Inclusion of chloroplast genes that have undergone expansion misleads phylogenetic reconstruction in the Chlorophyta

American Journal of Botany

Volumn 100, Issue 11, 2013, Pages 2194-2209

  Novis, Phil M ^a   Smissen, Rob ^a   Buckley, Thomas R ^b,c   Gopalakrishnan, Kishore ^d   Visnovsky, Gabriel ^d  

^a LANDCARE RESEARCH   (New Zealand)

^b LANDCARE RESEARCH   (New Zealand)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

Chlorophyta; Chloroplast genes; Genome evolution; Green algae; RpoB; Topological incongruence

Indexed keywords

CHLOROPLAST; DATA SET; GENE EXPRESSION; GREEN ALGA; PHYLOGENETICS; PROTEIN; SAMPLING;

ALGAL PROTEIN; CHLOROPLAST PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHLOROPLAST GENE; CLASSIFICATION; GENETICS; GENOME EVOLUTION; GREEN ALGA; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; POLYMERASE CHAIN REACTION; RPOB; SEQUENCE ALIGNMENT; TOPOLOGICAL INCONGRUENCE;

CHLOROPHYTA; CHLOROPLAST GENES; GENOME EVOLUTION; GREEN ALGAE; RPOB; TOPOLOGICAL INCONGRUENCE;

ALGAL PROTEINS; AMINO ACID SEQUENCE; CHLOROPHYTA; CHLOROPLAST PROTEINS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

EID: 84887364253     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200584     Document Type: Article

References (64)

1. ABASCAL, F., R. ZARDOYA, and D. POSADA. 2005. ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
2. BÉLANGER, A. S., J. S. BROUARD, P. CHARLEBOIS, C. OTIS, C. LEMIEUX, and M. TURMEL. 2006. Distinctive architecture of the chloroplast genome in the chlorophycean green alga Stigeoclonium helveticum. Molecular Genetics and Genomics 276: 464-477.
3. BROUARD, J.-S., C. OTIS, C. LEMIEUX, and M. TURMEL. 2008. Chloroplast DNA sequence of the green alga Oedogonium cardiacum (Chlorophyceae): Unique genome architecture, derived characters shared with the Chaetophorales and novel genes acquired through horizontal transfer. BMC Genomics 9: 290.
4. BROUARD, J.-S., C. OTIS, C. LEMIEUX, and M. TURMEL. 2010. The exceptionally large chloroplast genome of the green alga Floydiella terrestris illuminates the evolutionary history of the Chlorophyceae. Genome Biology and Evolution 2: 240-256.
5. BROUARD, J.-S., C.O TIS, C. LEMIEUX, and M. TURMEL. 2011. The chloroplast genome of the green alga Schizomeris leibleinii (Chlorophyceae) provides evidence for bidirectional DNA replication from a single origin in the Chaetophorales. Genome Biology and Evolution 3: 505-515.
6. COCQUYT, E., H. VERBRUGGEN, F. LELIAERT, and O. DE CLERCK. 2010. Evolution and cytological diversification of the green seaweeds (Ulvophyceae). Molecular Biology and Evolution 27: 2052-2061.
7. DE CAMBIAIRE, J. C., C. OTIS, C. LEMIEUX, and M. TURMEL. 2006. The complete chloroplast genome sequence of the chlorophycean green alga Scenedesmus obliquus reveals a compact gene organisation and a biased distribution of genes on the two DNA strands. BMC Evolutionary Biology 6: 37.
8. DE CAMBIAIRE, J. C., C. OTIS, M. TURMEL, and C. LEMIEUX. 2007. The chloroplast genome sequence of the green alga Leptosira terrestris: Multiple losses of the inverted repeat and extensive genome rearrangements within the Trebouxiophyceae. BMC Genomics 8: 213.
9. DE WEVER, A., F. LELIAERT, E. VERLEYEN, P. VANORMELINGEN, K. VAN DER GUCHT, D. A. HODGSON, K. SABBE, and W. VYVERMAN. 2009. Hidden levels of phylodiversity in Antarctic green algae: Further evidence for the existence of glacial refugia. Proceedings of the Royal Society, B, Biological Sciences 276: 3591-3599.
10. DERRIEN, B., W. MAJERAN, F. A. WOLLMAN, and O. VALLON. 2009. Multistep processing of an insertion sequence in an essential subunit of the chloroplast ClpP complex. Journal of Biological Chemistry 284: 15408-15415.
11. FINET, C., R. E. TIMME, C. F. DELWICHE, and F. MARLÉTAZ. 2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Current Biology 20: 2217-2222.
12. FRIEDL, T. 1995. Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: A phylogenetic analysis of 18S ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov.). Journal of Phycology 31: 632-639.
13. FRIEDL, T. 1996. Evolution of the polyphyletic genus Pleurastrum (Chlorophyta): Inferences from nuclear-encoded ribosomal DNA sequences and motile cell ultrastructure. Phycologia 35: 456-469.
14. FRIEDL, T., and C. ZELTNER. 1994. Assessing the relationships of some coccoid green lichen algae and the Microthamniales (Chlorophyta) with 18S ribosomal RNA gene sequence comparisons. Journal of Phycology 30: 500-506.
15. Fu and #x10D;íková, K, J. C. Rada, and L. A. Lewis. 2011. The tangled taxonomic history of Dictyococcus, Bracteacoccus, and Pseudomuriella (Chlorophyceae, Chlorophyta) and their distinction based on a phylogenetic perspective. Phycologia 50: 422-429.
16. GONNET, G. H., M. A. COHEN, and S. A. BENNER. 1992. Exhaustive matching of the entire protein sequence database. Science 256: 1443-1445.
17. GOULDING, S. E., R. G. OLMSTEAD, C. W. MORDEN, and K. H. WOLFE. 1996. Ebb and flow of the chloroplast inverted repeat. Molecular & General Genetics 252: 195-206.
18. GUINDON, S., and O. GASCUEL. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
19. HERRON, M. D., J. D.H ACKETT, F. O. AYLWARD, and R. E. MICHOD. 2009. Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences, USA 106: 3254-3258.
20. HUANG, C., S. WANG, L. CHEN, C. LEMIEUX, C. OTIS, M. TURMEL, and X. Q. LIU. 1994. The Chlamydomonas chloroplast clpP gene contains translated large insertion sequences and is essential for cell growth. Molecular & General Genetics 244: 151-159.
21. KRIENITZ, L., E. H. HEGEWALD, D. HEPPERLE, V. A. R. HUSS, T. ROHR, and M. WOLF. 2004. Phylogenetic relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae). Phycologia 43: 529-542.
22. LARKIN, M. A., G. BLACKSHIELDS, N. P. BROWN, R. CHENNA, P. A. MCGETTIGAN, H. MCWILLIAM, F. VALENTIN, ET AL. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
23. LEIGH, J. W., E. SUSKO, M. BAUMGARTNER, and A. J. ROGER. 2008. Testing congruence in phylogenomic analysis. Systematic Biology 57: 104-115.
24. LELIAERT, F., D. R. SMITH, H. MOREAU, M. HERRON, H. VERBRUGGEN, C. F. DELWICHE, and O. DE CLERCK. 2012. Phylogeny and molecular evolution of the green algae. Critical Reviews in Plant Sciences 31: 1-46.
25. LEMIEUX, C., C. OTIS, and M. TURMEL. 2007. A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biology 5: 2.
26. LEWIS, L. A. 2007. Chlorophyta on land. In J. Seckbach [ed.], Algae and cyanobacteria in extreme environments. Cellular origin, life in extreme habitats and astrobiology, vol. 11, 570-582. Springer, Dordrecht, Germany.
27. LEWIS, L. A., and R. M. MCCOURT. 2004. Green algae and the origin of land plants. American Journal of Botany 91: 1535-1556.
28. LIERE, K., A. WEIHE, and T. BÖRNER. 2011. The transcription machineries of plant mitochondria and chloroplasts: Composition, function, and regulation. Journal of Plant Physiology 168: 1345-1360.
29. LOCKHART, P. J., P. M. NOVIS, B. G. MILLIGAN, J. RIDEN, A. RAMBAUT, and T. LARKUM. 2006. Heterotachy and tree building: A case study with plastids and eubacteria. Molecular Biology and Evolution 23: 40-45.
30. LÜ, F., W. XÜ, C. TIAN, G. WANG, J. NIU, G. PAN, and S. HU. 2011. The Bryopsis hypnoides plastid genome: Multimeric forms and complete nucleotide sequence. PLoS ONE 6: e14663.
31. MAUL, J. E., J. W. LILLY, L. Y. CUI, C. W. DE PAMPHILIS, W. MILLER, E. H. HARRIS, and D. B.S TERN. 2002. The Chlamydomonas reinhardtti plastid chromosome: Islands of genes in a sea of repeats. Plant Cell 14: 2659-2679.
32. MARIN, B. 2012. Nested in the Chlorellales or independent class? Phylogeny and classification of the Pedinophyceae (Viridiplantae) revealed by molecular phylogenetic analyses of complete nuclear and plastid-encoded rRNA operons. Protist 163: 778-805.
33. MERCHANT, S. S., S. E. PROCHNIK, O. VALLON, E. H. HARRIS, S. J. KARPOWICZ, G. B. WITMAN, A. TERRY, ET AL. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
34. MONIZ, M. B. J., F. RINDI, P. M. NOVIS, P. A. BROADY, and M. D. GUIRY. 2012. Molecular phylogeny of Antarctic Prasiola (Prasiolales, Trebouxiophyceae) reveals extensive cryptic diversity. Journal of Phycology 48: 940-955.
35. NAYLOR, G. J. P., and W. M. BROWN. 1998. Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences. Systematic Biology 47: 61-76.
36. NOVIS, P. M. 2006. Taxonomy of Klebsormidium (Klebsormidiales, Charophyceae) in New Zealand streams, and the significance of low pH habitats. Phycologia 45: 293-301.
37. NOVIS, P. M., T. BEER, and J. VALLANCE. 2008. New records of microalgae from the New Zealand alpine zone, and their distribution and dispersal. New Zealand Journal of Botany 46: 347-366.
38. NOVIS, P. M., M. LORENZ, P. A. BROADY, and E. A. FLINT. 2010. Parallela Flint: Its phylogenetic position in the Chlorophyceae and the polyphyly of Radiofilum Schmidle. Phycologia 49: 373-383.
39. NOVIS, P. M., and G. VISNOVSKY. 2012. Novel alpine algae from New Zealand: Chlorophyta. Phytotaxa 39: 1-30.
40. PERLER, F. B. 2002. InBase, the intein database. Nucleic Acids Research 30: 383-384.
41. PHILIPPE, H., and M. J. TELFORD. 2006. Large-scale sequencing and the new animal phylogeny. Trends in Ecology & Evolution 21: 614-620.
42. POMBERT, J.-F., C. LEMIEUX, and M. TURMEL. 2006. The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinct quadripartite architecture in the chloroplast genome of early diverging ulvophytes. BMC Biology 4: 3.
43. POMBERT, J.-F., C. OTIS, C. LEMIEUX, and M. TURMEL. 2004. The complete mitochondrial DNA sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) highlights distinctive evolutionary trends in the Chlorophyta and suggests a sister-group relationship between the Ulvophyceae and Chlorophyceae. Molecular Biology and Evolution 21: 922-935.
44. POMBERT, J.-F., C. OTIS, C. LEMIEUX, and M. TURMEL. 2005. The chloroplast genome sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Molecular Biology and Evolution 22: 1903-1918.
45. PROCHNIK, S. E., J. UMEN, A. M. NEDELCU, A. HALLMANN, S. M. MILLER, I. NISHII, P. FERRIS, ET AL. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329: 223-226.
46. PRÖSCHOLD, T., and F. LELIAERT. 2007. Systematics of the green algae: Conflict of classic and modern approaches. In J. Brodie and J. Lewis [eds.], Unravelling the algae: The past, present, and future of algal systematics. Systematics Association Special Volume 75, 123-153. CRC Press, Boca Raton, Florida, USA.
47. RONQUIST, F., and J. P. HUELSENBECK. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
48. SMITH, D. R., F. BURKI, T. YAMADA, J. GRIMWOOD, I. V. GRIGORIEV, J. L. VAN ETTEN, and P. J. KEELING. 2011. The GC-rich mitochondrial and plastid genomes of the green alga Coccomyxa give insight into the evolution of organelle DNA nucleotide landscape. PLoS ONE 6: e23624.
49. SMITH, D. R., R. W. LEE, J. C.C USHMAN, J. K. MAGNUSON, D. TRAN, and J. E. W. POLLE. 2010. The Dunaliella salina organelle genomes: Large sequences, inflated with intronic and intergenic DNA. BMC Plant Biology 10: 83.
50. STAMATAKIS, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
51. STANCHEVA, R., R. G. SHEATH, and J. D. HALL. 2012. Systematics of the genus Zygnema (Zygnematophyceae, Charophyta) from Californian watersheds. Journal of Phycology 48: 409-422.
52. SWOFFORD, D. L. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods), ver. 4.0b10. Sinauer, Sunderland, Massachusetts, USA.
53. TIMME, R. E., T. R.B ACHVAROFF, and C. F. DELWICHE. 2012. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7: e29696.
54. TIMME, R. E., and C. F. DELWICHE. 2010. Uncovering the evolutionary origin of plant molecular processes: Comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biology 10: 96.
55. TURMEL, M., J.-S. BROUARD, C. GAGNON, C. OTIS, and C. LEMIEUX. 2008. Deep division in the Chlorophyceae (Chlorophyta) revealed by chloroplast phylogenomic analyses. Journal of Phycology 44: 739-750.
56. Turmel, M., M.-C. Gagnon, C. J. O'kelly, C. Otis, and C. Lemieux. 2009a. The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of prasinophytes and the origin of the secondary chloroplasts of euglenids. Molecular Biology and Evolution 26: 631-648.
57. TURMEL, M., and C. OTIS. 1994. The chloroplast gene cluster containing pspF, psbL, petG and rps3 is conserved in Chlamydomonas. Current Genetics 27: 54-61.
58. TURMEL, M., C. OTIS, and C. LEMIEUX. 1999. The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: Insights into the architecture of ancestral chloroplast genomes. Proceedings of the National Academy of Sciences, USA 96: 10248-10253.
59. TURMEL, M., C. OTIS, and C. LEMIEUX. 2006. The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Molecular Biology and Evolution 23: 1324-1338.
60. TURMEL, M., C. OTIS, and C. LEMIEUX. 2009b. The chloroplast genomes of the green algae Pedinomonas minor, Parachlorella kessleri, and Oocystis solitaria reveal a shared ancestry between the Pedinomonadales and Chlorellales. Molecular Biology and Evolution 26: 2317-2331.
61. WAKASUGI, T., T. NAGAI, M. KAPOOR, M. SUGITA, M. ITO, S. ITO, J. TSUDZUKI, et al. 1997. Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: The existence of genes possibly involved in chloroplast division. Proceedings of the National Academy of Sciences, USA 94: 5967-5972.
62. YAMAGUCHI, K., S. PRIETO, M. V. BELIGNI, P. A. HAYNESW, H. MCDONALD, J. R. YATES III, and S. P.M AYFIELD. 2002. Proteomic characterisation of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: Identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. The Plant Cell 14: 2957-2974.
63. ZHONG, B. J., O. DEUSCH, V. V. GOREMYKIN, D. PENNY, P. J. BIGGS, R. A. ATHERTON, S. V. NIKIFOROVA, and P. J. LOCKHART. 2011. Systematic error in seed plant phylogenomics. Genome Biology and Evolution 3: 1340-1348.
64. ZUCCARELLO, G. C., N. PRICE, H. VERBRUGGEN, F. LELIAERT. 2009. Analysis of a plastid multigene data set and the phylogenetic position of the marine macroalga Caulerpa filiformis (Chlorophyta). Journal of Phycology 45: 1206-1212.