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.

Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex

“…There have been many reports of decreased herbivory or reduced pathogen infection on plants hyperaccumulating metals (Poschenrieder et al, 2006;Boyd, 2007;Fones et al, 2010;Rascio and Navari-Izzo, 2011). However, in some studies no protective effect of metal hyperaccumulation against herbivory was observed (Noret et al, 2007), and designing trials to demonstrate such an effect in the field is particularly challenging, and hence further work is required to substantiate the selective advantage offered by metal hyperaccumulation.…”

Local adaptation is associated with zinc tolerance inPseudomonasendophytes of the metal-hyperaccumulator plantNoccaea caerulescens

“…In addition, 16S, rpoD and gyrB genes were sequenced (primers are given in electronic supplementary material, table S1) and used as queries for NCBI BLAST. In planta growth and pathogenicity assays were carried out as described [15].…”

“…Thus, high metal tolerance is associated with bacterial growth within metal-hyperaccumulating plants. In previous work, we demonstrated that zinc concentrations in the aerial tissues of plants of a natural Noccaea caerulescens (synonym Thlaspi caerulescens) population growing on an abandoned lead-zinc mine at Hafna, Snowdonia, UK, [22] are higher than those found to prevent the growth of pathogenic Pseudomonas syringae bacteria under laboratory conditions [15], suggesting that zinc tolerance is important for naturally occurring endophytes of these plants. Here, we investigate the possibility that the endophytic pseudomonads of metal hyperaccumulators have developed increased metal tolerance as a result of local adaptation to the metalrich environment of the hyperaccumulator leaves, a scenario that might drive the evolution of further metal hyperaccumulation in plants that use metals as a defence against pathogenic microorganisms.…”

Manganese hyperaccumulation from non-contaminated soil inChengiopanax sciadophylloidesFranch. et Sav. and its correlation with calcium accumulation

“…Furthermore, interference with neighboring plants is probably not a relevant mechanism in this case, since C. sciadophylloides occurs preferentially in shaded locations where soil is commonly not enriched with Mn. Accumulation of other metals, including Ni, Cd, As, Se, and Zn, by other species of hyperaccumulators may be a defense strategy (Behmer et al 2005;Jiang et al 2005;Jhee et al 2006;Rathinasabapathi et al 2007;Galeas et al 2008;Fones et al 2010). Many kinds of plant disease are affected by Mn availability, and Mn amendment reduces the incidence of some plant diseases (Thompson and Huber 2007).…”