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The maize cytosolic glyceraldehyde-3-phosphate dehydrogenase gene family: organ-specific expression and genetic analysis

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The distribution of the cytosolic glyceraldehyde-3-phosphate dehydrogenase gene family (Gpc) in the maize genome was investigated; a genetic variant of glyceraldehyde-3-phosphate dehydrogenase activity is also described. Restriction fragment length polymorphism analysis of an F2 population shows that the variant is not linked to the three known Gpc genes. However, this trait is linked to one of two genomic DNA fragments that hybridize to a fragment of the Gpc3 coding region, implying the existence of a fourth Gpc gene. Antibodies and cDNA clones were used to investigate the organ-specific expression of the Gpc genes. Results were compared with the expression of the alcohol dehydrogenase 1 (Adh1) gene. RNA and protein levels were examined in seedling roots and shoots, as well as the leaves, developing endosperm and embryo, and the aleurone. In general, it was found that Gpc3 expression behaves in parallel with Adh1 in these organs, and protein levels closely parallel that of RNA for each gene examined. Both Gpc3 and Adh1 show a marked increase in expression during endosperm development, reaching a maximum 15 days after pollination, but no expression is detected in the leaf. Gpc1 expression is similar to that of Gpc2, with an overall decrease in the level of RNA during endosperm development. This expression is discussed in terms of the common sequences found upstream of genes expressed in the developing maize seed.

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References

  • Brinkmann H, Martinez P, Quigley F, Martin W, Cerff R (1987) Endosymbiotic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Evol 26:320–328

    Google Scholar 

  • Cerff R (1982) Evolutionary divergence of chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from angiosperms. Fur J Biochem 126:513–515

    Google Scholar 

  • Cerff R, Kloppstech K (1982) Structural diversity and differential light control of mRNAs coding for angiosperm glyceraldehyde3-phosphate dehydrogenases. Proc Natl Acad Sci USA 79:7624–7628

    Google Scholar 

  • Chourey PS (1981) Genetic control of sucrose synthetase in maize endosperm. Mol Gen Genet 184:372–376

    Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: Version 2. Plant Mol Biol Rep 1:19–21

    Google Scholar 

  • Dennis ES, Gerlach WL, Pryor AJ, Bennetzen JL, Inglis A, Llewellyn D, Sachs MM, Ferl RJ, Peacock WJ (1984) Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res 12:3983–4000

    Google Scholar 

  • Dennis ES, Walker JC, Llewellyn DJ, Ellis JG, Singh K, Tokuhisa JG, Wolstenholme DR, Peacock WJ (1987) The response to anaerobic stress: Transcriptional regulation of genes for anaerobically induced proteins. In: von Wettstein D, Chua N-H (eds) Plant molecular biology. Plenum Publishing, NY, pp 407–417

    Google Scholar 

  • Devereux D, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Ehrenshaft M, Brambl R (1990) Respiration and mitochondrial biogenesis in germinating embryos of maize. Plant Physiol 93:295–304

    Google Scholar 

  • Feinberg AP, Vogelstein B (1984) Addendum: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137:266–267

    Google Scholar 

  • Ferl RJ (1990) ARF-B2: A protein complex that specifically binds to part of the anaerobic response element of maize Adh1. Plant Physiol 93:1094–1101

    Google Scholar 

  • Goodman MM, Bird RM (1977) The races of maize IV: tentative grouping of 219 Latin American races. Economic Bot 31:204–221

    Google Scholar 

  • Gross RH (1986) A DNA sequence analysis program for the Apple Macintosh. Nucleic Acids Res 14:591–596

    Google Scholar 

  • Hague DR, Sims TL (1980) Evidence for light-stimulated synthesis of phosphoenolpyruvate carboxylase in leaves of maize. Plant Physiol 66:505–509

    Google Scholar 

  • Harris JI, Waters M (1976) Glyceraldehyde-3-phosphate dehydrogenase. In: Boyer PD (ed) The enzymes, vol. 13. Academic Press, NY, pp 1–49

    Google Scholar 

  • Helentjaris T, Slocum M, Wright S, Schaefer A, Nienhuis J (1986) Construction of genetic linkage maps in maize and tomato using restriction fragment length polymorphisms. Theor Appl Genet 72:761–769

    Google Scholar 

  • Klein TM, Roth BA, Fromm ME (1989) Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc Natl Acad Sci USA 86:6681–6685

    Google Scholar 

  • Kodrzycki R, Boston RS, Larkins BA (1989) The opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell 1:105–114

    Google Scholar 

  • Kowles RV, Phillips RL (1988) Endosperm development in maize. Int Rev Cytol 112:97–101

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Larkins BA, Lending CR, Wallace JC, Galili G, Kawata EE, Geetha KB, Kriz AL, Martin DN, Broker CE (1989) Zein gene expression during endosperm development. In: Goldberg R (ed) The molecular basis of plant development. Alan R. Liss, NY, pp 109–120

    Google Scholar 

  • Leary JJ, Brigati DJ, Ward DC (1983) Rapid and sensitive colorimetric method for visualizing biotin labeled DNA probes hybridized to DNA or RNA immobilized on nitrocellulose: Bioblots. Proc Natl Acad USA 80:4045–4049

    Google Scholar 

  • Lemke-Keyes CA, Sachs MM (1989) Anaerobic tolerant null: A mutant that allows Adh1 nulls to survive anaerobic treatment. J Hered 80:316–319

    Google Scholar 

  • Martinez P, Martin W, Cerff R (1989) Structure, evolution and anaerobic regulation of a nuclear gene encoding cytosolic glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Biol 208:551–565

    Google Scholar 

  • McAlister L, Holland MJ (1985) Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15019–15027

    Google Scholar 

  • Okimoto R, Sachs MM, Porter EK, Freeling M (1980) Patterns of polypeptide synthesis in various maize organs under anaerobiosis. Planta 150:89–94

    Google Scholar 

  • Olive MR, Walker JC, Singh K, Dennis ES, Peacock WJ (1990) Functional properties of the anaerobic responsive element of the maize Adh1 gene. Plant Mol Biol 15:593–604

    Google Scholar 

  • Pan D, Strelow LL, Nelson OF (1990) Many maize inbreds lack an endosperm cytosolic phosphoglucomutase. Plant Physiol 93:1650–1653

    Google Scholar 

  • Paul A-L, Ferl RJ (1991) In vivo footprinting reveals unique cis-elements and different modes of hypoxic induction in maize Adh1 and Adh2. Plant Cell 3:159–168

    Google Scholar 

  • Peterson GL (1983) Determination of total protein. Methods Enzymol 91:95–119

    Google Scholar 

  • Rivoal J, Ricard B, Pradet A (1989) Glycolytic and fermentative enzyme induction during anaerobiosis in rice seedlings. Plant Physiol Biochem 27:43–52

    Google Scholar 

  • Roussell DL, Boston RS, Goldsbrough PB, Larkins BA (1988) Deletion of DNA sequences flanking an Mr 19,000 zein gene reduces its transcriptional activity in heterologous plant tissue. Mol Gen Genet 211:202–209

    Google Scholar 

  • Rubenstein I, Geraghty DE (1986) The genetic organization of zein. In: Pomeranz Y (ed) Advances in cereal science technology, vol VIII. American Association of Cereal Chemists, St. Paul, pp 297–315

    Google Scholar 

  • Russell DA, Sachs MM (1989) Differential expression and sequence analysis of the maize glyceraldehyde-3-phosphate dehydrogenase gene family. Plant Cell 1:793–803

    Google Scholar 

  • Russell DA, Wong DM-L, Sachs MM (1990) The anaerobic response of soybean. Plant Physiol 92:401–407

    Google Scholar 

  • Sachs MM, Freeling M, Okimoto R (1980) The anaerobic proteins of maize. Cell 20:761–767

    Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley. Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    Google Scholar 

  • Schwartz D, Endo T (1966) Alcohol dehydrogenase polymorphism in maize - simple and compound loci. Genetics 53:709–715

    Google Scholar 

  • Sheen J-Y, Bogorad L (1986) Expression of the ribulose-1,5-bisphosphate carboxylase large subunit gene and three small subunit genes in two cell types of maize leaves. EMBO J 5:3417–3422

    Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    Google Scholar 

  • Springer B, Werr W, Starlinger P, Bennett DC, Zokolica M, Freeling M (1986) The shrunken gene on chromosome 9 of Zea mays L is expressed in various plant tissues and encodes an anaerobic protein. Mol Gen Genet 205:461–468

    Google Scholar 

  • Sullivan TD, Christensen AH, Quail PH (1989) Isolation and characterization of a maize chlorophyll a/b binding protein gene that produces high levels of mRNA in the dark. Mol Gen Genet 215:431–440

    Google Scholar 

  • Takaiwa F, Oono K, lida Y, Sugiura M (1985) The complete sequence of a rice 25S RNA gene. Gene 37:255–259

    Google Scholar 

  • Towbin H, Staehelin T, Gordon G (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Vasil V, Clancy M, Ferl RJ, Vasil IK, Hannah LC (1989) Increased gene expression by the first intron of maize Shrunken-1 locus in grass species. Plant Physiol 91:1575–1579

    Google Scholar 

  • Walker JC, Howard EA, Dennis ES, Peacock WJ (1987) DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc Natl Acad Sci USA 84:6624–6628

    Google Scholar 

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Communicated by H. Saedler

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Russell, D.A., Sachs, M.M. The maize cytosolic glyceraldehyde-3-phosphate dehydrogenase gene family: organ-specific expression and genetic analysis. Molec. Gen. Genet. 229, 219–228 (1991). https://doi.org/10.1007/BF00272159

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