Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1989 Aug 25;17(16):6569–6580. doi: 10.1093/nar/17.16.6569

Wheat phosphoglycerate kinase: evidence for recombination between the genes for the chloroplastic and cytosolic enzymes.

M Longstaff 1, C A Raines 1, E M McMorrow 1, J W Bradbeer 1, T A Dyer 1
PMCID: PMC318350  PMID: 2780287

Abstract

We have isolated and sequenced cDNA clones containing the entire coding region of both the chloroplast and cytosolic versions of phosphoglycerate kinase from wheat. Comparison of these sequences reveals a higher than expected level of similarity between the nucleic acids and encoded proteins. Analysis of this data in relation to that for phosphoglycerate kinase sequences of mammals, prokaryotes and yeasts suggests that the wheat genes have recombined. This has resulted in the chloroplast and cytosolic kinases being more similar to each other than would be expected if the chloroplast enzyme had evolved directly from that of a prokaryotic progenitor.

Full text

PDF
6574

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alefounder P. R., Perham R. N. Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose 1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli. Mol Microbiol. 1989 Jun;3(6):723–732. doi: 10.1111/j.1365-2958.1989.tb00221.x. [DOI] [PubMed] [Google Scholar]
  2. Anderson C. M., Zucker F. H., Steitz T. A. Space-filling models of kinase clefts and conformation changes. Science. 1979 Apr 27;204(4391):375–380. doi: 10.1126/science.220706. [DOI] [PubMed] [Google Scholar]
  3. Anderson L. E., Advani V. R. Chloroplast and cytoplasmic enzymes: three distinct isoenzymes associated with the reductive pentose phosphate cycle. Plant Physiol. 1970 May;45(5):583–585. doi: 10.1104/pp.45.5.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Antequera F., Bird A. P. Unmethylated CpG islands associated with genes in higher plant DNA. EMBO J. 1988 Aug;7(8):2295–2299. doi: 10.1002/j.1460-2075.1988.tb03072.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Banks R. D., Blake C. C., Evans P. R., Haser R., Rice D. W., Hardy G. W., Merrett M., Phillips A. W. Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature. 1979 Jun 28;279(5716):773–777. doi: 10.1038/279773a0. [DOI] [PubMed] [Google Scholar]
  6. Beltzer J. P., Chang L. F., Hinkkanen A. E., Kohlhaw G. B. Structure of yeast LEU4. The 5' flanking region contains features that predict two modes of control and two productive translation starts. J Biol Chem. 1986 Apr 15;261(11):5160–5167. [PubMed] [Google Scholar]
  7. Bird A. P. CpG-rich islands and the function of DNA methylation. Nature. 1986 May 15;321(6067):209–213. doi: 10.1038/321209a0. [DOI] [PubMed] [Google Scholar]
  8. Bowen D., Littlechild J. A., Fothergill J. E., Watson H. C., Hall L. Nucleotide sequence of the phosphoglycerate kinase gene from the extreme thermophile Thermus thermophilus. Comparison of the deduced amino acid sequence with that of the mesophilic yeast phosphoglycerate kinase. Biochem J. 1988 Sep 1;254(2):509–517. doi: 10.1042/bj2540509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brinkmann H., Martinez P., Quigley F., Martin W., Cerff R. Endosymbiotic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Evol. 1987;26(4):320–328. doi: 10.1007/BF02101150. [DOI] [PubMed] [Google Scholar]
  10. Clements J. M., Roberts C. F. Transcription and processing signals in the 3-phosphoglycerate kinase (PGK) gene from Aspergillus nidulans. Gene. 1986;44(1):97–105. doi: 10.1016/0378-1119(86)90047-8. [DOI] [PubMed] [Google Scholar]
  11. Conway T., Ingram L. O. Phosphoglycerate kinase gene from Zymomonas mobilis: cloning, sequencing, and localization within the gap operon. J Bacteriol. 1988 Apr;170(4):1926–1933. doi: 10.1128/jb.170.4.1926-1933.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Karlin-Neumann G. A., Tobin E. M. Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J. 1986 Jan;5(1):9–13. doi: 10.1002/j.1460-2075.1986.tb04170.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Keegstra K., Bauerle C. Targeting of proteins into chloroplasts. Bioessays. 1988 Jul;9(1):15–19. doi: 10.1002/bies.950090105. [DOI] [PubMed] [Google Scholar]
  14. Kuntz G. W., Eber S., Kessler W., Krietsch H., Krietsch W. K. Isolation of phosphoglycerate kinases by affinity chromatography. Eur J Biochem. 1978 Apr 17;85(2):493–501. doi: 10.1111/j.1432-1033.1978.tb12265.x. [DOI] [PubMed] [Google Scholar]
  15. Larsson-Raźnikiewicz M. Graphical analyses on binding of ligands to a two-sited system. Theoretical treatments exemplified on yeast phosphoglycerate kinase. Arch Biochem Biophys. 1973 Oct;158(2):754–762. doi: 10.1016/0003-9861(73)90570-5. [DOI] [PubMed] [Google Scholar]
  16. Liskay R. M., Letsou A., Stachelek J. L. Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells. Genetics. 1987 Jan;115(1):161–167. doi: 10.1093/genetics/115.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Marchionni M., Gilbert W. The triosephosphate isomerase gene from maize: introns antedate the plant-animal divergence. Cell. 1986 Jul 4;46(1):133–141. doi: 10.1016/0092-8674(86)90867-6. [DOI] [PubMed] [Google Scholar]
  18. Martin W., Cerff R. Prokaryotic features of a nucleus-encoded enzyme. cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). Eur J Biochem. 1986 Sep 1;159(2):323–331. doi: 10.1111/j.1432-1033.1986.tb09871.x. [DOI] [PubMed] [Google Scholar]
  19. Mas M. T., Chen C. Y., Hitzeman R. A., Riggs A. D. Active human-yeast chimeric phosphoglycerate kinases engineered by domain interchange. Science. 1986 Aug 15;233(4765):788–790. doi: 10.1126/science.3526552. [DOI] [PubMed] [Google Scholar]
  20. Michelson A. M., Markham A. F., Orkin S. H. Isolation and DNA sequence of a full-length cDNA clone for human X chromosome-encoded phosphoglycerate kinase. Proc Natl Acad Sci U S A. 1983 Jan;80(2):472–476. doi: 10.1073/pnas.80.2.472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mikus M. D., Petes T. D. Recombination between genes located on nonhomologous chromosomes in Saccharomyces cerevisiae. Genetics. 1982 Jul-Aug;101(3-4):369–404. doi: 10.1093/genetics/101.3-4.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mori N., Singer-Sam J., Riggs A. D. Evolutionary conservation of the substrate-binding cleft of phosphoglycerate kinases. FEBS Lett. 1986 Aug 18;204(2):313–317. doi: 10.1016/0014-5793(86)80835-3. [DOI] [PubMed] [Google Scholar]
  23. Natsoulis G., Hilger F., Fink G. R. The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine tRNA synthetases of S. cerevisiae. Cell. 1986 Jul 18;46(2):235–243. doi: 10.1016/0092-8674(86)90740-3. [DOI] [PubMed] [Google Scholar]
  24. Osinga K. A., Swinkels B. W., Gibson W. C., Borst P., Veeneman G. H., Van Boom J. H., Michels P. A., Opperdoes F. R. Topogenesis of microbody enzymes: a sequence comparison of the genes for the glycosomal (microbody) and cytosolic phosphoglycerate kinases of Trypanosoma brucei. EMBO J. 1985 Dec 30;4(13B):3811–3817. doi: 10.1002/j.1460-2075.1985.tb04152.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Raines C. A., Lloyd J. C., Longstaff M., Bradley D., Dyer T. Chloroplast fructose-1,6-bisphosphatase: the product of a mosaic gene. Nucleic Acids Res. 1988 Aug 25;16(16):7931–7942. doi: 10.1093/nar/16.16.7931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rosenkrantz M., Alam T., Kim K. S., Clark B. J., Srere P. A., Guarente L. P. Mitochondrial and nonmitochondrial citrate synthases in Saccharomyces cerevisiae are encoded by distinct homologous genes. Mol Cell Biol. 1986 Dec;6(12):4509–4515. doi: 10.1128/mcb.6.12.4509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
  28. Shih M. C., Lazar G., Goodman H. M. Evidence in favor of the symbiotic origin of chloroplasts: primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenases. Cell. 1986 Oct 10;47(1):73–80. doi: 10.1016/0092-8674(86)90367-3. [DOI] [PubMed] [Google Scholar]
  29. Stocking C. R., Larson S. A chloroplast cytoplasmic shuttle and the reduction of extraplastid NAD. Biochem Biophys Res Commun. 1969 Oct 8;37(2):278–282. doi: 10.1016/0006-291x(69)90731-1. [DOI] [PubMed] [Google Scholar]
  30. Watson H. C., Walker N. P., Shaw P. J., Bryant T. N., Wendell P. L., Fothergill L. A., Perkins R. E., Conroy S. C., Dobson M. J., Tuite M. F. Sequence and structure of yeast phosphoglycerate kinase. EMBO J. 1982;1(12):1635–1640. doi: 10.1002/j.1460-2075.1982.tb01366.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weeden N. F. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol. 1981;17(3):133–139. doi: 10.1007/BF01733906. [DOI] [PubMed] [Google Scholar]
  32. Wu M., Tzagoloff A. Mitochondrial and cytoplasmic fumarases in Saccharomyces cerevisiae are encoded by a single nuclear gene FUM1. J Biol Chem. 1987 Sep 5;262(25):12275–12282. [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES