Why do plants need agrobacterial genes?

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Abstract

Agrobacterium mediated transformation in nature is the cause of the development of diseases: crown galls and hairy roots. These neoplasms are transgenic tissues on a non-transgenic plant. However, in nature, full-fledged GMOs arise, containing agrobacterial transgenes in every cell and transmitting them in a series of sexual generations. These plants are called naturally transgenic plants or natural GMOs. Over the past 3 years, the list of natural GMO species has been significantly expanded. Due to this, it became possible to make certain generalizations and more substantively discuss the possible evolutionary role of this phenomenon. The presented mini-review is devoted to the generalization of data on the possible functions of genes of agrobacterial origin in plant genomes.

About the authors

Tatyana V. Matveeva

Saint Petersburg State University

Author for correspondence.
Email: radishlet@gmail.com
ORCID iD: 0000-0001-8569-6665
SPIN-code: 3877-6598
Scopus Author ID: 7006494611
ResearcherId: J-6000-2013

Dr. Sci. (Biol.), Professor

Russian Federation, Saint Petersburg

References

  1. Ormeno-Orrillo E, Servín-Garciduenas LE, Rogel MA, et al. Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae fa¬mily in light of genomics. Syst Appl Microbiol. 2015;38(4):287–291. doi: 10.1016/j.syapm.2014.12.002
  2. Chilton MD. Agrobacterium Ti plasmids as a tool for genetic engineering in plants. In: Rains DW, Valentine RC, Hollaender A, editors. Genetic Engineering of Osmoregulation, Basic Life Sciences. Boston: Springer, MA, 1980;14:23–31. doi: 10.1007/978-1-4684-3725-6_3
  3. Nester EW. Agrobacterium: nature’s genetic engineer. Front Plant Sci. 2014;5:730. doi: 10.3389/fpls.2014.00730
  4. Matveeva TV. Agrobacterium-mediated transformation in the evolution of plants. Curr Top Microbiol Immunol. 2018;418:421–441. doi: 10.1007/82_2018_ 80
  5. Aubin E, El Baidouri M, Panaud O. Horizontal Gene Transfers in Plants. Life (Basel). 2021;11(8):857. doi: 10.3390/life11080857
  6. Koonin EV, Wolf YI. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Front Cell Infect Microbiol. 2012;13(2):119. doi: 10.3389/fcimb.2012.00119
  7. Richardson AO, Palmer JD. Horizontal gene transfer in plants. J Exp Bot. 2007;58(1):1–9. doi: 10.1093/jxb/erl148
  8. Husnik F, McCutcheon JP. Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol. 2018;16(2):67–79. doi: 10.1038/nrmicro.2017.137
  9. White FF, Garfinkel DJ, Huffman GA, et al. Sequences homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature. 1983;3012:348–350. doi: 10.1038/301348a0
  10. Kyndt T, Quispe D, Zhai H, et al. The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: an example of a naturally transgenic food crop. PNAS. 2015;112(18):5844–5849. doi: 10.1073/pnas.1419685112
  11. Matveeva TV, Bogomaz DI, Pavlova OA, et al. Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. Mol Plant Microbe Interact. 2012;25(12):1542–1551. doi: 10.1094/MPMI-07-12-0169-R
  12. Matveeva TV, Kosachev PA. Sequences homologous to Agrobacterium rhizogenes rolC in the genome of Linaria acutiloba. Proceedings of 2013 International Conference on Frontiers of Environment, Energy and Bioscience (ICFEEB2013). China, Beijing: 2013. P. 541–546.
  13. Matveeva TV, Sokornova SV. Biological traits of naturally transgenic plants and their evolutional roles. Russian Journal of Plant Physio¬logy. 2017;64(5):635–648. (In Russ.) doi: 10.1134/S1021443717050089
  14. Matveeva TV, Otten L. Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Mol Biol. 2019;101:415–437. doi: 10.1007/s11103-019-00913-y
  15. Matveeva TV. New naturally transgenic plants: 2020 update. Biol Commun. 2021;66(1):36–46. doi: 10.21638/spbu03.2021.105
  16. Lutova LA, Matveeva TV. Gennaya i kletochnaya inzheneriya v biotekhnologii vysshikh rastenii: uchebnik. Tikhonovich IA, editor. Saint Petersburg: Eco-Vector, 2016. 167 p. (In Russ.)
  17. https://www.plantarium.ru/ [Internet]. Plantarium. Rasteniya i lishainiki Rossii i sopredel’nykh stran: otkrytyi onlain atlas i opredelitel’ rastenii [cited 1 November 2021]. Available from: https://www.plantarium.ru/. (In Russ.)
  18. Morton J. Surinam cherry. In: Fruits of warm climates. Miami, 1987. P. 386–388.
  19. Murav’eva DA. Tropicheskie i subtropicheskie lekarstvennye rasteniya 2-e izd. pererab. i dop. Moscow: Meditsina, 1983. 336 p. (In Russ.)
  20. Elenevskii AG. Botanika. Sistematika vysshikh, ili nazemnykh, rastenii. Moscow: Akademiya, 2004. (In Russ.)
  21. Vladimirov IA, Matveeva TV, Lutova LA. Opine biosynthesis and catabolism genes of Agrobacterium tumefaciens and Agrobacterium rhizogenes. Russian Journal of Genetics. 2015;51(2):137–146. (In Russ.) doi: 10.1134/S1022795415020167
  22. Chen K, Dorlhac de Borne F, Sierro N, et al. Organization of the TC and TE cellular T-DNA regions in Nicotiana otophora and functional analysis of three diverged TE-6b genes. Plant J. 2018;94(2):274–287. doi: 10.1111/tpj.13853
  23. Chen K, Otten L. Natural Agrobacterium transformants: recent results and some theoretical considerations. Front Plant Sci. 2017;8:1600. DOI: 10.3389/ fpls.2017.01600
  24. Matveeva TV, Otten L. Opine biosynthesis in naturally transgenic plants: Genes and products. Phytochemistry. 2021;189:112813. doi: 10.1016/j.phytochem.2021.112813
  25. Chen K, Dorlhac de Borne F, Szegedi E, 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;80(4):669–682. doi: 10.1111/tpj.12661
  26. Otten L. Natural agrobacterium-mediated transformation in the genus Nicotiana. In: Ivanov N, Sierro N, Peitsch MC, editors. The Tobacco Plant Genome. Springer, 2020. P. 195–209. doi: 10.1007/978-3-030-29493-9_12
  27. Levesque H, Delepelaire P, Rouze 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. 1988;11:731–744. doi: 10.1007/BF00019514
  28. Altamura MM, Capitani F, Gazza L, et al. The plant oncogene rolB stimulates the formation of flower and root meristemoids in tobacco thin cell layers. New Phytol. 1994;126(2):283–293. doi: 10.1111/j.1469-8137.1994.tb03947.x
  29. Koltunow AM, Johnson SD, Lynch M, et al. Expression of rolB in apomictic Hieracium piloselloides Vill. causes ectopic meristems in planta and changes in ovule formation, where apomixis initiates at higher frequncy. Planta. 2001;214:196–205. doi: 10.1007/s004250100612
  30. Schmülling T, Schell J, Spena A. Single genes from Agrobacterium rhizogenes influence plant development. EMBO J. 1988;7(9): 2621–2629. doi: 10.1002/j.1460-2075.1988.tb03114.x
  31. Casanova E, Trillas MI, Moysset L, Vainstein A. Influence of rol genes in floriculture. Biotechnol Adv. 2005;23(1):3–39. doi: 10.1016/j.biotechadv.2004.06.002
  32. Gorpenchenko TY, Kiselev KV, Bulgakov VP, et al. The Agrobacterium rhizogenes rolC-gene induced somatic embryogenesis and shoot organogenesis in Panax ginseng transformed calluses. Planta. 2006;223:457–467. doi: 10.1007/s00425-005-0102-2
  33. Hansen G, Vaubert D, Heron JH, et al. Phenotypic effects of overexpression of Agrobacterium rhizogenes T-DNA ORF13 in transgenic tobacco plants are mediated by diffusible factor(s). Plant J. 1993;4(3):581–585. doi: 10.1046/j.1365-313X.1993.04030581.x
  34. Lemcke K, Schmülling T. Gain of function assays identify non-rol genes from Agrobacterium rhizogenes TL-DNA that alter plant morphogenesis or hormone sensitivity. Plant J. 1998;5(3):423–433. doi: 10.1046/j.1365-313X.1998.00223.x
  35. Stieger PA, Meyer AD, Kathmann P, et al. The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells. Plant Physiol. 2004;135(3):1798–1808. doi: 10.1104/pp.104.040899
  36. Kodahl N, Müller R, Lütken H. The Agrobacterium rhizogenes oncogenes rolB and ORF13 increase formation of generative shoots and induce dwarfism in Arabidopsis thaliana (L.) Heynh. Plant Sci. 2016;252:22–29. doi: 10.1016/j.plantsci.2016.06.020
  37. Matveeva TV, Lutova LA. Horizontal gene transfer from Agrobacterium to plants. Front Plant Sci. 2014;5:326. doi: 10.3389/fpls.2014.00326
  38. Aoki S, Kawaoka A, Sekine M, Ichikawa T, et al. 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. 1994 Jun 15;243(6):706–710. doi: 10.1007/BF00279581
  39. Matveeva TV, Bogomaz OD, Golovanova LA, et al. Homologs of the rolC gene of naturally transgenic toadflaxes Linaria vulgaris and Linaria creticola are expressed in vitro. Vavilov Journal of Genetics and Breeding. 2018;22(2):273–278. (In Russ.) doi: 10.18699/VJ18.359
  40. Quispe-Huamanquispe DG, Gheysen G, Yang J, et al. The horizontal gene transfer of Agrobacterium T-DNAs into the series Batatas (Genus Ipomoea) genome is not confined to hexaploid sweetpotato. Sci Rep. 2019;9:12584. doi: 10.1038/s41598-019-48691-3
  41. Aoki S, Syono K. 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. 1999;40(2):222–230. doi: 10.1093/oxfordjournals.pcp.a029531
  42. Aoki S, Syono K. Horizontal gene transfer and mutation: ngrol genes in the genome of Nicotiana glauca. PNAS. 1999;96(23): 13229–13234. doi: 10.1073/pnas.96.23.13229
  43. Mohajjel-Shoja H, Clément B, Perot J, et al. Biological activity of the Agrobacterium rhizogenes-derived trolC gene of Nicotiana tabacum and its functional relationship to other plast genes. Mol Plant Microbe Interact. 2011;24(1):44–53. doi: 10.1094/MPMI-06-10-0139
  44. Fründt C, Meyer AD, Ichikawa T, Meins F. A tobacco homologue of the Ri-plasmid orf13 gene causes cell proliferation in carrot root discs. Mol Gen Genet. 1998;259:559–568. doi: 10.1007/s004380050849
  45. Matveeva TV, Sokornova SV, Lutova LA. Influence of Agrobacterium oncogenes on secondary metabolism of plants. Phytochem Rev. 2015;14:541–554. doi: 10.1007/s11101-015-9409-1
  46. Matveeva T, Sokornova S. Agrobacterium rhizogenes Mediated Transformation of Plants for Improvement of Yields of Secondary Metabolites. In: Pavlov A, Bley T, editors. Reference Series in Phytochemistry. Bioprocessing of Plant in vitro Systems. Springer, 2016. 1–42 p. doi: 10.1007/978-3-319-32004-5_18-1
  47. Palazon J, Cusido RM, Gonzalo J, et al. Relation between the amount the rolC gene product and indole alkaloid accumulation in Catharanthus roseus transformed root cultures. J Plant Physiol. 1998a;153(5–6):712–718. doi: 10.1016/S0176-1617(98)80225-3
  48. Palazon J, Cusido RM, Roig C, Pino MT. Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Rep. 1998b;17:384–390. doi: 10.1007/s002990050411
  49. Amini G, Sokornova SV, Mohajjel-Shoja H, et al. Induced expression of rolC for study of its effect on the expression of genes associated with nicotine synthesis in tobacco. Ecological genetics. 2020;18(4):413–422. doi: 10.17816/ecogen33768
  50. Clément B, Perot J, Geoffroy P, et al. Abnormal accumulation of sugars and phenolics in tobacco roots expressing the Agrobacterium T-6b oncogene and the role of these compounds in 6b-induced growth. Mol Plant-Microbe Interact. 2007;20(1):53–62. doi: 10.1094/MPMI-20-0053
  51. Matveeva T, Berezina E, Isaeva I, et al. Influence of some rol genes on sugar content in Nicotiana and Vaccinium. BIO Web of Conferences. 2020;18:00020. doi: 10.1051/bioconf/20201800020
  52. Chen K, Dorlhac de Borne F, Julio E, et al. Root-specific expression of opine genes and opine accumulation in some cultivars of the naturally occurring GMO Nicotiana tabacum. Plant J. 2016;87(3):258–269. doi: 10.1111/tpj.13196
  53. Zhang Y, Wang D, Wang Y, et al. Parasitic plant dodder (Cuscuta spp.): a new natural Agrobacterium-to-plant horizontal gene transfer species. Sci China Life Sci. 2020;63:312–316. doi: 10.1007/s11427-019-1588-x
  54. Beauchamp CJ, Chilton WS, Dion P, Antoun H. Fungal catabolism of crown gall opines. Appl Environ Microbiol. 1990;56(1): 150–155. doi: 10.1128/aem.56.1.150-155.1990
  55. Sokornova SV, Matveeva TV. Phylogenetic Relationships of Ascomycetes Opine Synthases. BMC Bioinformatics. (accepted for publication)
  56. Geddes BA, Paramasivan P, Joffrin A, et al. Enginee¬ring transkingdom signalling in plants to control gene expression in rhizosphere bacteria. Nat Commun. 2019;10:3430. doi: 10.1038/s41467-019-10882-x

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2. Fig. 1. Number of genera of natural GMOs with different cT-DNA structures (a) and types of extended cT-DNA structures (b)

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3. Fig. 1. Number of genera of natural GMOs with different cT-DNA structures (a) and types of extended cT-DNA structures (b)

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Copyright (c) 2021 Matveeva T.V.

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