Molecular cloning and phylogenetic analysis of fructose-bisphosphate aldolase (cytoplasmic isozyme) in wheat, barley and rye

Abstract

Fructose-bisphosphate aldolase (FBA, EC 4.1.2.13) catalyzes an aldol cleavage of fructose-1, 6-bisphosphate to dihydroxyacetone-phosphate and glyceraldehyde 3-phosphate and a reversible aldol condensation. Three candidate genes with 1077bp coding for fructose-bisphosphate aldolase were cloned and sequenced in wheat, barley and rye. These genes could encode 358 amino acid residues. Sequence analysis indicated that wheat, barley and rye FBA genes were conserved with high identity (94.13%), while maize sequence had a 9bp deletion near the 3’ terminal. According to the alignment of 75 amino acid sequences, conserved domains of the FBAs were detected. These conserved domains might be the important functional sites of the FBAs. The cytoplasmic FBAs of wheat, barley and rye were clustered together, and the cluster was close to maize and rice FBAs. Nine peptides of the FBAs and the last amino acid Tyr (necessary for preference for fructose 1,6-bisphosphate over fructose 1-phosphate) were most conserved in plants, animals and algae. Current findings suggested that the FBAs could be divided into three main subgroups: plant cytoplasmic FBA, plant chloroplastic FBA and animal FBA. These results also indicated that the active and binding sites of FBAs had rare variations during the long-term evolution.

References

  1. Alexandrov, N.N., Brover, V.V., Freidin, S., Troukhan, M.E., Tatarinova, T.V., Zhang, H., Swaller, T.J., Lu, Y.P., Bouck, J., Flavell, R.B., Feldmann, K.A. 2009. Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol. Biol. 69:179–194.

    CAS  Article  Google Scholar 

  2. Choi, K.H., Shi, J., Hopkins, C.E., Tolan, D.R., Allen, K.N. 2001. Snapshots of catalysis: The structure of fructose-1,6-(bis) phosphate aldolase covalently bound to the substrate dihydroxyacetone phosphate. Biochemistry 40:13868–13875.

    CAS  Article  Google Scholar 

  3. Dennis, E.S., Gerlach, W.L., Walker, J.C., Lavin, M., Peacock, W.J. 1988. Anaerobically regulated aldolase gene of maize. A chimaeric origin? J. Mol. Biol. 202:759–767.

    CAS  Article  Google Scholar 

  4. Gamblin, S.J., Cooper, B., Millar, J.R., Davies, G.J., Littlechild, J.A., Watson, H.C. 1990. The crystal structure of human muscle aldolase at 3.0Å resolution. FEBS Lett. 262:282–286.

    CAS  Article  Google Scholar 

  5. Gross, W., Lenze, D., Nowitzki, U., Weiske, J., Schnarrenberger, C. 1999. Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. Gene 230:7–14.

    CAS  Article  Google Scholar 

  6. Hidaka, S., Kadowaki, K., Tsutsumi, K., Ishikawa, K. 1990. Nucleotide sequence of the rice cytoplasmic aldolase cDNA. Nucleic Acids. Res. 18:3991.

    CAS  Article  Google Scholar 

  7. Kelley, P.M., Tolan, D.R. 1986. The complete amino acid sequence for the anaerobically induced aldolase from maize derived from cDNA clones. Plant Physiol. 82:1076–1080.

    CAS  Article  Google Scholar 

  8. Kumar, S., Tamura, K., Nei, M. 2004. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 5:150–163.

    CAS  Article  Google Scholar 

  9. Lebherz, H.G., Leadbetter, M.M., Bradshaw, R.A. 1984. Isolation and characterization of the cytosolic and chloroplasts forms of spinach leaf fructose diphosphate aldolase. J. Biol. Chem. 259:1011–1017.

    CAS  PubMed  Google Scholar 

  10. Lorentzen, E., Siebers, B., Hensel, R., Pohl, E., 2004. Structure, function and evolution of the archaeal class I fructose-1,6-bisphosphate aldolase. Biochem. Soc. Trans. 32:259–263.

    CAS  Article  Google Scholar 

  11. Lorentzen, E., Pohl, E., Zwart, P., Stark, A., Russell, R.B., Knura, T., Hensel, R., Siebers, B. 2003. Crystal structure of an archaeal Class I aldolase and the evolution of (βα)8 barrel proteins. J. Biol. Chem. 278:47253–47260.

    CAS  Article  Google Scholar 

  12. Martin, W., Mustafa, A.Z., Henzel, K., Schnarrenberger, C. 1996. Higher-plant chloroplast and cytosolic fructose-l,6-bisphosphatase isoenzymes: Origins via duplication rather than prokaryote-eukaryote divergence. Plant Mol. Biol. 32:485–491.

    CAS  Article  Google Scholar 

  13. Patron, N.J., Rogers, M.B., Keeling, P.J. 2004. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryotic Cell 3:1169–1175.

    CAS  Article  Google Scholar 

  14. Plaxton, W.C. 1996. The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 47:185–214.

    CAS  Article  Google Scholar 

  15. Rogers, M.B., Patron, N.J., Keeling, P.J. 2007. Horizontal transfer of a eukaryotic plastid-targeted protein gene to cyanobacteria. BMC Biology 5:26.

    Article  Google Scholar 

  16. Rogers, M.B., Keeling, P.J. 2003. Lateral gene transfer and recompartmentalization of Calvin cycle enzymes in plants and algae. J. Mol. Evol. 58:367–375.

    Article  Google Scholar 

  17. Rutter, W.J. 1964. Evolution of aldolase. Fed. Proc. 23:1248–1257.

    CAS  PubMed  Google Scholar 

  18. Sanchez, L., Horner, D., Moore, D., Henze, K., Embley, T., Müller, M. 2002. Fructose-1,6-bisphosphate aldolases in amitochondriate protists constitute a single protein subfamily with eubacterial relationships. Gene 295:51–59.

    CAS  Article  Google Scholar 

  19. Schaeffer, G.W., Sharpe, F.T., Sicher, R.C. 1997. Fructose 1,6-bisphosphate aldolase activity in leaves of a rice mutant selected for enhanced lysine. Phytochemistry 46:1335–1338.

    CAS  Article  Google Scholar 

  20. Schnarrenberger, C., Pelzer-Reith, B., Yatsuki, H., Freund, S., Jacobshagen, S., Hori, K. 1994. Expression and sequence of the only detectable aldolase in Chlamydomonas reinhardtii. Arch. Biochern. Biophys. 313:173–178.

    CAS  Article  Google Scholar 

  21. Thompson, J.D., Higgins, D.G., Gibson, T.J. 1994. Clustal W: Improving the sensitivity of progressive multiple sequence aligment through sequence weighting matrix choice. Nucleic. Acids. Res. 22:4673–4680.

    CAS  Article  Google Scholar 

  22. Tsutsumi, K., Kagaya, Y., Hidaka, S., Suzuki, J., Tokairin, Y., Hirai, T., Hu, D., Ishikawa, K., Ejiri, S. 1994. Structural analysis of the chloroplastic and cytoplasmic aldolase-encoding genes implicated the occurrence of multiple loci in rice. Gene 141:215–220.

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Y. M. Wei.

Additional information

Communicated by A. Pécsváradi

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Cite this article

Wang, J.R., Yan, Z.H., Zheng, Y.L. et al. Molecular cloning and phylogenetic analysis of fructose-bisphosphate aldolase (cytoplasmic isozyme) in wheat, barley and rye. CEREAL RESEARCH COMMUNICATIONS 38, 489–496 (2010). https://doi.org/10.1556/CRC.38.2010.4.5

Download citation

Keywords

  • fructose-bisphosphate aldolase
  • cereal
  • molecular characterization
  • phylogenetic analysis