Evolution of nitrogen-fixing symbioses on the basis of bacterial migration from mycorrhizal fungi and soil into plant tissues

Abstract

A hypothesis is proposed on the emergence of N₂-fixing plant symbionts from soil diazotrophs and satellites of Glomeromycota fungi that form arbuscular mycorrhizae (AM). This universal form of plant-microbe symbiosis possibly appeared due to the integration of ancestral land plants (rhyniophytes, psylophytes) and microbial consortia composed of AM-fungi assimilating soil phosphates and bacteria fixing atmospheric CO₂ and/or N₂. The release of these bacteria from AM-fungal hyphae into plant tissues elicited the selection of genotypes capable of fungi-independent multiplication in plants, as well as the fixation in bacterial genomes of the genes for the synthesis of chitin-like signal factors stimulating the development of symbiotic structures. An early stage of this evolution might been represented by the formation of N₂-fixing syncyanoses, and the late stage might have been realized by the formation of nodular symbioses of dicots from the Eurosid I clade with rhizobia (α- and β-proteobacteria) and with the actinobacteria Frankia. The emergence of these symbioses was possibly based on the migration of soil and endophytic bacteria into the storage organs (modified stems or lateral roots), where the optimal conditions were established not only for N₂ fixation but also for the evolution of bacteria towards increased symbiotic activity. This evolution resulted in the emergence of primary rhizobia (Bradyrhizobium, Burkholderia), which acted as donors of sym genes for a broad spectrum of microbes transformed into secondary rhizobia (Rhizobium, Sinorhizobium). The subsequent evolution of nodular symbioses was directed at an increased efficiency of symbiotrophic nitrogen nutrition in host plants following two scenarios: (a) “expensive,” which is based on an increase in N₂-fixing activity via the transformation of bacteria into nonreproducible bacteroids; (b) “economical,” based on the acquisition of the determinate nodule structure and ureide nitrogen assimilation.