Abstract
Soil contamination by lead (Pb) has become one of the major ecological threats to the environment. Understanding the mechanisms of Pb transport and deposition in plants is of great importance to achieve a global Pb reduction. We exposed a collection of 360 Arabidopsis thaliana natural accessions to a Pb-polluted soil. Germination rates, growth, and leaf Pb concentrations showed extensive variation among accessions. These phenotypic data were subjected to genome wide association studies (GWAs) and we found a significant association on chromosome 1 for low leaf Pb accumulation. Genes associated with significant SNP markers were evaluated and we selected EXTENSIN18 (EXT18) and TLC (TRAM-LAG1-CLN8) as candidates for having a role in Pb homeostasis. Six Pb-tolerant accessions, three of them exhibiting low leaf Pb content, and three of them with high leaf Pb content; two Pb-sensitive accessions; two knockout T-DNA lines of GWAs candidate genes (ext18, tlc); and Col-0 were screened under control and high-Pb conditions. The relative expression of EXT18, TLC, and other genes described for being involved in Pb tolerance was also evaluated. Analysis of Darwinian fitness, root and leaf ionome, and TEM images revealed that Pb-tolerant accessions employ two opposing strategies: (1) low translocation of Pb and its accumulation into root cell walls and vacuoles, or (2) high translocation of Pb and its efflux to inactive organelles or intracellular spaces. Plants using the first strategy exhibited higher expression of EXT18 and HMA3, thicker root cell walls and Pb vacuolar sequestration, suggesting that these genes may contribute to the deposition of Pb in the roots. On the other hand, plants translocating high amounts of Pb showed upregulation of TLC and ABC transporters, indicating that these plants were able to properly efflux Pb in the aerial tissues. We conclude that EXT18 and TLC upregulation enhances Pb tolerance promoting its sequestration: EXT18 favors the thickening of the cell walls improving Pb accumulation in roots and decreasing its toxicity, while TLC facilitates the formation of dictyosome vesicles and the Pb encapsulation in leaves. These findings are relevant for the design of phytoremediation strategies and environment restoration.
Highlights
Lead is a neurotoxic element that even at low concentrations is highly dangerous for humans and animals
The rosette diameter (RD) of 5 weeks old plants varied significantly among all the accessions under both control and Pb stress conditions, the RD of almost all the accessions was reduced under high Pb conditions (RDMine/Control mean ± SD: 0.67 ± 0.18)
To inspect if this tolerance was associated with soil properties from the native habitats of the tested accessions, we used the public maps from the European Soil Data Centre (ESDAC) to extrapolate the pH and trace metal content of all the European sites (Figure 2A)
Summary
Lead is a neurotoxic element that even at low concentrations is highly dangerous for humans and animals. Due to its former use as gasoline additive, this contaminant is distributed all over the world with urban and heavy-traffic roadside areas mostly affected (Levin-Schwartz et al, 2021). In the case of agricultural soils, Pb release is generally attributed to metalliferous mining, smelting activities and the use of fertilizers and pesticides (Reboredo et al, 2019; Yuan et al, 2019). In contrast to humans, are relatively tolerant to soil Pb. Toxicity symptoms in the form of chlorosis, leaf browning, and stunted growth usually occur only in soils with close to 1000 mg/kg. A Pb2+ activity as low as 0.06 μM was found to be highly toxic to roots of cowpea (Kopittke et al, 2007)
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