Wounding of Arabidopsis halleri leaves enhances cadmium accumulation that acts as a defense against herbivory.

Sonia Plaza,Markus Geisler,Johann Weber,Enrico Martinoia,Simone Pajonk,Sylvain Pradervand,Maja Schellenberg,Ina N Talke,Bo Burla,Ute Krämer,Jérôme Thomas

doi:10.1007/s10534-015-9829-9

Abstract

Approximately 0.2 % of all angiosperms are classified as metal hyperaccumulators based on their extraordinarily high leaf metal contents, for example >1 % zinc, >0.1 % nickel or >0.01 % cadmium (Cd) in dry biomass. So far, metal hyperaccumulation has been considered to be a taxon-wide, constitutively expressed trait, the extent of which depends solely on available metal concentrations in the soil. Here we show that in the facultative metallophyte Arabidopsis halleri, both insect herbivory and mechanical wounding of leaves trigger an increase specifically in leaf Cd accumulation. Moreover, the Cd concentrations accumulated in leaves can serve as an elemental defense against herbivory by larvae of the Brassicaceae specialist small white (Pieris rapae), thus allowing the plant to take advantage of this non-essential trace element and toxin. Metal homeostasis genes are overrepresented in the systemic transcriptional response of roots to the wounding of leaves in A. halleri, supporting that leaf Cd accumulation is preceded by systemic signaling events. A similar, but quantitatively less pronounced transcriptional response was observed in A. thaliana, suggesting that the systemically regulated modulation of metal homeostasis in response to leaf wounding also occurs in non-hyperaccumulator plants. This is the first report of an environmental stimulus influencing metal hyperaccumulation.Electronic supplementary materialThe online version of this article (doi:10.1007/s10534-015-9829-9) contains supplementary material, which is available to authorized users.

Highlights

The essential micronutrients zinc and nickel, as well as the non-essential metal cadmium (Cd), can act as potent toxins when present in excess, endangering environmental and human health (Clemens et al 2013)
Grown (Massonneau et al 2001) 9-week-old Arabidopsis halleri and A. thaliana were transferred into a medium supplemented with 0.5 lM CdCl2 for 5 days before the initiation of wounding by herbivory through Pieris rapae larvae for 24 h, or mechanical wounding carried out with a razor blade on a single leaf simulating extent and shape of herbivory by P. rapae
To investigate the relationship between insect herbivory and Cd accumulation in A. halleri, larvae of Pieris rapae were allowed to feed for 24 h on 9-week-old A. halleri and A. thaliana plants, 5 days after the addition of a non-toxic concentration of 0.5 lM Cd to the hydroponic plant growth medium. 72 h after the initiation of feeding, intact leaves of A. halleri subjected to herbivory contained 1.97- to 3.72-fold higher Cd concentrations than leaves of non-wounded control plants (Fig. 1a; P = 0.02)

Summary

Introduction

The essential micronutrients zinc and nickel, as well as the non-essential metal cadmium (Cd), can act as potent toxins when present in excess, endangering environmental and human health (Clemens et al 2013). Within the characteristic vegetation shaped by high selection pressures occurring on heavy-metal rich soils, a small proportion of metallophyte plants— estimated to constitute around 1 % —accumulate extraordinarily high leaf metal concentrations (Baker and Brooks 1989). These rare metal hyperaccumulator plants are of considerable interest for the development of phytoremediation and phytomining technologies.

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