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Article|01 May 2020|OPEN
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
Ihsan Ullah1, Vinicius H. de Oliveira1,2, Samantha J. Hammond3, Stanislav Strekopytov4,5, Mark Tibbett1, Jim M. Dunwell1, Mark Rehkämper6 & Rebekah E. T. Moore6,
1School of Agriculture, Policy and Development, University of Reading, Reading RG6 6BZ, UK
2Present address: Department of Plant Biology, Institute of Biology, University of Campinas, Campinas, Sao Paulo 13083-970, Brazil
3School of Environment, Earth and Ecosystem Sciences, The Open University, Milton Keynes MK7 6AA, UK
4Imaging and Analysis Centre, The Natural History Museum, London SW7 5BD, UK
5Present address: National Measurement Laboratory, LGC, Queen’s Road, Teddington TW11 0LY, UK
6Department of Earth Science and Engineering, Imperial College, London SW7 2BP, UK

Horticulture Research 7,
Article number: 20071 (2020)
doi: 10.1038/hortres.2020.71
Views: 242

Received: 28 Jan 2020
Revised: 16 Mar 2020
Accepted: 20 Mar 2020
Published online: 01 May 2020

Abstract

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 Δ114/110Cdtot-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 Δ114/110Cdseq-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.