Differential Pb tolerance in metallicolous and non-metallicolous Zygophyllum fabago populations involves the strengthening of the antioxidative pathways

Zygophyllum fabago is a pioneer species that thrives in mine soils characterized by different levels of heavy metals as well as nutrient deficiencies. In order to obtain information on the adaptive mechanisms that enable Z. fabago to counteract heavy metal toxicity, seeds were collected from three populations, both non-metallicolous (NM) and metallicolous (M), grown in natural environments characterized by different levels of lead (Pb) and essential nutrients. Ionomic profiles of the seeds were in line with the different edaphic conditions of their natural environments. However ionomic profiles also indicated that the three populations carried out specific strategies in order to guarantee the appropriate supply of macro- and micronutrients in seed-storing tissues, in spite of the nutrient deficiencies present in mine soils. Seeds were germinated and grown in controlled conditions in the presence of sub-lethal doses of Pb(NO3)2 (0, 25 and 50 μM) for 30 d. Their germinability, seedling phenotyping characterization and fitness clearly showed that M populations were better adapted than NM population to cope with chronic exposure to Pb. M seedlings had constitutively higher levels of metabolites involved in antioxidative pathways, in particular ascorbate, carotenoids and total soluble phenols. In addition, when NM and M seedlings were exposed to different Pb concentrations, the antioxidative metabolism was altered probably in order to better counteract Pb toxicity. Analyses of catalase and ascorbate peroxidase gene expression and enzymatic activities also supported a more efficient ROS-scavenging capability in M than in NM populations. Interestingly, in M populations, the strengthening of the antioxidative pathways followed different patterns that seem to be determined by soil conditions. In fact, the relatively high levels of Pb found in M seeds could act as a priming stimulus, which facilitated a rapid response to counteract the toxic effects of chronic Pb exposure.