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.
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References
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.a029531
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) 42:979–991
Bouchez D, Tourneur J (1991) Organization of the agropine synthesis region of the T-DNA of the Ri plasmid from Agrobacterium rhizogenes. Plasmid 25:27–39
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.37.1.53
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 235:292–303
Chen K (2016) Sequencing and functional analysis of cT-DNAs in Nicotiana. Doctoral dissertation, University of Strasbourg, France
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.13196
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.12661
Chen K, Otten L (2016) Morphological analysis of the 6b oncogene-induced enation syndrome. Planta 243:131–148. https://doi.org/10.1007/s00425-015-2387-0
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
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 11:263–271
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/s11627-001-0120-0
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.x
De Cleene M, De Ley J (1981) The host range of infectious hairy-root. Bot Rev 47:147–194. https://doi.org/10.1007/BF02868853
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 173–197
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 259:559–568
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/10.1038/319422a0
Gelvin SB (2012) Traversing the cell: Agrobacterium T-DNA’s journey to the host genome. Front Plant Sci. https://doi.org/10.3389/fpls.2012.00052
Gordon JE, Christie PJ (2014) The Agrobacterium Ti plasmids. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.PLAS-0010-2013
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 77:2693–2697
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-6-092
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/s00438-002-0707-0
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 287:654–656
Hildebrand EM (1940) Cane gall of brambles caused by Phytomonas rubi n. sp. J Agric Res 61:685–696
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/10.1038/303179a0
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.2001.0927
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/BF02667740
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.2014.00340
Kerr A (1969) Transfer of virulence between isolates of Agrobacterium. Nature 223:1175–1176. https://doi.org/10.1038/2231175a0
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.x
Knapp S, Chase MW, Clarkson JJ (2004) nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73. https://doi.org/10.2307/4135490
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.1419685112
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.x
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/BF00019514
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 2:76
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/s40709-016-0048-5
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/s00299-012-1265-5
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
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-R
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 259:4795–4796
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, France
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-06-10-0139
Morris RO (1986) Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Annu Rev Plant Physiol 37:509–538
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.x
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/10.1099/00207713-40-3-236
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 8:205–213
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
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 41:507–540
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/BF00283873
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
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.1979.0026
Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629
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.x
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)90034-8
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/ncomms4833
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 261:108–121
Smith EF, Townsend CO (1907) A plant-tumor of bacterial origin. Science 25:671–673. https://doi.org/10.1126/science.25.643.671
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 6:3891–3899
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)00578-3
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.x
Tepfer D (1990) Genetic transformation using Agrobacterium rhizogenes. Physiol Plant 79:140–146. https://doi.org/10.1111/j.1399-3054.1990.tb05876.x
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/BF00276883
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)90500-2
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-09-031.1
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/10.1038/301348a0
White PR, Braun AC (1941) Crown gall production by bacteria-free tumor tissues. Science 94:239–241
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 79:6322–6326
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 2:2143–2150
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Since submission of this manuscript, it has been shown that a large number of natural plant species carry cT-DNA sequences (Matveeva and Otten 2019). Also, an important step towards the elucidation of the function of the N. otophora 6b gene was made by showing that the TE-6B protein targets the CIN-TCP transcription factors and thereby leads to important growth changes in the model plant Arabidopsis (Potuschak et al. 2019).
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Otten, L. (2020). Natural Agrobacterium-Mediated Transformation in the Genus Nicotiana. In: Ivanov, N.V., Sierro, N., Peitsch, M.C. (eds) The Tobacco Plant Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-29493-9_12
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