Uncoupling of reactive oxygen species accumulation and defence signalling in the metal hyperaccumulator plant Noccaea caerulescens

Abstract

SummaryThe metal hyperaccumulator plant Noccaea caerulescens is protected from disease by the accumulation of high concentrations of metals in its aerial tissues, which are toxic to many pathogens. As these metals can lead to the production of damaging reactive oxygen species (ROS), metal hyperaccumulator plants have developed highly effective ROS tolerance mechanisms, which might quench ROS-based signals. We therefore investigated whether metal accumulation alters defence signalling via ROS in this plant.We studied the effect of zinc (Zn) accumulation by N. caerulescens on pathogen-induced ROS production, salicylic acid accumulation and downstream defence responses, such as callose deposition and pathogenesis-related (PR) gene expression, to the bacterial pathogen Pseudomonas syringae pv. maculicola.The accumulation of Zn caused increased superoxide production in N. caerulescens, but inoculation with P. syringae did not elicit the defensive oxidative burst typical of most plants. Defences dependent on signalling through ROS (callose and PR gene expression) were also modified or absent in N. caerulescens, whereas salicylic acid production in response to infection was retained.These observations suggest that metal hyperaccumulation is incompatible with defence signalling through ROS and that, as metal hyperaccumulation became effective as a form of elemental defence, normal defence responses became progressively uncoupled from ROS signalling in N. caerulescens.

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

“…maculicola [15]. This supports the hypothesis that, if metal accumulation evolved as a defence, rapidly evolving pathogens are likely to have driven a subsequent arms race leading to the progressive enhancement of the metal-accumulation phenotype [16].…”

“…There is evidence that the use of metals in defence has led to an evolutionary trade-off between metal hyperaccumulation and some pathogen-induced defences [16][17][18]. At present, however, little evidence is available concerning the effect of metal hyperaccumulation and metal-based defences upon the endophytic bacteria of hyperaccumulator plants.…”

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

“…One possible explanation for these observations is that constitutively high levels of metal-induced ROS and other abiotic stress responses could result in constitutive expression of resource-expensive defense mechanisms in the absence of pathogens, ultimately leading to selection for both enhanced antioxidant mechanisms, and loss of induced defenses. Supporting this idea, Fones et al (2013) have shown that superoxide levels in N. caerulescens rise with zinc exposure, but not in response to pathogens ( Figure 2 ). Salicylic acid treatment has been reported to alleviate cadmium toxicity and cadmium-induced oxidative stress in non-metal hyperaccumulating plants such as barley, soybean, and Medicago sativa (Metwally et al, 2003; Drazic and Mihailovic, 2005; Cui et al, 2012).…”

“…This suggests negative cross-talk between abiotic stress (cadmium) and biotic stress (pathogen) responses. Work by Fones et al (2013) has shown that some pathogen-induced defenses such as callose deposition and PR gene induction appear to be absent in N. caerulescens , although the plants tested retained the ability to produce salicylic acid in response to infection. This study also showed that the ability of Pseudomonas syringae to infect N. caerulescens plants grown on low concentrations of zinc was dependent on a functional type III secretion system (T3SS), a pathogenicity mechanism used by Pseudomonas syringae to disable plant defenses, which suggests that certain defense mechanisms that are suppressed by T3SS-secreted effector proteins remain functional in this plant.…”

Got to hide your Zn away: Molecular control of Zn accumulation and biotechnological applications

“…In addition, A. halleri and certain ecotypes of N. caerulescens have better capacity to cope with oxidative stress compared to closely related non-accumulator species [110,127,128].…”