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Molecular analysis of the plant gene encoding cytosolic phosphoglucose isomerase

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Abstract

The gene encoding a cytosolic isozyme of phosphoglucose isomerase (PGI, EC 5.3.1.9) was isolated from Clarkia lewisii, a wild flower native to California, and the structure and sequence of the entire coding region determined. PGI catalyzes an essential step in glycolysis and carbohydrate biosynthesis in plants. Spanning about 6 kb, the gene has 23 exons and 22 introns, the highest number yet reported in plants. The exons range in size from 43 to 156 nt and encode a protein of 569 amino acids. The protein is about 44–46% identical to the inferred protein sequences of pig, Escherichia coli and Saccharomyces cerevisiae. All of the introns are bordered with the consensus 5′-GT...AG-3′ dinucleotides. The longest intron includes a large stem-loop structure bounded by a perfect 9 nt direct repeat. We cloned the PGI gene from a genomic library prepared from a single plant of known PGI genotype. The locus and allele of the clone were identified by matching restriction fragments to fragments from genetically defined genomic DNAs by Southern hybridization.

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References

  1. Achari A, Marshall SE, Muirhead H, Palmieri RH, Noltmann EA: Glucose-6-phosphate isomerase. Phil Trans R Soc Lond [B] 293: 145–157 (1981).

    Google Scholar 

  2. Camirand A, St-Pierre B, Marineau C, Brisson N: Occurrence of a copia-like transposable element in one of the introns of the potato starch phosphorylase gene. Mol Gen Genet 224: 33–39 (1990).

    PubMed  Google Scholar 

  3. Campbell WH, Gowri G: Codon usage in higher plants, green algae and cyanobacteria. Plant Physiol 92: 1–11 (1990).

    Google Scholar 

  4. Chaput M, Claes V, Portetelle D, Cludts I, Cravador A, Burney A, Gras H, Tartar A: The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 332: 454–455 (1988).

    Article  PubMed  Google Scholar 

  5. Dennis ES, Gerlach WL, Walker JC, Lavin M, Peacock WJ: Anaerobically regulated aldolase gene of maize: a chimeric origin? J Mol Biol 202: 759–767 (1988).

    PubMed  Google Scholar 

  6. Faik P, Walker JI, Redmill AAM, Morgn MJ: Mouse glucose-6-phosphate isomerase and neuroleukin have identical 3′ sequences. Nature 332: 455–456 (1988).

    Article  PubMed  Google Scholar 

  7. Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Addendum. Anal Biochem 132: 266–267 (1983).

    Google Scholar 

  8. Fisher RL, Goldberg RL: Structure and flanking regions of soybean seed protein genes. Cell 29: 651–660 (1982).

    Article  PubMed  Google Scholar 

  9. Froman BE, Tait RC, Gottlieb LD: Isolation and characterization of the phosphoglucose isomerase gene from Escherichia coli. Mol Gen Genet 217: 126–131 (1989).

    Article  PubMed  Google Scholar 

  10. Gottlieb LD: Evidence for duplication and divergence of the structural gene for phosphoglucose isomerase in diploid species of Clarkia. Genetics 86: 289–307 (1977).

    Google Scholar 

  11. Gottlieb LD: Conservation and duplication of isozymes in plants. Science 216: 373–380 (1982).

    Google Scholar 

  12. Gottlieb LD, Higgins RC: Evidence from subunit molecular weight suggests hybridization was the source of the phosphoglucose isomerase gene duplication in Clarkia. Theor Appl Genet 68: 369–373 (1984).

    Article  Google Scholar 

  13. Gottlieb LD, Higgins RC: Phosphoglucose isomerase expression in species of Clarkia with and without a duplication of the coding gene. Genetics 107: 131–140 (1984).

    Google Scholar 

  14. Gottlieb LD, Weeden NF: Gene duplication and phylogeny in Clarkia. Evolution 33: 1024–1039 (1979).

    Google Scholar 

  15. Green JBA, Wright APH, Cheung WY, Lancashire WE, Hartley BS: The structure and regulation of phosphoglucose isomerase in Saccharomyces cerevisiae. Mol Gen Genet 215: 100–106 (1988).

    Article  Google Scholar 

  16. Gurney ME, Heinrich SP, Lee MR, Yin HS: Molecular cloning and expression of neuroleukin, a neurotrophic factor for spinal and sensory neurons. Science 234: 566–574 (1986).

    Google Scholar 

  17. Hall TC, Ma Y, Buchbinder BU, Pyne HW, Sun SM, Bliss FA: Messenger RNA from G1 protein of French bean seeds: cell-free translation and product characterization. Proc Natl Acad Sci USA 75: 3196–3200 (1978).

    Google Scholar 

  18. Henikoff S: Unidirectional digestion with exonuclease III created targeted breakpoints for DNA sequencing. Gene 28: 351–359 (1984).

    Article  PubMed  Google Scholar 

  19. Herbert M, Schnarrenberger C: Purification and subunit structure of glucosephosphate isomerase 2 from spinach leaves and immunochemical comparison with other isomerases. Arch Biochem Biophys 217: 452–459 (1982).

    PubMed  Google Scholar 

  20. Higgins RC, Gottlieb LD: Subunit hybridization and immunological studies of duplicated phosphoglucose isomerase isozymes. Biochem Genet 22: 957–979 (1984).

    PubMed  Google Scholar 

  21. Higgins DG, Sharp PM: CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73: 237–244 (1988).

    PubMed  Google Scholar 

  22. Holmes DS, Quigley M: A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem 114: 193–197 (1981).

    PubMed  Google Scholar 

  23. Jones TWA, Pichersky E, Gottlieb LD: Enzyme activity in EMS-induced null mutations of duplicated genes encoding phosphoglucose isomerases in Clarkia. Genetics 113: 101–114 (1986).

    Google Scholar 

  24. Kawasaki ES: Amplification of RNA. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A Guide to Methods and Applications, pp. 21–27. Academic Press, San Diego (1990).

    Google Scholar 

  25. Kruckeberg AL, Neuhaus HE, Feil R, Gottlieb LD, Stitt M: Decreased activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. I. Impact on mass-action ratios and fluxes to sucrose and starch, and estimation of flux control coefficients and elasticity coefficients. Biochem J 261: 457–467 (1989).

    PubMed  Google Scholar 

  26. Lewis H: The origin of diploid neospecies in Clarkia. Am Naturalist 107: 161–170 (1973).

    Article  Google Scholar 

  27. Lewis H, Lewis ME: The genus Clarkia. Univ Calif Publ Bot 20: 241–392 (1955).

    Google Scholar 

  28. Marchand M, Kooystra U, Wierenga RK, Lambeir AM, Beeumen JV, Opperdoes FR, Michels PAM: Glucose-phosphate isomerase from Trypanosoma brucei cloning and characterization of the gene and analysis of the enzyme. Eur J Biochem 184: 455–464 (1989).

    PubMed  Google Scholar 

  29. Marchionni M, Gilbert W: The triosephosphate isomerase gene from maize: introns antedate the plant-animal divergence. Cell 46: 133–141 (1986).

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  31. Narayan RKJ: Evolutionary significance of DNA variation in plant. Evol Trends Plants 2: 121–130 (1988).

    Google Scholar 

  32. Nevers P, Shepherd NS, Saedler H: Plant transposable elements. Adv Bot Res 12: 103–203 (1986).

    Google Scholar 

  33. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  34. Schnarrenberger C, Oeser A: Two isozymes of glucose-phosphate isomerase from spinach leaves and their intracellular compartmentation. Eur J Biochem 45: 77–82 (1974).

    PubMed  Google Scholar 

  35. Shih MC, Heinrich P, Goodman HM: Intron existence predated the divergence of eukaryotes and prokaryotes. Science 242: 1164–1166 (1988).

    PubMed  Google Scholar 

  36. Simcox PD, Dennis DT: Isoenzymes of the glycolytic and pentose phosphate pathways in proplastids from the developing endosperm of Ricinis communis. Plant Physiol 61: 871–877 (1978).

    Google Scholar 

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

    PubMed  Google Scholar 

  38. Sytsma KJ, Gottlieb LD: Chloroplast DNA evolution and phylogenetic relationships in Clarkia sect. Peripetasma (Onagraceae). Evolution 40: 1248–1261 (1986).

    Google Scholar 

  39. Tait RC, Froman BE, Laudencia-Chingcuanco DL, Gottlieb LD: Plant phosphoglucose isomerase genes lack introns and are expressed in Escherichia coli. Plant Mol Biol 11: 381–388 (1988).

    Google Scholar 

  40. Tanksley SD: Organization of the nuclear genome in tomato and related species. Am Naturalist 130 (suppl) S46-S61 (1987).

    Article  Google Scholar 

  41. Van der Straeten D, Rodrigues-Pousada RA, Goodman HM, Montagu MV: Plant enolase: gene structure, expression and evolution. Plant Cell 3: 719–735 (1991).

    Article  PubMed  Google Scholar 

  42. Walker JIH, Faik P, Morgen MJ: Characterization of the 5′ end of the gene for human glucose phosphate isomerase (GPI). Genomics 7: 638–643 (1990).

    PubMed  Google Scholar 

  43. Weeden NF, Gottlieb LD: Distinguishing allozymes and isozymes of phosphoglucose isomerases by electrophoretic comparison of pollen and somatic tissues. Biochem Genet 17: 287–296 (1979).

    PubMed  Google Scholar 

  44. Weeden NF, Gottlieb LD: The genetics of chloroplast isozymes. J Hered 71: 392–396 (1980).

    Google Scholar 

  45. Werr W, Frommer WB, Maas C, Starlinger P: Structure of the sucrose synthase gene on chromosome 9 of Zea mays L. EMBO J 4: 1373–1380 (1985).

    Google Scholar 

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Authors and Affiliations

  1. Department of Genetics, University of California, 95616, Davis, CA, USA

    B. R. Thomas, D. Laudencia-Chingcuanco & L. D. Gottlieb

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  1. B. R. Thomas
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  2. D. Laudencia-Chingcuanco
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  3. L. D. Gottlieb
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Thomas, B.R., Laudencia-Chingcuanco, D. & Gottlieb, L.D. Molecular analysis of the plant gene encoding cytosolic phosphoglucose isomerase. Plant Mol Biol 19, 745–757 (1992). https://doi.org/10.1007/BF00027071

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