Hyperaccumulation of zinc by Noccaea caerulescens results in a cascade of stress responses and changes in the elemental profile

Noccaea caerulescens (J. & C. Presl) F. K. Meyer is a metal hyperaccumulating plant which can accumulate more than 2% zinc (Zn) dry tissue mass in its aerial tissues. At this concentration Zn is toxic to most plants due to inhibition of enzyme function, oxidative damage and mineral deficiencies. In this study the elemental and metabolite profiles of N. caerulescens plants grown in four different Zn concentrations were measured. This revealed broad changes in the metabolite and elemental profiles with the hyperaccumulation of Zn. The Zn treated plants exhibited no typical signs of stress such as chlorosis or reduced biomass, however, a range of metabolic stress responses, such as the modification of galactolipids and the major membrane lipids of plastids, and increases in oxylipins, which are precursors to the signalling molecules jasmonic and abscisic acids, as well as the increased synthesis of glucosinolates, was observed. Increases in particular organic acids and the ubiquitous metal cation chelator nicotianamine were also observed. The small molecule metabolite changes observed, however, did not account for the extreme Zn concentrations in the leaf tissue showing that the increase in nicotianamine production most likely negates Fe deficiency. The elemental analyses also revealed significant changes in other essential micronutrients, in particular, significantly lower Mn concentrations in the high Zn accumulating plants, yet higher Fe concentrations. This comprehensive elemental and metabolite analysis revealed novel metabolite responses to Zn and offers evidence against organic acids as metal-storage ligands in N. caerulescens.