Linking Plant Adaptation, Stress Responses, and Plant-Soil-Microbe Interactions in Metal Contaminated Mine Tailings: Phytoremediation Potential of Atriplex Lentiformis

Abstract

Phytoremediation is a sustainable and eco-friendly approach to reclaim legacy mine sites. However, unfavorable biogeochemical characteristics of legacy mine tailings, including low fertility, high salinity, lack of soil structure, and high concentrations of toxic metal(loid)s, often hinder plant establishment and limit the success of phytoremediation, particularly in arid and semi-arid areas. To overcome these challenges, various strategies have been implemented, such as capping tailings with a topsoil layer or utilizing compost-assisted direct planting. Yet, the success of these methods remains inconsistent due to specific plant responses and their sensitivity to local environmental conditions. Moreover, prolonged exposure to adverse abiotic and biotic conditions may not only trigger stress responses but also drive cumulative adaptive changes in plants. Therefore, this study explores multiple aspects of plant adaptation, stress responses, and plant–soil–microbe interactions in phytoremediation.The selected model species for this study is Atriplex lentiformis - a metal-tolerant, halophytic species native to the U.S. Southwest and northern Mexico. Despite its frequent use in phytoremediation projects, the species’ responses to diverse environmental conditions, its establishment across various soil substrates, and its patterns of metal tolerance and accumulation patterns remain poorly understood. This dissertation aims to: i) investigate how long-term exposure to metal-contaminated mine tailings influences reproductive strategies, including germination success, elemental uptake, and allocation within seeds; ii) assess how biochemical variability in topsoil stockpile materials affects A. lentiformis seed germination and early plant establishment; and iii) examine metal accumulation patterns and stress responses in this species along a gradient of metal toxicity. Key findings highlight the strong dependence of A. lentiformis on soil chemical properties and microbial community structure. Long-term exposure of A. lentiformis individuals to metal-contaminated mine tailings induced significant changes in seed development and elemental allocation, with notable increases in Zn accumulation. Elevated Zn was particularly evident as hotspots of high concentrations in critical seed embryo regions, raising concerns about the potential impact on seed viability. Germination and early seedling growth were found to be controlled by distinct biochemical soil variables, with the species exhibiting poor performance in degraded, nutrient-deficient soils derived from topsoil stockpiles. Finally, while the species generally exhibited a tolerance and exclusion strategy for most toxic metal(loid)s in soil, extreme soil metal concentrations triggered a shift to Zn accumulation in leaves. This switch to accumulation was strongly linked to specific microbial taxa originating from legacy mine tailings, highlighting the importance of plant-microbe interactions in phytoremediation projects. This dissertation provides a comprehensive evaluation of A. lentiformis for phytoremediation applications, while also highlighting potential ecological trade-offs associated with metal accumulation in plant tissues. Ultimately, these findings contribute to refining revegetation and phytoremediation strategies by identifying the conditions under which A. lentiformis is best suited for phytostabilization or phytoextraction, thereby enhancing the effectiveness of mine site reclamation efforts.