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

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.