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Mother-plant-mediated pumping of zinc into the developing seed

Nature Plants volume 2, Article number: 16036 (2016) Cite this article

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Abstract

Insufficient intake of zinc and iron from a cereal-based diet is one of the causes of ‘hidden hunger’ (micronutrient deficiency), which affects some two billion people1,2. Identifying a limiting factor in the molecular mechanism of zinc loading into seeds is an important step towards determining the genetic basis for variation of grain micronutrient content and developing breeding strategies to improve this trait3. Nutrients are translocated to developing seeds at a rate that is regulated by transport processes in source leaves, in the phloem vascular pathway, and at seed sinks. Nutrients are released from a symplasmic maternal seed domain into the seed apoplasm surrounding the endosperm and embryo by poorly understood membrane transport processes4–6. Plants are unique among eukaryotes in having specific P1B-ATPase pumps for the cellular export of zinc7. In Arabidopsis, we show that two zinc transporting P1B-ATPases actively export zinc from the mother plant to the filial tissues. Mutant plants that lack both zinc pumps accumulate zinc in the seed coat and consequently have vastly reduced amounts of zinc inside the seed. Blockage of zinc transport was observed at both high and low external zinc supplies. The phenotype was determined by the mother plant and is thus due to a lack of zinc pump activity in the seed coat and not in the filial tissues. The finding that P1B-ATPases are one of the limiting factors controlling the amount of zinc inside a seed is an important step towards combating nutritional zinc deficiency worldwide.

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Figure 1: The distribution of zinc is shifted from the embryo to the seed coat of mature hma2 ,hma4 seeds.
Figure 2: Zinc accumulates in the seed coat of mature hma4 and hma2 ,hma4 mutant seeds.
Figure 3: Lack of zinc pumps in the seed coat but not in filial tissues blocks zinc loading into seeds.
Figure 4: Zinc export from the seed coat to filial tissues depends on zinc pumps in maternal tissues.
Figure 5: AtHMA2 and AtHMA4 are expressed in developing seeds.

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References

  1. Wessells, K. R. & Brown, K. H. Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS One 7, e50568 (2012).

    Article  Google Scholar 

  2. von Grebmer, K. et al. Global hunger index: the challenge of hidden hunger (International Food Policy Research Institute, 2014).

    Google Scholar 

  3. Palmgren, M. G. et al. Zinc biofortification of cereals problems and solutions. Trends Plant Sci. 13, 464–473 (2008).

    Article  CAS  Google Scholar 

  4. Stadler, R., Lauterbach, C. & Sauer, N. Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 139, 701–712 (2005).

    Article  CAS  Google Scholar 

  5. Zhang, W. et al. Nutrient loading of developing seeds. Funct. Plant Biol. 34, 314–331 (2007).

    Article  CAS  Google Scholar 

  6. Radchuk, V. & Borisjuk, L. Physical, metabolic and developmental functions of the seed coat. Front. Plant Sci. 5, 510 (2014).

    Article  Google Scholar 

  7. Williams, L. E. & Mills, R. F. P1B-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci. 10, 491–502 (2005).

    Article  CAS  Google Scholar 

  8. Baxter, I. et al. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol. 132, 618–628 (2003).

    Article  CAS  Google Scholar 

  9. Kim, Y.-Y. et al. AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. Plant J. 58, 737–753 (2009).

    Article  CAS  Google Scholar 

  10. Seigneurin-Berny, D. et al. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J. Biol. Chem. 281, 2882–2892 (2006).

    Article  CAS  Google Scholar 

  11. Morel, M. et al. AtHMA3, a P(1B)-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. 149, 894–904 (2009).

    Article  CAS  Google Scholar 

  12. Hussain, D. et al. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16, 1327–1339 (2004).

    Article  CAS  Google Scholar 

  13. Sinclair, S. A. et al. The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytol. 174, 39–45 (2007).

    Article  CAS  Google Scholar 

  14. Verret, F. et al. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. 576, 306–312 (2004).

    Article  CAS  Google Scholar 

  15. Hanikenne, M. et al. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453, 391–396 (2008).

    Article  CAS  Google Scholar 

  16. Kim, S. A. et al. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295–1298 (2006).

    Article  CAS  Google Scholar 

  17. Schnell Ramos, M. et al. Using μPIXE for quantitative mapping of metal concentration in Arabidopsis thaliana seeds. Front Plant Sci. 4, 168 (2013).

    Article  Google Scholar 

  18. Le, B. H. et al. Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl Acad. Sci. USA 107, 8063–8070 (2010).

    Article  CAS  Google Scholar 

  19. Song, W.-Y. et al. Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell 22, 2237–2252 (2010).

    Article  CAS  Google Scholar 

  20. Morth, J. P. et al. A structural overview of the plasma membrane Na+,K+-ATPase and H+-ATPase ion pumps. Nature Rev. Mol. Cell Biol. 12, 60–70 (2011).

    Article  CAS  Google Scholar 

  21. Mills, R. F. et al. HvHMA2, a P1B-ATPase from barley, is highly conserved among cereals and functions in Zn and Cd transport. PLoS One 7, e42640 (2012).

    Article  CAS  Google Scholar 

  22. Tauris, B. et al. A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J. Exp. Bot. 60, 1333–1347 (2009).

    Article  CAS  Google Scholar 

  23. Satoh-Nagasawa, N. et al. Mutations in rice (Oryza sativa) Heavy Metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 53, 213–224 (2012).

    Article  CAS  Google Scholar 

  24. Takahashi, R. et al. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ. 35, 1948–1957 (2012).

    Article  CAS  Google Scholar 

  25. Yamaji, N. et al. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 162, 927–939 (2013).

    Article  CAS  Google Scholar 

  26. Barabasz, A. et al. Metal accumulation in tobacco expressing Arabidopsis halleri metal hyperaccumulation gene depends on external supply. J. Exp. Bot. 61, 3057–3067 (2010).

    Article  CAS  Google Scholar 

  27. Siemianowski, O. et al. Expression of the P1B-type ATPase AtHMA4 in tobacco modifies Zn and Cd root to shoot partitioning and metal tolerance. Plant Biotechnol. J. 9, 64–74 (2011).

    Article  CAS  Google Scholar 

  28. Cun, P. et al. Modulation of Zn/Cd P1B2-ATPase activities in Arabidopsis impacts differently on Zn and Cd contents in shoots and seeds. Metallomics 6, 2109–2916 (2014).

    Article  CAS  Google Scholar 

  29. Kendziorek, M. et al. Approach to engineer tomato by expression of AtHMA4 to enhance Zn in the aerial parts. J. Plant Physiol. 171, 1413–1422 (2014).

    Article  CAS  Google Scholar 

  30. Truernit, E. et al. High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20, 1494–1503 (2008).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank C.S. Cobbett (University of Melbourne) for providing hma2-4, hma4-2, and hma2-4, hma4-2 mutant seeds and the Centre for Advanced Bioimaging (University of Copenhagen) for support and use of microscopes. We acknowledge the Paul Scherrer Institut, Villigen, Switzerland, for providing the synchrotron radiation beamtime at beamline microXAS of the SLS. The research leading to these results was funded by the University of Copenhagen's Excellency Programme KU2016, the People Programme (Marie Curie Actions) of the European Union's Seventh Framework Programme (FP7/2007-2013) under REA grant agreement no. PIEF-GA-2012-331680, and the European programme CALIPSO (no. 312284).

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Authors and Affiliations

  1. Centre for Membrane Pumps in Cells and Disease-PUMPKIN, Danish National Research Foundation, Denmark

    Lene Irene Olsen, Jeppe Thulin Østerberg, Robert D. Hoffmann & Michael Palmgren

  2. Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg, Denmark

    Lene Irene Olsen, Thomas H. Hansen, Jeppe Thulin Østerberg, Robert D. Hoffmann, Johannes Liesche, Søren Husted & Michael Palmgren

  3. Department of Plant Physiology, Ruhr University Bochum, D-44801 Bochum, Germany

    Camille Larue & Ute Krämer

  4. ECOLAB, Université de Toulouse, CNRS, INPT, UPS, F-31062 Toulouse, France

    Camille Larue & Stéphanie Cadarsi

  5. College of Life Sciences, Northwest A&F University, CN-712100 Yangling, China

    Johannes Liesche

  6. LEEL, NIMBE-CEA-CNRS, Université Paris-Saclay, CEA Saclay, F-91191 Gif-sur-Yvette Cedex, France

    Suzy Surblé

  7. microXAS beamline, Swiss Light Source, CH-5232 Villigen, Switzerland

    Vallerie Ann Samson & Daniel Grolimund

  8. Institute of Environmental Medicine, Karolinska Institutet, SE-171 77 Stockholm, Sweden

    Michael Palmgren

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  1. Lene Irene Olsen
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Contributions

L.I.O., T.H.H., C.L., J.T.H., J.L., S.S., S.C. and V.S. performed the experimental work. L.I.O., T.H.H., C.L., R.D.H., J.L., S.S., U.K., S.H. and M.P. performed data analysis. D.G., U.K., S.H. and M.P. oversaw project planning. L.I.O. and M.P. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Michael Palmgren.

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Olsen, L., Hansen, T., Larue, C. et al. Mother-plant-mediated pumping of zinc into the developing seed. Nature Plants 2, 16036 (2016). https://doi.org/10.1038/nplants.2016.36

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