Adaptive macroevolution of legume-rhizobia symbiosis

Legume-rhizobia symbiosis (LRS) is considered as a unique model of evolutionary biology, which allows us to study the trade-off between the adaptive and progressive evolution in biological systems formed by prokaryotes and eukaryotes. Macroevolution of LRS results is establishing the compartments for hosting microsymbionts that activate the development of N 2-fixing nodules by special signals - lipo-сhito-oligosaccharide Nod-factors. This evolution is dissected into a number of stages connected with the formation of: a) nodule endophytic associations (ancestral forms of rhizobia which retained the ability to fix CO 2 and N 2 in pure culture characteristic for their ancestors, occupy the intercellular spaces in nodules); b) primitive subcellular symbiosis (rhizobia which lost the ability to fix CO 2 are located in infection threads penetrating into plant cells); c) intracellular mutualism (rhizobia, penetrated the plant cells to form the non-specialized symbiosomes where fix N 2, maintaining the reproductive activity); d) symbiosis of altruistic type (rhizobia in specialized symbiosomes differentiate into bacteroids which irreversibly lost their reproductive activity providing a sharp increase in the N 2-fixation intensity). This evolution occurs under the influence of natural selection induced in endosymbiotic populations, which can be individual (Darwinian, frequency-dependent) or group (inter-deme, kin) depending on the structure of microbial populations defined by mechanisms of host infection. Under the influence of this selection, complexity of the organization and the integrity of the LRS are increased, which serve as criteria for its evolutionary progress, as well as ecological efficiency of symbiosis (its impact on the partners’ productivity). This interaction between bacteria and plants has been evolved from pleiotropic symbioses (dynamic equilibrium between mutualism and antagonism) to the mutual partners’ exploitation (their equivalent exchange by products of N 2 fixation and photosynthesis) and then to a highly-efficient mutualism of «altruistic» type (increased intensity of the symbiotrophic plant nutrition by nitrogen is the result of viability loss by bacteroids). Characteristics of macro- and microevolution of symbiosis opens the broad prospects for the construction of highly efficient forms of LRS, including the creation of «altruistic» rhizobia strains (in which an increased symbiotic efficiency is combined with a reduced survival outside plant) as well as a combination of alternative development programs for effective symbiosis (expensive and economical) independently arisen in different groups of legumes.