Biological traits of naturally transgenic plants and their evolutional roles

Russian Journal of Plant Physiology

Volumn 64, Issue 5, 2017, Pages 635-648

  Matveeva, T V ^a   Sokornova, S V ^a  

^a ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

cT DNA; horizontal gene transfer; naturally transgenic plants

Indexed keywords

EID: 85027832958     PISSN: 10214437     EISSN: None     Source Type: Journal    
DOI: 10.1134/S1021443717050089     Document Type: Review

References (87)

1. http://isaaa.org
2. Chilton, M.D., Drummond, M.H., Merio, D.J., Sciaky, D., Montoya, A.L., Gordon, M.P., and Nester, E.W., Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis, Cell, 1977, vol. 11, no. 2, pp. 263–271.
3. Otten, L., de Greye, H., Hernalsteens, J.P., van Montagu, M., Schieder, O., Straub, J., and Schell, J., Mendelian transmission of genes introduced into plants by the Ti plasmids of Agrobacterium tumefaciens, Mol. Gen. Genet., 1981, vol. 183, no. 2, pp. 209–213.
4. Britton, M.T., Escobar, M.A., and Dandekar, A.M., The oncogenes of Agrobacterium tumefaciens and Agrobacterium rhizogenes, in Agrobacterium: from Biology to Biotechnology, Tzfira, T. and Citovsky, V., Eds., New York: Springer, 2008, pp. 523–563.
5. Meyer, A., Tempe, J., and Costantino, P., Hairy root: a molecular overview. Functional analysis of Agrobacterium rhizogenes T-DNA genes, in Plant Microbe Interactions, Stacey, G. and Keen, N.T., Eds., St. Paul: APS Press, 2000, pp. 93–139.
6. Vain, P., Thirty years of plant transformation technology development, Plant Biotechnol. J., 2007, vol. 5, pp. 221–229.
7. White, F.F., Garfinkel, D.J., Huffman, G.A., Gordon, M.P., and Nester, E.W., Sequence homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants, Nature, 1983, vol. 301, pp. 348–350.
8. Furner, I.J., Huffman, G.A., Amasino, R.M., Garfinkel, D.J., Gordon, M.P., and Nester, E.W., An Agrobacterium transformation in the evolution of the genus Nicotiana, Nature, 1986, vol. 319, no. 6052, pp. 422–427.
9. Chen, K., Dorlhac, de Borne, F., Szegedi, E., and Otten, L., 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., 2014, vol. 80, no. 4, pp. 669–682.
10. Matveeva, T.V., Bogomaz, D.I., Pavlova, O.A., Nester, E.W., and Lutova, L.A., Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature, Mol. Plant–Microbe Interact., 2012, vol. 25, pp. 1542–1551.
11. Kyndt, T., Quispe, D., Zhai, H., Jarret, R., Ghislain, M., Liu, Q., Gheysen, G., and Kreuze, J.F., 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. USA, 2015, vol. 112, no. 18, p. 5844–5849.
12. Matveeva, T.V., Naturally transgenic plants as a model for the study of the delayed environmental risks of GMO cultivation, Russ. J. Genet., 2016, vol. 6, no. 6, pp. 698–704.
13. Suzuki, K., Yamashita, I., and Tanaka, N., Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution, Plant J., 2002, vol. 32, no. 5, pp. 775–787.
14. Intrieri, M.C. and Buiatti, M., The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana, Mol. Phylogenet. Evol., 2001, vol. 20, pp. 100–110.
15. Pavlova, O.A., Nucleotide sequences in Linaria dalmatica (L.) P. Mill, acquired as a result of horizontal gene transfer, Extended Abstract of Cand. Sci. (Biol.) Dissertation, St. Petersburg: St. Petersburg Gos. Univ., 2013.
16. Angiosperm Phylogeny Group, An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV, Bot. J. Linn. Soc., 2016, vol. 181, no. 1, pp. 1–20.
17. Knapp, S., Chase, M.W., and Clarkson, J.J., Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae), Taxon, 2014, vol. 53, no. 1, pp. 73–82.
18. Goodspeed, T.H., The Genus Nicotiana, Waltham, MA: Chronica Botanica, 1954.
19. Clarkson, J.J., Knapp, S., Garcia, V.F., Olmstead, R.G., Leitch, A.R., and Chase, M.W., Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions, Mol. Phylogenet. Evol., 2004, vol. 33, pp. 75–90.
20. Mohajjel-Shoja, H., Clément, B., Perot, J., Alioua, M., and Otten, L., Biological activity of the Agrobacterium rhizogenes-derived trolC gene of Nicotiana tabacum and its functional relation to other plast genes, Mol. Plant–Microbe Interact., 2011, vol. 24, no. 1, pp. 44–53.
21. Matveeva, T.V. and Kosachev, P.A., Sequences homologous to Agrobacterium rhizogenes rolC in the genome of Linaria acutiloba, in Int. Conf. on Frontiers of Environment, Energy and Bioscience (ICFEEB 2013), Zheng, D., Ed., Lancaster: DES Tech. Publ. Inc., 2013, pp. 541–546.
22. Blanco-Pastor, J.L., Vargas, P., and Pfeilm, B.E., Coalescent simulations reveal hybridization and incomplete lineage sorting in Mediterranean Linaria, PLoS One, 2012, vol. 7: e39089, doi: org/ doi 10.1371/journal.pone.0039089
23. White, F.F., Taylor, B.H., Huffman, G.A., Gordon, M.P., and Nester, E.W., Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes, J. Bacteriol., 1985, vol. 164, no. 1, pp. 33–44.
24. Schmülling, T., Fladung, M., Grossmann, K., and Schell, J., Hormonal content and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA, Plant J., 1993, pp. 371–382.
25. Matveeva, T.V., Frolova, N.V., Dodueva, I.E., Buzovkina, I.S., Lutova, L.A., Smets, R., and Onckelen, H.V., Hormonal control of tumor formation in radish, J. Plant Growth Regul., 2004, vol. 23, no. 1, pp. 37–43.
26. Frolova, N.V., Matveeva, T.V., and Lutova, L.A., Use of the in vivo agrobacterial transformation for obtaining phenoicopies of tumor-formation in non-tumorous line of Raphanus sativus L., Biotech. Russia, 2004, no. 4, pp. 1–7.
27. Ichikawa, T., Ozeki, Y., and Syono, K., Evidence for the expression of the rol genes of Nicotiana glauca in genetic tumors of N. glauca × N. langsdorfii, Mol. Gen. Genet., 1990, vol. 220, pp. 177–180.
28. Naf, U., Studies on tumor formation in Nicotiana hybrids. I. The classification of the parents into two etiologically significant groups, Growth, 1958, vol. 22, pp. 167–180.
29. Plant Genetic Engineering. Laboratory Manual, Draper, J., Scott, R., Armitage, P., and Walden, R., Eds., London: Blackwell Scientific Ltd., 1988.
30. Bogani, P., Buiatti, M., Tegli, S., Pellegrini, M.G., Bettini, P., and Scala, A., Interspecific differences in differentiation and dedifferentiation patterns in the genus Nicotiana, Plant Syst. Evol., 1985, vol. 151, pp. 19–29.
31. Matveeva, T.V., Pavlova, O.A., Ivanitskii, K.I., and Lutova, L.A., Horizontal gene transfer from Agrobacterium to Nicotiana genus plants: evolutionary prerequisites and consequences, Vestn. St. Petersburg Gos. Univ., Ser. 3, 2009, no. 4, pp. 58–65.
32. Matveeva, T.V., Pigichka, T.Yu., and Lutova, L.A., Characteristics of morphogenetic reactions of Nicotiana langsdorffii transformed by wild-type Agrobacterium strains in vitro, Ecol. Genet., 2007, vol. 5, no. 3, pp. 21–24.
33. Matveeva, T.V., Horizontal gene transfer from Agrobacterium spp. to the higher plants, Extended Abstract of Doctoral (Biol.) Dissertation, St. Petersburg: St. Petersburg Gos. Univ., 2013.
34. Dessai, A.P., Gosukonda, R.M., Blay, E., Dumenyo, C.K., Medina-Bolivar, F., and Prakash, C. S., Plant regeneration of sweetpotato (Ipomoea batatas L.) from leaf explants in vitro using a two-stage protocol, Sci. Hortic., 1995, vol. 62, no. 4, pp. 217–224.
35. Kumar, A.H.G., Ku, A.T., Agarwal, P., Mahesh, S., and Yeh, K.W., Protuberance-mediated high frequency of adventitious shoot regeneration from sweet potato leaf explants [Ipomoea batatas (L.) Lam.], Biotechnology, 2013, vol. 94, no. 4, pp. 445–450.
36. Bogani, P., Intrieri, M.C., and Buiatti, M., Genetic and epigenetic factors in the control of dedifferentiation/tumourisation in Nicotiana species and hybrids, Plant Biosyst., 2011, pp. 511–521.
37. Domoratskaya, D.A. and Matveeva, T.V., Optimization method for obtaining a culture of Linaria maroccana L. “hairy roots,” in Mater. V Mezhd. Shkoly dlya molodykh uchenykh “Embriologiya, genetika i biotekhnologiya,” Tezisy dokladov (Proc. V Int. School for Young Scientists “Embryology, Genetics, and Biotechnology,” Abstracts of Papers), St. Petersburg, 2016, p. 68.
38. Newell, C.A., Lowe, J.M., Merryweather, A., Rooke, L.M., and Hamilton, W.D.O., Transformation of sweet potato (Ipomoea batatas (L.) Lam.) with Agrobacterium tumefaciens and regeneration of plants expressing cowpea trypsin inhibitor and snowdrop lectin, Plant Sci., 1995, vol. 107, no. 2, pp. 215–227.
39. Gama, M.I.C., Leite, J.R.P., Cordeiro, A.R., and Cantliffe, D.J., Transgenic sweet potato plants obtained by Agrobacterium tumefaciens mediated transformation, Plant Cell Tissue Organ Cult., 1996, vol. 46, pp. 237–244.
40. Limami, M.A., Sun, L.Y., Douatm, C., Helgeson, J., and Tepfer, D., Natural genetic transformation by Agrobacterium rhizogenes. Annual flowering in two biennials, Belgian endive and carrot, Plant Physiol., 1998, vol. 118, pp. 543–550.
41. Goodspeed, T.H., On the evolution of the genus Nicotiana, Proc. Natl. Acad. Sci. USA, 1947, vol. 33, pp. 158–171.
42. Sutton, D.A., A Revision of the Tribe Antirrhineae, London: Oxford University Press, 1988.
43. http://ngb.org/year_of/index.cfm?YOID=27
44. https://florabase.dpaw.wa.gov.au
45. Scott, G.I., Best, R., Rosegrant, M., and Bokanga, M., Roots and Tubers in the Global Food System: A Vision Statement to the Year 2020, Lima, Peru: Int. Potato Center, 2000.
46. Hong, S.B., Hwang, I., Dessaux, Y., Guyon, P., Kim, K.S., and Farrand, S.K., A T-DNA gene required for agropine biosynthesis by transformed plants is functionally and evolutionary related to a Ti plasmid gene required for catabolism by Agrobacterium strains, J. Bacteriol., 1997, vol. 179, pp. 4831–4840.
47. Gelvin, S.B., Chemical signaling between Agrobacterium and its host plant, in Molecular Signals in Plant–Microbe Communications, Verma, D.P.S., Ed., 1992, pp. 137–167.
48. Oger, P.M., Mansouri, H., Nesme, X., and Dessaux, Y., Engineering root exudation of Lotus toward the production of two novel carbon compounds leads to the selection of distinct microbial populations in the rhizosphere, Microb. Ecol., 2004, vol. 47, no. 1, p. 96–103.
49. Oger, P., Petit, A., and Dessaux, Y., Genetically engineered plants producing opines alter their biological environment, Nat. Biotechnol., 1997, vol. 15, pp. 369–372.
50. Beauchamp, C.J., Chilton, W.S., Dion, P., and Antoun, H., Fungal catabolism of crown gall opines, Appl. Environ. Microbiol., 1990, vol. 56, no. 1, pp. 150–155.
51. Flores, H.E., Hoy, M.W., and Pickard, J.J., Secondary metabolites from root cultures, Trends Biotechnol., 1987, vol. 5, no. 3, pp. 64–69.
52. Hamill, J.D., Parr, A.J., Rhodes, M.J.C., Robins, R.J., and Walton, N.J., New routes to plant secondary products, Nat. Biotechnol., 1987, vol. 5, pp. 800–804.
53. Rhodes, M.J.C., Robins, R.J., Hamill, J.D., Parr, A.J., and Walton, N.J., Secondary product formation using Agrobacterium rhizogenes-transformed “hairy root” cultures, News Lett., 1987, vol. 53, p. 2–15.
54. Matveeva, T.V., Sokornova, S.V., and Lutova, L.A., Influence of Agrobacterium oncogenes on secondary metabolism of plants, Phytochem. Rev., 2015, vol. 14, p. 541.
55. Matveeva, T. and Sokornova, S., Agrobacterium rhizogenes mediated transformation of plants for improvement of yields of secondary metabolites, in Reference Series in Phytochemistry. Bioprocessing of Plant In Vitro Systems, Pavlov, A. and Bley, T., Eds., Springer, 2016, pp. 1–42.
56. Widhalm, J.R. and Rhodes, D., Biosynthesis and molecular actions of specialized 1,4-naphthoquinone natural products produced by horticultural plants, Hortic. Res., 2016, vol. 3, p. 16046.
57. Kuang, K.R. and Lu, A.M., Flora of China, Bejing: Beijing Science and Technology Press, 2005.
58. Janakat, S. and Al-Merie, H., Evaluation of hepatoprotective effect of Pistacia lentiscus, Phillyrea latifolia and Nicotiana glauca, J. Ethnopharmacol., 2002, vol. 83, nos. 1–2, pp. 135–138.
59. Stojanov, N., Our Medicinal Plants, Stojanov, N., Ed., Sofia: Nauka i Iskustvo, 1973, part II.
60. Kitagawa, I., Yoshihara, M., Tani, T., and Yosioka, I., On the constituents of Linaria japonica Miq. II. The structure of linaridial, a new cis-clerodane-type diterpene dialdehyde, Chem. Pharm. Bull., 1976, vol. 24, no. 2, pp. 294–302.
61. Pochapski, M.T., Fosquiera, E.C., Esmerino, L.A., dos Santos, E.B., Farago, P.V., Santos, F.A., and Groppo, F.C., Phytochemical screening, antioxidant, and antimicrobial activities of the crude leaves extract from Ipomoea batatas (L.) Lam., Pharmacogn. Mag., 2011, vol. 7, no. 26, pp. 165–170.
62. Matveeva, T.V. and Lutova, L.A., Horizontal gene transfer from Agrobacterium to plants, Front. Plant Sci., 2014, vol. 5, p. 326.
63. Venditti, A., Serrilli, A.M., and di Cecco, M., Phytochemical analysis of Plantago sempervirens from Majella National Park, Nat. Prod. Res., 2012, vol. 26, no. 2, pp. 2035–2039.
64. El-Naggar, L.J. and Beal, J.L., Iridoids. An updated review. Part I, J. Nat. Prod., 1980, vol. 43, pp. 649–707.
65. Boros, C.A. and Stermitz, F.R., Iridoids. An updated review. Part II, J. Nat. Prod., 1990, vol. 53, pp. 1055–1147.
66. Harborne, J.B. and Valdés, B., Identification of scutellarein 40-methyl ether in Linaria aeruginea, Phytochem. Rev., 1971, vol. 10, pp. 2850–2851.
67. Kuptsova, L.P. and Ban’kovskii, A.I., A new flavonoid from some species of toadflax, Khim. Prir. Soed., 1970, vol. 6, no. 1, pp. 128–129.
68. Smirnova, I.P., Zapesochnaya, G.G., Sheichenko, V.I., and Ban’kovskii, A.I., Structure of acetylpectolinarin, a new acylated flavonoid from plants of the genus Linaria, Chem. Nat. Compd., 1974, vol. 10, no. 3, pp. 320–324.
69. Ercil, D. and Sakar, M.K., Chemical constituents of Linaria aucheri, Turk. J. Chem., 2004, vol. 28, pp. 133–139.
70. Kitagawa, I., Yoshihara, M., and Kamigauchi, T., Linarienone, a new cis-clerodane-type diteppene from the subterranean part of Linaria japonica Miq., Tetrahedron Lett., 1977, vol. 14, pp. 1221–1224.
71. Kitagawa, I., Yoshihara, M., Tani, T., and Yosioka, I., Linaridial, a new cis-clerodane-type diterpene dialdehyde, from Linaria japonica Miq., Tetrahedron Lett., 1975, vol. 1, pp. 23–26.
72. Feliciano, A.S., Gordaliza, M., del Corral, J.M.M., Mahiques, M.M., Castro, M.A., and Feliciano, A.S., Neoclerodane diterpenoids from roots of Linaria saxatilis var. glutinosa, Phytochemistry, 1993, vol. 33, no. 3, pp. 631–633.
73. Sticher, O., Plant mono-, di- and sesquiterpenoids with pharmacological or therapeutical activity, in Proc. the 1st Int. Congr. on Medicinal Plant Research, Section A “New Natural Products and Plant Drugs with Pharmacological, Biological or Therapeutical Activity” (September 6–10, 1976, Germany, Univ. Munich), Wagner, H. and Wolff, P., Eds., Berlin: Springer, 1977, pp. 137–176.
74. Marak, H.B., Biere, A., and van Damme, J.M.M., Two herbivore-deterrent iridoid glycosides reduce the in vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L., Chemoecology, 2002, vol. 12, pp. 185–192.
75. Marak, H.B., Biere, A., and van Damme, J.M.M., Systemic, genotype-specific induction of two herbivoredeterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (Rob.) Niessel, J. Chem. Ecol., 2002, vol. 28, no. 12, pp. 2429–2448.
76. Biere, A., Marak, H.B., and van Damme, J.M.M., Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia, 2004, vol. 140, pp. 430–441.
77. Nicoletti, M., Serafini, M., Garbarino, J.A., and Gambaro, V., A chemosystematic study of Scrophulariaceae iridoid glycosides, G. Bot. Ital., 1988, vol. 122, nos. 1–2, pp. 13–24.
78. Sampaio-Santos, M.I. and Kaplan, M.A.C., Biosynthesis significance of iridoids in chemosystematics, J. Braz. Chem. Soc., 2001, vol. 12, no. 2, p. 144.
79. Meira, M., Silva, E.P., David, J.M., and David, J.P., Review of the genus Ipomoea: traditional uses, chemistry and biological activities, Rev. Bras. Farmacogn., 2012, vol. 22, no. 3, pp. 682–713.
80. Fatibello-Filho, O. and Vieira, I.C., Flow injection spectrophotometric determination of sulfite using a crude extract of sweet potato root (Ipomoea batatas (L.) Lam.) as a source of polyphenol oxidase, Anal. Chim. Acta, 1997, vol. 354, nos. 1–3, pp. 51–57.
81. Mwenifumbo, J.C. and Tyndale, R.F., Molecular genetics of nicotine metabolism, in Nicotine Psychopharmacology, Henningfield, J.E., Calvento, E., and Pogun, S., Eds., Berlin: Springer, 2009.
82. Weeks, W.W., Relationship between leaf chemistry and organoleptic properties of tobacco smoke, in Tobacco: Production, Chemistry, and Technology, Davis, D.L. and Nielsen, M.T., Eds., Malden, MA: Iowa State Press, Blackwell Science, Inc., 1999, pp. 304–312.
83. Bailey, J.A., Burden, R.S., and Vincent, G.G., Capsidiol: an antifungal compound produced in Nicotiana tabacum and Nicotiana clevelandii following infection with tobacco necrosis virus, Phytochemistry, 1975, vol. 14, pp. 597–582.
84. Bailey, J.A., Vincent, G.G., and Burden, R.S., The antifungal activity of glutinosone and capsidiol and their accumulation in virus-infected tobacco species, Physiol. Mol. Plant Path., 1976, vol. 8, pp. 35–41.
85. Palazón, J., Cusidó, R.M., Roig, C., and Pinol, M.T., Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants, Plant Cell Rep., 1998, vol. 17, no. 3, pp. 84–90.
86. Kessler, D., Bhattacharya, S., Diezel, C., Rothe, E., Gase, K., Schottner, M., and Baldwin, I.T., Unpredictability of nectar nicotine promotes outcrossing by hummingbirds in Nicotiana attenuata, Plant J., 2012, vol. 71, pp. 529–538.
87. Bush, L., Hempflin, W.P., and Burton, H., Biosynthesis of nicotine and related compounds, in Analytical Determination of Nicotine and Related Compounds and Their Metabolites, Gorrod, J.W. and Jacob, P., III, Eds., Amsterdam, Netherlands: Elsevier Science, 1999, pp. 13–44.