Experimental Evolution of a Plant Pathogen into a Legume Symbiont

<div><p>Rhizobia are phylogenetically disparate α- and β-proteobacteria that have achieved the environmentally essential function of fixing atmospheric nitrogen in symbiosis with legumes. Ample evidence indicates that horizontal transfer of symbiotic plasmids/islands has played a crucial role in rhizobia evolution. However, adaptive mechanisms that allow the recipient genomes to express symbiotic traits are unknown. Here, we report on the experimental evolution of a pathogenic <em>Ralstonia solanacearum</em> chimera carrying the symbiotic plasmid of the rhizobium <em>Cupriavidus taiwanensis</em> into <em>Mimosa</em> nodulating and infecting symbionts. Two types of adaptive mutations in the <em>hrpG</em>-controlled virulence pathway of <em>R. solanacearum</em> were identified that are crucial for the transition from pathogenicity towards mutualism. Inactivation of the <em>hrcV</em> structural gene of the type III secretion system allowed nodulation and early infection to take place, whereas inactivation of the master virulence regulator <em>hrpG</em> allowed intracellular infection of nodule cells. Our findings predict that natural selection of adaptive changes in the legume environment following horizontal transfer has been a major driving force in rhizobia evolution and diversification and show the potential of experimental evolution to decipher the mechanisms leading to symbiosis.</p></div>

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