Description of new naturally transgenic plants and estimation of time intervals of horizontal gene transfer events from agrobacteria to plants
- Authors: Shaposhnikov A.D.1, Matveeva T.V.2,3
-
Affiliations:
- St. Petersburg State University
- Saint Petersburg State University
- All-Russian Research Institute of Plant Protection
- Section: Opinions, discussions
- Submitted: 17.10.2025
- Accepted: 19.11.2025
- Published: 19.11.2025
- URL: https://journals.eco-vector.com/ecolgenet/article/view/693516
- DOI: https://doi.org/10.17816/ecogen693516
- ID: 693516
Cite item
Full Text
Abstract
BACKGROUND: Horizontal gene transfer from agrobacteria to dicotyledonous plants leads to the emergence of naturally transgenic species containing DNA fragments known as cellular T-DNA (cT-DNA). Such plants are also referred to as natural GMOs (nGMOs). The continuous expansion of nucleotide databases and the development of bioinformatic methods have enabled the systematic identification of natural transgenes in the deposited genomes of various dicot species, expanding the list of known nGMOs. Detailed investigation of the horizontally transferred sequences opens up opportunities for their comparative analysis.
AIM: The aim of this work was to search for and analyze sequences homologous to Agrobacterium T-DNA in the genomes of dicotyledonous plants, and to subsequently determine the timing of horizontal gene transfer events based on a comparison of extended inverted repeats of cT-DNA.
METHODS: The work used data from the WGS and TSA nucleotide sequence databases, as well as BLAST alignment algorithms.
RESULTS: As a result, 93 new species of naturally transgenic plants were discovered. Based on the analysis of cT-DNA presented as inverted repeats, the approximate timing of horizontal gene transfer events was estimated for 28 nGMO species. The conducted analysis revealed many common features in the evolution of transgenes between the nGMOs we discovered and other examples of horizontal gene transfer. It was established that the transfer events occurred in the period from 0.62 to 24 million years ago, which spans three periods of the Cenozoic era.
CONCLUSION: The discovery of new naturally transgenic plant species expands our understanding of the prevalence of horizontal gene transfer from agrobacteria to dicotyledonous plants and the evolutionary role of cT-DNA, while also providing material for further research and comparison with other cases of horizontal gene transfer. Dating the events of horizontal gene transfer makes it possible to estimate the time frame of this process in the evolution of naturally transgenic plants.
Full Text
About the authors
Anton D. Shaposhnikov
St. Petersburg State University
Author for correspondence.
Email: st096319@student.spbu.ru
ORCID iD: 0009-0002-7905-2999
SPIN-code: 5145-8352
junior researcher
Russian Federation, 7–9 Universitetskaya emb., Saint Petersburg, 199034, Russian Federation;Tatiana V. Matveeva
Saint Petersburg State University; All-Russian Research Institute of Plant Protection
Email: radishlet@gmail.com
ORCID iD: 0000-0001-8569-6665
SPIN-code: 3877-6598
Scopus Author ID: 7006494611
Dr. Sci. (Biology), Professor, department of genetics and biotechnology
Russian Federation, 7–9 Universitetskaya emb., Saint Petersburg, 199034, Russian Federation; Podbelskogo, 3, St.Petersburg – Pushkin, 196608, Russian FederationReferences
- Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: building the web of life. Nat Rev Genet. 2015;16(8):472-482. doi: 10.1038/nrg3962
- Matveeva T. New naturally transgenic plants: 2020 update. BioComm. 2021;66(1). doi: 10.21638/spbu03.2021.105
- White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW. Sequences homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature. 1983;301(5898):348-350. doi: 10.1038/301348a0
- Intrieri MC, Buiatti M. The Horizontal Transfer of Agrobacterium rhizogenes Genes and the Evolution of the Genus Nicotiana. Molecular Phylogenetics and Evolution. 2001;20(1):100-110. doi: 10.1006/mpev.2001.0927
- Matveeva TV, Bogomaz DI, Pavlova OA, Nester EW, Lutova LA. Horizontal Gene Transfer from Genus Agrobacterium to the Plant Linaria in Nature. MPMI. 2012;25(12):1542-1551. doi: 10.1094/MPMI-07-12-0169-R
- 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. Proc Natl Acad Sci USA. 2015;112(18):5844-5849. doi: 10.1073/pnas.1419685112
- 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. The Plant Journal. 2018;94(2):274-287. doi: 10.1111/tpj.13853
- Matveeva TV, Bogomaz OD, Golovanova LA, Li YuS, Dimitrov D. Homologs of the rolC gene of naturally transgenic toadflaxes Linaria vulgaris and Linaria creticola are expressed in vitro. Vestn VOGiS. 2018;22(2):273-278. doi: 10.18699/VJ18.359
- Matveeva TV, Otten L. Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Mol Biol. 2019;101(4-5):415-437. doi: 10.1007/s11103-019-00913-y
- Matveeva TV. Why do plants need agrobacterial genes? Ecological genetics. 2021;19(4):365-375. doi: 10.17816/ecogen89905
- Matveeva TV. Agrobacterium-Mediated Transformation in the Evolution of Plants. In: Gelvin SB, ed. Agrobacterium Biology. Vol 418. Current Topics in Microbiology and Immunology. Springer International Publishing; 2018:421-441. doi: 10.1007/82_2018_80
- Matveeva TМ. Natural GMOs: a history of research. Ecological genetics. 2022;20(1S):7-8. doi: 10.17816/ecogen112371
- Zhidkin RR, Matveeva TV. Phylogeny problems of the genus Vaccinium L. and ways to solve them. Ecological genetics. 2022;20(2):151-164. doi: 10.17816/ecogen109142
- Zhidkin R, Zhurbenko P, Bogomaz O, et al. Biodiversity of rolB/C-like Natural Transgene in the Genus Vaccinium L. and Its Application for Phylogenetic Studies. IJMS. 2023;24(8):6932. doi: 10.3390/ijms24086932
- Chen K, Zhurbenko P, Danilov L, Matveeva T, Otten L. Conservation of an Agrobacterium cT-DNA insert in Camellia section Thea reveals the ancient origin of tea plants from a genetically modified ancestor. Front Plant Sci. 2022;13:997762. doi: 10.3389/fpls.2022.997762
- Matveeva TV. Naturally transgenic plants as a model for the study of delayed environmental risks of cultivation of GMOs. Ecological genetics. 2015;13(2):118-126. doi: 10.17816/ecogen132118-126
- Lipatov PYu, Bogomaz FD, Gosudarev KD, et al. New cellular T-DNAs in naturally transgenic plants. Ecological genetics. 2022;20(1S):40-41. doi: 10.17816/ecogen112352
- Altschul S. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. 1997;25(17):3389-3402. doi: 10.1093/nar/25.17.3389
- The 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;181(1):1-20. doi: 10.1111/boj.12385
- Gaut BS, Morton BR, McCaig BC, Clegg MT. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA. 1996;93(19):10274-10279. doi: 10.1073/pnas.93.19.10274
- Bogomaz FD, Matveeva TV. Expression sequences of opine synthase genes in natural GMOs based on analysis of their transcriptomes. Biotehnologiâ i selekciâ rastenij. 2022;5(3):15-24. doi: 10.30901/2658-6266-2022-3-o2
- Pavlova OA, Matveeva TV, Lutova LA. Genome of Linaria dalmatica contains the homolog of Agrobacterium rhizogenes rolC gene. Ecological genetics. 2013;11(2):10-15. doi: 10.17816/ecogen11210-15
- 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. The Plant Journal. 2014;80(4):669-682. doi: 10.1111/tpj.12661
- Otten L, Liu H, Meeprom N, Linan A, Puglisi C, Chen K. Accumulation of numerous cellular T‐ DNA sequences in the genus Diospyros by multiple rounds of natural transformation. The Plant Journal. 2025;122(3):e70202. doi: 10.1111/tpj.70202
- Van Kregten M, De Pater S, Romeijn R, Van Schendel R, Hooykaas PJJ, Tijsterman M. T-DNA integration in plants results from polymerase-θ-mediated DNA repair. Nature Plants. 2016;2(11):16164. doi: 10.1038/nplants.2016.164
- 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
- Li WH, Gojobori T, Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981;292(5820):237-239. doi: 10.1038/292237a0
- Alsmark C, Foster PG, Sicheritz-Ponten T, Nakjang S, Martin Embley T, Hirt RP. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 2013;14(2):R19. doi: 10.1186/gb-2013-14-2-r19
- Chen R, Huangfu L, Lu Y, et al. Adaptive innovation of green plants by horizontal gene transfer. Biotechnology Advances. 2021;46:107671. doi: 10.1016/j.biotechadv.2020.107671
- Weisberg AJ, Davis EW, Tabima J, et al. Unexpected conservation and global transmission of agrobacterial virulence plasmids. Science. 2020;368(6495):eaba5256. doi: 10.1126/science.aba5256
Supplementary files


