Dynamic Evolution of the Chloroplast Genome in the Green Algal Classes Pedinophyceae and Trebouxiophyceae

Genome Biology and Evolution

Volumn 7, Issue 7, 2015, Pages 2062-2082

  Turmel, Monique ^a   Otis, Christian ^a   Lemieux, Claude ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

genome rearrangements; horizontal transfer; introns; inverted repeat; Pedinophyceae; plastid genomics; repeats; Trebouxiophyceae

Indexed keywords

VEGETABLE PROTEIN;

CHLOROPLAST GENOME; CLASSIFICATION; DNA BASE COMPOSITION; GENE ORDER; GENETICS; GENOME SIZE; GREEN ALGA; INTRON; INVERTED REPEAT; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PLANT GENE;

BASE COMPOSITION; CHLOROPHYTA; EVOLUTION, MOLECULAR; GENE ORDER; GENES, PLANT; GENOME SIZE; GENOME, CHLOROPLAST; INTRONS; INVERTED REPEAT SEQUENCES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS;

EID: 84964694065     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv130     Document Type: Article

References (76)

1. Amin SA, Green DH, Al Waheeb D, Gardes A, Carrano CJ. 2012. Iron transport in the genus Marinobacter. Biometals 25:135-147.
2. Bao Z, Eddy SR. 2002. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 12:1269-1276.
3. Bélanger AS, et al. 2006. Distinctive architecture of the chloroplast genome in the chlorophycean green alga Stigeoclonium helveticum. Mol Genet Genomics. 276:464-477.
4. Bourque G, Pevzner PA. 2002. Genome-scale evolution: reconstructing gene orders in the ancestral species. Genome Res. 12:26-36.
5. Brouard JS, Otis C, Lemieux C, Turmel M. 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.
6. Brouard JS, Otis C, Lemieux C, Turmel M. 2010. The exceptionally large chloroplast genome of the green alga Floydiella terrestris illuminates the evolutionary history of the Chlorophyceae. Genome Biol Evol. 2:240-256.
7. Brouard JS, Otis C, Lemieux C, Turmel M. 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 Biol Evol. 3:505-515.
8. Civan P, Foster PG, Embley MT, Seneca A, Cox CJ. 2014. Analyses of charophyte chloroplast genomes help characterize the ancestral chloroplast genome of land plants. Genome Biol Evol. 6:897-911.
9. Cui L, et al. 2006. Adaptive evolution of chloroplast genome structure inferred using a parametric bootstrap approach. BMC Evol Biol. 6:13.
10. Darling AE, Mau B, Perna NT. 2010. progressive Mauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147.
11. de Cambiaire JC, Otis C, Lemieux C, Turmel M. 2006. The complete chloroplast genome sequence of the chlorophycean green alga Scenedesmus obliquus reveals a compact gene organization and a biased distribution of genes on the two DNA strands. BMC Evol Biol. 6:37.
12. de Cambiaire JC, Otis C, Turmel M, Lemieux C. 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.
13. Delannoy E, Fujii S, Colas des Francs-Small C, Brundrett M, Small I. 2011. Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol. 28:2077-2086.
14. Friedl T, Rybalka N. 2012. Systematics of the green algae: a brief introduction to the current status. In: Luttge U, Beyschlag W, Budel B, Francis D, editors. Progress in botany. vol. 73. Berlin (Germany): Springer-Verlag. p. 259-280.
15. Fucikova K, et al. 2014. New phylogenetic hypotheses for the core Chlorophyta based on chloroplast sequence data. Front Ecol Evol. 2:63.
16. Goulding SE, Olmstead RG, Morden CW, Wolfe KH. 1996. Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet. 252:195-206.
17. Gray MW, Archibald JM. 2012. Origins of mitochondria and plastids. In: Bock R, Knoop V, editors. Genomics of chloroplasts and mitochondria. Dordrecht (The Netherlands): Springer. p. 1-30.
18. Green BR. 2011. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 66:34-44.
19. Gueneau de Novoa P, Williams KP. 2004. The tmRNA website: reductive evolution of tmRNA in plastids and other endosymbionts. Nucleic Acids Res. 32:D104-D108.
20. Guisinger MM, Kuehl JV, Boore JL, Jansen RK. 2011. Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Mol Biol Evol. 28:583-600.
21. Haberle RC, Fourcade HM, Boore JL, Jansen RK. 2008. Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol. 66:350-361.
22. Hiratsuka J, et al. 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.
23. Hu F, Lin Y, Tang J. 2014. MLGO: phylogeny reconstruction and ancestral inference from gene-order data. BMC Bioinformatics 15:354.
24. Jansen RK, Ruhlman TA. 2012. Plastid genomes of seed plants. In: Bock R, Knoop V, editors. Genomics of chloroplasts and mitochondria. Dordrecht (The Netherlands): Springer. p. 103-126.
25. Kashino Y, et al. 2007. Ycf12 is a core subunit in the photosystem II complex. Biochim Biophys Acta. 1767:1269-1275.
26. Kittichotirat W, Bumgarner R, Chen C. 2010. Markedly different genome arrangements between serotype a strains and serotypes b or c strains of Aggregatibacter actinomycetemcomitans. BMC Genomics 11:489.
27. Knox EB. 2014. The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms. Proc Natl Acad Sci U S A. 111:11097-11102.
28. Kurtz S, et al. 2001. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29:4633-4642.
29. Lambowitz AM, Zimmerly S. 2011. Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol. 3:a003616.
30. Lang BF, Nedelcu AM. 2012. Plastid genomes of algae. In: Bock R, Knoop V, editors. Genomics of chloroplasts and mitochondria. Dordrecht (The Netherlands): Springer. p. 59-87.
31. Leliaert F, et al. 2012. Phylogeny and molecular evolution of the green algae. CRC Crit Rev Plant Sci. 31:1-46.
32. Leliaert F, Lopez-Bautista JM. 2015. The chloroplast genomes of Bryopsis plumosa and Tydemania expeditiones (Bryopsidales, Chlorophyta): compact genomes and genes of bacterial origin. BMC Genomics 16:204.
33. Lemieux C, Otis C, Turmel M. 2014a. Chloroplast phylogenomic analysis resolves deep-level relationships within the green algal class Trebouxiophyceae. BMC Evol Biol. 14:211.
34. Lemieux C, Otis C, Turmel M. 2014b. Six newly sequenced chloroplast genomes from prasinophyte green algae provide insights into the relationships among prasinophyte lineages and the diversity of streamlined genome architecture in picoplanktonic species. BMC Genomics 15:857.
35. Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants. Am J Bot. 91:1535-1556.
36. Lohse M, Drechsel O, Bock R. 2007. Organellar Genome DRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet. 52:267-274.
37. Lu F, et al. 2011. The Bryopsis hypnoides plastid genome: multimeric forms and complete nucleotide sequence. PLoS One 6:e14663.
38. Lynch M. 2007. The origins of genome architecture. Sunderland (MA): Sinauer Associates.
39. Maddison DR, Maddison WP. 2000. MacClade 4: analysis of phylogeny and character evolution. Sunderland (MA): Sinauer Associates.
40. Maddison WP, Maddison DR. 2015. Mesquite: a modular system for evolutionary analysis. Version 3.02. Available from: http://mesquiteproject.org
41. 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.
42. Maul JE, et al. 2002. The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659-2679.
43. Melton JT 3rd, Leliaert F, Tronholm A, Lopez-Bautista JM. 2015. The complete chloroplast and mitochondrial genomes of the green macroalga Ulva sp. UNA00071828 (Ulvophyceae, Chlorophyta). PLoS One 10:e0121020.
44. Michel F, Umesono K, Ozeki H. 1989. Comparative and functional anatomy of group II catalytic introns - a review. Gene 82:5-30.
45. Michel F, Westhof E. 1990. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol. 216:585-610.
46. Palmer JD. 1991. Plastid chromosomes: structure and evolution. In: Vasil IK, editor. The molecular biology of plastids. San Diego (CA): Academic Press. p. 5-53.
47. Palmer JD. 2003. The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39:4-12.
48. Pombert JF, Lemieux C, Turmel M. 2006. The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging ulvophytes. BMC Biol. 4:3.
49. Pombert JF, Otis C, Lemieux C, Turmel M. 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. Mol Biol Evol. 22:1903-1918.
50. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European molecular biology open software suite. Trends Genet. 16:276-277.
51. Robbens S, et al. 2007. The complete chloroplast and mitochondrial DNA sequence of Ostreococcus tauri: organelle genomes of the smallest eukaryote are examples of compaction. Mol Biol Evol. 24:956-968.
52. Rodriguez-Ezpeleta N, et al. 2005. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol. 15:1325-1330.
53. Ruhlman T, Jansen R. 2014. The plastid genomes of flowering plants. In: Maliga P, editor. Chloroplast biotechnology. New York: Humana Press. p. 3-38.
54. Servin-Garciduenas LE, Martinez-Romero E. 2012. Complete mitochondrial and plastid genomes of the green microalga Trebouxiophyceae sp. strain MX-AZ01 isolated from a highly acidic geothermal lake. Eukaryot Cell. 11:1417-1418.
55. Shao R, Dowton M, Murrell A, Barker SC. 2003. Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol Biol Evol. 20:1612-1619.
56. Smith DR, et al. 2010. The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA. BMC Plant Biol. 10:83.
57. Smith DR, et al. 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.
58. Smith DR, et al. 2013. Organelle genome complexity scales positively with organism size in volvocine green algae. Mol Biol Evol. 30:793-797.
59. Smith DR, Lee RW. 2009. The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genomics 10:132.
60. Soria-Carrasco V, Talavera G, Igea J, Castresana J. 2007. The K tree score: quantification of differences in the relative branch length and topology of phylogenetic trees. Bioinformatics 23:2954-2956.
61. Stoddard BL. 2014. Homing endonucleases from mobile group I introns: discovery to genome engineering. Mob DNA. 5:7.
62. Tesler G. 2002. GRIMM: genome rearrangements web server. Bioinformatics 18:492-493.
63. Turmel M, Brouard JS, Gagnon C, Otis C, Lemieux C. 2008. Deep division in the Chlorophyceae (Chlorophyta) revealed by chloroplast phylogenomic analyses. J Phycol. 44:739-750.
64. Turmel M, Gagnon MC, O'Kelly CJ, Otis C, Lemieux C. 2009. 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. Mol Biol Evol. 26:631-648.
65. Turmel M, Otis C, Lemieux C. 2002. The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci U S A. 99:11275-11280.
66. Turmel M, Otis C, Lemieux C. 2005. The complete chloroplast DNA sequences of the charophycean green algae Staurastrum and Zygnema reveal that the chloroplast genome underwent extensive changes during the evolution of the Zygnematales. BMC Biol. 3:22.
67. Turmel M, Otis C, Lemieux C. 2009. The chloroplast genomes of the green algae Pedinomonas minor, Parachlorella kessleri, and Oocystis solitaria reveal a shared ancestry between the Pedinomonadales and Chlorellales. Mol Biol Evol. 26:2317-2331.
68. Turmel M, Otis C, Lemieux C. 2013. Tracing the evolution of streptophyte algae and their mitochondrial genome. Genome Biol Evol. 5:1817-1835.
69. Turmel M, Pombert JF, Charlebois P, Otis C, Lemieux C. 2007. The green algal ancestry of land plants as revealed by the chloroplast genome. Int J Plant Sci. 168:679-689.
70. Wakasugi T, 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. Proc Natl Acad Sci U S A. 94:5967-5972.
71. Wang RJ, et al. 2008. Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol. 8:36.
72. Weng ML, Blazier JC, Govindu M, Jansen RK. 2014. Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Mol Biol Evol. 31:645-659.
73. Wolf PG, Karol KG. 2012. Plastomes of bryophytes, lycophytes and ferns. In: Bock R, Knoop V, editors. Genomics of chloroplasts and mitochondria. Dordrecht (The Netherlands): Springer. p. 89-102.
74. Wu CS, Chaw SM. 2014. Highly rearranged and size-variable chloroplast genomes in conifers II clade (cupressophytes): evolution towards shorter intergenic spacers. Plant Biotechnol J. 12:344-353.
75. Xia X. 2013. DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol. 30:1720-1728.
76. Xu W, Jameson D, Tang B, Higgs PG. 2006. The relationship between the rate of molecular evolution and the rate of genome rearrangement in animal mitochondrial genomes. J Mol Evol. 63:375-392..