (Linaria dalmatica) and Yellow Toadflax (Linaria vulgaris). Invasive Plant Sci Manag 2:369–378.  https://doi.org/10.1614/IPSM-09-031.1CrossRefGoogle Scholar
  65. White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW (1983) Sequences homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature 301:348–350.  https://doi.org/10.1038/301348a0CrossRefGoogle Scholar
  66. White PR, Braun AC (1941) Crown gall production by bacteria-free tumor tissues. Science 94:239–241CrossRefGoogle Scholar
  67. Yadav NS, Vanderleyden J, Bennett DR, Barnes WM, Chilton MD (1982) Short direct repeats flank the T-DNA on a nopaline Ti plasmid. Proc Natl Acad Sci U S A 79:6322–6326CrossRefGoogle Scholar
  68. Zambryski P, Joos H, Genetello C, Leemans J, Montagu MV, Schell J (1983) Ti plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity. EMBO J 2:2143–2150CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Institut de Biologie Moléculaire des PlantesUniversity of StrasbourgStrasbourgFrance

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