Advertisement

The Genetics and Biochemistry of Maize Zein Storage Proteins

  • Rebecca S. Boston
  • Brian A. Larkins

Zeins, the most abundant proteins in the maize seed, have been studied for over 100 years. We have learned a great deal about the structure, synthesis and genetic regulation of these proteins, making them a valuable model system to study storage protein synthesis. In this review, we explore longstanding questions and controversies regarding zeins in light of new information from genomic sequencing, improved protein detection methods and molecular characterization of mutants.

Keywords

Unfold Protein Response Protein Body Seed Storage Protein Quality Protein Maize Maize Endosperm 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anfinsen, C.B. (1973) Principles that govern the folding of protein chains. Science 181: 223–230.PubMedCrossRefGoogle Scholar
  2. Argos, P., K. Pedersen, M.D. Marks, and B.A. Larkins (1982) A structural model for maize zein proteins. J. Biol. Chem. 257: 9984–9990.PubMedGoogle Scholar
  3. Azevedo, R.A., C. Damerval, J. Landry, P.J. Lea, C.M. Bellato, L.W. Meinhardt, M. Le Guilloux, S.Delhaye, A.A. Toro, S.A. Gaziola, and B.D. Berdejo (2003) Regulation of maize lysinemetabolism and endosperm protein synthesis by opaque and floury mutations. Eur J Biochem. 270: 4898–908.PubMedCrossRefGoogle Scholar
  4. Bagga, S., H. Adams, J.D. Kemp, and C. Sengupta-Gopalan (1995) Accumulation of 15-kilodalton zein in novel protein bodies in transgenic tobacco. Plant Physiol. 107: 13–23.PubMedGoogle Scholar
  5. Bagga, S., H.P. Adams, F.D. Rodriguez, J.D. Kemp, and C. Sengupta-Gopalan (1997) Coexpression of the maize delta-zein and beta-zein genes results in stable accumulation of delta-zein in endoplasmic reticulum-derived protein bodies formed by beta-zein. Plant Cell 9: 1683–1696.PubMedCrossRefGoogle Scholar
  6. Balconi, C., E. Rizzi, M. Motto, F. Salamini, and R.D. Thompson (1993) The accumulation of zein polypeptides and zein mRNA in cultured endosperms of maize is modulated by nitrogen supply. The Plant J. 3: 325–334.Google Scholar
  7. Bellucci, M., A. Alpini, F. Paolocci, L. Cong, and S. Arcioni (2000) Accumulation of maize ?-zein and ?-zein:KDEL to high levels in tobacco leaves and differential increase of BiP synthesis in transformants. Theor Appl Genet. 101: 796–804CrossRefGoogle Scholar
  8. Boston, R.S., E.B. Fontes, B.B. Shank, and R.L. Wrobel (1991) Increased expression of the maize immunoglobulin binding protein homolog b-70 in three zein regulatory mutants. Plant Cell 3: 497–505.PubMedCrossRefGoogle Scholar
  9. Burr, B. and F.A. Burr (1976) Zein synthesis in maize endosperm by polyribosomes attached to protein bodies. Proc. Natl. Acad. Sci. U. S. A. 73: 515–519.PubMedCrossRefGoogle Scholar
  10. Burr, B., F.A. Burr, T.P. St. John, M. Thomas, and R.W. Davis (1982) Zein storage protein gene family of maize. An assessment of heterogeneity with cloned messenger RNA sequences. J. Mol. Biol. 154: 33–49.Google Scholar
  11. Chui, C.F. and S.C. Falco (1995) A new methionine-rich seed storage protein from maize. Plant Physiol. 107: 291.PubMedCrossRefGoogle Scholar
  12. Ciceri, P., S. Castelli, M. Lauria, B. Lazzari, A. Genga, L. Bernard, M. Sturaro, and A. Viotti (2000) Specific combinations of zein genes and genetic backgrounds influence the transcription of the heavy-chain zein genes in maize opaque-2 endosperms. Plant Physiol. 124: 451–460.PubMedCrossRefGoogle Scholar
  13. Ciceri, P., F. Locatelli, A. Genga, A. Viotti, and R.J. Schmidt (1999) The activity of the maize Opaque2 transcriptional activator is regulated diurnally. Plant Physiol. 121: 1321–1328.PubMedCrossRefGoogle Scholar
  14. Coleman, C.E., E.M. Herman, K. Takasaki, and B.A. Larkins (1996) The maize ?-zein sequesters a-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm. Plant Cell 8: 2335–2345.PubMedCrossRefGoogle Scholar
  15. Coleman, C.E., M.A. Lopes, J.W. Gillikin, R.S. Boston, and B.A. Larkins (1995) A defective signal peptide in the maize high-lysine mutant floury 2. Proc. Natl. Acad. Sci. U. S. A. 92: 6828–6831.PubMedCrossRefGoogle Scholar
  16. Consoli, L. and C. Damerval (2001) Quantification of individual zein isoforms resolved by two-dimensional electrophoresis: Genetic variability in 45 maize inbred lines. Electrophoresis 22: 2983–2989.PubMedCrossRefGoogle Scholar
  17. Das, O.P. and J.W. Messing (1987) Allelic variation and differential expression at the 27-kilodalton zein locus in maize. Mol. Cell Biol. 7: 4490–4497.PubMedGoogle Scholar
  18. Duvick, D.N. (1961) Protein granules of maize endosperm cells. Cereal Chem. 38: 374–385.Google Scholar
  19. Emrich, S.J., W.B. Barbazuk, L. Li, and P.S. Schnable (2007) Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Res. 17: 69–73.PubMedCrossRefGoogle Scholar
  20. Esen, A. (1986) Separation of alcohol-soluble proteins (zeins) from maize into three fractions by differential solubility. Plant Physiol. 80: 623–627.PubMedCrossRefGoogle Scholar
  21. Esen, A. (1987) A proposed nomenclature for the alcohol-soluble proteins (zeins) of maize (Zea mays-L). J. Cereal Sci. 5: 117–128.CrossRefGoogle Scholar
  22. Esen, A. and D.A. Stetler (1992) Immunocytochemical localization of the delta-zein in protein bodies of maize endosperm cells. Amer. J. Bot. 79: 243–248.Google Scholar
  23. Fontes, E.B., B.B. Shank, R.L. Wrobel, S.P. Moose, G.R. OBrian, E.T. Wurtzel, and R.S. Boston (1991) Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant. Plant Cell 3: 483–496.PubMedCrossRefGoogle Scholar
  24. Galante, E., A. Vitale, L. Manzocchi, C. Soave, and F. Salamini (1983) Genetic control of a membrane component and zein deposition in maize endosperm. Mol. Gen. Genet. 192: 316–321.CrossRefGoogle Scholar
  25. Garratt, R., G. Oliva, I. Caracelli, A. Leite, and P. Arruda (1993) Studies of the zein-like alpha-prolamins based on an analysis of amino acid sequences: implications for their evolution and three-dimensional structure. Proteins: Structure, Function and Genetics 15: 88–99.CrossRefGoogle Scholar
  26. Geetha, K.B., C.R. Lending, M.A. Lopes, J.C. Wallace, and B.A. Larkins (1991) opaque-2 modifiers increase ?-zein synthesis and alter its spatial distribution in maize endosperm. Plant Cell 3: 1207–1219.PubMedCrossRefGoogle Scholar
  27. Geli, M.I., M. Torrent, and D. Ludevid (1994) Two structural domains mediate two sequential events in ?-zein targeting: protein endoplasmic reticulum retention and protein body formation. Plant Cell 6: 1911–1922.PubMedCrossRefGoogle Scholar
  28. Geraghty, D., Peifer, M.A., Rubenstein, I. and Messing, J. (1981). The primary structure of a plant storage protein: Zein. Nucl. Acids Res. 9: 5163–5174.CrossRefGoogle Scholar
  29. Geraghty, D.E., J. Messing, and I. Rubenstein (1982) Sequence analysis and comparison of cDNAs of the zein multigene family. EMBO J. 1: 1329–1335.PubMedGoogle Scholar
  30. Gianazza, E., V. Viglienghi, P.G. Righetti, F. Salamini, and C. Soave (1977) Amino acid composition of zein molecular components. Phytochem. 16: 315–317.CrossRefGoogle Scholar
  31. Gillikin, J.W., F. Zhang, C.E. Coleman, H.W. Bass, B.A. Larkins, and R.S. Boston (1997) A defective signal peptide tethers the floury-2 zein to the endoplasmic reticulum membrane. Plant Physiol. 114: 345–352.PubMedCrossRefGoogle Scholar
  32. Habben, J.E., A.W. Kirleis, and B.A. Larkins (1993) The origin of lysine-containing proteins in opaque-2 maize endosperm. Plant Mol. Biol. 23: 825–838.PubMedCrossRefGoogle Scholar
  33. Hagen, G. and I. Rubenstein (1981) Complex organization of zein genes in maize. Gene 13: 239–249.PubMedCrossRefGoogle Scholar
  34. Hartings, H., M. Maddaloni, N. Lazzaroni, N. Di Fonzo, M. Motto, F. Salamini, and R. Thompson (1989) The O2 gene which regulates zein deposition in maize endosperm encodes a protein with structural homologies to transcriptional activators. EMBO J. 8: 2795–2801.PubMedGoogle Scholar
  35. Hinnebusch, A.G. and K. Natarajan (2002) Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1: 22–32.PubMedCrossRefGoogle Scholar
  36. Holding, D.R., M.S. Otegui, B. Li, R.B. Meeley, T. Dam, B.G. Hunter, R. Jung, and B.A. Larkins (2007) The maize Floury1 gene encodes a novel endoplasmic reticulum protein involved in zein protein body formation. Plant Cell 19: 2569–2582.PubMedCrossRefGoogle Scholar
  37. Hu, N.T., M.A. Peifer, G. Heidecker, J. Messing, and I. Rubenstein (1982) Primary structure of a genomic zein sequence in maize. EMBO J. 1: 1337–1342.PubMedGoogle Scholar
  38. Huang, S., W.R. Adams, Q. Zhou, K.P. Malloy, D.A. Voyles, J. Anthony, A.L. Kriz, and M.H.Luethy (2004) Improving nutritional quality of maize proteins by expressing sense and antisense zein genes. J. Agric. Food Chem. 52: 1958–1964.PubMedCrossRefGoogle Scholar
  39. Hunter, B.G., M.K. Beatty, G.W. Singletary, B.R. Hamaker, B.P. Dilkes, B.A. Larkins, and R. Jung (2002) Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14: 2591–2612.PubMedCrossRefGoogle Scholar
  40. Kim, C.S., B.C. Gibbon, J.W. Gillikin, B.A. Larkins, R.S. Boston, and R. Jung (2006) The maize Mucronate mutation is a deletion in the 16-kDa ?-zein gene that induces the unfolded protein response. The Plant J. 48: 440–451.CrossRefGoogle Scholar
  41. Kim, C.S., B.G. Hunter, J. Kraft, R.S. Boston, S. Yans, R. Jung, and B.A. Larkins (2004) A defective signal peptide in a 19-kD alpha-zein protein causes the unfolded protein response and an opaque endosperm phenotype in the maize De*-B30 mutant. Plant Physiol. 134: 380–387.PubMedCrossRefGoogle Scholar
  42. Kim, C.S., Y.-m. Woo, A.M. Clore, R.J. Burnett, N.P. Carneiro, and B.A. Larkins (2002) Zein protein interactions, rather than the asymmetric distribution of zein mRNAs on endoplasmic reticulum membranes, influence protein body formation in maize endosperm. Plant Cell 14: 655–672.PubMedCrossRefGoogle Scholar
  43. Kirihara, J.A., J.B. Petri, and J. Messing (1988) Isolation and sequence of a gene encoding a methionine-rich 10-kDa zein protein from maize. Gene 71: 359–370.PubMedCrossRefGoogle Scholar
  44. Kirst, M.E., D.J. Meyer, B.C. Gibbon, R. Jung, and R.S. Boston (2005) Identification and characterization of endoplasmic reticulum-associated degradation proteins differentially affected by endoplasmic reticulum stress. Plant Physiol. 138: 218–231.PubMedCrossRefGoogle Scholar
  45. Kriz, A.L., R.S. Boston, and B.A. Larkins (1987) Structural and transcriptional analysis of DNA sequences flanking genes that encode 19 kilodalton zeins. Mol. Gen. Genet. 207: 90–98.PubMedCrossRefGoogle Scholar
  46. Landry, J. and T. Moureaux (1970) Héterogénéite des glutélines du grain de mais: extraction sélective et composition en acidés aminés des trois fractions isolées. Bull. Soc. Chim. Biol. 52: 1021–1037.PubMedGoogle Scholar
  47. Larkins, B.A. and A. Dalby (1975) In vitro synthesis of zein-like protein by maize polyribosomes. Biochem. Biophys. Res. Commun. 66: 1048–1054.PubMedCrossRefGoogle Scholar
  48. Larkins, B.A. and W.J. Hurkman (1978) Synthesis and deposition of zein in protein bodies of maize endosperm. Plant Physiol. 62: 256–263.PubMedCrossRefGoogle Scholar
  49. Larkins, B.A., K. Pedersen, A.K. Handa, W.J. Hurkman, and L.D. Smith (1979) Synthesis and processing of maize storage proteins in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. U. S. A. 76: 6448-–6452.PubMedCrossRefGoogle Scholar
  50. Larkins, B.A., J.C. Wallace, G. Galili, C.R. Lending, and E. Kawata (1989) Structural analysis and modification of maize storage proteins. Dev. Indust. Micro. 30: 203–209.Google Scholar
  51. Lawton, J.W. (2002) Zein: A history of processing and use. Cereal Chem. 79: 1–18.CrossRefGoogle Scholar
  52. Leaver, C.J. (1980) Genome Organization and Expression in Plants. Plenum Press, New York.Google Scholar
  53. Lee, K.H., R.A. Jones, A. Dalby, and C.Y. Tsai (1976) Genetic regulation of storage protein content in maize endosperm. Biochem. Genet. 14: 641–650.PubMedCrossRefGoogle Scholar
  54. Lending, C.R., A.L. Kriz, B.A. Larkins, and C.E. Bracker (1988) Structure of maize protein bodies and immunocytochemical localization of zeins. Protoplasma 143: 51–62.CrossRefGoogle Scholar
  55. Lending, C.R. and B.A. Larkins (1989) Changes in the zein composition of protein bodies during maize endosperm development. Plant Cell 1: 1011–1023.PubMedCrossRefGoogle Scholar
  56. Lending, C.R. and B.A. Larkins (1992) Effect of the floury-2 locus on protein body formation during maize endosperm development. Protoplasma 171: 123–133.CrossRefGoogle Scholar
  57. Lund, G., P. Ciceri, and A. Viotti (1995) Maternal-specific demethylation and expression of specific alleles of zein genes in the endosperm of Zea mays L. The Plant J. 8: 571–581.CrossRefGoogle Scholar
  58. Lund, G., M. Lauria, P. Guldberg, and S. Zaina (2003) Duplication-dependent CG suppression of the seed storage protein genes of maize. Genetics 165: 835–848.PubMedGoogle Scholar
  59. Maier, U.G., J.W. Brown, C. Tologcyzki, and G. Feix (1987) Binding of a nuclear factor to a consensus sequence in the 5′ flanking region of zein genes from maize. EMBO J. 6: 17–22.PubMedGoogle Scholar
  60. Marks, M.D. and B.A. Larkins (1982) Analysis of sequence microheterogeneity among zein messenger RNAs. J. Biol. Chem. 257: 9976–9983.PubMedGoogle Scholar
  61. Marocco, A., A. Santucci, S. Cerioli, M. Motto, N. Di Fonzo, R. Thompson, and F. Salamini (1991) Three high-lysine mutations control the level of ATP-binding HSP70-like proteins in the maize endosperm. Plant Cell 3: 507–515.PubMedCrossRefGoogle Scholar
  62. McKinney, L.L. (1958) Zein. In: The Encyclopedia of Chemistry (G.L. Clark, ed.). Reinhold, N.Y., pp. 319–320.Google Scholar
  63. Mertz, E.T., L.S. Bates, and O.E. Nelson (1964) Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145: 279–280.PubMedCrossRefGoogle Scholar
  64. Misra, P.S., E.T. Mertz, and D.V. Glover (1975) Characteristics of proteins in single and double endosperm mutants of maize. In: High Quality Protein Maize (Bauman, L. F., E. T. Mertz, A. Caballo, and E. W. Sprague, eds.) Dowden, Hutchinson and Ross, Inc., Stroudsburg, PA, pp. 291–305.Google Scholar
  65. Motto, M., M. Maddaloni, G. Ponziani, M. Brembilla, R. Marotta, N. Fonzo, C. Soave, R. Thompson, and F. Salamini (1988) Molecular cloning of the o2-m5 allele of Zea mays using transposon marking. Mol. Gen. Genet. 212: 488–494.CrossRefGoogle Scholar
  66. Nelson, O.E., E.T. Mertz, and L.S. Bates (1965) Second mutant gene affecting the amino acid pattern of maize endosperm proteins. Science 150: 1469–1470.PubMedCrossRefGoogle Scholar
  67. Osborne, T.B. (1897) Amount and properties of the proteins of the maize kernel. J. Amer. Chem. Soc. 19: 525–532.CrossRefGoogle Scholar
  68. Osborne, T.B. (1908) Our present knowledge of plant proteins. Science 28: 417–427.PubMedCrossRefGoogle Scholar
  69. Park, W.D., E.D. Lewis, and I. Rubenstein (1980) Heterogeneity of zein mRNA and protein in maize. Plant Physiol. 65: 98–106.PubMedCrossRefGoogle Scholar
  70. Paulis, J.W., C. James, and J.S. Wall (1969) Comparison of glutelin proteins in normal and high-lysine corn. J. Agric. Food Chem. 17: 1301–1305.CrossRefGoogle Scholar
  71. Paulis, J.W. and J.S. Wall (1971) Fractionation and properties of alkylated-reduced corn glutelin proteins. Biochim. Biophys. Acta. 251: 57–69.PubMedGoogle Scholar
  72. Pedersen, K., P. Argos, S.V. Naravana, and B.A. Larkins (1986) Sequence analysis and characteri zation of a maize gene encoding a high-sulfur zein protein of Mr 15,000. J. Biol. Chem. 261: 6279–6284.PubMedGoogle Scholar
  73. Pedersen, K., K.S. Bloom, J.N. Anderson, D.V. Glover, and B.A. Larkins (1980) Analysis of the complexity and frequency of zein genes in the maize genome. Biochemistry 19: 1644–1650.PubMedCrossRefGoogle Scholar
  74. Pedersen, K., J. Devereux, D.R. Wilson, E. Sheldon, and B.A. Larkins (1982) Cloning and sequence analysis reveal structural variation among related zein genes in maize. Cell 29: 1015–1026.PubMedCrossRefGoogle Scholar
  75. Prat, S., J. Cortadas, P. Puigdomenech, and J. Palau (1985) Nucleic acid (cDNA) and amino acid sequences of the maize endosperm protein glutelin-2. Nucleic Acids Res. 13: 1493–1504.PubMedCrossRefGoogle Scholar
  76. Prat, S., L. Perez-Grau, and P. Puigdomenech (1987) Multiple variability in the sequence of a family of maize endosperm proteins. Gene 52: 41–49.PubMedCrossRefGoogle Scholar
  77. Pysh, L.D., M.J. Aukerman, and R.J. Schmidt (1993) OHP1: a maize basic domain/leucine zipper protein that interacts with Opaque2. Plant Cell 5: 227 #x2013;236.PubMedCrossRefGoogle Scholar
  78. Randall, J.J., D.W. Sutton, S.F. Hanson, and J.D. Kemp (2005) BiP and zein binding domains within the delta zein protein. Planta 221: 656–666.PubMedCrossRefGoogle Scholar
  79. Righetti, P.G., E. Gianazza, A. Viotti, and C. Soave (1977) Heterogeneity of storage proteins in maize. Planta 136: 115–123.CrossRefGoogle Scholar
  80. Schmidt, R.J., F.A. Burr, M.J. Aukerman, and B. Burr (1990) Maize regulatory gene opaque-2 encodes a protein with a “leucine-zipper ” motif that binds to zein DNA. Proc. Natl. Acad. Sci. U. S. A. 87: 46 –50.PubMedCrossRefGoogle Scholar
  81. Schmidt, R.J., F.A. Burr, and B. Burr (1987) Transposon tagging and molecular analysis of the maize regulatory locus opaque-2. Science 238: 960 –963.PubMedCrossRefGoogle Scholar
  82. Segal, G., R. Song, and J. Messing (2003) A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165: 387 –397.PubMedGoogle Scholar
  83. Shank, K.J., P. Su, I. Brglez, W.F. Boss, R.E. Dewey, and R.S. Boston (2001) Induction of lipid metabolic enzymes during the endoplasmic reticulum stress response in plants. Plant Physiol. 126: 267 –277.PubMedCrossRefGoogle Scholar
  84. Soave, C., R. Reggiani, N. Di Fonzo, and F. Salamini (1981) Clustering of genes for 20 kd zein subunits in the short arm of maize chromosome 7. Genetics 97: 363 –377.PubMedGoogle Scholar
  85. Soave, C. and F. Salamini (1984) Organization and regulation of zein in maize endosperm. Phil. Trans. R. Soc. Lond. B. 304: 341 –347.CrossRefGoogle Scholar
  86. Soave, C., N. Surman, A. Viotti, and F. Salamini (1978) Linkage relationships between regulatory and structural gene loci involved in zein synthesis in maize. Theor. Appl. Genet. 52: 263 –267.CrossRefGoogle Scholar
  87. Sodek, L. and C.M. Wilson (1971) Amino acid composition of proteins isolated from normal, opaque-2 and floury-2 corn endosperms by a modified Osborne procedure. J. Agric. Food Chem. 19: 1144 –1150.CrossRefGoogle Scholar
  88. Song, R., V. Llaca, E. Linton, and J. Messing (2001) Sequence, regulation, and evolution of the maize 22-kD alpha zein gene family. Genome Res. 11: 1817 –1825.PubMedGoogle Scholar
  89. Song, R. and J. Messing (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc. Natl. Acad. Sci. U. S. A. 100: 9055 –9060.PubMedCrossRefGoogle Scholar
  90. Spena, A., A. Viotti, and V. Pirrotta (1983) Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction pattern. J. Mol. Biol. 169:799 –811.PubMedCrossRefGoogle Scholar
  91. Spena, A., A. Viotti, and V. Pirrotta (1982) A homologous repetitive block structure underlies the heterogeneity of heavy and light chain zein genes. EMBO J. 1: 1589 –1594.PubMedGoogle Scholar
  92. Swarup, S., Timmermans, M.C.P., Chaudhuri, S., and Messing, J. (1995). Determinants of the high-methionine trait in wild and exotic germplasm may have escaped selection during early cultivation of maize. The Plant J. 8: 359 –368.CrossRefGoogle Scholar
  93. Tatham, A.S., J.M. Field, V.J. Morris, K.J. IœAnson, L. Cardle, M.J. Dufton, and P.R. Shewry (1993) Solution conformational analysis of the alpha-zein proteins of maize. J. Biol. Chem. 268: 26253 –26259.PubMedGoogle Scholar
  94. Thompson, G.A., D.R. Siemieniak, L.C. Sieu, J.L. Slightom, and B.A. Larkins (1992) Sequence analysis of linked maize 22 kDa alpha-zein genes. Plant Mol. Biol. 18: 827 –833.PubMedCrossRefGoogle Scholar
  95. Ueda, T., Wang, Z., Pham, N., and Messing, J. (1994). Identification of a transcriptional activator- binding element in the 27-kilodalton zein promoter, the -300 element. Mol. Cell. Biol. 14: 4350 –4359.PubMedGoogle Scholar
  96. Valentini, G., C. Soave, and E. Ottaviano (1979) Chromosomal location of zein genes in Zea mays. Heredity 42: 33 –46.CrossRefGoogle Scholar
  97. Vicente-Carbajosa, J., S.P. Moose, R.L. Parsons, and R.J. Schmidt (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc. Natl. Acad. Sci. U. S. A. 94: 7685 –7690.PubMedCrossRefGoogle Scholar
  98. Viotti, A., E. Sala, P. Alberi, and C. Soave (1978) Heterogeneity of zein synthesized in vitro. Plant Sci. Lett. 13.Google Scholar
  99. Viotti, A., E. Sala, R. Marotta, P. Alberi, C. Balducci, and C. Soave (1979) Genes and mRNAs coding for zein polypeptides in Zea mays. Eur. J. Biochem. 102: 211 –222.PubMedCrossRefGoogle Scholar
  100. Wang, Z., Ueda, T., and Messing, J. (1998). Characterization of the maize prolamin box-binding factor-1 (PBF-1) and its role in developmental regulation of the zein multigene family. Gene 223: 321 –332.PubMedCrossRefGoogle Scholar
  101. Wang, Z., and Messing, J. (1998). Modulation of gene expression by DNA-protein and protein- protein interactions in the promoter region of the zein multigene family. Gene 223: 333 –345.PubMedCrossRefGoogle Scholar
  102. Washida, H., A. Sugino, J. Messing, A. Esen, and T.W. Okita (2004) Asymmetric localization of seed storage protein RNAs to distinct subdomains of the endoplasmic reticulum in developing maize endosperm cells. Plant Cell Physiol. 45: 1830 –1837.PubMedCrossRefGoogle Scholar
  103. Weinand, U., C. Bruschke, and G. Feix (1979) Cloning of double stranded DNAs derived from polysomal mRNA of maize endosperm: isolation and characterisation of zein clones. Nucleic Acids Res. 6: 2707 –2715.PubMedCrossRefGoogle Scholar
  104. Wienand, U., P. Langridge, and G. Feix (1981) Isolation and characterization of a genomic sequence of maize coding for a zein gene. Mol. Gen. Genet. 182: 440 –444.CrossRefGoogle Scholar
  105. Wilson, D.R. and B.A. Larkins (1984) Zein gene organization in maize and related grasses. J. Mol. Evol. 20: 330 –340.PubMedCrossRefGoogle Scholar
  106. Wolf, M.J., U. Khoo, and H.L. Seckinger (1969) Distribution and subcellular structure of endosperm protein in varieties of ordinary and high-lysine maize. Cereal Chem. 46: 253 –263.Google Scholar
  107. Woo, Y.M., D.W. Hu, B.A. Larkins, and R. Jung (2001) Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13: 2297 –2317.PubMedCrossRefGoogle Scholar
  108. Zhang, F. and R.S. Boston (1992) Increases in binding protein (BiP) accompany changes in protein body morphology in three high-lysine mutants of maize. Protoplasma 171: 142 –152.CrossRefGoogle Scholar
  109. Zimmerberg, J. and M.M. Kozlov (2006) How proteins produce cellular membrane curvature. Nat.Rev. Mol. Cell Biol. 7: 9 –19.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  • Rebecca S. Boston
  • Brian A. Larkins

There are no affiliations available

Personalised recommendations