Does slow and steady win the race? Root growth dynamics of Arabidopsis halleri ecotypes in soils with varying trace metal element contamination

Hyperaccumulating plants possess complex traits, allowing them to thrive in soils with high concentrations of trace metal elements (TME). Accordingly, their TME hypertolerance and hyperaccumulation capacities have been intensely studied from physiological, evolutionary, and ecological perspectives. Little is known, however, about their root system development in TME enriched vs natural soils. We assessed temporal and quantitative changes in root systems of the model species Arabidopsis halleri, using a novel combination of root phenotyping in rhizoboxes and multitemporal digital imaging. We continuously monitored root growth of two non-metallicolous and two metallicolous populations in different substrate treatments, including homogeneous and horizontal layer applications of metalliferous and non-metalliferous soils. Non-metallicolous plants on non-metalliferous soils produced deep-reaching and wide roots, whereas metallicolous plants on metalliferous soil had smaller roots. This pattern was reversed when transplanting seedlings to foreign substrates, indicating that environment rather than ecotype determines root growth in A. halleri. Dampened root development in metalliferous and favored root proliferation in non-metalliferous soils indicate cost of tolerance and TME foraging, respectively. Importantly, root propagation into metalliferous soil was strongly promoted by a non-metalliferous “capping” layer that facilitated initial plant development. Hence, growing on non-polluted substrate in the early stage provides plants with a robust and optimal root system that facilitates seedling establishment and subsequent development under TME enriched conditions. These findings improve our understanding of plant performance in metalliferous environments and can help refine management practices for the sustainable reclamation of degraded lands.