Convergent evolution and adaptive diversification of root symbioses.

Mutualistic symbioses between plants and microorganisms have served as a cornerstone for terrestrial ecosystem establishment since the colonization of land by plants ca. 470 million years ago (Ma). These mutualisms diversified in symbiont partners and ecological functions in response to dynamic environmental shifts, with root-based architectures emerging later as a key adaptive innovation. Phylogenomic analyses reveal a conserved common symbiotic signalling pathway (CSSP) through the mycorrhizal-actinorhizal-rhizobial (MAR) evolutionary trajectory, underscoring convergent evolutionary mechanisms that facilitated the repeated emergence of mutualistic root-microbe interactions. Despite this shared foundation, recent studies highlight lineage-specific adaptations in symbiont recognition, immune evasion, and nutrient exchange, reflecting divergent evolutionary pressures and ecological niches. For instance, actinorhizal symbioses, although understudied compared to legume-rhizobia systems, exhibit unique adaptations in host specificity and nitrogen-fixation efficiency, offering untapped potential for sustainable agriculture and reforestation. This review synthesizes information from different disciplines to elucidate the origin and diversification of root symbioses, emphasizing molecular innovations and ecological drivers that shaped their evolution. We further explore the role of environmental pressures, such as resource availability and climate change, in driving the adaptive diversification of these symbiotic relationships. By integrating evolutionary, molecular, and ecological perspectives, this work advances our understanding of root symbioses as dynamic systems shaped by both conserved mechanisms and context-dependent adaptations.