Advances and perspectives in the evolutionary hypothesis of root nodule symbiosis

A subset of flowering plants has evolved the ability to associate with diazotrophic symbionts, converting atmospheric N2 into bioavailable nitrogen for host nutrition. However, nodulation is restricted to species within the “nitrogen-fixing nodulation clade”, scattered across several families in four plant orders. Two primary competing hypotheses currently exist for this patchy distribution: multiple independent gains versus a single gain. Through a systematic synthesis of validated evidence from the two competing hypotheses, we aim to reconstruct the evolutionary origins of root nodule symbiosis. Synthesis of molecular and phylogenetic data reveals that the evolution of root nodule symbiosis was enabled by five critical innovations, including suppression of host immune responses, acquisition of the PACE, neofunctionalization of the NIN gene, recruitment of the SHORTROOT-SCARECROW stem cell regulatory module, and evolutionary specialization of NOD26. Meanwhile, The genetic basis of intracellular symbiotic relationships is highly conserved, leading to evolutionary stability in symbiotic nodulation. The innovations at the molecular and developmental levels have provided evolutionary clues for the development of two hypotheses, offering new insights and understandings into the origin and evolution of nitrogen-fixing symbiotic root nodules.