Adaptation of Arabidopsis halleri to extreme metal pollution through limited metal accumulation involves changes in cell wall composition and metal homeostasis.

Abstract

Metallophytes constitute powerful models to study metal homeostasis, adaptation to extreme environments and the evolution of naturally-selected traits. Arabidopsis halleri is a pseudometallophyte which shows constitutive Zn/Cd tolerance and Zn hyperaccumulation but high intraspecific variability in Cd accumulation. To examine the molecular basis of the variation in metal tolerance and accumulation, ionome, transcriptome and cell-wall glycan array profiles were compared in two genetically close A. halleri populations from metalliferous and non-metalliferous sites in Northern Italy. The metallicolous population displayed increased tolerance to, reduced hyperaccumulation of Zn and limited accumulation of Cd, as well as altered metal homeostasis, compared to the non-metallicolous population. This correlated well with the differential expression of transporter genes involved in trace metal entry and in Cd/Zn vacuolar sequestration in roots. Many cell wall-related genes were also more expressed in roots of the metallicolous population. Glycan array and histological staining analyses supported major differences between the two populations in the accumulation of specific root pectins and hemicelluloses epitopes. Our results supported a role for specific cell wall components and regulation of transporter genes of Arabidopsis halleri in limiting accumulation of metals on contaminated sites.