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The evolutionary origin of red algae as deduced from the nuclear genes encoding cytosolic and chloroplast glyceraldehyde-3-phosphate dehydrogenases from Chondrus crispus

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Abstract

Algae are a heterogeneous group of photosynthetic eukaryotes traditionally separated into three major subdivisions: rhodophytes, chlorophytes, and chromophytes. The evolutionary origin of rhodophytes or red algae and their links to other photosynthetic and nonphotosynthetic eukaryotes have been a matter of much controversy and speculation. Here we present the first cDNAs of nuclear protein genes from red algae: Those encoding cytosolic and chloroplast glyceraldehyde-3-phosphate dehydrogenases (GAPDH) from Chondrus crispus. A phylogenetic analysis including GAPDH gene sequences from a number of eukaryotic taxa, cyanobacteria, and purple bacteria suggests that chloroplasts and rhodoplasts together form a monophyletic group of cyanobacterial descent and that rhodophytes separated from chlorophytes at about the same time as animals and fungi. The composite GAPDH tree further demonstrates that chloroplast and cytosolic GAPDH genes are closely related to their homologs in cyanobacteria and purple bacteria, respectively, the presumptive ancestors of chloroplasts and mitochondria, thereby firmly establishing the endosymbiotic origin of these nuclear genes and their fixation in eukaryotic cells before the rhodophyte/chlorophyte separation. The present data are in conflict with phylogenetic inferences based on plastid-encoded rbcL sequences supporting a polyphyletic origin of rhodoplasts and chloroplasts. Comparison of rbcL to GAPDH phylogenies suggests that rbcL trees may be misleading because they are composed of branches representing ancient duplicated (paralogous) genes.

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References

  • Alefounder PR, Perham RN (1989) 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 3:723–732

    Google Scholar 

  • Assali N-E, Mache R, Loiseaux-de Goër S (1990) Evidence for a composite phylogenetic origin of the plastid genome of the brown alga Pylaiella littoralis (L.) Kjellm. Plant Mol Biol 15:307–315

    Google Scholar 

  • Assali N-E, Martin WF, Sommerville CC, Loiseaux-De Goer S (1991) Evolution of the Rubisco operon from prokaryotes to algae: structure and analysis of the rbcS gene of the brown algae Pylaiella littoralis. Plant Mol Biol 17:853–863

    Google Scholar 

  • Bhattacharya D, Elwood HJ, Goff LJ, Sogin ML (1990) Phylogeny of Gracilaria lemaneiformis (rhodophyta) based on sequence analysis of its small subunit ribosomal RNA coding region. J Phycol 26:181–186

    Google Scholar 

  • Branlant G, Branlant C (1985) Nucleotide sequence of the Escherichia coli gap gene. Different evolutionary behavior of the NAD+-binding domain and the catalytic domain of D-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 150:61–66

    Google Scholar 

  • Brinkmann H, Cerff R, Salomon M, Soll (1989) Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. Plant Mol Biol 13: 81–94

    Google Scholar 

  • Brinkmann H, Martinez P, Martin W, Quigley F, 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 

  • Cavalier-Smith T (1991) The evolution of cells. In: Osawa S, Honjo T (eds) Evolution of life. Fossils, molecules, and culture, pp 271–304. Springer-Verlag, Tokyo

    Google Scholar 

  • Cerff R (1982) Separation and purification of NAD- and NADP-linked glyceraldehyde-3-phosphate dehydrogenases from higher plants. In: Edelmann M, Hallick RB, Chua NH (eds) Methods in chloroplast molecular biology. Elsevier Biomedical Press, Amsterdam, pp 683–694

    Google Scholar 

  • Conway T, Sewell GW, Ingram LO (1987) Glyceraldehyde-3-phosphate dehydrogenase gene from Zymomonas mobilis: cloning, sequencing, and identification of promotor region. J Bacteriol 169:5653–5662

    Google Scholar 

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

    Google Scholar 

  • Doolittle RF, Feng DF, Anderson KL, Alberro MR (1990) A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote. J Mol Evol 31:383–388

    Google Scholar 

  • Doolittle WF (1988) Bacterial evolution. Can J Microbiol 34:547–551

    Google Scholar 

  • Douglas SE, Durnford DG, Morden CW (1990) Nucleotide sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from Cryptomonas F: evidence supporting the polyphyletic origin of plastids. J Phycol 26:508–522

    Google Scholar 

  • Douglas SE, Turner S (1991) Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. J Mol Evol 33: 267–273

    Google Scholar 

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

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Fothergill-Gillmore LA, Michels PAM (1993) Evolution of glycolysis. Prog Biophys Mol Biol 59:105–235

    Google Scholar 

  • Gavel Y, von Heijne G (1990) A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett 261:455–458

    Google Scholar 

  • Gibson JL, Tabita FR (1988) J Bacteriol 170:2153–2158

    Google Scholar 

  • Gray MW (1989) The evolutionary origins of organelles. Trends Genet 5:294–299

    Google Scholar 

  • Hendriks L, De Baere R, Van de Peer Y, Neefs J, Goris A, De Wachter R (1991) The evolutionary position of the rhodophyte Porphyra umbilicalis and the basidiomycete Leucosporidium scodi among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J Mol Evol 32:167–177

    Google Scholar 

  • Hohn B (1979) In vitro packaging of I and cosmid DNA. Methods Enzymol 68:299

    Google Scholar 

  • Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472

    Google Scholar 

  • Le Gall Y, Brand JP, Kloareg B (1990) Protoplast production in Chondrus crispus gametophytes (Gigartinales, Rhodophyta). Plant Cell Rep 8:582–585

    Google Scholar 

  • Liaud M-F, Zhang DX, Cerff R (1990) Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate genes to the nucleus. Proc Natl Acad Sci USA 87:8918–8922

    Google Scholar 

  • Lipscomb DL (1989) Relationships among the eukaryotes. In: Fernholm B, Bremer K, Jörnvall H (eds) The hierarchy of life. Elsevier Science Publishers, Amsterdam, Netherlands, pp 161–178

    Google Scholar 

  • Margulis L, Schwartz KV (1982) Five kingdoms: an illustrated guide to the phyla of life on earth, 338. WH Freeman, New York

    Google Scholar 

  • Martin W, Brinkmann H, Savona C, Cerff R (1993b) Evidence for a chimaeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90:8692–8696

    Google Scholar 

  • Martin W, Cerff R (1986) Prokaryotic features of a nucleus-encoded enzyme. cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). Eur J Biochem 159:323–331

    Google Scholar 

  • Martin W, Gierl A, Saedler H (1989) Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:46–48

    Google Scholar 

  • Martin W, Lydiate D, Brinkmann H, Forkmann G, Saedler H, Cerff R (1993a) Molecular phylogenies in angiosperm evolution. Mol Biol Evol 10:140–162

    Google Scholar 

  • Martin W, Sommerville CC, Loiseaux-de Goër (1992) Molecular phylogenies of plastid origins and algal evolution. J Mol Evol 35:385–403

    Google Scholar 

  • Michels PAM, Marchand M, Kohl L, Allert S, Wierenga RK, Opperdoes FR (1991) The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship. Eur J Biochem 198:421–428

    Google Scholar 

  • Morden CW, Golden SS (1991) Sequence analysis and phylogenetic reconstruction of the genes encoding the large and small subunits of ribulose-1,5-bisphosphate carboxylase/oxygenase from the chlorophyll b-containing prokaryote Prochlorothrix hollandica. J Mol Evol 32:379–395

    Google Scholar 

  • Nei M (1991) Relative efficiencies of different tree making methods for molecular data. In: Miymoto MM, Cracraft JL (eds) Recent advances in phylogenetic studies of DNA sequences. Oxford University Press, Oxford, pp 90–128

    Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous substitutions. Mol Biol Evol 3:418–426

    Google Scholar 

  • Perasso R, Baroin A, Qu LH, Bachellerie JP, Adoutte A (1989) Origin of the algae. Nature 339:142–144

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Scagel RF, Bandoni RJ, Maze JR, Rouse GE, Schofield WB, Stein JR (1982) Nonvascular plants: an evolutionary survey. Wadsworth, Inc, Belmont, CA, p 570

    Google Scholar 

  • Shih MC, Lazar G, Goodman HM (1986) Evidence in favor of the symbiotic origin of chloroplasts: primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenases. Cell 47:73–80

    Google Scholar 

  • Shih MC, Lazar G, Goodman HM (1992) Cloning and chromosomal mapping of nuclear genes encoding chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana (Corrigendum). Gene 119:317–319

    Google Scholar 

  • Smith TL (1989) Disparate evolution of yeasts and filamentous fungi indicated by phylogenetic analysis of glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 86:7063–7066

    Google Scholar 

  • Smith TL, Leong SA (1990) Isolation and characterization of a Ustilago maydis glyceraldehyde-3-phosphate dehydrogenase-encoding gene. Gene 93:111–117

    Google Scholar 

  • Ueda K, Shibuya H (1993) Molecular phylogeny of rbcL and its bearing on the origin of plastids: bacteria or cyanophyta. In: Endocytobiology V. Tübingen University Press, pp. 369–376

  • Valentin K, Zetsche K (1990) Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222:425–430

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Google Scholar 

  • Young RA, Davis RW (1983) Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci USA 80:1194

    Google Scholar 

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Correspondence to: R. Cerff

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Liaud, MF., Valentin, C., Martin, W. et al. The evolutionary origin of red algae as deduced from the nuclear genes encoding cytosolic and chloroplast glyceraldehyde-3-phosphate dehydrogenases from Chondrus crispus . J Mol Evol 38, 319–327 (1994). https://doi.org/10.1007/BF00163149

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  • DOI: https://doi.org/10.1007/BF00163149

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