Rhizospheric Fungi Drive the Adaptive Evolution of Phytolacca americana Populations to Cadmium Stress in Invaded Areas

The successful invasion of alien plants in heavy metal-contaminated environments often involves rapid adaptive evolution. Rhizospheric microorganisms, particularly fungi, are considered key drivers, yet the specific mechanisms by which they mediate adaptive evolution under heavy metal stress remain unclear. In this study, we employed a common garden experiment to compare the responses of native and invasive populations of Phytolacca americana to cadmium stress in both microbe-deficient substrate soil and natural soil, aiming to systematically elucidate the ecological and evolutionary mechanisms of cadmium tolerance. Results indicated that the enhanced cadmium tolerance of the invasive populations is a result of post-invasion adaptive evolution and that their growth advantage is highly dependent on the soil microbial environment. In natural soil, compared to the native populations, the invasive populations exhibited significant increases in plant height, basal diameter, and biomass respectively. The rhizospheric fungal community of the invasive populations underwent significant restructuring, characterized by a simplified network topology with increased modularity. Moreover, the invasive populations formed highly functionally differentiated plant-fungal interaction networks, where multiple fungal taxa collaboratively regulated the processes of cadmium uptake, translocation, and accumulation. This study confirms that the adaptation of Phytolacca americana to cadmium stress is driven by both plant adaptive evolution and the rhizospheric fungal community. The invasive populations enhance cadmium tolerance through a dual mechanism of "biomass dilution" and "microbially-mediated resistance". These findings provide novel insights into microbially-mediated ecological adaptation and evolution and emphasize the necessity of incorporating the holistic "plant-soil-microorganism" system into assessments of invasion potential.