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DNA Transfer to Plants by Agrobacterium rhizogenes: A Model for Genetic Communication Between Species and Biospheres

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Transgenesis and Secondary Metabolism

Part of the book series: Reference Series in Phytochemistry ((RSP))

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Abstract

Agrobacterium rhizogenes genetically transforms dicotyledonous plants, producing a transformed phenotype caused by the Ri TL-DNA (root-inducing, left hand, transferred DNA). Phenotypic changes include wrinkled leaves, reduced apical dominance, shortened internodes, changes in flowering, including a switch from biennialism to annualism, and altered secondary metabolite production, including increases in alkaloids. The transformed phenotype is correlated with a reduction in the accumulation of polyamines; it is mimicked using an inhibitor of polyamine synthesis. Roots transformed by A. rhizogenes grow in axenic culture, permitting the production of secondary metabolites in bioreactors, the modeling of the rhizosphere, and the propagation of arbuscular micorrhizal fungi for biofertilization.

A general view of parasexual DNA transfer postulates the exchange of genetic information among genetically distant plant genomes, with A. rhizogenes acting as an intermediary, thanks to its wide host spectrum for DNA transfer to plant, fungal, and animal cells and to exchange with other bacteria, including Acinetobacter baylyi, which uses homologous recombination to incorporate plant DNA into its genome. Marker exchange served to document DNA transfer from leaves and roots to A. baylyi. Transferred functions in this hypothetical system connecting phylogenetically distant genomes included genes encoding antibiotic resistance, nutritional mediators of plant/microorganism interactions (calystegins and betaines), and an elicitor of plant host defense responses (β-cryptogein), whose expression in tobacco resulted in increased resistance to Phytophthora. Thus, DNA encoding a trait of adaptive significance in a plant could be acquired by soil bacteria and eventually transferred into multiple plant species, thanks to the presence on the Ri TL-DNA of genes that increase developmental plasticity (organ formation) in the host plant, ensuring the sexual transmission of the foreign DNA. The image of genetic football is invoked to convey the multiple facets of this largely theoretical system of this parasexual DNA transfer.

The plausibility of a role for DNA transfer in the origin and future of our biosphere was tested by attaching unprotected DNA and seeds of Arabidopsis thaliana and tobacco to the outside of the International Space Station to simulate an interplanetary transfer of life. Seeds and fragments of DNA survived 18 months of exposure, indicating that DNA transfer could play a role in biosphere formation and evolution, particularly when protected from short wavelength UV by flavonoids in the seed coat.

So what molecular biology has done you see, is to prove beyond any doubt but in a totally new way the complete independence of the genetic information from events occurring outside or even inside the cell, to prove by the very structure of the genetic code and the way it is transcribed that no information from outside of any kind can ever penetrate the inheritable genetic message.

Jacques Monod one of the founders of molecular biology, quoted in the Eighth day of Creation, by Horace Freeland Judson, Simon and Schuster 1979.

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Abbreviations

crypt :

Gene encoding β-cryptogein

DFMO:

DL-Difluoromethylornithine

DNA:

Deoxyribonucleic acid

HGT:

Horizontal gene transfer

nptII :

Gene encoding kanamycin resistance

PCR:

Polymerase chain reaction

Ri TL-DNA:

Root-inducing left hand, transferred DNA

RNA:

Ribonucleic acid

rolA,B… :

Root locus A B… from the Ri TL-DNA

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Acknowledgments

The core research was performed at the Institut National de la Recherche Agronomique by Tepfer, D., Goldmann, A., Message, B., Pamboukdjian, N., and Maille, M. I am indebted to my collaborators for their hard work, dedication, and tolerance: Ackerman, C. Ba, A.M., Balaji, B., Bandyopadhyay, M., Ben-Hayyim, G., Blackhalla, N., Boivin, C., Bonnett, H., Bouchez, D., Broglie, R., Burchell, M., Burnet, M., Burtin, D., Casse-Delbart, F., Charbonnier, C., Charpin, I., Chaudhuri, K., Chevalier, D., Chilton, M.D., Chioccioli, M., Cocking, E., Damon, J.P., Das, S., Davey, M., David, C., Delepelaire, P., Dénarié, J., Deni, J., Devendra, B.N., Drong, R., Ducrot, P.H., Durand-Tardif, M., El Amrani, A., Elbein, A.D., Fosket, D., Garcia-Gonzales, R., Ghosh, B., Goldmann, A., Gonzaleza, M.C., Guetarda, D., Guyon, P., Heisler, L., Helgeson, J., Hoffmann, S.V., Corbineau, F., Jerling, A., Jha, S., Jouanin, L., Jung, G., Kenney, J., Kollmann, A., Kostrzak, A., Lallemand, J.Y., Lambert, C., Larue, T.A., Leach F., Leach, S., Lee, S.-H., Lépingle, A., Levesque, H., Limami A., Maille, M., Mansouri, H., Martin, C., Martin-Tanguy, J., Message, B., Metzger, L., Michael, A., Milat, M.L., Molyneux, R., Monneuse, M.O., Mugnier, J., Pamboukdjian, N., Pan, Y.T., Paynot, M., Pellegrineschi, A., Perica, M.C., Petit, A., Piche, Y., Pniewski, T., Power, B., Prost, R., Rosenberg, C., Rouzé, P., Sala M., Seruga, M., Slightom, J., Sun, L.Y., Tempé, J., Touraud, G., Wain-Hobson, S., Yacoub, A. For materials, moral support, and advice I am indebted to (among others) the following benefactors: Adholeya, A., Bevan, M., Bourgin, J.P., Chua, N.-H., Cambell, R., Crespin, M., de Vries, J., Descoins, C., Field, D., Grunstein, M., Helgeson, J., Horneck, G., Kemp, J., Maliga, P., Ohkawa, H., Rabbow, E., Schneiderman, H., Shields, R., Tempé, J., Tepfer, M., Tepfer, R., Tobin, E., Torrey, J., and Wackernagel, W. Support (partial list) came from CEFIPRA, the Rockefeller Foundation, the Universities of Oregon, Aarhaus, Kobe, Singapore and Zagreb, from INRA, the CNRS, ESA, the CNES, TERI, the DLR, and NATO.

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  1. Institut National de la Recherche Agronomique, PESSAC, Versailles, 78026, France

    David Tepfer

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  1. Department of Botany, Calcutta University, Kolkata, West Bengal, India

    Sumita Jha

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Tepfer, D. (2016). DNA Transfer to Plants by Agrobacterium rhizogenes: A Model for Genetic Communication Between Species and Biospheres. In: Jha, S. (eds) Transgenesis and Secondary Metabolism. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-27490-4_19-1

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  • DOI: https://doi.org/10.1007/978-3-319-27490-4_19-1

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