The current status of the elemental defense hypothesis in relation to pathogens

Abstract

Metal hyperaccumulating plants are able to accumulate exceptionally high concentrations of metals, such as zinc, nickel, or cadmium, in their aerial tissues. These metals reach concentrations that would be toxic to most other plant species. This trait has evolved multiple times independently in the plant kingdom. Recent studies have provided new insight into the ecological and evolutionary significance of this trait, by showing that some metal hyperaccumulating plants can use high concentrations of accumulated metals to defend themselves against attack by pathogenic microorganisms and herbivores. Here, we review the evidence that metal hyperaccumulation acts as a defensive trait in plants, with particular emphasis on plant–pathogen interactions. We discuss the mechanisms by which defense against pathogens might have driven the evolution of metal hyperaccumulation, including the interaction of this trait with other forms of defense. In particular, we consider how physiological adaptations and fitness costs associated with metal hyperaccumulation could have resulted in trade-offs between metal hyperaccumulation and other defenses. Drawing on current understanding of the population ecology of metal hyperaccumulator plants, we consider the conditions that might have been necessary for metal hyperaccumulation to be selected as a defensive trait, and discuss the likelihood that these were fulfilled. Based on these conditions, we propose a possible scenario for the evolution of metal hyperaccumulation, in which selective pressure for resistance to pathogens or herbivores, combined with gene flow from non-metallicolous populations, increases the likelihood that the metal hyperaccumulating trait becomes established in plant populations.

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

“…Previously, we have demonstrated that endophytic bacteria of the zinc hyperaccumulator N. caerulescens show higher zinc tolerance when compared with bacteria pathogenic on related non-accumulator plants [15], an idea supported by other studies of bacteria associated with metal-hyperaccumulating plants [18,19,[38][39][40]. Considered alongside evidence for a role of hyperaccumulated metals in defence of plants such as N. caerulescens against disease [ [13][14][15]41,42], this suggests that local adaptation of pathogens to high-metal concentrations in the rhizosphere and phyllosphere of metal-accumulating plants might drive the evolution of further defensive hyperaccumulation in a form of coevolutionary arms race [15,43].…”

A comprehensive set of transcript sequences of the heavy metal hyperaccumulator Noccaea caerulescens

“…As part of this adaptation, they not only tolerate exposure to normally lethal concentrations of both metals, but also hyperaccumulate them in their shoots, probably as protection against herbivory and microbial infection (Hoerger et al, 2013). N. caerulescens is the only species that also hyperaccumulates Ni and Pb.…”

Evolutionary tinkering of the expression of PDF1s suggests their joint effect on zinc tolerance and the response to pathogen attack

“…The “joint effect” hypothesis is based on the idea that organic defences increase the defensive effect of metals (Boyd, 2007, 2012b). On this basis, conceptual models have been developed which might explain the evolutionary emergence of the hyperaccumulation trait (Boyd, 2012a,b; Hörger et al, 2013). …”