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Widespread occurrence of natural genetic transformation of plants by Agrobacterium

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Abstract

Key message

Naturally transgenic plant species occur on an unexpectedly large scale.

Abstract

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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Acknowledgements

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

Funding for T.M. was obtained from the Russian Science Foundation (Grant No. 16-16-10010).

Author information

Authors and Affiliations

  1. St. Petersburg State University, University Emb., 7/9, Saint Petersburg, Russia

    Tatiana V. Matveeva

  2. Institut de Biologie Moléculaire des Plantes, 12 Rue du Général Zimmer, 67084, Strasbourg, France

    Léon Otten

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  1. Tatiana V. Matveeva
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  2. Léon Otten
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Contributions

TM found new naturally transgenic plants, TM and LO characterized cT-DNA structures and prepared the manuscript.

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Correspondence to Léon Otten.

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Electronic supplementary material

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11103_2019_913_MOESM1_ESM.jpg

Supplementary material 1 (JPEG 1906 kb) Fig. 1. cus and mas2′ homologs in the genomes of species of genus Arachis and their possible origin

11103_2019_913_MOESM2_ESM.jpg

Supplementary material 2 (JPEG 289 kb) Fig. 2. Species of genus Juglans: relationship (based on ITS) and presence of cT-DNA. Modified from Stanford et al. 2000. J. sigillata has been added according to Dong et al. 2017. Underlined species have been sequenced. Asterisk: species with cT-DNA

11103_2019_913_MOESM3_ESM.jpg

Supplementary material 3 (JPEG 191 kb) Fig. 3. Molecular phylogenetic analysis of vis homologs in P. andersonii, T. orientalis, H. lupulus lupulus and H. lupulus cordifolius by Maximum Likelihood method. L and R: left and right arm of repeat. The percentage of trees in which the associated taxa clustered together is shown next to the branches. The tree is drawn to scale, with branch lengths measured in number of substitutions per site. The analysis involved eight nucleotide sequences. There were a total of 1074 positions in the final dataset. Evolutionary analyses were conducted in MEGA7 (Kumar et al. 2016)

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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

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