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Ancient horizontal gene transfer from Rhizobium rhizogenes to European genera of the Figwort family (Scrophulariaceae)

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Abstract

Rhizobium rhizogenes exploits horizontal gene transfer as part of its mechanism of pathogenesis. In this respect, genetic material, transfer DNA (T-DNA) from the bacterium, is transferred transiently to the host plant genome. However, plant species within Nicotiana, Linaria and Ipomea genera contain genomic traces of ancient bacterial T-DNA. To determine if ancient bacterial T-DNA is present in uncultivated plants of European genera within Scrophulariaceae, seeds of Linaria, Antirrhinum, Digitalis, and Veronica were analysed for the presence of one of the root oncogenic loci genes; rolC of R. rhizogenes. This study discloses remnants of ancient rolC haplotypes in several species of Linaria, Antirrhinum, Digitalis and Veronica. The distribution of plant species harbouring rolC sequences within each genus was not uniform. In total, 7 of the 16 investigated species were found to be positive for at least one of the rolC haplotypes, where 6 of these are new additions to the group of naturally transformed plants. Sequence alignment showed high interspecies homology of rolC. Five unique rolC haplotypes (rolCa-rolCe) were found in several plant species. The most abundant, rolCa, was identified in all the plant species holding ancient bacterial DNA. Transcripts of rolC were not detected in leaves, which indicates that rolC may not have a function in leaves under non-stress conditions. This study adds Antirrhinum, Digitalis and Veronica to the list of plant genera within Scrophulariaceae which have been subjected to ancient transformation events via horizontal gene transfer from bacteria to plants.

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Data availability

Sequence data that support the findings of this study have been deposited in GenBank with the accession codes LvRolCa (MN097818), LvRolCb (MN097819), LvRolCc (MN097820), LvRolCd (MN097821), LpRolCa (MN097822), AmRolCa (MN097823), DpRolCa (MN097824), DpRolCb (MN097828), DpRolCd (MN097833), DpRolCe (MN097834), VaRolCa (MN097825), VaRolCb (MN097829), VbRolCa (MN097826), VbRolCb (MN097830), VcRolCa (MN097827), VcRolCb (MN097831), VcRolCc (MN097832) and VcRolCe (MN097835).

References

  • Albach DC, Meudt HM, Oxelman B (2005) Piecing together the “new” Plantaginaceae. Am J Bot 92:297–315

    Article  CAS  Google Scholar 

  • Aranda PS, LaJoie DM, Jorcyk CL (2012) Bleach gel: a simple agarose gel for analyzing RNA quality. Electrophoresis 33:366–369

    Article  CAS  Google Scholar 

  • Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2013) GenBank. Nucleic Acids Res 41:D36–D42

    Article  CAS  Google Scholar 

  • Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 101:17747–17752

    Article  CAS  Google Scholar 

  • Chen K, Otten L (2017) Natural Agrobacterium transformants: recent results and some theoretical considerations. Front Plant Sci 8:1600

    Article  Google Scholar 

  • Coordinators NR (2013) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 41:D8–D20

    Article  Google Scholar 

  • Fernandez-Mazuecos M, Blanco-Pastor JL, Vargas P (2013) A phylogeny of Toadflaxes (Linaria Mill.) based on nuclear internal transcribed spacer sequences: systematic and evolutionary consequences. Int J Plant Sci 174:234–249

    Article  CAS  Google Scholar 

  • Fürner IJ, Huffman GA, Amasino RM, Garfinkel DJ, Gordon MP, Nester EW (1986) An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature 329:422–427

    Article  Google Scholar 

  • Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266:605

    Article  CAS  Google Scholar 

  • Hegelund JN, Liang C, Lauridsen UB, Kemp O, Lutken H, Muller R (2018) Increasing genetic variability in oilseed rape (Brassica napus)—genotypes and phenotypes of oilseed rape transformed by wild type Agrobacterium rhizogenes. Plant Sci 271:20–26

    Article  CAS  Google Scholar 

  • Hildebrand EM (1940) Cane gall of brambles caused by Phytomonas rubi n. sp. J Agric Res 61:685–696

    Google Scholar 

  • Hong SB, Hwang I, Dessaux Y, Guyon P, Kim KS, Farrand SK (1997) A T-DNA gene required for agropine biosynthesis by transformed plants is functionally and evolutionarily related to a Ti plasmid gene required for catabolism of agropine by Agrobacterium strains. J Bacteriol 179:4831–4840

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Kyndt T, Quispe D, Zhai H, Jarret R, Ghislain M, Liu Q, Gheysen G, 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 112:5844–5849

    Article  CAS  Google Scholar 

  • Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:W636–W641

    Article  CAS  Google Scholar 

  • 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 25:1542–1551

    Article  CAS  Google Scholar 

  • Matveeva TV, Bogomaz OD, Golovanova LA, Li YS, Dimitrov D (2018) Homologs of the rolC gene of naturally transgenic toadflaxes Linaria vulgaris and Linaria creticola are expressed in vitro. Vavilovskij Žurnal Genetiki i Selekcii 22:273–278

    Google Scholar 

  • Matveeva TV, Otten L (2019) Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Mol Biol 101:415–437

    Article  CAS  Google Scholar 

  • Mordhorst AP, Toonen MAJ, Vries SCd (1997) Plant embryogenesis. Crit Rev Plant Sci 16:535–576

    Article  Google Scholar 

  • Ophel K, Kerr A (1990) Agrobacterium vitis-new species for strains of Agrobacterium biovar 3 from grapevine. Int J Syst Bacteriol 40:236–241

    Article  CAS  Google Scholar 

  • Pavlova OA, Matveeva TV, Lutova LA (2014) Genome of Linaria dalmatica contains Agrobacterium rhizogenes rolC gene homolog. Russ J Genet Appl Res 4:461–465

    Article  Google Scholar 

  • Richardson AO, Palmer JD (2006) Horizontal gene transfer in plants. J Exp Bot 58:1–9

    Article  Google Scholar 

  • Riker AJ (1930) Studies on infectious hairy root of nursery apple trees. J Agric Res 41:507–540

    Google Scholar 

  • Surina B, Pfanzelt S, Einzmann HJR, Albach DC (2014) Bridging the Alps and the Middle East: evolution, phylogeny and systematics of the genus Wulfenia (Plantaginaceae). Taxon 63:843–858

    Article  Google Scholar 

  • Syvanen M (1994) Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet 28:237–261

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115–e115

    Article  CAS  Google Scholar 

  • Vargas P, Rossello JA, Oyama R, Güemes J (2004) Molecular evidence for naturalness of genera in the tribe Antirrhineae (Scrophulariaceae) and three independent evolutionary lineages from the New World and the Old. Plant Syst Evol 249:151–172

    Article  CAS  Google Scholar 

  • Vigalondo B, Fernández-Mazuecos M, Vargas P, Sáez L (2015) Unmasking cryptic species: morphometric and phylogenetic analyses of the Ibero-North African Linaria incarnata complex. Bot J Linn Soc 177:395–417

    Article  Google Scholar 

  • Visscher AM, Paul A-L, Kirst M, Guy CL, Schuerger AC, Ferl RJ (2010) Growth performance and root transcriptome remodeling of Arabidopsis in response to Mars-like levels of magnesium sulfate. PLoS ONE 5:e12348

    Article  Google Scholar 

  • White FF, Ghidossi G, Gordon MP, Nester EW (1982) Tumor induction by Agrobacterium rhizogenes involves the transfer of plasmid DNA to the plant genome. Proc Natl Acad Sci USA 79:3193–3197

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Danish Agency for Science and Higher Education as part of the innovation consortium “Innovative Plants”. Botanischer Garten der Universität Hamburg in Germany, Royal Botanic Gardens (KEW) in England and the University Gardens, Frederiksberg Campus and the seed collection, Taastrup Campus, Faculty of Science, University of Copenhagen in Denmark are acknowledged for providing plant material. Martin Himmelboe and Mikkel Kok Jensen are acknowledged for design of primers. We thank Jesper Cairo Westergaard for proofreading the article.

Funding

This study was funded by the Danish Agency for Science and Higher Education as part of the innovation consortium “Innovative Plants”.

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Authors and Affiliations

  1. Department of Plant and Environmental Sciences, University of Copenhagen, Højbakkegård Allé 9-13, 2630, Taastrup, Denmark

    Sophia Schiermacher Stavnstrup, Jaime Pérez Molina, Henrik Lütken, Renate Müller & Josefine Nymark Hegelund

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  1. Sophia Schiermacher Stavnstrup
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  2. Jaime Pérez Molina
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  3. Henrik Lütken
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  4. Renate Müller
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  5. Josefine Nymark Hegelund
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Contributions

SSS, JPM, RM and JNH conceived and designed the study. SSS and JPM planned and performed experiments with assistance of JNH and HL. SSS and JNH wrote the manuscript. All authors critically revised the manuscript, read and approved the final manuscript.

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Correspondence to Josefine Nymark Hegelund.

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Stavnstrup, S.S., Molina, J.P., Lütken, H. et al. Ancient horizontal gene transfer from Rhizobium rhizogenes to European genera of the Figwort family (Scrophulariaceae). Euphytica 216, 186 (2020). https://doi.org/10.1007/s10681-020-02722-7

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