Evidence for saponin diversity–mycobiome links and conservatism of plant–fungi interaction patterns across Holarctic disjunct Panax species

Abstract

Although interplays between plant and coevolved microorganisms are believed to drive landscape formation and ecosystem services, the relationships between the mycobiome and phytochemical evolution and the evolutionary characteristics of plant–mycobiome interaction patterns are still unclear. The present study explored fungal communities from 405 multiniche samples of three Holarctic disjunct Panax species. The overall mycobiomes showed compartment-dominated variations and dynamic universality. Neutral models were fitted for each compartment at the Panax genus (I) and species (II) levels to infer the community assembly mechanism and identify fungal subgroups potentially representing different plant–fungi interaction results, i.e., the potentially selected, opposed, and neutral taxa. Selection contributed more to the endosphere than to external compartments. The nonneutral taxa showed significant phylogenetic clustering. In Model I, the opposed subgroups could best reflect Panax saponin diversities (r = 0.69), and genera with highly positive correlations to specific saponins were identified using machine learning. Although mycobiomes in the three species differed significantly, subgroups in Model II were phylogenetically clustered based on potential interaction type rather than plant species, indicating potentially conservative plant–fungi interactions. In summary, the finding of strong links between invaders and saponin diversity can help explore the underlying mechanisms of saponin biosynthesis evolution from microbial insights, which is important to understanding the formation of the current landscape. The potential conservatism of plant–fungi interaction patterns suggests that the related genetic modules and selection pressures were convergent across Panax species, advancing our understanding of plant interplay with biotic environments.