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

Hester Blommaert (1) , Hiram Castillo-Michel (2) , Giulia Veronesi (3, 2) , Rémi Tucoulou (2) , Jacques Beauchêne (4) , Pathmanathan Umaharan (5) , Erik Smolders (6) , Geraldine Sarret (1)

1 ISTerre - Institut des Sciences de la Terre
2 ESRF - European Synchrotron Radiation Facility [Grenoble]
3 COMX - Chimie computationnelle, modélisation et rayons X
4 UMR ECOFOG - Ecologie des forêts de Guyane
5 The University of the West Indies
6 Division Soil and Water Management

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.

Mots clés: Ca-oxalate; Distribution; Imaging; Metal pathways; O-ligands; S-ligands; Speciation; Synchrotron; Theobroma cacao; LX-Ray absorption; spectroscopy

Domaines: Botanique; Biochimie [q-bio.BM]

Hester Blommaert, Hiram Castillo-Michel, Giulia Veronesi, Rémi Tucoulou, Jacques Beauchêne, et al.. Ca-oxalate crystals are involved in cadmium storage in a high Cd accumulating cultivar of cacao. Environmental and Experimental Botany, 2024, 221, pp.105713. ⟨10.1016/j.envexpbot.2024.105713⟩. ⟨hal-04571252⟩