Metal Hyperaccumulation Armors Plants against Disease

Abstract

Metal hyperaccumulation, in which plants store exceptional concentrations of metals in their shoots, is an unusual trait whose evolutionary and ecological significance has prompted extensive debate. Hyperaccumulator plants are usually found on metalliferous soils, and it has been proposed that hyperaccumulation provides a defense against herbivores and pathogens, an idea termed the ‘elemental defense’ hypothesis. We have investigated this hypothesis using the crucifer Thlaspi caerulescens, a hyperaccumulator of zinc, nickel, and cadmium, and the bacterial pathogen Pseudomonas syringae pv. maculicola ( Psm). Using leaf inoculation assays, we have shown that hyperaccumulation of any of the three metals inhibits growth of Psm in planta. Metal concentrations in the bulk leaf and in the apoplast, through which the pathogen invades the leaf, were shown to be sufficient to account for the defensive effect by comparison with in vitro dose–response curves. Further, mutants of Psm with increased and decreased zinc tolerance created by transposon insertion had either enhanced or reduced ability, respectively, to grow in high-zinc plants, indicating that the metal affects the pathogen directly. Finally, we have shown that bacteria naturally colonizing T. caerulescens leaves at the site of a former lead–zinc mine have high zinc tolerance compared with bacteria isolated from non-accumulating plants, suggesting local adaptation to high metal. These results demonstrate that the disease resistance observed in metal-exposed T. caerulescens can be attributed to a direct effect of metal hyperaccumulation, which may thus be functionally analogous to the resistance conferred by antimicrobial metabolites in non-accumulating plants.

Author Summary

Soils rich in heavy metals support communities of distinctive metal-tolerant plants, a number of which exhibit a remarkable trait known as metal hyperaccumulation. These plants accumulate exceptionally high concentrations of metallic elements in their leaves, but whether this trait confers any adaptive advantage is controversial. In this study, we test the hypothesis that metal hyperaccumulation provides protection against disease. We demonstrate that Thlaspi caerulescens becomes resistant to bacterial leaf spot caused by Pseudomonas syringae pv. maculicola ( Psm) when it accumulates zinc, nickel, or cadmium, and show that the metal concentrations in these plants are sufficient to account for their observed disease resistance. We also show that there is a close correlation between the zinc tolerance of different strains of Psm and their ability to colonize T. caerulescens leaves with high zinc content. In a field study, bacteria isolated from the leaves of T. caerulescens plants growing on the site of a former lead–zinc mine were found to possess a higher degree of metal tolerance than bacteria isolated from crop plants. Our findings show that metal hyperaccumulation in plants can act as a mechanism to prevent attack by pathogenic microorganisms, but that metal tolerant pathogens can overcome this defense.