Letter

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

  • Nature Plants 2, Article number: 16036 (2016)
  • doi:10.1038/nplants.2016.36
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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,​5,​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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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).

Author information

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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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Michael Palmgren.

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