Abstract
Background and aims
Cereals can be made safer and more nutritious by reducing cadmium (Cd) and enhancing zinc (Zn) levels. To respectively regulate the accumulation of these chemically similar elements in grains, it is essential to understand the differences between Cd and Zn allocation to grains.
Methods
In durum wheat (Triticum durum), dual-isotope (111Cd and 67Zn) labeling was used to trace the post-anthesis uptake fluxes separately from the remobilization of pre-anthesis vegetative pools. Laser ablation inductively coupled mass spectrometry was used to investigate the spatial distribution of Cd and Zn in the uppermost node.
Results
Among the shoot organs, both pre- and post-anthesis derived Cd was more allocated to the high-transpiring organs (i.e., bracts and flag leaves) whereas Zn was more to the grain. Cadmium was likely less efficiently transferred from the xylem to the phloem as suggested by the elemental maps which showed that Cd was more abundant than Zn in the xylem of the uppermost node. Furthermore, unlike Zn, Cd was not significantly remobilized from the high-transpiring organs, which further limited the allocation of Cd to the grain.
Conclusion
High-transpiring organs are sources of grain Zn but irreversible sinks of Cd. Agronomic strategies that enhance Cd sequestration and Zn remobilization in high-transpiring organs could contribute to producing grains with low Cd and high Zn concentrations.
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References
Brinton J, Uauy C (2019) A reductionist approach to dissecting grain weight and yield in wheat. J Integr Plant Biol 61:337–358. https://doi.org/10.1111/jipb.12741
Buckley WT, Buckley KE, Huang JJ (2010) Root cadmium desorption methods and their evaluation with compartmental modeling. New Phytol 188:280–290. https://doi.org/10.1111/j.1469-8137.2010.03354.x
Cakmak I, Kutman UB (2017) Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci 69:172–180. https://doi.org/10.1111/ejss.12437
Chan DY, Hale BA (2004) Differential accumulation of cd in durum wheat cultivars: uptake and retranslocation as sources of variation. J Exp Bot 55:2571–2579. https://doi.org/10.1093/jxb/erh255
Chaney RL (2010) Cadmium and zinc. Trace Elements in Soils, In, pp 409–439. https://doi.org/10.1002/9781444319477.ch17
Chang T-G, Zhu X-G (2017) Source–sink interaction: a century old concept under the light of modern molecular systems biology. J Exp Bot 68:4417–4431. https://doi.org/10.1093/jxb/erx002
Chen H, Zhang W, Yang X, Wang P, McGrath SP, Zhao F-J (2018) Effective methods to reduce cadmium accumulation in rice grain. Chemosphere 207:699–707. https://doi.org/10.1016/j.chemosphere.2018.05.143
Clemens S (2019) Safer food through plant science: reducing toxic element accumulation in crops. J Exp Bot 70:5537–5557. https://doi.org/10.1093/jxb/erz366
Clemens S (2022) The cell biology of zinc. J Exp Bot 73:1688–1698. https://doi.org/10.1093/jxb/erab481
Cunha KPV, Nascimento CWA, Pimentel RMM, Ferreira CP (2008) Cellular localization of cadmium and structural changes in maize plants grown on a cadmium contaminated soil with and without liming. J Hazard Mater 160:228–234. https://doi.org/10.1016/j.jhazmat.2008.02.118
Curie C et al (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11. https://doi.org/10.1093/aob/mcn207
Detterbeck A et al (2016) Spatially resolved analysis of variation in barley (Hordeum vulgare) grain micronutrient accumulation. New Phytol 211:1241–1254. https://doi.org/10.1111/nph.13987
Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65:3783–3798. https://doi.org/10.1093/jxb/ert477
Dürr-Auster T, Wiggenhauser M, Zeder C, Schulin R, Weiss DJ, Frossard E (2019) The use of Q-ICPMS to apply enriched zinc stable isotope source tracing for organic fertilizers. Front Plant Sci 10:1382. https://doi.org/10.3389/fpls.2019.01382
Frick H, Pizzolato TD (1987) Adaptive value of the xylem discontinuity in partitioning of photoassimilate to the grain. Bull Torrey Bot Club 114:252–259. https://doi.org/10.2307/2996462
Grant CA, Di Fonzo N, Pisante M (2012) CHAPTER 3 - agronomy of durum wheat Production11Cynthia Grant is an employee of Agriculture and Agri-Food Canada. ©her majesty the queen in right of Canada, as represented by the minister of Agriculture and Agri-Food Canada. In: Sissons M, Abecassis J, Marchylo B, Carcea M (eds) Durum wheat, 2nd edn. AACC International Press, pp 37–55. https://doi.org/10.1016/B978-1-891127-65-6.50008-8
Gray CW, McLaren RG, Roberts AHC, Condron LM (1999) Cadmium phytoavailability in some New Zealand soils. Soil Res 37:461–478. https://doi.org/10.1071/S98070
Harris NS, Taylor GJ (2013) Cadmium uptake and partitioning in durum wheat during grain filling. BMC Plant Biol 13:103. https://doi.org/10.1186/1471-2229-13-103
Hegelund J, Pedas P, Husted S, Schiller M, Schjoerring J (2012) Zinc fluxes into developing barley grains: use of stable Zn isotopes to separate root uptake from remobilization in plants with contrasting Zn status. Plant Soil 361:241–250. https://doi.org/10.1007/s11104-012-1272-x
Herren T, Feller U (1994) Transfer of zinc from xylem to phloem in the peduncle of wheat. J Plant Nutr 17:1587–1598. https://doi.org/10.1080/01904169409364831
Herren T, Feller U (1997) Transport of cadmium via xylem and phloem in maturing wheat shoots: comparison with the translocation of zinc, strontium and rubidium. Ann Bot 80:623–628. https://doi.org/10.1006/anbo.1997.0492
Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208. https://doi.org/10.1016/j.taap.2009.04.020
Kutman UB, Kutman BY, Ceylan Y, Ova EA, Cakmak I (2012) Contributions of root uptake and remobilization to grain zinc accumulation in wheat depending on post-anthesis zinc availability and nitrogen nutrition. Plant Soil 361:177–187. https://doi.org/10.1007/s11104-012-1300-x
Ma JF, Shen RF, Shao JF (2021) Transport of cadmium from soil to grain in cereal crops: a review. Pedosphere 31:3–10. https://doi.org/10.1016/S1002-0160(20)60015-7
Maccaferri M et al (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51:885–895. https://doi.org/10.1038/s41588-019-0381-3
Maillard A et al (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci 6:317. https://doi.org/10.3389/fpls.2015.00317
Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259. https://doi.org/10.1111/j.1365-313X.2008.03410.x
Moore KL et al (2014) Combined NanoSIMS and synchrotron X-ray fluorescence reveal distinct cellular and subcellular distribution patterns of trace elements in rice tissues. New Phytol 201:104–115. https://doi.org/10.1111/nph.12497
Neff C, Becker P, Günther D (2022) Parallel flow ablation cell for short signal duration in LA-ICP-TOFMS element imaging. J Anal At Spectrom 37:677–683. https://doi.org/10.1039/D1JA00421B
Neff C, Keresztes Schmidt P, Garofalo PS, Schwarz G, Günther D (2020) Capabilities of automated LA-ICP-TOFMS imaging of geological samples. J Anal At Spectrom 35:2255–2266. https://doi.org/10.1039/D0JA00238K
Nishiyama R, Kato M, Nagata S, Yanagisawa S, Yoneyama T (2012) Identification of Zn–nicotianamine and Fe–2′-deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L.). Plant Cell Physiol 53:381–390. https://doi.org/10.1093/pcp/pcr188
Patrick JW, Offler CE (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52:551–564. https://doi.org/10.1093/jexbot/52.356.551
Peel K, Weiss D, Chapman J, Arnold T, Coles B (2008) A simple combined sample-standard bracketing and inter-element correction procedure for accurate mass bias correction and precise Zn and cu isotope ratio measurements. J Anal At Spectrom 23:103–110. https://doi.org/10.1039/b710977f
Pottier M, Masclaux-Daubresse C, Yoshimoto K, Thomine S (2014) Autophagy as a possible mechanism for micronutrient remobilization from leaves to seeds. Front Plant Sci 5:11. https://doi.org/10.3389/fpls.2014.00011
Rodda MS, Li G, Reid RJ (2011) The timing of grain cd accumulation in rice plants: the relative importance of remobilisation within the plant and root cd uptake post-flowering. Plant Soil 347:105–114. https://doi.org/10.1007/s11104-011-0829-4
Sasaki A, Yamaji N, Mitani-Ueno N, Kashino M, Ma JF (2015) A node-localized transporter OsZIP3 is responsible for the preferential distribution of Zn to developing tissues in rice. Plant J 84:374–384. https://doi.org/10.1111/tpj.13005
Smolders E, Wagner S, Prohaska T, Irrgeher J, Santner J (2020) Sub-millimeter distribution of labile trace element fluxes in the rhizosphere explains differential effects of soil liming on cadmium and zinc uptake in maize. Sci Total Environ 738:140311. https://doi.org/10.1016/j.scitotenv.2020.140311
Stanton C, Sanders D, Kramer U, Podar D (2022) Zinc in plants: integrating homeostasis and biofortification. Mol Plant 15:65–85. https://doi.org/10.1016/j.molp.2021.12.008
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and cd in rice. Plant Cell Environ 35:1948–1957. https://doi.org/10.1111/j.1365-3040.2012.02527.x
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301. https://doi.org/10.1126/science.1133649
White PJ (2012) Long-distance transport in the xylem and phloem. In: Marschner P (ed) Marschner's mineral nutrition of higher plants, 3rd edn. Academic Press, San Diego, pp 49–70. https://doi.org/10.1016/B978-0-12-384905-2.00003-0
White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080. https://doi.org/10.1093/aob/mcq085
Wiggenhauser M, Aucour AM, Telouk P, Blommaert H, Sarret G (2021) Changes of cadmium storage forms and isotope ratios in rice during grain filling. Front Plant Sci 12:645150. https://doi.org/10.3389/fpls.2021.645150
Wiggenhauser M, Bigalke M, Imseng M, Keller A, Archer C, Wilcke W, Frossard E (2018) Zinc isotope fractionation during grain filling of wheat and a comparison of zinc and cadmium isotope ratios in identical soil–plant systems. New Phytol 219:195–205. https://doi.org/10.1111/nph.15146
Wiggenhauser M et al (2016) Cadmium isotope fractionation in soil–wheat systems. Environ Sci Technol 50:9223–9231. https://doi.org/10.1021/acs.est.6b01568
Wu CY et al (2010) Uptake, translocation, and remobilization of zinc absorbed at different growth stages by rice genotypes of different Zn densities. J Agric Food Chem 58:6767–6773. https://doi.org/10.1021/jf100017e
Yamaguchi N, Ishikawa S, Abe T, Baba K, Arao T, Terada Y (2012) Role of the node in controlling traffic of cadmium, zinc, and manganese in rice. J Exp Bot 63:2729–2737
Yamaji N, Ma JF (2017) Node-controlled allocation of mineral elements in Poaceae. Curr Opin Plant Biol 39:18–24. https://doi.org/10.1016/j.pbi.2017.05.002
Yamaji N, Xia J, Mitani-Ueno N, Yokosho K, Feng Ma J (2013) Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol 162:927–939. https://doi.org/10.1104/pp.113.216564
Yan B-F et al (2018) Contribution of remobilization to the loading of cadmium in durum wheat grains: impact of post-anthesis nitrogen supply. Plant Soil 424:591–606. https://doi.org/10.1007/s11104-018-3560-6
Yan BF et al (2019) Cadmium allocation to grains in durum wheat exposed to low cd concentrations in hydroponics. Ecotoxicol Environ Saf 184:109592. https://doi.org/10.1016/j.ecoenv.2019.109592
Zhang L, Gao C, Chen C, Zhang W, Huang X-Y, Zhao F-J (2020) Overexpression of Rice OsHMA3 in wheat greatly decreases cadmium accumulation in wheat grains. Environ Sci Technol 54:10100–10108. https://doi.org/10.1021/acs.est.0c02877
Zheng L, Yamaji N, Yokosho K, Ma JF (2012) YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. Plant Cell 24:3767–3782. https://doi.org/10.1105/tpc.112.103820
Acknowledgments
This study was supported by the National Natural Science Foundation of China (grant number 42007331), Guangdong Basic and Applied Basic Research Foundation (grant number 2021A1515012222), and the Group of Plant Nutrition at ETH Zurich. We thank Mr. Christophe Zeder from the Laboratory of Human Nutrition at ETH Zurich for the support in the Cd concentration analysis using GF-AAS and the staff of the Group of Plant Nutrition at ETH Zurich for their support in the laboratory.
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B.F. Yan conceptualized and conducted most of the experiment. C. Nguyen, J.Y. Cornu, and E. Frossard strongly supported experimental design, data evaluation and interpretation, and manuscript writing. L. Schönholzer-Mauclaire provided advice on the methodology and participated in isotope measurements and data analysis. C. Neff and D. Günther conducted the elemental mapping of the node. All authors reviewed the manuscript and provided suggestions.
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Yan, BF., Nguyen, C., Cornu, JY. et al. Differential allocation of cadmium and zinc in durum wheat during grain filling as revealed by stable isotope labeling. Plant Soil 489, 177–191 (2023). https://doi.org/10.1007/s11104-023-06005-7
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DOI: https://doi.org/10.1007/s11104-023-06005-7