A quarter-century ago, a sequence homologous to the Ri plasmid (pRi) T-DNA of Agrobacterium rhizogenes was detected in the genome of untransformed tree tobacco, Nicotiana glauca, and was named “cellular T-DNA” (cT-DNA). The origin of the homologous sequences in tobacco remained unknown for a long period, but at present, it has been clearly demonstrated that the cT-DNA is the pRi T-DNA inserted by ancient infection with mikimopine-type A. rhizogenes. The cT-DNA of N. glauca is composed of an imperfect inverted repeat and it contains homologues of some pRi T-DNA genes involved in adventitious root formation and opine synthesis, which are called NgrolB, NgrolC, NgORF13, NgORF14, and Ngmis. In spite of the footprint of ancient insertion of pRi T-DNA, these homologues are still expressed not only in genetic tumors of F1 hybrids of N. glauca x N. langsdorffii but also in some organs of N. glauca, although at a low level. The cT-DNA is also found in some other species of the genus Nicotiana, with mikimopine-type cT-DNA contained in at least three, N. tomentosa, N. tomentosiformis, and N. tabacum. Therefore, there is a possibility that multiple infection events occurred independently in several ancestors of Nicotiana. Furthermore, some plant species in different families also contain cT-DNA-like sequences, although the details are still unknown. Tumors are spontaneously generated on some plants in the absence of tumorigenic microorganisms. Hybrid plants of Nicotiana species also form genetic tumors, but the mechanism of this tumorigenesis is still unknown. One of the parents of the hybrid usually contains cT-DNA, implying that it is the causal factor of tumorigenesis, although the causal association between the cT-DNA and tumorigenesis remains unsolved. Since pRi-transgenic plants exhibit a peculiar phenotype, the so-called “hairy root syndrome”, which shows advantageous traits in some cases, ancient pRi-transformed plants might also have predominated in competition with parental plants or survived under a harsh climate. Therefore, the insertion events of T-DNA into the genome of plants might have influenced their evolution, resulting in the creation of new plant species.
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7 References
Ahuja MA (1962) A cytogenetic study of heritable tumors in Nicotiana species hybrids. Genetics 47: 865-880
Ahuja MA (1966) Genetic tumors and introgression in Nicotiana. Genetics 54: 316
Ahuja MA (1968) An hypothesis and evidence concerning the genetic components controlling tumor formation in Nicotiana. Mol Gen Genet 103: 176-184
Ahuja MA (1998) Genetic tumors in Nicotiana and other plants. Q Rev Biol 73: 439-462
Ames IH, Mistretta PW (1975) Auxin: its role in genetic tumor induction. Plant Physiol 56: 744-746
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
Aoki S, Ito M (2000) Molecular phylogeny of Nicotiana (Solanaceae) based on the nucleotide sequence of the matK gene. Plant Bio 2: 316-324
Aoki S, Ito M (2001) Consideration of the classification system and phytogeogra-phy of the Nicotiana (Solanaceae) by the analysis of molecular phylogeny. Pro Jap Soc PI Tax 16: 49-67
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 tumours of N. glauca × N. langsdorffii. Mol Gen Genet 243: 706-710
Aoki S, Syono K (1999a) Function of Ngrol genes in the evolution of Nicotiana glauca: Conservation of the function of NgORF13 and NgORF14 after an-cient infection by an Agrobacterium rhizogenes-like ancestor. Plant Cell Physiol 40: 222-230
Aoki S, Syono K (1999b) Horizontal gene transfer and mutation: Ngrol genes in the genome of Nicotiana glauca. Proc Natl Acad Sci USA 96: 13229-13234
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: 323-334
Bayer MH (1967) Thin-layer chromatography of auxin and inhibitors in Nicotiana glauca, N. langsdorffii and three of their tumor-forming hybrids. Planta 72: 329-337
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
Broothaerts W, Mitchell HJ, Weir B, Kaines S, Smith LM, Yang W, Mayer JE, Roa-Rodriguez C, Jefferson RA (2005) Gene transfer to plants by diverse species of bacteria. Nature 433: 629-633
Camilleri C, Jouanin L (1991) The TR-DNA region carrying the auxin synthesis genes of the Agrobacterium rhizogenes agropine-type plasmid pRiA4: nucleo-tide sequence analysis and introduction into tobacco plants. Mol Plant-Microbe Interact 4: 155-162
Casanova E, Trillas MI, Moysset L, Vainstein A (2005) Influence of rol genes in floriculture. Biotechnol Adv 23: 3-39
De Buck S, Jacobs A, Van Montagu M, Depicker A (1999) The DNA sequences of T-DNA junctions suggest that complex T-DNA loci are formed by a re-combination process resembling T-DNA integration. Plant J 20: 295-304
Dessaux Y, Petit A, Tempé J (1993) Chemistry and biochemistry of opines, chemical mediators of parasitism. Phytochemistry 34: 31-38
Feng XH, Dube SK, Bottino PJ, Kung SD (1990) Restoration of shooty morphol-ogy of a nontumorous mutant of Nicotiana glauca × N. langsdorffii by cyto-kinin and the isopentenyltransferase gene. Plant Mol Biol 15: 407-420
Fründt C, Meyer AD, Ichikawa T, Meins F, Jr. (1998) A tobacco homologue of the Ri-plasmid orf13 gene causes cell proliferation in carrot root discs. Mol Gen Genet 259: 559-568
Fujita T (1994) Screening of genes related to tumor formation in tobacco genetic tumors. Plant Tiss Cult Lett 11: 171-177
Fujita T, Ichikawa T, Syono K (1991) Changes in morphology, levels of endoge-nous IAA and protein composition in relation to the development of tobacco genetic tumor induced in the dark. Plant Cell Physiol 32: 169-177
Furner IJ, A. HG, Amasino RM, Garfinkel DJ, Gordon MP, Nester EW (1986) An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature 319: 422-427
Gelvin SB (2005) Agricultural biotechnology: gene exchange by design. Nature 433: 583-584
Goodspeed TH (1954) The Genus Nicotiana, Chronica Botanica. Waltham, Mas-sachusetts
Handayani NSN, Moriuchi H, Yamakawa M, Yamashita I, Yoshida K, Tanaka N (2005) Characterization of the rolB promoter on mikimopine-type pRi1724 T-DNA. Plant Sci 108: 1353-1364
Hansen G, Larribe M, Vaubert D, Tempé J, Biermann BJ, Montoya AL, Chilton M-D, Brevet J (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
Ichikawa T, Kobayashi M, Nakagawa S, Sakurai A, Syono K (1989) Morphologi-cal observations and qualitative and quantitative studies of auxins after induc-tion of tobacco genetic tumor. Plant Cell Physiol 30: 57-63
Ichikawa T, Ozeki Y, Syono K (1990) Evidence for the expression of the rol genes of Nicotiana glauca in genetic tumors of N. glauca X N. langsdorffii. Mol Gen Genet 220: 177-180
Japan Tobacco Inc. (1990) Illustrated Book of The Genus Nicotiana. Seibundo Shinkosha Publishing Co., Tokyo, Japan
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
Journin L, Bouchezs D, Drong RF, Tepfer D, Slightom JL (1989) Analysis of TR-DNA/plant junctions in the genome of Convolvulus arvensis clone trans-formed by Agrobacterium rhizogenes strain A4. Plant Mol Biol 12: 72-85
Kostoff D (1930) Tumors and other malformations on certain Nicotiana hybrids. Zentralbl Bakteriol Parasitenkd Infectionskr Hyg Abt 1: Org 81: 244-260
Kung SD (1989) Genetic tumors in Nicotiana. Bot Bull Acad Sinica 30: 231-240
Kwok WW, Nester EW, Gordon MP (1985) Unusual plasmid DNA organization in an octopine crown gall tumor. Nucleic Acids Res 13: 459-471
Limami MA, Sun LY, Douat C, Helgeson J, Tepfer D (1998) Natural genetic transformation by Agrobacterium rhizogenes . Annual flowering in two bien-nials, belgian endive and carrot. Plant Physiol 118: 543-550
Meyer AD, Ichikawa T, Meins F, Jr. (1995) Horizontal gene transfer: regulated expression of a tobacco homologue of the Agrobacterium rhizogenes rolC gene. Mol Gen Genet 249: 265-273
Moriguchi K, Maeda Y, Satou M, Hardayani NS, Kataoka M, Tanaka N, Yoshida K (2001) The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rhizobiaceae. J Mol Biol 307: 771-784
Moriuchi H, Okamoto C, Nishihama R, Yamashita I, Machida Y, Tanaka N (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
Nachmias B, Ugolini S, Ricci MD, Pellegrini MG, Bogani P, Bettini P, Inzé D, Buiatti M (1987) Tumor formation and morphogenesis on different Nicotiana sp. and hybrids induced by Agrobacterium tumefaciens T-DNA mutants. Dev Genet 8: 61-71
Näf U (1958) Studies on tumor formation in Nicotiana hybrids. I. The classifica-tion of the parents into two etiologically significant groups. Growth 22: 167-180
Nagata N, Kosono S, Sekine M, Shinmyo A, Syono K (1995) The regulatory func-tions of the rolB and rolC genes of Agrobacterium rhizogenes are conserved in the homologous genes (Ngrol) of Nicotiana glauca in tobacco genetic tu-mors. Plant Cell Physiol 36: 1003-1012
Nagata N, Kosono S, Sekine M, Shinmyo A, Syono K (1996) Different expression patterns of the promoter of the NgrolB and NgrolC genes during the devel-opment of tobacco genetic tumors. Plant Cell Physiol 37: 489-493
Nandi SK, de Klerk GJM, Parker CW, Palni LSM (1990a) Endogenous cytokinin levels and metabolism of zeatin riboside in genetic tumour tissues and non-tumourous tissues of tobacco. Physiol Plant 78: 197-204
Nandi SK, Palni LSM, Parker CW (1990b) Dynamic of endogenous cytokinin during the growth cycle of a hormone-autotrophic genetic tumor line of to-bacco. Plant Physiol 94: 1084-1089
Oger P, Mansouri H, Dessaux Y (2000) Effect of crop rotation and soil cover on alteration of the soil microflora generated by the culture of transgenic plants producing opines. Mol Ecol 9: 881-890
Oger P, Petit A, Dessaux Y (1997) Genetically engineered plants producing opines alter their biological environment. Nat Biotechnol 15: 369-372
Okamuro JK, Goldberg RB (1985) Tobacco single-copy DNA is highly homolo-gous to sequences present in the genomes of its diploid progenies. Mol Gen Genet 198: 290-298
Röder FT, Schmulling 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
Serino G, Clerot D, Brevet J, Costantino P, Cardarelli M (1994) rol genes of Agrobacterium rhizogenes cucumopine strain: sequence, effects and pattern of expression. Plant Mol Biol 26: 415-422
Sinkar VP, White FF, Furner IJ, Abrahamsen M, Pythoud F, Gordon MP (1988) Reversion of aberrant plants transformed with Agrobacterium rhizogenes is associated with the transcriptional inactivation of the TL-DNA genes. Plant Physiol 86: 584-590
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 HH (1968) Recent cytogenetic studies in the genus Nicotiana. Adv Genet 14: 1-54
Smith HH (1988) The inheritance of genetic tumors in Nicotiana hybrids. J Hered-ity 79: 277-283
Spanò L, Pomponi M, Costantino P, van Slogteren GMS, Tempé J (1982) Identifi-cation of T-DNA in the root-inducting plasmid of the agropine type Agrobac-terium rhizogenes 1855. Plant Mol Biol 1: 291-300
Suzuki K, Tanaka N, Kamada H, Yamashita I (2001) Mikimopine synthase (mis) gene on pRi1724. Gene 263: 49-58
Suzuki K, Yamashita I, Tanaka N (2002) Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution. Plant J 32: 775-787
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
Tanaka N, Matsumoto T (1993) Regenerants from Ajuga hairy roots with high productivity of 20-hydroxyecdysone. Plant Cell Rep 13: 87-90
Tanaka N, Yamakawa M, Yamashita I (1998) Characterization of transcription of genes involved in hairy root induction on pRi1724 core-T-DNA in two Ajuga reptans hairy root lines. Plant Sci 137: 95-105
Taylor BH, White FF, Nester EW, Gordon MP (1985) Transcription of Agrobac-terium rhizogenes A4 T-DNA. Mol Gen Genet 201: 546-553
Tepfer D (1982) La transfromation génétique de plants supérieures par Agrobacte-rium rhizogenes. In 2ed Colloque sur les Recherches Fruitéres - Bordeaux, pp 47-59
Tepfer D (1984) Transformation of several species of higher plants by Agrobacte-rium rhizogenes: sexual transmission of the transformed genotype and pheno-type. Cell 37: 959-967
Thomashow MF, Nutter R, Montoya AL, Gordon MP, Nester EW (1980) Integra-tion and organization of Ti plasmid sequences in crown gall tumors. Cell 19: 729-739
Udagawa M, Aoki S, Syono K (2004) Expression analysis of the NgORF13 pro-moter during the development of tobacco genetic tumors. Plant Cell Physiol 45: 1023-1031
White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW (1983) Sequence homologous to Agrobacterium rhizogenes T-DNA in the genomes of unin-fected plants. Nature 301: 348-350
White FF, Ghidossi G, Gordon MP, Nester EW (1982) Tumor induction by Agro-bacterium rhizogenes involves the transfer of plasmid DNA to the plant ge-nome. Proc Natl Acad Sci USA 79: 3193-3197
Yang F, Simpson RB (1981) Revertant seedling from crown gall tumors retain a portion of the bacterial Ti plasmid sequences. Proc Natl Acad Sci USA 78: 4151-4155
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Tanaka, N. (2008). Horizontal Gene Transfer. In: Tzfira, T., Citovsky, V. (eds) Agrobacterium: From Biology to Biotechnology. Springer, New York, NY. https://doi.org/10.1007/978-0-387-72290-0_17
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