Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids

American Journal of Botany

Volumn 88, Issue 8, 2001, Pages 1390-1400

  Müller, Kirsten M ^a,d   Oliveira, Mariana C ^b   Sheath, Robert G ^a   Bhattacharya, Debashish ^c  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Bangiophycidae; Phylogeny; Plastid; Rhodophyta; Rubisco; Secondary symbiosis; Small subunit rRNA

Indexed keywords

EID: 0347039141     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.2307/3558445     Document Type: Article

References (86)

1. ABBOTT, I. A., AND G. J. HOLLENBERG. 1976. Marine algae of California. Stanford University Press, Stanford, California, USA.
2. ANDERSEN, R. A., S. L. MORTON, AND J. P. SEXTON. 1997. Provasoli-Guillard National Center for Culture of Marine Phytoplankton: 1997 List of strains. Journal of Phycology 33 (Supplement): 1-75.
3. BHATTACHARYA, D. 1998. The origin and evolution of protist group I introns. Protist 149: 113-122.
4. _, H. J. ELWOOD, L. J. GOFF, AND M. L. SOGIN. 1990. The phylogeny of Gracilaria lemaneiformis (Rhodophyta) based on the sequence analysis of its small subunit ribosomal RNA coding region. Journal of Phycology 26: 181-186.
5. _, T. HELMCHEN, C. BIBEAU, AND M. MELKONIAN. 1995. Comparisons of nuclear-encoded small-subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Molecular Biology and Evolution 12: 415-420.
6. _, AND L. MEDLIN. 1995. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. Journal of Phycology 31: 489-498.
7. _, AND _. 1998. Algal phylogeny and the origin of land plants. Plant Physiology 116: 9-15.
8. BIRD, C. J., AND J. L. MCLACHLAN. 1992. Seaweed flora of the Maritimes. 1. Rhodophyta - the red algae. Biopress, Bristol, UK.
9. BOILLOT, A. 1978. Les ponctuations intercellulaires du Rhodochaele parvual Thuret (Rhodophycées, Bagniophycidées). Revue Algologique, Nova Scotia 13: 251-258.
10. BOURRELLY, P. 1985. Les algues d'eau douce - initiation à la systematique, tome III: Les algues bleues et rouges, les eugléniens, peridiniens et cyrptomonadines. Nouvelle Edition, Boubée, Paris, France.
11. BROADWATER, S., AND,J. SCOTT. 1994. Ultrastructure of unicellular red algae. In J. Seckbach [ed.], Evolutionary pathway and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells, 215-230. Kluwer Academic, Dordrecht, The Netherlands.
12. _, _. S. P. A. GOSS, AND D. SAUNDERS. 1995. Ultrastructure of vegetative organization and cell division in Glaucosphaera vacuolata Korshikov (Porphyridiales, Rhodophyta). Phycologia 34: 351-361.
13. BROOM, J. E., W. A. JONES, D. F. HILL, G. A. KNIGHT, AND W. A. NELSON. 1999. Species recognition in New Zealand Porphyra using 18S rDNA sequencing. Journal of Applied Phycology 11: 421-428.
14. BURGER, G., D. SAINT-LOUIS, M. W. GRAY, AND B. F. LANG. 1999. Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea: cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11: 1675-1694.
15. CAVALIER-SMITH, T. 1982. The origins of plastids. Biological Journal of the Linnean Society 17: 289-306.
16. _. 2000. Membrane heredity and early chloroplast evolution. Trends in Plant Science 5: 174-182.
17. CHADEFAUD, M. 1969. La morphologie des vegetaux inférieur: données fondamentales et problèmes. Bulletin de la Societé Botanique France, Mémoires 115: 5-41.
18. CHAPMAN, D. J. 1974. Taxonomic status of Cyanidium caldarium, the Porphyridiales and Goniotrichales. Nova Hedwigia 25: 673-682.
19. DAUGBJERG, N., AND R. A. ANDERSEN. 1997. Phylogenetic analyses of the rbcl sequences from haptophytes and heterokont algae suggest their chloroplasts are unrelated. Molecular Biology and Evolution 14: 1242-1251.
20. DOUGLAS, S. E., C. A. MURPHY, D. E SPENCER, AND M. W. GRAY. 1991. Molecular evidence that cryptomonad algae are chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350: 148-151.
21. _, AND S. L. J. PENNY. 1999. The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. Journal of Molecular Evolution 48: 236-244.
22. DREW, K. 1956. Conferva ceramicola Lyngbye. Botanisk Tidsskrift 53: 67-74.
23. DURNFORD, D. G., J. A. DEANE, S. TAN, G. I. MCFADDEN, E. GANTT, AND B. R. GREEN. 1999. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. Journal of Molecular Evolution 48: 59-68.
24. ELWOOD, H. J., G. J. OLSEN, AND M. L. SOGIN. 1985. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution 2: 399-410.
25. FELSENSTEIN, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
26. FRESHWATER, W., S. FREDERICQ, B. S. BUTLER, M. H. HOMMERSAND, AND M. W. CHASE. 1994. A gene phylogeny of the red algae (Rhodophyta) based on plastid rbcL. Proceedings of the National Academy of Sciences USA 91: 7281-7285.
27. FRITSCH, F. E. 1945. The structure and reproduction of the algae, vol. 2. Cambridge University Press, Cambridge, UK.
28. GABRIELSON, P. W., AND J. D. GARBARY. 1985. Systematics of the red algae (Rhodophyta). Critical Reviews in Plant Sciences 3: 325-366.
29. _, _, AND R. F. SCAGEL. 1985. The nature of ancestral red algae: inferences from a cladistic analysis. Biosystems 18: 335-346.
30. _, _, M. R. SOMMERFELD, R. A. TOWNSEND, AND P. L. TYLER. 1990. Phylum Rhodophyta. In L. Margulis, J. O. Corliss, M. Melkonian, and D. J. Chapman [eds.], Handbook of protoctista. 102-118. Jones and Bartlett, Boston, Massachusetts, USA.
31. GANTT, E., J. SCOTT, AND C. LIPSCHULTZ. 1986. Phycobiliprotein composition and chloroplast structure in the freshwater red alga Compsopogon coeruleus (Rhodophyta). Journal of Phycology 22: 480-484.
32. GARBARY, D. J., AND P W. GABRIELSON. 1990. Taxonomy and evolution. In K. M. Cole and R. G. Sheath [eds.], Biology of the red algae, 477-498. Cambridge University Press, Cambridge, UK.
33. _, G. I. HANSEN, AND R. F. SCAGEL. 1980. A revised classification of the Bangiophyceae (Rhodophyta). Nova Hedwigia 33: 145-166.
34. GARGUILO, G. M., F. DE MASI, AND G. TRIPODI. 1987. Thallus morphology and spore formation in cultured Erythrocladia irregularis Rosenvinge (Rhodophyta, Bangiophycidae). Journal of Phycology 23: 351-359.
35. GILBERT. D. G. 1992. SeqApp, version. 1.9a169. Biology Department, Indiana University, Bloomington, Indiana, USA.
36. GRAY, M. W., ET AL. 1998. Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Research 26: 865-878.
37. GUTELL, R. R. 1996. Comparative sequence analysis and the structure of 16S and 23S rRNA. In R. A. Zimmermann and A. E. Dahlberg [eds.], Ribosomal RNA: structure, evolution, processing, and function in protein biosynthesis, 111-128. CRC Press, Boca Raton, Florida, USA.
38. HASEGAWA, M., H. KISHINO, AND T. YANO. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160-174.
39. HELMCHEN, T., D. BHATTACHARYA, AND M. MELKONIAN. 1995. Analyses of ribosomal RNA sequences from glaucocyscophyte cyanelles provide new insights into the evolutionary relationships of plastids. Journal of Molecular Evolution 41: 203-210.
40. KIES, L., AND B. P. KREMER. 1986. Typification of the Glaucocystophyta. Taxon 35: 128-135.
41. KISHINO, H., AND M. HASEGAWA. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. Journal of Molecular Evolution 29: 170-179.
42. KYLIN, H. 1956. Die Gattungen der Rhodophyceen. CWK, Gleerups Forlag, Lund, Sweden.
43. LEBLANC, C., C. BOYEN, AND S. LOISEAUX-DE GOER. 1995. Organization of the plastid genome from the rhodophyte Chondrus crispus (Gigartinales); sequence and phylogeny of the 16S rRNA gene. European Journal of Phycology 30: 133-140.
44. LOCKHART, P. J., M. A. STEEL, AND D. PENNY. 1994. Recovering the correct tree under a more realistic model of evolution. Molecular Biology and Evolution 11: 605-612.
45. MADDISON, W. P., AND D. R. MADDISON. 1997. MacClade, version 3.07. Sinauer, Sunderland, Massachusetts, USA.
46. MAGNE, F. 1960. Le Rhodochaete parvula Thuret (Bangioidée) et sa reproduction sexuée. Cahiers Biologie Marin 1: 407-420.
47. MAGNE, F. 1989. Classification et phylogénie des Rhodophycées. Cryptogamie, Algologie 10: 101-115.
48. MCCRACKEN, D. A., M. J. NADAKAVUKAREN, AND J. R. CAIN. 1980. A biochemical and ultrastructural evaluation of the taxonomic position of Glaucosphaera vacuolata Korsch. New Phytologist 86: 39-44.
49. MCFADDEN, G. I. 1999. Plastids and protein targeting. Journal of Eukaryotic Mirobiology 46: 339-346.
50. MEDLIN, L. K., A. COOPER, C. HILL, S. WRIEDEN, AND U. WELLBROOK. 1995. Phylogenetic position of the Chromista plastids based on small subunit rRNA coding regions. Current Genetics 28: 560-565.
51. _, H. J. ESLWOOD, S. STICKEL, AND M. L. SOGIN. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491-499.
52. _, W. H. C. F. KOOISTRA, D. POTTER, G. W. SAUNDERS, AND R. A. ANDERSEN. 1997. Phylogenetic relationships of the "golden" algae (haptophytes, heterokont chromophytes) and their plastids. In D. Bhattacharya [ed.], Origins of algae and their plastids, 187-220. Springer-Verlag, Wien, Austria.
53. MOREIRA, D., H. LE GUYADER, AND H. PHILIPPE. 2000. The origin of red algae and the evolution of chloroplasts. Nature 405: 69-72.
54. MÜLLER, K. M., R. G. SHEATH, M. L. VIS, J. CREASE, AND K. M. COLE. 1998. Biogeography and systematics of Bangia (Bangiales, Rhodophyta) based on the rubisco spacer, rbcL gene and 18S rRNA gene sequences and morphometric analyses. 1. North America. Journal of Phycology 37: 195-207.
55. OLIVEIRA, M. C., AND D. BHATTACHARYA. 2000. Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. American Journal of Botany 87: 482-492.
56. _, J. KURNIAWAN, C. J. BIRD, E. L. RICE, C. A. MURPHY, R. K. SINGH, R. R. GUTELL, AND M. A. RAGAN. 1995. A preliminary investigation of the order Bangiales (Bangiophycidae, Rhodophyta) based on sequences of nuclear small-subunit ribosomal RNA genes. Phycological Research 43: 71-79.
57. _, AND M. A. RAGAN. 1994. Variant forms of a group I intron in nuclear small-subunit rRNA genes of the marine red alga Porphyra spiralis var. amplifolia. Molecular Biology and Evolution 11: 195-207.
58. OLSEN, G. J., H. MATSUDA, R. HAGSTROM, AND R. OVERBEEK. 1994. FastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Computational Applications in Biosciences 10: 41-48.
59. PALMER, J. D., AND C. F. DELWICHE. 1996. Second-hand chloroplasts and the case of the disappearing nucleus. Proceedings of the National Academy of Sciences, USA 93: 7432-7435.
60. PUESHEL, C. M., AND F. MAGNE. 1987. Pit plugs and other ultrastructural features of systematic value in Rhodochaete parvula (Rhodophyta, Rhodochaetales). Cryptogamic Algology 8: 201-209.
61. RAGAN, M. A., C. J. BIRD, E. L. RICE, R. R. GUTELL, C. A. MURPHY, AND R. K. SINGH. 1994. A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proceedings of the National Academy of Sciences, USA 91: 7276-7280.
62. RINTOUL, T. L., M. L. VIS, AND R. G. SHEATH. 1999. Systematics of the Compsopogonales (Rhodophyta) with emphasis on the freshwater families in North America. Phycologia 38: 517-527.
63. SAITOU, N., AND M. NEI. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
64. SAUNDERS, G. W. 1993. Gel purification of red algal genomic DNA: an inexpensive and rapid method for the isolation of polymcrase chain reaction-friendly DNA. Journal of Phycology 29: 251-254.
65. _, AND G. T. KRAFT. 1994. Small-subunit rRNA gene sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). 1. Evidence for the Plocamiales ord. nov. Canadian Journal of Botany 72: 1250-1263.
66. _, AND _. 1997. A molecular perspective on red algal evolution: focus on the Florideophycidae. Plant Systematics and Evolution [Supplement] 11: 115-138.
67. SCHLÖSSER, U. G. 1994. SAG-Sammlung von Algenkulturen at the University of Göttingen. Botanica Acta 107: 111-186.
68. SCOTT, J. L., S. T. BROADWATER, B. D. SAUNDERS, J. P. THOMAS, AND P. W. GABRIELSON. 1992. Ultrastructure of vegetative organization and cell division in the unicellular red alga Dixoniella grisea gen. nov. (Rhodophyta) and a consideration of the genus Rhodella. Journal of Phycology 28: 649-690.
69. SECKBACH, J., AND F. D. OTT. 1994. Systematic position and phylogenetic status of Cyanidium caldarium Geitler 1933. In J. Seckbach [ed.], Evolutionary pathway and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells, 133-143. Kluwer Academic, Dordrecht, The Netherlands.
70. SHEATH, R. G. 1984. The biology of the freshwater red algae. Progress in Phycological Research 3: 89-157.
71. SILVA, P. C., P. W. BASSON, AND R. L. MOE. 1996. Catalogue of the benthic marine algae of the Indian Ocean. University of California Press, Berkeley, California, USA.
72. SKUJA, H. 1939. Versuch einer systematischen Einteilung der Bangioideen oder Protoflorideen. Acta Horti Botaniska Universitets Latavia 11: 23-40.
73. STARR, R. C., AND J. A. ZEIKUS. 1993. The Culture Collection of Algae at The University of Texas at Austin: 1993 list of cultures. Journal of Phycology 29 (Supplement): 1-106.
74. STEGENGA, H., J. J. BOLTON, AND R. J. ANDERSON. 1997. Seaweeds of the South African west coast. Contributions from the Bolus Herbarium Number 18, University of Cape Town, Cape Town, South Africa.
75. STILLER, J. W., AND B. D. HALL. 1997. The origin of the red algae: implications for plastid evolution. Proceedings of the National Academy of Sciences, USA 94: 4520-4525.
76. STRIMMER, K., AND A. VAN HAESELER. 1996. Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13: 964-969.
77. SWOFFORD, D. L. 2000. PAUP*: phylogenetic analysis using parsimony, version 4.0b4a. Smithsonian Institution, Washington, D.C., USA.
78. TAYLOR, W. R. 1960. Marine algae of the eastern tropical and subtropical coasts of the Americas. University of Michigan Press, Ann Arbor, Michigan, USA.
79. TOMAS, X., P. LOPEZ, R. MARGALEF-MIR, AND F. A. COMIN. 1980. Distribution and ecology of Compsopogon occidentales sp. nov. (Rhodophyta). Lilloa 35: 35-37.
80. VAN DEN HOEK, C., D. G. MANN, AND H. M. JAHNS. 1995. Algae: an introduction to phycology. Cambridge University Press, Cambridge, UK.
81. VAN DE PEER, Y., J. JANSEN, P. DE RIJK, AND R. DE WACHTER. 1997. Database on the structure of small ribosomal subunit RNA. Nucleic Acids Research 25: 111-116.
82. _, S. A. RENSING, U.-G. MAIER, AND R. DE WACHTER. 1996. Substitution rate calibration of small subunit rRNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proceedings of the National Academy of Sciences, USA 93: 7732-7736.
83. VIS, M. L., AND R. G. SHEATH. 1997. Biogeography of Batrachospermum gelatinosum (Batrachospermales, Rhodophyta) in North America based on molecular and morphological data. Journal of Phycology 33: 520-526.
84. WHITE, T. J., T. BRUNS, S. LEE, AND J. TAYLOR. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: a guide to methods and applications, 315-322. Academic Press, San Diego, California, USA.
85. WOMERSLEY, H. B. S. 1994. The marine benthic flora of southern Australia. Rhodophyta - part IIIA. Australian Biological Resources Study, Canberra, ACT, Australia.
86. ZUCCARELLO, G., J. WEST, A. BITANS, AND G. KRAFT. 2000. Molecular phylogeny of Rhodochaete parvula (Bangiophycidae, Rhodophyta). Phycologia 39: 75-81.