Cadmium isotope fractionation reveals genetic variation in Cd uptake and translocation by Theobroma cacao and role of natural resistance-associated macrophage protein 5 and heavy metal ATPase-family transporters

• Published in: Horticulture research Vol. 7; no. 1
• Main Authors: Moore, Rebekah E. T., Ullah, Ihsan, de Oliveira, Vinicius H., Hammond, Samantha J., Strekopytov, Stanislav, Tibbett, Mark, Dunwell, Jim M., Rehkämper, Mark
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 2020; Oxford University Press
• Subjects: 631/449/2491/2046; 631/45/321; Adenosine triphosphatase; Agriculture; Biocompatibility; Biomedical and Life Sciences; Cadmium; Cloning; Ecology; Fractionation; Genetic diversity; Heavy metals; Hydroponics; Isotope fractionation; Isotopes; Isotopic enrichment; Leaves; Life Sciences; Macrophages; Plant Breeding/Biotechnology; Plant Genetics and Genomics; Plant Sciences; Protein transport; Proteins; Roots; Sequestering; Theobroma cacao; Transgenic plants; Translocation; Yeast; Yeasts
• ISSN: 2662-6810; 2052-7276
• DOI: 10.1038/s41438-020-0292-6

In response to new European Union regulations, studies are underway to mitigate accumulation of toxic cadmium (Cd) in cacao (
Theobroma cacao
, Tc). This study advances such research with Cd isotope analyses of 19 genetically diverse cacao clones and yeast transformed to express cacao natural resistance-associated macrophage protein (NRAMP5) and heavy metal ATPases (HMAs). The plants were enriched in light Cd isotopes relative to the hydroponic solution with Δ
114/110
Cd
tot-sol
 = −0.22 ± 0.08‰. Leaves show a systematic enrichment of isotopically heavy Cd relative to total plants, in accord with closed-system isotope fractionation of Δ
114/110
Cd
seq-mob
 = −0.13‰, by sequestering isotopically light Cd in roots/stems and mobilisation of remaining Cd to leaves. The findings demonstrate that (i) transfer of Cd between roots and leaves is primarily unidirectional; (ii) different clones utilise similar pathways for Cd sequestration, which differ from those of other studied plants; (iii) clones differ in their efficiency of Cd sequestration. Transgenic yeast that expresses
TcNRAMP5
(
T. cacao
natural resistance-associated macrophage gene) had isotopically lighter Cd than did cacao. This suggests that NRAMP5 transporters constitute an important pathway for uptake of Cd by cacao. Cd isotope signatures of transgenic yeast expressing HMA-family proteins suggest that they may contribute to Cd sequestration. The data are the first to record isotope fractionation induced by transporter proteins in vivo.