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Biochemical characterization of atypical biotinylation domains in seed proteins

Published online by Cambridge University Press:  22 February 2007

Claudette Job ,
Stéphanie Laugel ,
Manuel Duval ,
Karine Gallardo  and
Dominique Job
Claudette Job
Affiliation:
Laboratoire Mixte CNRS/INRA/Aventis (UMR1932), Aventis CropScience, 14–20 rue Pierre Baizet, 69263, Lyon CEDEX 9, France
Stéphanie Laugel
Affiliation:
Laboratoire Mixte CNRS/INRA/Aventis (UMR1932), Aventis CropScience, 14–20 rue Pierre Baizet, 69263, Lyon CEDEX 9, France
Manuel Duval
Affiliation:
Department of Biology, Texas A & M University, College Station, TX 77843, USA
Karine Gallardo
Affiliation:
Laboratoire Mixte CNRS/INRA/Aventis (UMR1932), Aventis CropScience, 14–20 rue Pierre Baizet, 69263, Lyon CEDEX 9, France
Dominique Job*
Affiliation:
Laboratoire Mixte CNRS/INRA/Aventis (UMR1932), Aventis CropScience, 14–20 rue Pierre Baizet, 69263, Lyon CEDEX 9, France
*
*Correspondence Fax: (+33) 4 72 85 22 97 Email: dominique.job@aventis.com
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Abstract

Homologues of the pea SBP65, a late embryogenesis abundant (LEA) biotinylated protein that behaves as a putative sink for the free vitamin biotin during embryo development, were characterized biochemically in various plant species, including soybean, lentil, peanut, rape, cabbage, carrot and sugarbeet. Based on sequence homologies, the genome of Arabidopsis thaliana contains a gene putatively encoding a homologue of pea SBP65. These proteins exhibit two remarkable features. First, they only accumulate in seeds, particularly during late stages of embryo development. The results strongly suggest that these seed-specific biotinylated proteins belong to the class of plant proteins called seed maturation proteins, which are presumed to play major roles in embryo development. Secondly, covalent attachment of biotin occurs at a lysine residue within a conserved motif of (V/M)GKF, which shows no resemblance to the highly conserved AMKM tetrapeptide that houses the target lysine residue in the well-characterized biotin-dependent carboxylases and decarboxylases. These findings highlight novel structural features for protein biotinylation.

Keywords

seed maturationgerminationLEA proteinsbiotinylated proteinsbiotinArabidopsis thalianacabbage (Brassica oleracea)carrot (Daucus carota)lentil (Lens culinaris)pea (Pisum sativum)peanut (Arachis hypogaea)rape (Brassica napus)soybean(Glycine max (L.) Merrill)sugarbeet (Beta vulgaris)
Type
Research Article
Information
Seed Science Research , Volume 11 , Issue 2 , June 2001 , pp. 149 - 162
Copyright
Copyright © Cambridge University Press 2001

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References

Alban, C., Baldet, P., Axiotis, S. and Douce, R. (1993) Purification and characterization of 3-methylcrotonyl-coenzyme A carboxylase from higher plant mitochondria. Plant Physiologyz 102, 957–965.Google Scholar
Alban, C., Job, D. and Douce, R. (2000) Biotin metabolism in plants. Annual Review of Plant Physiology and Plant Molecular Biology 51, 17–47.Google Scholar
Anderson, M.D., Che, P., Song, J.P., Nikolau, B.J. and Wurtele, E.S. (1998) 3-Methylcrotonyl coenzyme A carboxylase is a component of the mitochondrial leucine catabolic pathway in plants. Plant Physiology 118, 1127–1138.Google Scholar
Beckett, D., Kovaleva, E. and Schatz, P.J. (1999) A minimal peptide substrate in biotin holoenzyme synthetasecatalyzed biotinylation. Protein Science 8, 921–929.Google Scholar
Bewley, J.D. and Black, M. (1994) Seeds: physiology and germination (2nd edition). New York, Plenum Press.Google Scholar
Blackman, S.A., Wettlaufer, S.H., Obendorf, R.L. and Leopold, A.C. (1991) Maturation proteins associated with desiccation tolerance in soybean. Plant Physiology 96, 868–874.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Capron, I., Corbineau, F., Dacher, F., Job, C., Côme, D. and Job, D. (2000) Sugarbeet seed priming: effects of priming conditions on germination, solubilization of 11-S globulin and accumulation of LEA proteins. Seed Science Research 10, 243–254.Google Scholar
Chapman-Smith, A. and Cronan, J.E. Jr. (1999a) The enzymatic biotinylation of proteins: a post-translational modification of exceptional specificity. Trends in Biochemical Sciences 24, 359–363.Google Scholar
Chapman-Smith, A. and Cronan, J.E. Jr. (1999b) Molecular biology of biotin attachment to proteins. Journal of Nutrition 129, 477S–484S.Google Scholar
Craft, D.V., Goss, N.H., Chandramouli, N. and Wood, H.G. (1985) Purification of biotinidase from human plasma and its activity on biotinyl peptides. Biochemistry 24, 2471–2476.Google Scholar
Dehaye, L., Alban, C., Job, C., Douce, R. and Job, D. (1994) Kinetics of the two forms of acetyl-CoA carboxylase from Pisum sativum. Correlation of the substrate specificity of the enzymes and sensitivity towards aryloxyphenoxypropionate herbicides. European Journal of Biochemistry 225, 1113–1123.Google Scholar
Dehaye, L., Duval, M., Viguier, D., Yaxley, J. and Job, D. (1997) Cloning and expression of the pea gene encoding SBP65, a seed-specific biotinylated protein. Plant Molecular Biology 35, 605–621.Google Scholar
Dure, L. III (1993a) The LEA proteins of higher plants. pp. 325–335 in Verma, D.P.S. (Ed.) Control of plant gene expression. Boca Raton, CRC Press, Inc.Google Scholar
Dure, L. III (1993b) A repeating 11-mer amino acid motif and plant desiccation. Plant Journal 3, 363–369.Google Scholar
Duval, M. (1995) La semence et la biotine. Découverte d'une protéine à biotine chez Pisum sativum L., marqueur moléculaire de la maturation des semences et des phases précoces de la germination. PhD thesis, University Joseph Fourier, Grenoble, France.Google Scholar
Duval, M., DeRose, R.T., Job, C., Faucher, D., Douce, R. and Job, D. (1994a) The major biotinyl protein from Pisum sativum seeds covalently binds biotin at a novel site. Plant Molecular Biology 26, 265–273.Google Scholar
Duval, M., Job, C., Alban, C., Douce, R. and Job, D. (1994b) Developmental patterns of free and protein-bound biotin during maturation and germination of seeds of Pisum sativum. Characterization of a novel seed-specific biotinylated protein. Biochemical Journal 299, 141–150.Google Scholar
Duval, M., Pépin, R., Job, C., Derpierre, C., Douce, R. and Job, D. (1995) Ultrastructural localization of the major biotinylated protein from Pisum sativum seeds. Journal of Experimental Botany 46, 1783–1786.Google Scholar
Galau, G.A. and Dure, L.S. III (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing mRNA populations as shown by reciprocal heterologous cDNA-mRNA hybridization. Biochemistry 20, 4169–4178.Google Scholar
Goumon, Y., Lugardon, K., Gadroy, P., Strub, J.-M., Welters, I.D., Stefano, G.B., Aunis, D. and Metz-Boutigue, M.H. (2000) Processing of proenkephalin-A in bovine chromaffin cells. Identification of natural derived fragments by N-terminal sequencing and matrix-assisted laser desorption ionization-time of flight mass spectrometry. Journal of Biological Chemistry 275, 38355–38362.Google Scholar
Hsing, Y.C., Tsou, C.H., Hsu, T.F., Chen, Z.Y., Hsieh, K.L., Hsieh, J.S. and Chow, T.Y. (1998) Tissue- and stagespecific expression of a soybean (Glycine max L.) seedmaturation, biotinylated protein. Plant Molecular Biology 38, 481–490.Google Scholar
Hymes, J. and Wolf, B. (1998) Human biotinidase isn't just for recycling biotin. Journal of Nutrition 129, 485S–489S.Google Scholar
Hymes, J., Fleischhauer, K. and Wolf, B. (1995) Biotinylation of biotinidase following incubation with biocytin. Clinica Chimica Acta 233, 39–45.Google Scholar
Job, C., Kersulec, A., Ravasio, L., Chareyre, S., Pépin, R. and Job, D. (1997) The solubilization of the basic subunit of sugarbeet seed 11-S globulin during priming and early germination. Seed Science Research 7, 225–243.Google Scholar
Job, D., Capron, I., Job, C., Dacher, F., Corbineau, F. and Côme, D. (2000) Identification of germination-specific protein markers and their use in seed priming technology. pp. 449–459 in Black, M.; Bradford, K.J.; Vázquez-Ramos, J. (Eds) Seed biology : advances and applications. Wallingford, CABI Publishing.Google Scholar
Knowles, J.R. (1989) The mechanism of biotin-dependent enzymes. Annual Review of Biochemistry 58, 195–221.Google Scholar
Kyte, J. and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157, 105–132.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.Google Scholar
Lane, M.D., Rominger, K.L., Young, D.L. and Lynen, F. (1964) The enzymatic synthesis of holotranscarboxylase from apotranscarboxylase and (+) biotin. Journal of Biological Chemistry 239, 2865–2871.Google Scholar
Morgenstern, B., Dress, A. and Werner, T. (1996) Multiple DNA and protein sequence alignment based on segment-to-segment comparison. Proceedings of the National Academy of Sciences USA 93, 12098–12103.Google Scholar
Neto, J.B.F., Shatters, R.G. and West, S.H. (1997) Developmental pattern of biotinylated proteins during embryogenesis and maturation of soybean seed. Seed Science Research 7, 377–384.Google Scholar
Newman, W., Beall, L.D. and Randhawa, Z.I. (1990) Biotinylation of peptide hormones: Structural analysis and application to flow cytometry. Methods in Enzymology 184, 275–285.Google Scholar
Patton, D.A., Schetter, A.L., Franzmann, L.H., Nelson, K., Ward, E.R. and Meinke, D.W. (1998) An embryodefective mutant of Arabidopsis disrupted in the final step of biotin synthesis. Plant Physiology 116, 935–946.Google Scholar
Reche, P. and Perham, R.N. (1999) Structure and selectivity in post-translational modification: Attaching the biotinyl-lysine and lipoyl-lysine swinging arms in multifunctional enzymes. EMBO Journal 18, 2673–2682.Google Scholar
Roesler, K.R., Savage, L.J., Shintani, D.K., Shorrosh, B.S. and Ohlrogge, J.B. (1996) Co-purification, coimmunoprecipitation, and coordinate expression of acetyl-coenzyme A carboxylase activity, biotin carboxylase, and biotin carboxyl carrier protein of higher plants. Planta 198, 517–525.Google Scholar
Rosenberg, L.A. and Rinne, R.W. (1986) Moisture loss as a prerequisite for seedling growth in soybean seeds (Glycine max (L.) Merr.). Journal of Experimental Botany 37, 1663–1674.CrossRefGoogle Scholar
Russouw, P.S., Farrant, J., Brandt, W. and Lindsley, G.G. (1997) The most prevalent protein in a heat-treated extract of pea (Pisum sativum) embryos is an LEA group I protein; its conformation is not affected by exposure to high temperature. Seed Science Research 7, 117–123.Google Scholar
Samols, D., Thornton, C.G., Murtif, V.L., Kumar, G.K., Haase, F.C. and Wood, H.G. (1988) Evolutionary conservation among biotin enzymes. Journal of Biological Chemistry 263, 6461–6464.Google Scholar
Schatz, P.J. (1993) Use of peptide libraries to map the substrate specificity of a peptide modifying enzyme: A 13 residue consensus peptide specifies biotinylation in Escherichia coli. Biotechnology 11, 1138–1143.Google Scholar
Schneider, T., Dinkins, R., Robinson, K., Shellhammer, J. and Meinke, D.W. (1989) An embryo-lethal mutant of Arabidopsis thaliana is a biotin auxotroph. Developmental Biology 131, 161–167.Google Scholar
Shatters, R.G., Boo, S.P., Neto, J.B.F. and West, S.H. (1997) Identification of biotinylated proteins in soybean [Glycine max (L.) Merrill] seeds and their characterization during germination and seedling growth. Seed Science Research 7, 373–376.Google Scholar
Shenoy, B.C., Paranjape, S., Murtif, V.L., Kumar, G.K., Samols, D. and Wood, H.G. (1988) Effects of mutations at Met-88 and Met-90 on the biotinylation of Lys-89 of the apo 1.3S subunit of transcarboxylase. FASEB Journal 2, 2505–2511.Google Scholar
Shenoy, B.C., Xie, Y., Park, V.L., Kumar, G.K., Beegan, H., Wood, H.G. and Samols, D. (1992) The importance of methionine residues for the catalysis of the biotin enzyme, transcarboxylase. Analysis by site-directed mutagenesis. Journal of Biological Chemistry 267, 18407–18412.Google Scholar
Shellhammer, J. and Meinke, D. (1990) Arrested embryos from the bio1 auxotroph of Arabidopsis thaliana contain reduced levels of biotin. Plant Physiology 93, 1162–1167.Google Scholar
Tissot, G., Job, D., Douce, R. and Alban, C. (1996) Protein biotinylation in higher plants: Characterization of biotin holocarboxylase synthetase activity from pea (Pisum sativum) leaves. Biochemical Journal 314, 391–395.Google Scholar
Tissot, G., Douce, R. and Alban, C. (1997) Evidence for multiple forms of biotin holocarboxylase synthetase in pea (Pisum sativum) and in Arabidopsis thaliana: Subcellular fractionation studies and isolation of a cDNA clone. Biochemical Journal 323, 179–188.Google Scholar
Tissot, G., Pépin, R., Job, D., Douce, R. and Alban, C. (1998) Purification and properties of the chloroplastic form of biotin holocarboxylase synthetase from Arabidopsis thaliana overexpressed in Escherichia coli. European Journal of Biochemistry 258, 586–596.Google Scholar
Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets. Procedures and some applications. Proceedings of the National Academy of Sciences USA 76, 4350–4354.Google Scholar
Walters, C., Ried, J.L. and Walker-Simmons, M.K. (1997) Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties. Seed Science Research 7, 125–134.Google Scholar
Wilm, M. (2000) Mass spectrometric analysis of proteins. Advances in Protein Chemistry 54, 1–30.Google Scholar
Wurtele, E.S. and Nikolau, B.J. (1990) Plants contain multiple biotin enzymes: discovery of 3-methylcrotonyl-CoA carboxylase, propionyl-CoA carboxylase and pyruvate carboxylase in the plant kingdom. Archives of Biochemistry and Biophysics 278, 179–186.Google Scholar
Wurtele, E.S. and Nikolau, B.J. (1992) Differential accumulation of biotin enzymes during carrot somatic embryogenesis. Plant Physiology 99, 1699–1703.Google Scholar