Summary
An overview of recent molecular analyses regarding origins of plastids in algal lineages is presented. Since different phylogenetic analyses can yield contradictory views of algal plastid origins, we have examined the effect of two distance measurement methods and two distance matrix tree-building methods upon topologies for the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit nucleotide sequence data set. These results are contrasted to those from bootstrap parsimony analysis of nucleotide sequence data subsets. It is shown that the phylogenetic information contained within nucleotide sequences for the chloroplast-encoded gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase, integral to photosynthesis, indicates an independent origin for this plastid gene in different plant taxa. This finding is contrasted to contrary results derived from 16S rRNA sequences. Possible explanations for discrepancies observed for these two different molecules are put forth. Other molecular sequence data which address questions of early plant evolution and the eubacterial origins of algal organelles are discussed.
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Andersen K, Caton J (1987) Sequence analysis of the Alcaligenes eutrophus chromosomally encoded ribulose-1,5-bisphosphate carboxylase large and small subunit genes and their gene products. J Bateriol 169:4547–4558
Ariztia E, Anderson R, Sogin M (1991) A new phlogeny for chromophyte algae using 16S-like rRNA sequences from Mallomonas papillosa (Synurophyceae) and Tribonema aequale(Xanthophyceae). J Phycol 27:428–436
Assali N, Martin W, Sommerville C, Loiseaux-de Goër S (1991a) Evolution of the Rubisco operon from prokaryotes to algae: Structure and analysis of the rbcS gene of the brown alga Pylaiella littoralis. Plant Mol Biol 17:853–863
Assali N, Loiseaux-de Goër S (1992) Sequence and phylogeny of the psaB gene of the brown alga Pylaiella littoralis. J Phycol 28:209–213
Baldauf S, Palmer J (1990) Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature 344:262–265
Bartnicki-Garcia S (1987) The cell wall: A crucial structure in fungal evolution. In: Rayner A, Brasier CM, Moore D (eds) Evolutionary biology of the fungi. Cambridge University Press, Cambridge, pp 389–403
Beakes G (1989) Oomycete fungi: their phylogeny and relationship to chromophyte algae. In: Green J, Leadbeater BSC, Diver WL (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford, pp 325–342
Bhattacharya D, Elwood HJ, Goff L, 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
Boczar BA, Delaney TP, Cattolico RA (1989) The gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci USA 86:4996–4999
Brinkmann H, Martinez P, Quigley F, Martin W, Cerff R (1987) Endosymbiotic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Evol 26:24–33
Cattolico RA, Loiseaux-de Goër S (1989) Analysis of chloroplast evolution and phylogeny: A molecular approach. In: Green J, Leadbeater BSC, Diver WL (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford, pp 85–100
Cavalier-Smith T (1986) The kingdom chromista: origin and systematics. Prog Phycol Res 4:309–347
Cavalier-Smith T (1987a) The origin of eukaryote and archaebacterial cells. Ann NY Acad Sci 503:17–54
Cavalier-Smith T (1987b) The simultaneous symbiotic origin of mitochondria, chloroplasts and microbodies. Ann NY Acad Sci 503:55–71
Chan R, Keller M, Canaday S, Weil J, Imbault P (1990) Eight small subunits of Euglena ribulose-1,5-bisphosphate carboxylase/oxygenase are translated from a large mRNA as a polyprotein. EMBO J 9:333–338
Christen R, Ratto A, Baroin A, Perasso R, Grell K, Adouette A (1991) An analysis of the origins of the metazoans, using comparisons of partial sequences of the 28S RNA, reveals an early emergence of tripoblasts. EMBO J 10:499–503
Christensen T (1989) The Chromophyta, past and present. In: Green J et al. (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford
Christensen T (1989) The Chromophyta, past and present. In: Green J et al. (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford
Christopher DA, Cushman JC, Price CA, Hallick RB (1988) Organisation of ribosomal protein genes rpl23, rpl12, rps19, rpl22 and rps3 on the Euglena gracilis chloroplast genome. Curr Genet 14:275–286
Clegg M, Learn G, Golenberg E (1991) Molecular evolution of chloroplast DNA. In: Selander R, Clark A, Whittam TS (eds) Evolution at the molecular level. Sinauer, Sunderland, MA, pp 135–149
Curtis SE, Haselkorn R (1983) Isolation and sequence of the gene for the large subunit of ribulose-a,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 80:1835–1839
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
Dickerson R (1980) Evolution and gene transfer in purple photosynthetic bacteria. Nature 283:210–212
Douglas S, Dunford D, Morden C (1990) Nucleotide sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from Cryptomonas ϕ:Evidence supporting the polyphyletic origin of plastids. J Phycol 26:500–508
Douglas S, Murphy C, Spencer D, Gray M (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151
Douglas S, Turner S (1991) Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. J Mol Evol 33: 267–273
Dover GA (1987) DNA Turnover and the molecular clock. J Mol Evol 26:47–58
Dover GA (1989) Linkage disequilibrium and molecular drive in the rDNA multigene family. Genetics 122:249–252
Dron M, Rahire M, Rochaix JD (1982) Sequence of the chloroplast region of Chlamydomonas reinhardtii containing the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162:775–793
Elwood HJ, Olsen GJ, Sogin M (1985) The small subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytrocha nova and Stylonicha pustulata. Mol Biol Evol 2: 399–410
Eschbach S, Wolters J, Sitte P (1991) Primary and secondary structure of the nuclear small subunit ribosomal RNA of the cryptomonad Pyrenomonas salina as inferred from the gene sequence: Evolutionary implications. J Mol Evol 32:247–252
Falcone D, Tabita F (1991) Expression of endogenous and foreign ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) genes in a RuBisCO deletion mutant of Rhodobacter sphaeroides. J Bacteriol 173:2099–2108
Farmer MA, Roberts KR (1990) Organelle loss in the endosymbiont of Gymnodinium acidotum Dinophyceae. Protoplasma 153:178–185
Felsenstein J (1981) Evolutionary trees from DNA sequences: A maximum-likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1988) Phylogenies from molecular sequences: Inference and reliability. Annu Rev Genet 22:521–565
Fields SD, Rhodes RG (1991) Ingestion and retention of Chroomonas spp. (Cryptophyceae) by Gymnodinium acidotum (Dinophyceae). J Phycol 27:525–529
Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284
Förster H, Coffey M, Elwood H, Sogin M (1990) Sequence analysis of the small subunit ribosomal RNAs of three zoosporic fungi and implications for fungal evolution. Mycologia 82: 306–312
Fox G, Stackebrandt E, Hespell R, Gibson J, Maniloff J, Dyer T, Wolf R, Balch W, Tanner R, Magrum L, Zablen L, Blekemore R, Gupta R, Bonen L, Lewis B, Stahl D, Luehrsen K, Chen K, Woese C (1980) The phylogeny of prokaryotes. Science 209:457–463
Gibbs S (1978) The chloroplasts of Euglena may have evolved from symbiotic green algae. Can J Bot 56:2883–2889
Gibbs S (1981) The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann NY Acad Sci 361:193–207
Gibbs S (1990) The evolution of algal chloroplasts. In: Weissner W et al. (eds) Experimental phycology I. Springer, Berlin
Gibson JL, Falcone DL, Tabita FR (1991) Nucleotide sequence, transcriptional analysis and expression of genes encoded within the form I CO2 fixation operon of Rhodobacter sphaeroides. J Biol Chem 266:14646–14653
Gingrich JC, Hallick RB (1985) The Euglena gracilis chloroplast ribulose-1,5-bisphosphate carboxylase gene. J Biol Chem 260:16162–16168
Giovannoni S, Turner S, Olsen G, Barns S, Lane D, Pace N (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592
Gouy M, Li W-H (1989a) Molecular phylogeny of the kingdoms Animalia, Plantae, and Fungi. Mol Biol Evol 6:109–122
Gouy M, Li W-H (1989b) Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339:145–147
Gray M, Cedergren R, Abel Y, Sankoff D (1989) On the evolutionary origin of the plant mitochondrion and its genome. Proc Natl Acad Sci USA 86:2267–2271
Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin M (1987) Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc Natl Acad Sci USA 84:5823–5827
Hase T, Inoue K, Hagihara N, Matsubara H, Williams M, Rogers L (1983) Ferredoxin from Aphanothece haplophitica, a unicellular blue-green alga: close relationship to ferredoxins from filamentous blue-green algae and phylogenetic implications. J Biochem 94:1457–1464
Hendriks L, Goris A, Neefs J-M, van de Peer Y, Hennebert G, de Wachter R (1989) The nucleotide sequence of the small ribosomal subunit RNA of the yeast Candida albans and the evolutionary position of the fungi among the eukaryotes. System Appl Microbiol 12:223–229
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 scottii among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J Mol Evol 32:167–177
Higgins DH, Sharp PM (1988) CLUSTAL: A package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244
Hillis DM, Moritz C, Porter C, Baker J (1991) Evidence for biased gene conversion in ribosomal DNA. Science 251:308–310
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun C-R, Meng B-Y, Li Y-Q, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194
Hori H, Lim B-L, Osawa S (1985) Evolution of green plants as deduced from 5S rRNA sequences. Proc Natl Acad Sci USA 82:820–823
Hwang S-R, Tabita FR (1991) Cotranscription, deduced primary structure, and expression of the chloroplast-encoded rbcL and rbcS genes of the marine diatom Cylindrotheca sp. strain N1. J Biol Chem 266:6271–6279
Jeffrey SW, Vesk M (1976) Further evidence for a membrane-bound endosymbiont within the dinoflagellate Peridinium foliaceum. J Phycol 12:450–455
Jin L, Nei M (1990) Limitations of the evolutionary parsimony method of phylogenetic analysis. Mol Biol Evol 7:82–102
Johnson CH, Kruft K, Subramanian AR (1990) Identification of a plastid-specific ribosomal protein in the 30S subunit of chloroplast ribosomes and isolation of the cDNA clone encoding its cytoplasmic precursor. J Biol Chem 265:12790–12795
Kabnick K, Peattie D (1991) Giardia: A missing link between prokaryotes and eukaryotes. Am Scientist 79:34–43
Kemmerer EC, Lei M, Wu R (1991) Structure and molecular evolutionary analysis of a plant cytochrome c gene: Surprising implications for Arabidopsis thaliana. J Mol Evol 32:227–237
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kostrzewa M, Valentin K, Maid U, Radetzky R, Zetsche K (1990) Structure of the rubisco operon from the multicellular red alga Antithamnion spec. Curr Genet 18:465–460
Kowallik K (1989) Molecular aspects and phylogenetic implications of plastid genomes of certain chromophytes. In: Green J et al. (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford
Larsen J (1988) An ultrastructural study of Amphidinium poecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27:366–377
Leedale G (1967) Euglenoid flagellates. Prentice Hall, Englewood Cliffs, NJ
Li W-H, Wu C-I, Luo C-C (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174
Li W-H, Tanimura M (1987) The molecular clock runs more slowly in man than in apes and monkeys. Nature 326:93–96
Li W-H (1989) A statistical test of phylogenies estimated from sequence data. Mol Biol Evol 6:424–435
Liaud M-F, Zhang DX, Cerff R (1990) Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus. Proc Natl Acad Sci USA 87:8918–8922
Loiseaux-de Goër S, Markowicz Y, Dalmon J, Audren H (1988) Physical maps of the two circular plastid DNA molecules of the brown alga Pylaiella littoralis (L.) Kjellm. Curr Genet 14:155–162
Loomis W, Smith D (1990) Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison. Proc Natl Acad Sci USA 87:9093–9097
Ludwig W, Weizenegger D, Betzl D, Leidel E, Lenz T, Ludvigsen D, Möllenhoff D, Wenzig P, Schleifer KH (1990) Complete nucleotide sequences of seven eubacterial genes coding for the elongation factor Tu: functional, structural and phylogenetic evaluations. Arch Microbiol 153:241–247
Mache R (1990) Chloroplast ribosomal proteins and their genes. Plant Sci 72:1–12
Margulis L (1981) Symbiosis in cell evolution. Freeman, San Francisco
Markowicz Y, Loiseaux-de Goër S (1991) Plastid genomes of Rhodophyta and Chromophyta share a common origin which differs from that of Chlorophyta and have a composite origin as do those of Euglenophytes. Curr Genet 20:427–430
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
Martin W, Gierl A, Saedler H (1989) Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:46–48
Martin W, Lagrange T, Li Y-F, Bisanz-Seyer C, Mache R (1990) Hypothesis for the evolutionary origin of the chloroplast ribosomal protein L21 of spinach. Curr Genet 18:553–556
McIntosh L, Poulsen C, Bogorad L (1980) Chloroplast gene sequence for the large subunit of ribulose bisphosphate carboxylase from maize. Nature 288:556–560
Melkonian M (1991) Systematics and evolution of the algae. Prog Botany 52:271–307
Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604
Mereschkowsky C (1910) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol Centralbl 30:278–288
Mereschkowsky C (1910b) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol Centralbl 30:289–303
Mereschkowsky C (1910c) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol Centralbl 30:322–347
Mereschkowsky C (1910d) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol Centralbl 30:353–367
Michels P, Marchand M, Kohl L, Allert S, Vellieux FMD, Wierenga R, Opperdoes F (1991) The cytosolic and glycosomal isozymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship. Eur J Biochem 198:421–428
Miyata T, Yasunga T (1980) Molecular evolution of mRNA: A method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol 16:23–36
Morden CW, Golden SS (1989) psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385
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
Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169
Narang F, McIntosh L, Sommerville C (1984) Nucleotide sequence of the ribulose bisphosphate carboxylase gene from Rhodospirillium rubrum. Mol Gen Genet 193:220–224
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
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous substitutions. Mol Biol Evol 3:418–426
Nelson K, Whittam TS, Selander RK (1991) Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli. Proc Natl Acad Sci USA 88:6667–6671
Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organisation deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574
Olson JM, Pierson BK (1987) Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol 108:209–248
Palmer J, Jansen RK, Micheals HJ, Chase MW, Manhart JR (1988) Chloroplast DNA variation and plant phylogeny. Ann Missouri Bot Gard 75:1180–1206
Palmer J, Baldauf S, Calie P, de Pamphilis C (1989) Chloroplast gene instability and transfer to the nucleus. In: Clegg M, O'Brein S (eds) Molecular evolution. Alan R Liss, New York, pp 97–106
Penny D, Hendy M (1986) Estimating the reliability of evolutionary trees. Mol Biol Evol 3:403–417
Perasso R, Baroin A, Qu L-H, Bachellerie J-P, Adoutte A (1989) Origin of the algae. Nature 339:142–144
Peschek GA (1987) Respiratory electron transport. In: Fay P, van Baalen C (eds) The cyanobacteria. Elsevier, Amsterdam
Pühler G, Leffers H, Gropp F, Palm P, Klenk H-P, Lottspeich F, Garrett R, Zillig W (1989) Archaebacterial DNA dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci USA 86:4569–4573
Raven P (1970) A multiple origin for plastids and mitochondria. Science 169:641–646
Saitou N, Imanishi T (1989) Relative efficiencies of the Fitch-Margoliash, Maximum-Parsimony, Maximum-Likelihood, Minimum-Evolution and Neighbor-Joining methods of phylogenetic tree construction in obtaining the correct tree. Mol Biol Evol 6:514–525
Saitou N, Nei M (1987) The Neighbor-Joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schimper A (1883) Über die Entwicklung der Chlorophyllkörner und Farbkörper. Bot Ztg 41:105–114
Schwartz R, Dayhoff M (1981) Chloroplast origins: Inferences from protein and nucleic acid sequences. Ann NY Acad Sci 361:260–269
Shinozaki K, Sugiura M (1982) The nucleotide sequence of the tobacco chloroplast for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase gene. Gene 20:91–102
Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng B-Y, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organisation and expression. EMBO J 5: 2043–2049
Siemeister G, Hachtel W (1990) Structure and expression of a gene encoding the large subunit of ribulose-1,5-bisphosphate carboxylase (rbcL) in the colourless euglenoid flagellate Astasia longa. Plant Mol Biol 14:825–833
Sitte P (1990) Phylogenetische Aspekte der Zellevolution. Biol Rundsch 28:1–18
Smeekens S, Weisbeek P, Robinson C (1990) Protein transport into and within chloroplasts. Trends Biochem Sci 15:73–76
Sogin M, Gunderson J, Elwood H, Alonso R, Peattie D (1989) Phylogenetic meaning of the kingdom concept: an unusual Ribosomal RNA from Girdia lamblia. Science 243:75–77
Solomon JA, Walne PL, Dawson NS, Willey RL (1991) Structural characterisation of Eutreptia (Euglenophyta) II. The flagellar root system and putative vestigal cytopharnyx. Phycologia 30:402–414
Somerville CC, Jouannic S, Loiseaux-de Goër S (1992) Sequence, proposed secondary structure and phylogenetic analysis of the chloroplast 5S rRNA gene of the brown alga Pylaiella littoralis (L.) Kjellm. J Mol Evol 34:246–253
Sourdis J, Krimbas C (1987) Accuracy of phylogenetic trees estimated from DNA sequence data. Mol Biol Evol 4:159–166
Stackebrandt E, Murray RGE, Trüper HG (1988) Proteobacteria classis nov., a name for the phylogenetic taxon that includes the “purple bacteria and their relatives.” Int J Syst Bacteriol 38:321–325
Stein JL, Haygood M, Felbeck H (1990) Nucleotide sequence and expression of a deep-sea ribulose-1,5-bisphosphate carboxylase gene cloned from a chemoautotrophic bacterial endosymbiont. Proc Natl Acad Sci USA 87:8850–8854
Subramanian AP, Stahl D, Prombona A (1991) Ribosomal proteins, ribosomes, and translation in plastids. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids. Academic Press, New York, pp 191–215
Swofford DL (1989) PAUP: phylogenetic analysis using parsimony, Version 3. Illinois Natural History Survey, Champaign, IL
Swofford DL, Olsen GJ (1990) Phylogeny reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer, Sunderland, MA
Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285
Tomas R, Cox E (1973) Observations on the symbiosis of Peridinium balticum and its intracellular alga. J Phycol 9:273–289
Turner S, Burger-Wiersma T, Giovannini S, Murr L, Pace N (1989) The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337:380–382
Valentin K, Zetsche K (1989) The genes of both subunits of ribulose-1,5-bisphosphate carboxylase constitute an operon in the plastome of a red aga. Curr Genet 16:203–209
Valentin K, Zetsche K (1990a) Rubisco genes indicate a close phylogenetic relationship between the plastids of Chromophyta and Rhodophyta. Plant Mol Biol 15:575–584
Valentin K, Zetsche K (1990b) Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: Evidence for a polyphyletic origin of plastids. Mol Gen Genet 222:425–430
Valentin K, Zetsche K (1990c) Nucleotide sequence for the large subunit of Rubisco from Cyanophora paradoxa. Phylogenetic implications. Curr Genet 18:199–202
Van den Eynde H, De Baere R,De Roeck E, Van de Peer Y, Vandenberghe A, Willekens P, De Wachter R (1988) The 5S ribosomal RNA Sequences of a red algal chloroplast and a gymnosperm chloroplast. Implications for the evolution of plastids and cyanobacteria. J Mol Evol 27:126–132
van Gorkom HJ (1987) Evolution of photosynthesis. In: Amesz J (ed) Photosynthesis. Elsevier, Amsterdam, pp 343–350
Viale AM, Kobayashi H, Akazawa T (1989) Expressed genes for plant-type ribulose-1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium Chromatium vinosum, which possesses two complete sets of the genes. J Bacteriol 117: 2391–2400
Walne PL, Kivic PA (1990) Phylum Euglenida. In: Margulis et al. (eds) Handbook of Protoctista. Jones and Bartlett, Boston
Wanatabe MM, Tsutomu S, Inouye I, Suda S, Sawaguchi T, Chihara M (1987) A green dinoflagellate with chlorophylls a and b: Morphology, fine structure of the chloroplast and chlorophyll composition. J Phycol 23:382–389
Wanatabe MM, Suda S, Inouye I, Sawaguchi T, Chihara M (1990) Lepidodinium viridae gen. et sp. nov. (Gymnodiniales, Dinophyta): A green dinoflagellate with a chlorophyll a and 1b-containing endosymbiont. J Phycol 26:741–751
Whatley J (1981) Chloroplast evolution: Ancient and modern. Annals NY Acad Sci 361:154–164
Whatley J (1989) Chromophyte chloroplasts: a polyphyletic origin? In: Green J et al. (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford
Wilcox LW, Wedemayer GJ (1985) Dinoflagellates with blue-green chloroplasts derived from an endosymbiotic eukaryote. Science 227:192–194
Witt D, Stackebrandt E (1988) Disproving the hypothesis of a common ancestry for the Ochromonas danica chrysoplast and Heliobacterium chlorum. Arch Microbiol 150:244–248
Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271
Wolfe KH, Li W-H, Sharp P (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058
Wolter F, Fritz C, Willmitzer L, Schell J, Schreier P (1988) rbcS genes in Solanum tuberosum: conservation of transit peptide and exon shuffling during evolution. Proc Natl Acad Sci USA 85:846–850
Wolters J, Erdmann V, Stackebrandt E (1989) Current status of the molecular phylogeny of plastids. In: Nardon P, Gianinazzi-Pearson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology IV. INRA, Lyon, pp 545–552
Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447
Yoshinaga K, Ohta T, Suzuki Y, Sugiura M (1988) Chlorella chloroplast DNA sequence containing a gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase and a part of a possible gene for the β′ subunit of RNA polymerase. Plant Mol Biol 10:245–250
Zavarin GA, Stackebrandt E, Murray RGE (1991) A correlation of phylogenetic diversity in the Proteobacteria with influences of ecological forces. Can J Microbiol 37:1–6
Zhou D-X, Mache R (1989) Presence in the stroma of chloroplasts of a large pool of a ribosomal protein not structurally related to any E. coli ribosomal protein. Mol Gen Genet 219: 204–208
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Martin, W., Somerville, C.C. & Loiseaux-de Goër, S. Molecular phylogenies of plastid origins and algal evolution. J Mol Evol 35, 385–404 (1992). https://doi.org/10.1007/BF00171817
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DOI: https://doi.org/10.1007/BF00171817