Evolution of symbiotic genetic systems in rhizobia

Probable molecular and population-genetic mechanisms of microevolution of the genetic systems controlling interactions of root nodule bacteria with legumes, as well as the main pathways of their macroevolution, are reviewed. It is suggested that synchronization of the rates of bacterial and plant genome evolution was the condition necessary for coevolution of root nodule bacteria and legumes. This could have been achieved via an increase in recombination activity of the bacterial genome during the formation of the virulence gene system. The latter process was associated with changes in the pattern of certain genes controlling different metabolic functions in nonsymbiotic nitrogen-fixing organisms (origin of Bradyrhizobium and Azorhizobium, the ''primary'' root nodule bacteria capable of nitrogen fixation ex planta). Increased genetic instability could have been to the transfer of main symbiotic genes into plasmids. This, in turn, resulted in the development of a complex genetic population structure (origin of ''nonsymbiotic'' subpopulations providing for a high frequency of horizontal transfer of symbiotic genes) and made possible the development of new rhizobia forms via symbiotic gene transfer to different soil bacteria (origin of Rhizobium, the ''secondary'' root nodule bacteria incapable of nitrogen fixation ex planta). Comparing the patterns of genes controlling interactions with plants in Rhizobium and Agrobacterium showed that symbiotic and parasitic traits of these related microorganisms developed independently, although similar mechanisms could be responsible for evolution of nodulation in the rhizobia-legume system and for evolution of phytoparasitic systems. It is suggested that both Rhizobium and Agrobacterium originated from saprophytic soil microorganisms capable of synthesizing certain cell wall molecules (polysaccharides, glucans, etc.) allowing them to persist in tissues of higher plants.