Variation in defence strategies in the metal hyperaccumulator plant Noccaea caerulescens is indicative of synergies and trade-offs between forms of defence

Abstract

In the metal hyperaccumulator plant Noccaea caerulescens, zinc may provide a defence against pathogens. However, zinc accumulation is a variable trait in this species. We hypothesize that this variability affects the outcome of interactions between metal accumulation and the various constitutive and inducible defences that N. caerulescens shares with non-accumulator plants. We compare zinc concentrations, glucosinolate concentrations and inducible stress responses, including reactive oxygen species (ROS) and cell death, in four N. caerulescens populations, and relate these to the growth of the plant pathogen Pseudomonas syringae, its zinc tolerance mutants and Pseudomonas pathogens isolated from a natural population of N. caerulescens. The populations display strikingly different combinations of defences. Where defences are successful, pathogens are limited primarily by metals, cell death or organic defences; there is evidence of population-dependent trade-offs or synergies between these. In addition, we find evidence that Pseudomonas pathogens have the capacity to overcome any of these defences, indicating that the arms race continues. These data indicate that defensive enhancement, joint effects and trade-offs between different forms of defence are all plausible explanations for the variation we observe between populations, with factors including metal availability and metal-tolerant pathogen load probably shaping the response of each population to infection.

Intraspecific Variation in Nickel Tolerance and Hyperaccumulation among Serpentine and Limestone Populations of Odontarrhena serpyllifolia (Brassicaceae: Alysseae) from the Iberian Peninsula

“…Similar trends have been reported for zinc in Noccaea (=Thlaspi) caerulescens [22,74] and Arabidopsis halleri [75,76], as well as for cadmium in N. caerulescens [51]. The possibility that populations on low-metal soils may possess greater physiological ability to take up and concentrate metals than those on high-metal soils is intriguing in the context of hypotheses that metal hyperaccumulation may provide adaptive benefits for plants [77,78]. However, this conclusion must be treated with caution in the present case.…”

Trace elements in Athyrium distentifolium from alpine vegetation in the Karkonosze, SW Poland

“…Iron is reported as necessary for microbial pathogens thus organisms evolved mechanisms of suppressing this metal as protection against invasion by pathogens (Becker and Skaar 2014). Zinc is used in defence either by lowering the amount to deprive the pathogen of the metal or by increasing the amount to cause lethal effects in pathogens (Weiss and Carver 2018;Fones et al 2019). Morkunas et al (2018) report that both the hormetic effect (effect of metals at low doses) and toxic doses of trace metals may enhance plant resistance against pathogens.…”

Root and Shoot Response to Nickel in Hyperaccumulator and Non-Hyperaccumulator Species

“…Thlaspi ) hyperaccumulate Ni in the serpentinitic soil, whereas other populations are capable to uptake Zn and Cd [ 89 ], suggesting that hyperaccumulation is monophyletic [ 90 ]. N. caerulescens also known as ‘montane crucifer’ [ 91 ] or ‘alpine pennycress’ [ 92 ] includes populations that differ in morphological and physiological characteristics, exhibiting a wide range of accumulation and metal tolerance [ 93 ]. In Europe, N. caerulescens shows three ecological groups that correspond to three edaphic environments [ 94 ].…”