Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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 processes46. 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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 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. 2

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

    Google Scholar 

  3. 3

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

    CAS  Article  Google Scholar 

  4. 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).

    CAS  Article  Google Scholar 

  5. 5

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

    CAS  Article  Google Scholar 

  6. 6

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

    Article  Google Scholar 

  7. 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).

    CAS  Article  Google Scholar 

  8. 8

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

    CAS  Article  Google Scholar 

  9. 9

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

    CAS  Article  Google Scholar 

  10. 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).

    CAS  Article  Google Scholar 

  11. 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).

    CAS  Article  Google Scholar 

  12. 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).

    CAS  Article  Google Scholar 

  13. 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).

    CAS  Article  Google Scholar 

  14. 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).

    CAS  Article  Google Scholar 

  15. 15

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

    CAS  Article  Google Scholar 

  16. 16

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

    CAS  Article  Google Scholar 

  17. 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. 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).

    CAS  Article  Google Scholar 

  19. 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).

    CAS  Article  Google Scholar 

  20. 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).

    CAS  Article  Google Scholar 

  21. 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).

    CAS  Article  Google Scholar 

  22. 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).

    CAS  Article  Google Scholar 

  23. 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).

    CAS  Article  Google Scholar 

  24. 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).

    CAS  Article  Google Scholar 

  25. 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).

    CAS  Article  Google Scholar 

  26. 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).

    CAS  Article  Google Scholar 

  27. 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).

    CAS  Article  Google Scholar 

  28. 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).

    CAS  Article  Google Scholar 

  29. 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).

    CAS  Article  Google Scholar 

  30. 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).

    CAS  Article  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).

Author information

Affiliations

Authors

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.

Corresponding author

Correspondence to Michael Palmgren.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing