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Missing pieces in protein deposition and mobilization inside legume seed storage vacuoles: calcium and magnesium ions

Published online by Cambridge University Press:  25 September 2012

Cláudia N. Santos ,
Marta M. Alves ,
Isabel T. Bento  and
Ricardo B. Ferreira
Cláudia N. Santos
Affiliation:
Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Apartado 127, 2781-901Oeiras, Portugal
Marta M. Alves
Affiliation:
Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Apartado 127, 2781-901Oeiras, Portugal
Isabel T. Bento
Affiliation:
Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Apartado 127, 2781-901Oeiras, Portugal
Ricardo B. Ferreira*
Affiliation:
Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Apartado 127, 2781-901Oeiras, Portugal Instituto Superior de Agronomia, Universidade Técnica de Lisboa, 1349-017Lisboa, Portugal
*
*Correspondence Email: rbferreira@itqb.unl.pt
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Abstract

During the maturation of dicotyledonous seeds, organic carbon, nitrogen and sulphur are stored in protein storage vacuoles (PSVs) as storage globulins. Several studies point to the coexistence of storage proteins with proteases responsible for their degradation inside PSVs. Different mechanisms have been proposed to explain why there is no proteolysis during this period. Protein aggregation to form large supramolecular structures resistant to proteolytic attack could be the reason. However, during germination, and particularly following its completion, the globulin aggregates must undergo disintegration to allow protease attack for protein reserve mobilization. Based on the well-described concentration-dependent ability of Ca2+ and Mg2+ to promote in vitro aggregation and disaggregation of globulins, we explored a possible role for these alkaline earth cations in globulin packaging and mobilization. Ca2+ and Mg2+ measurements in purified PSVs [6.37 μmol and 43.9 μmol g− 1 dry weight (DW) of cotyledons, respectively] showed the presence of these two alkaline earth cations within this compartment. To our knowledge, this is the first time that Ca2+ and Mg2+ have been quantified in purified PSVs from Lupinus albus seeds. Considering the importance of these two alkaline earth cations inside PSVs, which represent 14.6% and 60.7% of the total seed Mg2+and Ca2+, respectively, globulin aggregation and disaggregation profiles were assayed using experimental conditions closer to those that are physiologically present (proportion of Ca2+ and Mg2+, and acidic pH). Based on: (1) the high in vivo abundance of Ca2+ and Mg2+ inside PSVs; and (2) globulin aggregation and disaggregation profiles, together with structural and physiological evidence already reported in the literature, an important physiological role for Ca2+ and Mg2+ in globulin packaging and mobilization inside PSVs is suggested.

Keywords

calciumglobulin aggregation-disaggregationLupinus albusmagnesiumprotein storage vacuoles
Type
Research Papers
Information
Seed Science Research , Volume 22 , Issue 4 , December 2012 , pp. 249 - 258
Copyright
Copyright © Cambridge University Press 2012

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References

Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The protein data bank. Nucleic Acids Research 28, 235–242.CrossRefGoogle ScholarPubMed
Britton, H. and Robinson, R. (1931) Universal buffer solutions and the dissociation constant of veronal. Journal of the Chemical Society CXCVIII, 1456–1462.CrossRefGoogle Scholar
Bucking, H., Kuhn, A.J., Schroder, W.H.andHeyser, W. (2002) The fungal sheath of ectomycorrhizal pine roots: an apoplastic barrier for the entry of calcium, magnesium, and potassium into the root cortex? Journal of Experimental Botany 53, 1659–1669.CrossRefGoogle ScholarPubMed
Clarkson, D. (1980) The mineral nutrition in higher plants. Annual Review of Plant Physiology 31, 239–298.CrossRefGoogle Scholar
Crouch, M.L. and Sussex, I.M. (1981) Development and storage-protein synthesis in Brassica napus L. embryos in vivo and in vitro. Planta 153, 64–74.CrossRefGoogle ScholarPubMed
DeLano, W.L. (2002) The PyMOL molecular graphics system. San Carlos, California, DeLano Scientific.Google Scholar
Dumas, B., Freyssinet, G. and Pallett, K.E. (1995) Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiology 107, 1091–1096.CrossRefGoogle ScholarPubMed
Duranti, M., Scarafoni, A., Di Cataldo, A. and Sessa, F. (2001) Interaction of metal ions with lupin seed conglutin gamma. Phytochemistry 56, 529–533.CrossRefGoogle ScholarPubMed
Einhoff, W., Fleischmann, G., Freier, T., Kummer, H. and Rudiger, H. (1986) Interactions between lectins and other components of leguminous protein bodies. Biological Chemistry Hoppe–Seyler 367, 15–25.CrossRefGoogle ScholarPubMed
Ferreira, R., Melo, T. and Teixeira, A. (1995) Catabolism of the seed storage proteins from Lupinus albus: fate of globulins during germination and seedling growth. Functional Plant Biology 22, 373–381.CrossRefGoogle Scholar
Ferreira, R.B., Franco, E. and Teixeira, A.R. (1999) Calcium- and magnesium-dependent aggregation of legume seed storage proteins. Journal of Agricultural and Food Chemistry 47, 3009–3015.CrossRefGoogle ScholarPubMed
Ferreira, R.B., Freitas, R.L. and Teixeira, A.R. (2003) Self-aggregation of legume seed storage proteins inside the protein storage vacuoles is electrostatic in nature, rather than lectin-mediated. FEBS Letters 534, 106–110.CrossRefGoogle ScholarPubMed
Franceschi, V. (1989) Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma 148, 130–137.CrossRefGoogle Scholar
Franceschi, V.R. and Nakata, P.A. (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41–71.CrossRefGoogle ScholarPubMed
Franco, E., Ferreira, R.B. and Teixeira, A.R. (1997) Utilization of an improved methodology to isolate Lupinus albus conglutins in the study of their sedimentation coefficients. Journal of Agricultural and Food Chemistry 45, 3908–3913.CrossRefGoogle Scholar
Fukuda, T., Maruyama, N., Salleh, M.R., Mikami, B. and Utsumi, S. (2008) Characterization and crystallography of recombinant 7S globulins of Adzuki bean and structure–function relationships with 7S globulins of various crops. Journal of Agricultural and Food Chemistry 56, 4145–4153.CrossRefGoogle ScholarPubMed
García, M.C., Torre, M., Marina, M.L., Laborda, F. and Rodriquez, A.R. (1997) Composition and characterization of soybean and related products. Critical Reviews in Food Science and Nutrition 37, 361–391.CrossRefGoogle ScholarPubMed
Greiner, R. (2002) Purification and characterization of three phytases from germinated lupin seeds (Lupinus albus var. amiga). Journal of Agricultural and Food Chemistry 50, 6858–6864.CrossRefGoogle ScholarPubMed
Gruis, D., Schulze, J. and Jung, R. (2004) Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases. The Plant Cell 16, 270–290.CrossRefGoogle ScholarPubMed
He, F., Huang, F., Wilson, K.A. and Tan-Wilson, A. (2007) Protein storage vacuole acidification as a control of storage protein mobilization in soybeans. Journal of Experimental Botany 58, 1059–1070.CrossRefGoogle ScholarPubMed
Ilarslan, H., Palmer, R. and Horner, H. (2001) Calcium oxalate crystals in developing seeds of soybean. Annals of Botany 88, 243–257.CrossRefGoogle Scholar
Jain, E., Bairoch, A., Duvaud, S., Phan, I., Redaschi, N., Suzek, B.E., Martin, M.J., Mcgarvey, P. and Gasteiger, E. (2009) Infrastructure for the life sciences: design and implementation of the UniProt website. BMC Bioinformatics 10, 136.CrossRefGoogle ScholarPubMed
Jiang, L. and Rogers, J.C. (2002) Compartmentation of proteins in the protein storage vacuole: a compound organelle in plant cells. Advances in Botanical Research 35, 140–170.Google Scholar
Jiang, L., Phillips, T.E., Rogers, S.W. and Rogers, J.C. (2000) Biogenesis of the protein storage vacuole crystalloid. Journal of Cell Biology 150, 755–770.CrossRefGoogle ScholarPubMed
Jin, T., Albillos, S.M., Guo, F., Howard, A., Fu, T.J., Kothary, M.H. and Zhang, Y.Z. (2009) Crystal structure of prunin-1, a major component of the almond (Prunus dulcis) allergen amandin. Journal of Agricultural and Food Chemistry 57, 8643–8651.CrossRefGoogle Scholar
Kanauchi, M., Milet, J. and Bamforth, C. (2009) Oxalate and oxalate oxidase in malt. Journal of the Institute of Brewing 115, 232–237.CrossRefGoogle Scholar
Khan, S., Verma, G. and Sharma, S. (2010) A novel Ca2+-activated protease from germinating Vigna radiata seeds and its role in storage protein mobilization. Journal of Plant Physiology 167, 855–861.CrossRefGoogle ScholarPubMed
Lott, J.N.A. and Buttrose, M.S. (1978) Thin sectioning, freeze fracturing, energy dispersive X-ray analysis, and chemical analysis in the study of inclusions in seed protein bodies: almond, Brazil nut, and quandong. Canadian Journal of Botany 56, 2050–2061.CrossRefGoogle Scholar
Magni, C., Scarafoni, A., Herndl, A., Sessa, F., Prinsi, B., Espen, L. and Duranti, M. (2007) Combined 2D electrophoretic approaches for the study of white lupin mature seed storage proteome. Phytochemistry 68, 997–1007.CrossRefGoogle Scholar
Maruyama, Y., Maruyama, N., Mikami, B. and Utsumi, S. (2004) Structure of the core region of the soybean β-conglycinin α' subunit. Acta Crystallographica Section D Biological Crystallography 60, 289–297.CrossRefGoogle ScholarPubMed
Muntz, K. (2007) Protein dynamics and proteolysis in plant vacuoles. Journal of Experimental Botany 58, 2391–2407.CrossRefGoogle ScholarPubMed
Muntz, K., Belozersky, M.A., Dunaevsky, Y.E., Schlereth, A. and Tiedemann, J. (2001) Stored proteinases and the initiation of storage protein mobilization in seeds during germination and seedling growth. Journal of Experimental Botany 52, 1741–1752.CrossRefGoogle ScholarPubMed
Okubo, K., Myers, D.V. and Iacobucci, G.A. (1976) Binding of phytic acid to glycinin. Cereal Chemistry 53, 513–524.Google Scholar
Otegui, M.S., Herder, R., Schulze, J., Jung, R. and Staehelin, L.A. (2006) The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. The Plant Cell 18, 2567–2581.CrossRefGoogle ScholarPubMed
Ramagli, L.S. (1999) Quantifying protein in 2-D PAGE solubilization buffers. Methods in Molecular Biology 112, 99–103.Google ScholarPubMed
Regvar, M., Eichert, D., Kaulich, B., Gianoncelli, A., Pongrac, P., Vogel-Mikus, K. and Kreft, I. (2011) New insights into globoids of protein storage vacuoles in wheat aleurone using synchrotron soft X-ray microscopy. Journal of Experimental Botany 62, 3929–3939.CrossRefGoogle ScholarPubMed
Rendle, A.B. (1888) On the development of the aleurone-grains in the lupin. Annals of Botany 2, 161–167.CrossRefGoogle Scholar
Sharon, N. and Lis, H. (1990) Legume lectins – a large family of homologous proteins. FASEB Journal 4, 3198–3208.CrossRefGoogle ScholarPubMed
Shewry, P.R. and Casey, R. (1999) Seed proteins. pp. 1–10in (Eds) Seed proteins. Dordrecht, The Netherlands, Kluwer Academic Publishers.CrossRefGoogle Scholar
Shutov, A.D., Baumlein, H., Blattner, F.R. and Muntz, K. (2003) Storage and mobilization as antagonistic functional constraints on seed storage globulin evolution. Journal of Experimental Botany 54, 1645–1654.CrossRefGoogle ScholarPubMed
Tan-Wilson, A.L. and Wilson, K.A. (2012) Mobilization of seed protein reserves. Physiologia Plantarum 145, 140–153.CrossRefGoogle ScholarPubMed
Trugo, L.C., Donangelo, C.M., Duarte, Y.A. and Tavares, C.L. (1993) Phytic acid and selected mineral composition of seed from wild species and cultivated varieties of lupin. Food Chemistry 47, 391–394.Google Scholar
Weber, E. and Neumann, D. (1980) Protein bodies, storage organelles in plant seeds. Biochemie und Physiologie der Pflanzen 175, 279–306.CrossRefGoogle Scholar