Ca-oxalate crystals are involved in cadmium storage in a high Cd accumulating cultivar of cacao

Abstract

Cadmium (Cd) concentrations in cacao often exceed food limits. A better understanding of the molecular mechanisms of Cd accumulation in cacao trees is necessary to advance Cd mitigation strategies. This study explores Cd distribution and speciation (i.e., chemical form) within the vegetative organs of a high Cd accumulating cacao cultivar growing in soil with background Cd concentrations (0.28 mg Cd kg −1 ) by synchrotron radiation-based micro- and nano-X-ray fluorescence imaging and X-ray absorption spectroscopy on duplicate samples of roots, young branches, mature branches, and leaves. In both the roots and branches, the incorporation of Cd in Ca-oxalate crystals with binding to oxygen-ligands was identified as a major mechanism of Cd regulation. The Ca-oxalate crystals were more abundant in the branches than in the roots. We suggest that the incorporation of Cd into the Ca-oxalate crystals may limit the transfer of Cd to other organs like the leaves and beans. The roots also featured Cd-sulfur species in dilated cells of the wood, probably for the retention of Cd in the roots by strong binding with Cd to thiol-containing ligands. A Cd hotspot in large, secreting channels of the branches suggested that mucilage may play a role in the transport of Cd within cacao trees. The leaves had local Cd enrichments in the parenchymatous tissues and displayed a higher Cd concentration in the mesophyll compared to the epidermis. These insights in Cd distribution and speciation underscore that Theobroma cacao L. develops original Cd detoxification strategies, strongly different from non-tolerant species such as cereals. • The distribution and speciation of Cd in Theobroma cacao L. organs was studied. • Mucilage in the branches may be important for Cd transfer. • Cd accumulated more in the mesophyll than in the epidermis of the leaves. • At natural Cd concentrations, Cd-O species were more prevalent than Cd-S species. • Cd was present in Ca-oxalate crystals in roots and branches, but not in leaves.