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Iron transport and storage within the seed coat and embryo of developing seeds of pea (Pisum sativum L.)

Published online by Cambridge University Press:  19 September 2008

Eduardo Marentes
Affiliation:
US Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, TX 77030-2600, USA
Michael A. Grusak*
Affiliation:
US Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, TX 77030-2600, USA

Abstract

To understand the cellular processes related to iron transport and sequestration within the developing pea seed (Pisum sativum), total iron and ferritin iron were analysed in seed coat and embryo tissues of the iron-hyperaccumulating pea mutant, Sparkle [dgl, dgl], and its wild-type parent, cv. Sparkle. For plants grown hydroponically with 2 μM Fe, embryo Fe concentrations averaged 65 μg g−1 dry weight in mature wild-type seeds and 163 μg g−1 dry weight in mature dgl seeds; iron concentrations were also higher in dgl seed coats. Extracted and electrophoretically separated seed proteins were probed with a polyclonal antibody raised against pea seed ferritin. In both genotypes, ferritin was detected in the embryo, but not in the seed coat. Ferritin iron accounted for 92% of the total iron in mature wild-type embryos, but only 42% of the total iron in mature dgl embryos. Radiotracer studies using 59Fe were used to characterize the movement of iron within the seed coat. Unequal distribution of 59Fe in opposing sections taken from the two hemispheres of the seed coat demonstrated that iron was symplastically phloem unloaded. These results suggest that iron resides transiently within the nonvascular seed coat cells and that all cells at the inner surface of the seed coat may be involved in the release of iron to the embryo apoplast. However, the form of iron resident within the seed coat and/or taken up by the embryo is presently unknown.

Type
Physiology & Biochemistry
Copyright
Copyright © Cambridge University Press 1998

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References

Bouis, H. (1996) Enrichment of food staples through plant breeding: A new strategy for fighting micronutrient malnutrition. Nutrition Reviews 54, 131137.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Briat, J.-F. and Lobréaux, S. (1997) Iron transport and storage in plants. Trends in Plant Science 2, 187193.CrossRefGoogle Scholar
Chung, M.C.-M. (1985) A specific iron stain for iron-binding proteins in polyacrylamide gels: Application to transferrin and lactoferrin. Analytical Biochemistry 148, 498502.CrossRefGoogle ScholarPubMed
Fobis-Loisy, I., Loridon, K., Lobréaux, S., Lebrun, M. and Briat, J.-F. (1995) Structure and differential expression of two maize ferritin genes in response to iron and abscisic acid. European Journal of Biochemistry 231, 609619.CrossRefGoogle ScholarPubMed
Fox, T.C., Shaff, J.E., Grusak, M.A., Norvell, W.A., Chen, Y., Chaney, R.L. and Kochian, L.V. (1996) Direct measurement of 59Fe-labeled Fe2+ influx in roots of pea using a chelator buffer system to control free Fe2+ in solution. Plant Physiology 111, 93100.CrossRefGoogle ScholarPubMed
Gaymard, F., Boucherez, J. and Briat, J.-F. (1996) Characterization of a ferritin mRNA from Arabidopsis thaliana accumulated in response to iron through an oxidative pathway independent of abscisic acid. Biochemical Journal 318, 6773.CrossRefGoogle ScholarPubMed
Gottschalk, W.G. (1987) Improvement of the selection value of gene dgl through recombination. Pisum Newsletter 19, 911.Google Scholar
Graham, R.D. and Welch, R.M. (1996) Breeding for staple food crops with high micronutrient density, pp 172in Bouis, H.E. (Ed.) Working papers on agricultural strategies for micronutrients. Washington, D.C., International Food Policy Research Institute.Google Scholar
Grusak, M.A. (1994) Iron transport to developing ovules of Pisum sativum. I. Seed import characteristics and phloem iron-loading capacity of source regions. Plant Physiology 104, 649655.CrossRefGoogle ScholarPubMed
Grusak, M.A. (1995) Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L. (Fabaceae): Relevance to the iron nutrition of developing seeds. Planta 197, 111117.CrossRefGoogle Scholar
Grusak, M.A. and Minchin, P.E.H. (1988) Seed coat unloading in Pisum sativum — Osmotic effects in attached versus excised empty ovules. Journal of Experimental Botany 39, 543549.CrossRefGoogle Scholar
Grusak, M.A. and Pezeshgi, S. (1996) Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiology 110, 329334.CrossRefGoogle ScholarPubMed
Grusak, M.A., Welch, R.M. and Kochian, L.V. (1990) Physiological characterization of a single-gene mutant of Pisum sativum exhibiting excess iron accumulation. I. Root iron reduction and iron uptake. Plant Physiology 93, 976981.CrossRefGoogle ScholarPubMed
Hardham, A.R. (1976) Structural aspects of the pathways of nutrient flow to the developing embryo and cotyledons of Pisum sativum L. Australian Journal of Botany 24, 711721CrossRefGoogle Scholar
Hocking, P.J. and Pate, J.S. (1977) Mobilization of minerals to developing seeds of legumes. Annals of Botany 41, 12591278.CrossRefGoogle Scholar
Hyde, B.B., Hodge, A.J., Kahn, A. and Birnstiel, M.L. (1963) Studies on phytoferritin. I. Identification and localization. Journal of Ultrastructure Research 9, 248258.CrossRefGoogle Scholar
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 668685.CrossRefGoogle ScholarPubMed
Laszlo, J.A. (1990) Mineral contents of soybean seed coats and embryos during development. Journal of Plant Nutrition 13, 231248.CrossRefGoogle Scholar
Laulhère, J.-P., Lescure, A.-M., and Briat, J.-F. (1988) Purification and characterization of ferritins from maize, pea, and soyabean seeds. Distribution in various pea organs. Journal of Biological Chemistry 263, 1028910294.CrossRefGoogle ScholarPubMed
Laulhère, J.-P., Labouré, A.-M. and Briat, J.-F. (1989) Mechanism of the transition from plant ferritin to phytosiderin. Journal of Biological Chemistry 264, 36293635.CrossRefGoogle ScholarPubMed
Laulhère, J.-P., Labouré, A.-M. and Briat, J.-F. (1990) Photoreduction and incorporation of iron into ferritins. Biochemical Journal 268, 7984.CrossRefGoogle Scholar
Laulhère, J.-P., Barcelò, F. and Fontecave, M. (1995) Dynamic equilibria in iron uptake and release by ferritin. BioMetals 9, 303309.CrossRefGoogle Scholar
Lescure, A.-M., Proudhon, D., Pesey, H., Ragland, M., Theil, E.C. and Briat, J.-F. (1991) Ferritin gene transcription is regulated by iron in soybean cell cultures. Proceedings of the National Academy of Sciences, USA 88, 82228226.CrossRefGoogle ScholarPubMed
Lobréaux, S. and Briat, J.-F. (1991) Ferritin accumulation and degradation in different organs of pea during development. Biochemical Journal 274, 601606.CrossRefGoogle ScholarPubMed
Lobréaux, S., Massenet, O. and Briat, J.-F. (1992) Iron induces ferritin synthesis in maize plantlets. Plant Molecular Biology 19, 563575.CrossRefGoogle ScholarPubMed
Lobréaux, S., Thoiron, S. and Briat, J.-F. (1995) Induction of ferritin synthesis in maize leaves by an iron-mediated oxidative stress. Plant Journal 8, 443449.CrossRefGoogle Scholar
Theil, E.C. (1987) Ferritin: structure, gene regulation, and cellular function in animals, plants and microorganisms. Annual Review of Biochemistry 56, 289315.CrossRefGoogle ScholarPubMed
Thorne, J.H. (1981) Morphology and ultrastructure of maternal seed tissues of soybean in relation to the import of photosynthate. Plant Physiology 67, 10161025.CrossRefGoogle Scholar
Thorne, J.H. (1985) Phloem unloading of C and N assimilates in developing seeds. Annual Review of Plant Physiology 36, 317343.CrossRefGoogle Scholar
Thorpe, M.R. and Minchin, P.E.H. (1996) Mechanisms of long- and short-distance transport from sources to sinks, pp 261282in Zamski, E., Schaffer, A.A. (Eds) Photoassimilate distribution in plants and crops. Source-sink relationships. New York, New York, Marcel Dekker, Inc.Google Scholar
Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 43504354.CrossRefGoogle ScholarPubMed
Wade, V.J., Treffry, A., Laulhère, J.-P., Bauminger, E.R., Cleton, M.I., Mann, S., Briat, J.-F. and Harrison, P.M. (1993) Structure and composition of ferritin cores from pea seed (Pisum sativum). Biochimica et Biophysica Acta 1161, 9196.CrossRefGoogle ScholarPubMed
Waldo, G.S., Wright, E., Whang, Z.-H., Briat, J.-F., Theil, E.C. and Sayers, D.E. (1995) Formation of the ferritin iron mineral occurs in plastids. An X-ray absorption spectroscopy study. Plant Physiology 109, 797802.CrossRefGoogle Scholar