Abstract
Genomic clones encoding the plastidic fructose- 1,6-bisphosphate aldolase ofChlamydomonas reinhardtii were isolated and sequenced. The gene contains three introns which are located within the coding sequence for the mature protein. No introns are located within or near the sequence encoding the transit-peptide, in contrast to the genes for plastidic aldolases of higher plants. Neither the number nor the positions of the three introns of theC. reinhardtii aldolase gene are conserved in the plastidic or cytosolic aldolase genes of higher plants and animals. The 5′ border sequences of introns in the aldolase gene ofC. reinhardtii exhibit the conserved plant consensus sequence. The 3′ acceptor splice sites for introns 1 and 3 show much less similarity to the eukaryotic consensus sequences than do those of intron 2. The plastidic aldolase gene has two tandemly repeated CAAT box motifs in the promoter region. Genomic Southern blots indicate that the gene is encoded by a single locus in theC. reinhardtii genome.
Similar content being viewed by others
References
Anderson LE, Advani VR (1970) Chloroplast and cytoplasmic enzymes. Three distinct isoenzymes associated with the reductive pentose phosphate cycle. Plant Physiol 45: 583–585
Ausubel FM, Brent R, Kingston RE, Moore DA, Smith JA, Seideman JG, Strube K (1987) Current protocols in molecular biology. John Wiley, New York
Birnboim HC, Doly J (1979) A rapid alkaline procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523
Brochamp HP, Kula MR (1990) Purification and characterization of a class I fructose 1,6-bisphosphate aldolase fromStaphylococcus carnosus. Appl Microbiol Biotechnol 34: 287–291
Cavalier-Smith T (1991) Intron phylogeny: a new hypothesis. Trends Genet 7:145–148
Chopra S, Dolferus R, Jacob M (1990) Cloning and sequencing of theArabidopsis aldolase gene. Plant Mol Biol 15:517–520
Dennis ES, Gerlach WL, Walter JC, Lavin M, Peacock WJ (1988) Anaerobically regulated aldolase of maize. A chimaeric gene? J Mol Biol 202:759–767
Doolittle RF (1994) Convergent evolution: the need to be explicit. Trends Biochem Sci 19:15–18
Doolitle WF, Stoltzfus A (1993) Genes-in-pieces revisited. Nature 361:403
Dorit RL, Schoenbach L, Gilbert W (1990) How big is the universe of exons. Science 250:1377–1381
Gamblin SJ, Cooper B, Müller JR, Davies GJ, Littlechild JA, Watson HG (1990) The crystal structure of human muscle aldolase at 3.0 Å resolution. FEBS Lett 262:282–286
Gilbert W, Marchionni M, McKnight G (1986) On the antiquity of introns. Cell 46:151–154
Go M (1991) Module organization in proteins and exon shuffling. In: Osawa S, Honjo T (eds) Evolution of life. Springer-Verlag, Tokyo, pp 109–122
Goldschmidt-Clermont M (1986) The two genes for the small subunit of RuBP carboxylase/oxygenase are closely linked inChlamydomonas reinhardtii. Plant Mol Biol 6:13–21
Goldschmidt-Clermont M, Rahire M (1986) Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphospate carboxylase/oxygenase inChlamydomonas reinhardtii. J Mol Biol 191:421–432
Götz F, Fischer S, Schleifer KH (1980) Purification and characterisation of an unusually heat-stable and acid/base-stable class I fructose- 1,6-bisphosphate aldolase fromStaphylococcus aureus. Eur J Biochem 108:295–301
Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351–359
Hidaka S, Kadowaki K, Tsutsumi K, Ishikawa K (1990) Fructose bisphosphate aldolase (EC 4.1.2.13) of rice. Nucleic Acids Res 18:3991
Joh K, Arai Y, Mukai T, Hori K (1986) Expression of three mRNA species from a single rat aldolase A gene, differing in their 5′ non-coding regions. J Mol Biol 190:401–410
Joshi CP (1987) An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucleic Acids Res 15:6643–6653
Katagiri F, Chua N-H (1992) Plant transcription factors: present knowledge and future challenges. Trends Genet 8:22–26
Kersanach R, Brinkmann H, Liaud M-F, Zhang D-X, Martin W, Cerff R (1994) Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature 367: 387–389
Krüger I, Schnarrenberger C (1983) Purification, subunit structure, and immunological comparison of fructose-bisphospate aldolases from spinach and corn leaves. Eur J Biochem 136:101–106
Kukita A, Mukai T, Miyata T, Hori K (1988) The structure of brain specific rat aldolase C mRNA and the evolution of aldolase isozyme genes. Eur J Biochem 171:471–478
Lebherz HG, Leadbetter MM, Bradshow RA (1984) Isolation and characterization of the cytosolic and chloroplast form of spinach leaf fructose diphosphate aldolase. J Biol Chem 259:1011–1017
Liaud ME, Zhang DX, Cerff R (1990) Differential loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus. Proc Natl Acad Sci USA 87:8918–8922
Maire P, Gauttrons S, Hakim V, Gregori C, Mennecier F, Kahn Å (1987) Characterization of three optional promoters in the 5′-region of the human aldolase Å gene. J Mol Biol 197:425–438
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: Å laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Marsh JJ, Lebherz HG (1992) Fructose-bisphosphate aldolases: an evolutionary history. Trends Biochem Sci 17:110–113
Martin W, Brinkmann H, Savonna C, Cerff R (1993) Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90:8692–8696
Motoki K, Kitajima Y, Hori K (1993) Isoenzyme-specific modules on human aldolase Å molecule. J Biol Chem 268:1677–1683
Mukai T, Yatsuki H, Arai Y, Joh K, Matsuhashi S, Hori K (1987) Human aldolase B gene. Characterization of the genomic aldolase B gene and analysis of sequence required for multiple polyadenylations. J Biochem 102:1043–1051
Palmer JD, Logsdon JM (1991) The recent origins of introns. Curr Opinion Genet Dev 1:470–477
Pelzer-Reith B, Penger Å, Schnarrenberger C: (1993) Plant aldolase cDNA and deduced amino acid sequence of the chloroplast and cytosol enzyme from spinach. Plant Mol Biol 21:331–340
Proudfoot N (1991) Poly(A) signals. Cell 64:671–674
Quigley F, Martin WF, Cerff R (1988) Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc Natl Acad Sci USA 85:2672–2676
Radzan K, Heinrickson RL, Zurcher-Neely H, Morris PW, Anderson LE (1992) Chloroplast and cytoplasmic enzymes: isolation and sequencing of cDNAs coding for two distinct pea chloroplast aldolases. Arch Biochem Biophys 208:721–727
Rochaix JD, Mayfield S, Goldschmidt-Clermont M, Erickson J (1988) Molecular biology ofChlamydomonas In: Shaw CH (ed) Plant molecular biology. IRL Press, Oxford, pp 253–275
Rottmann WH, Deselms KR, Niclas J, Camerato T, Holman PS, Green CJ, Tolan DR (1987) The complete amino acid sequence of human aldolase C isozyme derived from genomic clones. Biochemistry 69:137–145
Rutter WJ (1964) Evolution of aldolase. Fed Proc 23:1248–1257
Schnarrenberger C, Gross W, Pelzer-Reith B, Wiegand S (1992) The evolution of isoenzymes of sugar phosphate metabolism in algae. In: Stabenau H, Tolbert NE (eds) Phylogentic changes in peroxisomes of algae. Phylogeny of plant peroxisomes. University of Oldenburg, Oldenburg, pp 310–329
Schnarrenberger C, Pelzer-Reith B, Yatsuki H, Freund S, Jacobshagen S, Hori K (1994) Expression and sequence of the only detectable aldolase inChlamydomonas reinhardtii. Arch Biochem Biophys 313:173–178
Shih M-C, Heinrich P, Goodman HM (1988) Intron existence predated the divergence of eukaryotes and prokaryotes. Science 242:1164–1166
Sinibaldi R, Mettler I (1992) Intron splicing and intron mediated enhanced expression in monocots. Prog Nucleic Acid Res Mol Biol 42:229–257
Stoltzfus Å, Spencer DF, Zuker M, Logsdon JM, Doolitle WF (1994) Testing the exon theory of genes: the evidence from protein structure. Science 265:202–207
Surzycki S (1972) Synchronously grown cultures ofChlamydomonas reinhardtii. Methods Enzymol 23:833–841
Sygusch J, Beaudry D, Allaire M (1987) Molecular architecture of rabbit skeletal muscle aldolase at 2.7 Å resolution. Proc Natl Acad Sci USA 84:7846–7850
Tsutsumi K, Mukai T, Tsutsumi R, Hidaka S, Arai Y, Hori K, Ishikawa K (1985) Structure and genomic organization of the rat aldolase B gene. J Mol Biol 181:153–160
Tsutsumi K, Kagaya Y, Hidaka S, Suzuki J, Tokairin Y, Hirai T, Hu D-L, Ihikawa 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
Witke C, Götz F (1993) Cloning, sequencing, and characterization of the gene encoding the class I fructose- 1,6-bisphosphate aldolase ofStaphylococcus carnosus. J Bacteriol 175: 7495–7499
Author information
Authors and Affiliations
Additional information
Communicated by H. Saedler
Rights and permissions
About this article
Cite this article
Pelzer-Reith, B., Freund, S., Schnarrenberger, C. et al. The plastid aldolase gene fromChlamydomonas reinhardtii: Intron/exon organization, evolution, and promoter structure. Molec. Gen. Genet. 248, 481–486 (1995). https://doi.org/10.1007/BF02191648
Received:
Accepted:
Issue date:
DOI: https://doi.org/10.1007/BF02191648