Naturally transgenic plant species occur on an unexpectedly large scale.
Agrobacterium-mediated gene transfer leads to the formation of crown galls or hairy roots, due to expression of transferred T-DNA genes. Spontaneous regeneration of transformed cells can produce natural transformants carrying cellular T-DNA (cT-DNA) sequences of bacterial origin. This particular type of horizontal gene transfer (HGT) could play a role in plant evolution. However, the material available today is not enough for generalizations concerning the role of Agrobacterium in HGT from bacteria to plants. In this study, we searched for T-DNA-like genes in the sequenced genomes of dicots and monocots. We demonstrate the presence of cT-DNAs in 23 out of 275 dicot species, within genera Eutrema, Arachis, Nissolia, Quillaja, Euphorbia, Parasponia, Trema, Humulus, Psidium, Eugenia, Juglans, Azadirachta, Silene, Dianthus, Vaccinium, Camellia, and Cuscuta. Analysis of transcriptome data of 356 dicot species yielded 16 additional naturally transgenic species. Thus, HGT from Agrobacterium to dicots is remarkably widespread. Opine synthesis genes are most frequent, followed by plast genes. Species in the genera Parasponia, Trema, Camellia, Azadirachta, Quillaja, and Diospyros contain a combination of plast and opine genes. Some are intact and expressed, but the majority have internal stop codons. Among the sequenced monocot species, Dioscorea alata (greater yam) and Musa acuminata (banana) also contain T-DNA-like sequences. The identified examples are valuable material for future research on the role of Agrobacterium-derived genes in plant evolution, for investigations on Agrobacterium strain diversity, and for studies on the function and evolution of cT-DNA genes in natural transformants.
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Acuna R, Padilla BE, Florez-Ramos CP, Rubio JD, Herrera JC, Benavides P, Lee SJ, Yeats TH, Egan AN, Doyle JJ, Rose JK (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci USA 109:4197–4202
Angiosperm Phylogeny Group (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181(1):1–20
Binns AN, Sciaky D, Wood HN (1982) Variation in hormone autonomy and regenerative potential of cells transformed by strain A66 of Agrobacterium tumefaciens. Cell 31:605–612
Chen K (2016) Sequencing and functional analysis of cT-DNAs in Nicotiana. PhD Thesis University of Strasbourg, France
Chen K, Otten L (2017) Natural Agrobacterium transformants: recent results and some theoretical considerations. Front Plant Sci 8:e1600
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
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 GMO Nicotiana tabacum. Plant J 87:258–269
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
Cormier F, Lawac F, Maledon E, Gravillon MC, Nudol E, Mourmet P, Vignes H, Chaïr H, Arnau G (2019) A reference high-density genetic map of greater yam (Dioscorea alata L.). Theor Appl Genet 132:1733–1744
Dong W, Xu C, Li W, Xie X, Lu Y, Liu Y, Jin X, Suo Z (2017) Phylogenetic resolution in Juglans based on complete chloroplast genomes and nuclear DNA sequences. Front Plant Sci 8:e1148
e Santos DN, de Souza L, Nilson JF, de Oliveira AL (2015) Study of supercritical extraction from Brazilian cherry seeds (Eugenia uniflora L.) with bioactive compounds. Food Bioprod Process 94:365–374
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fournier P, Paulus F, Otten L (1993) IS870 requires a 5′-CTAG-3′ sequence to generate the stop codon for its large ORF1. J Bact 175:3151–3160
Gao C, Reno X, Mason AS, Liu H, Xiao M, Li J, Fu D (2014) Horizontal gene transfer in plants. Funct Integr Genomics 14(1):23–29
Gelvin SB (2017) Integration of Agrobacterium T-DNA into the plant genome. Annu Rev Genet 51:195–217
Guillermo S, Lavia GI, Fernandez A, Krapovickas A, Ducasse DA, Bertioli DJ, Moscone EA (2007) Genomic relationships between the cultivated peanut (Arachis hypogaea, Leguminosae) and its close relatives revealed by double GISH. Am J Bot 94(12):1963–1971
Hansen G, Larribe M, Vaubert D, Tempé J, Biermann B, Montoya AL, Chilton M-D, Brevet J (1991) Agrobacterium rhizogenes pRi8196: mapping and DNA sequence of functions involved in mannopine synthesis and hairy root function. Proc Natl Acad Sci USA 88:7763–7767
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
Kausik B, Chattopadhyay I, Banerjee RK, Bandyopadhyay U (2002) Biological activities and medicinal properties of Neem (Azadirachta indica). Curr Sci 82(11):1336–1345
Kochert G, Stalker HT, Gimenes M, Galgaro L, Lopes CR, Moore K (1996) RFLP and cytogenetic evidence on the origin and evolution of allotetraploid domesticated peanut, Arachis hypogaea (Leguminosae). Am J Bot 83:1282–1291
Kononov ME, Bassuner B, Gelvin SB (1997) Integration of T-DNA binary vector ‘backbone’ sequences into the tobacco genome: evidence for multiple complex patterns of integration. Plant J 11:945–957
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Kyndt T, Quispe D, Zhai H, Jarret R, Ghislain M, Gheysen Liu Q, 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 USA 112(18):5844–5849
Machida Y, Sakurai M, Kiyokawa S, Ubasawa A, Suzuki Y, Ikeda J-E (1984) Nucleotide sequence of the insertion sequence found in the T-DNA region of mutant Ti plasmid pTiA66 and distribution of its homologues in octopine Ti plasmid. Proc Natl Acad Sci USA 81:7495–7499
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(12):1542–1551
Matveeva TV, Bogomaz OD, Golovanova LA, Li YuS, Dimitrov D (2018) Homologs of the rolC gene of naturally transgenic toadflaxes Linaria vulgaris and Linaria creticola are expressed in vitro. Vavilovskii Zhurnal Genetiki i Selektsii 22(2):273–278
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 relationship to other plast genes. Mol Plant Microbe Interact 24:44–53
Morton J (1987) Surinam cherry. In: Fruits of warm climates. Miami, p 386–388
Muravieva DA (1983) Tropical and subtropical medicinal plants. Moscow: Medicine (in Russian)
O’Leary NA, Wright MW, Brister JR et al (2016) Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44(D1):D733–D745
Ooms G, Bakker A, Molendijk L, Wullems GJ, Gordon MP, Nester EW, Schilperoort RA (1982) T-DNA organization in homogeneous and heterogeneous octopine-type crown gall tissues of Nicotiana tabacum. Cell 30:589–597
Op den Camp RHM, Polone E, Fedorova E, Roelofsen W, Squartini A, Op den Camp HJM, Bisseling T, Geurts R (2012) Nonlegume Parasponia andersonii deploys a broad Rhizobium host range strategy resulting in largely variable symbiotic effectiveness. Mol Plant Microbe Interact 25:954–963
Otten L (2018) The Agrobacterium phenotypic plasticity (plast) genes. Curr Top Microbiol Immunol 418:375–419
Otten L, Canaday J, Gérard JC, Fournier P, Crouzet P, Paulus F (1992) Evolution of agrobacteria and their Ti plasmids: a review. Mol Plant Microbe Interact 5:79–87
Pattee HE, Stalker HT, Giesbrecht FG (1998) Reproductive efficiency in reciprocal crosses of Arachis monticola with A. hypogaea subspecies. Peanut Sci 25:7–12
Pavlova OA, Matveeva TV, Lutova LA (2013) Linaria dalmatica genome contains a homologue of rolC gene of Agrobacterium rhizogenes. Ecol Genet 11:10–15
Ramanathan V, Veluthambi K (1995) Transfer of non-T-DNA portions of the Agrobacterium tumefaciens Ti plasmid from the left terminus of TL-DNA. Plant Mol Biol 28:1149–1154
Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, McLeod R, Roberts CW (2006) Evolutionary origins of the eukaryotic shikimate pathway: gene fusions horizontal gene transfer and endosymbiotic replacements. Eukaryot Cell 5(9):1517–1531
Schäfer W, Görz A, Kahl G (1987) T-DNA integration and expression in a monocot crop plant after induction of Agrobacterium. Nature 327:529–532
Stanford AM, Harden R, Parks CR (2000) Phylogeny and biogeography of Juglans (Juglandaceae) based on matK and ITS sequence data. Am J Bot 87:872–882
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tanaka Y, Brugliera F, Chandler S (2009) Recent progress of flower colour modification by biotechnology. Int J Mol Sc 10:5350–5369
Ulker B, Li Y, Rosso MG, Logemann E, Somssich IE, Weisshaar B (2008) T-DNA-mediated transfer of Agrobacterium tumefaciens chromosomal DNA into plants. Nat Biotech 26:1015–1017
van Kregten M, de Pater S, Romeijn R, van Schendel R, Hooykaas PJJ, Tijsterman M (2016) T-DNA integration in plants results from polymerase-θ—mediated DNA repair. Nat Plants 2:16164
Wei C, Yang H, Wang S et al (2018) Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. Proc Natl Acad Sci USA 115(18):E4151–E4158
White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW (1983) Sequence homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature 301:348–350
This work was partially carried out using the software of the St. Petersburg State University Resource Center “Development of molecular and cellular technologies”. We would like to dedicate this work to the memory of Rob Schilperoort, one of the pioneers in Agrobacterium research and founder of Plant Molecular Biology.
Funding for T.M. was obtained from the Russian Science Foundation (Grant No. 16-16-10010).
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Matveeva, T.V., Otten, L. Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Mol Biol 101, 415–437 (2019). https://doi.org/10.1007/s11103-019-00913-y
- Naturally transgenic plants
- Horizontal gene transfer
- Whole-genome shotgun contigs
- Transcriptome shotgun assembly