Skip to main content

Plastid Genomes of Algae

  • Chapter
  • First Online:
Genomics of Chloroplasts and Mitochondria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 35))

Summary

Algae are characterized by the presence of plastids (chloroplasts), which are organelles of cyanobacterial origin. Plastids have their own genome, machineries for replication, transcription and translation, and are the site of photosynthesis (except in secondarily non-photosynthetic species) and a variety of other biological functions. Algae are subdivided into those whose plastids can be traced back to a common cyanobacterial endosymbiont (algae with primary plastids), and others in which plastids are second-hand acquisitions that were introduced by eukaryote-eukaryote endosymbioses.

Only a fraction of plastid components is encoded in plastid DNA; the majority of genes coding for plastid proteins are in the nucleus, many of which originated through transfers (in some cases still ongoing) from the organelle to the nuclear genome. Despite the broad phylogenetic affiliation of algae, most plastid genomes are fairly homogenous, coding for about 100–250 genes, except in non-photosynthetic algae that rapidly lose genes involved in photosynthesis. The most gene-rich and cyanobacteria-like plastid genomes are in red algae, followed by glaucophyte and green algae. Genomes in secondary or higher-order plastids usually have a reduced gene count, compared to their primary photosynthetic donors. In this chapter, we provide an overview on the evolutionary history, organization and coding properties of algal plastid genomes, for which complete (or almost complete) sequences are publicly available.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

aa –:

Amino acid;

CASH –:

Cryptophyta Alveolata, Stramenopila plus Haptophyta their plastids are of red algal origin and pt genomes are closely related (which is incompatible with respective nuclear genome phylogenies).

CW –:

‘Clockwise’ arrangement of flagellar basal bodies in Chlamydomonadales;

DO –:

‘Directly opposed’ arrangement of flagellar basal bodies in Sphaeropleales;

IR –:

Inverted genomic repeat region occurs in a large number of ptDNAs;

LBA –:

Long Branch Attraction phylogenetic artifact that leads to the incorrect grouping of fast-evolving species or attraction to distant outgroups, due to evolutionary model violations and under-estimation of repeated sequence change;

mtDNA –:

Mitochondrial DNA protists – eukaryotes other than fungi animals and plants;

pt –:

Plastid (chloroplast);

ptDNA –:

Plastid DNA;

SC –:

Single-copy regions separating large inverted repeats in ptDNAs;

tmRNA –:

Transfer mRNA occurs in bacterial some plastid and jakobid mitochondrial genomes typically contains a tRNA-like and a protein-coding domain involved in releasing ribosomes that are stalled by degraded mRNAs without in-frame stop codons

References

  • Andersen ES, Rosenblad MA, Larsen N, Westergaard JC, Burks J, Wower IK, Wower J, Gorodkin J, Samuelsson T, Zwieb C (2006) The tmRDB and SRPDB resources. Nucleic Acids Res 34:D163–D168

    Article  PubMed  CAS  Google Scholar 

  • Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:R81–R88

    Article  PubMed  CAS  Google Scholar 

  • Archibald JM, Keeling PJ (2002) Recycled plastids: a ‘green movement’ in eukaryotic evolution. Trends Genet 18:577–584

    Article  PubMed  CAS  Google Scholar 

  • Bachvaroff TR, Sanchez Puerta MV, Delwiche CF (2005) Chlorophyll c-containing plastid relationships based on analyses of a multigene data set with all four chromalveolate lineages. Mol Biol Evol 22:1772–1782

    Article  PubMed  CAS  Google Scholar 

  • Baurain D, Brinkmann H, Petersen J, Rodriguez-Ezpeleta N, Stechmann A, Demoulin V, Roger AJ, Burger G, Lang BF, Philippe H (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 27:1698–1709

    Article  PubMed  CAS  Google Scholar 

  • Beck N, Lang BF (2009) RNAweasel, a webserver for identification of mitochondrial, structured RNAs. http://megasun.bch.umontreal.ca/RNAweasel

  • Beck N, Lang BF (2010) MFannot, organelle genome annotation websever. http://megasun.bch.umontreal.ca/papers/MFannot

  • Belanger AS, Brouard JS, Charlebois P, Otis C, Lemieux C, Turmel M (2006) Distinctive architecture of the chloroplast genome in the chlorophycean green alga Stigeoclonium helveticum. Mol Genet Genomics 276:464–477

    Article  PubMed  CAS  Google Scholar 

  • Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16:1661–1666

    Article  PubMed  CAS  Google Scholar 

  • Bendich AJ (2007) The size and form of chromosomes are constant in the nucleus, but highly variable in bacteria, mitochondria and chloroplasts. Bioessays 29:474–483

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya D, Yoon HS, Hackett JD (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26:50–60

    Article  PubMed  Google Scholar 

  • Booton AS, Floyd GL, Fuerst PA (1998) Polyphyly of tetrasporalean green algae inferred from nuclear small subunit rDNA. J Phycol 34:306–311

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Buchheim MA, Michalopulos EA, Buchheim JA (2001) Phylogeny of the Chlorophyceae with special references to the Sphaeropleales. J Phycol 37:819–835

    Article  CAS  Google Scholar 

  • Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, Jakobsen KS, Pawlowski J (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2:e790

    Article  PubMed  CAS  Google Scholar 

  • Burki F, Inagaki Y, Brate J, Archibald JM, Keeling PJ, Cavalier-Smith T, Sakaguchi M, Hashimoto T, Horak A, Kumar S, Klaveness D, Jakobsen KS, Pawlowski J, Shalchian-Tabrizi K (2009) Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, telonemia and centroheliozoa, are related to photosynthetic chromalveolates. Genome Biol Evol 1:231–238

    Article  PubMed  CAS  Google Scholar 

  • Cattolico RA, Jacobs MA, Zhou Y, Chang J, Duplessis M, Lybrand T, McKay J, Ong HC, Sims E, Rocap G (2008) Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains. BMC Genomics 9:211

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? Biosystems 14:461–481

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354

    PubMed  CAS  Google Scholar 

  • Chaal BK, Green BR (2007) Protein targeting in “secondary” or “complex” chloroplasts. Methods Mol Biol 390:207–217

    Article  PubMed  CAS  Google Scholar 

  • Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, Bhattacharya D (2011) Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol 21:328–333

    Article  PubMed  CAS  Google Scholar 

  • Copertino DW, Hallick RB (1993) Group II and group III introns of twintrons: potential relationships with nuclear pre-mRNA introns. Trends Biochem Sci 18:467–471

    Article  PubMed  CAS  Google Scholar 

  • Cui L, Veeraraghavan N, Richter A, Wall K, Jansen RK, Leebens-Mack J, Makalowska I, dePamphilis CW (2006) ChloroplastDB: the chloroplast genome database. Nucleic Acids Res 34:D692–D696

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • de Koning A, Keeling P (2006) The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol 4:12

    Article  PubMed  CAS  Google Scholar 

  • Deschamps P, Moreira D (2009) Signal conflicts in the phylogeny of the primary photosynthetic eukaryotes. Mol Biol Evol 26:2745–2753

    Article  PubMed  CAS  Google Scholar 

  • Donaher N, Tanifuji G, Onodera NT, Malfatti SA, Chain PS, Hara Y, Archibald JM (2009) The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate. Genome Biol Evol 1:439–448

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE (1998) Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev 8:655–661

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE, Gray MW (1991) Plastid origins. Nature 352:290

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE, Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48:236–244

    Article  PubMed  CAS  Google Scholar 

  • Durnford DG, Gray MW (2006) Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot Cell 5:2079–2091

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (1996) Hidden Markov models. Curr Opin Struct Biol 6:361–365

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Eddy S (2008) Infernal website. http://infernal.janelia.org

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  PubMed  CAS  Google Scholar 

  • Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426

    Article  PubMed  CAS  Google Scholar 

  • Felsner G, Sommer MS, Maier UG (2010) The physical and functional borders of transit peptide-like sequences in secondary endosymbionts. BMC Plant Biol 10:223

    Article  PubMed  CAS  Google Scholar 

  • Floyd GL, Okelly CJ (1984) Motile cell ultrastructure and the circumscription of the orders Ulotrichales and Ulvales (Ulvophyceae, Chlorophyta). Am J Bot 71:111–120

    Article  Google Scholar 

  • Foth BJ, McFadden GI (2003) The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. Int Rev Cytol 224:57–110

    Article  PubMed  Google Scholar 

  • Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299:705–708

    Article  PubMed  CAS  Google Scholar 

  • 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, Trebouxiohyceae Cl-Nov). J Phycol 31:632–639

    Article  CAS  Google Scholar 

  • Funes S, Davidson E, Reyes-Prieto A, Magallón S, Herion P, King MP, González-Halphen D (2002) A green algal apicoplast ancestor. Science 298:2155

    Article  PubMed  CAS  Google Scholar 

  • Funes S, Reyes-Prieto A, Pérez-Martínez X, González-Halphen D (2004) On the evolutionary origins of apicoplasts: revisiting the rhodophyte vs. chlorophyte controversy. Microbes Infect 6:305–311

    Article  PubMed  Google Scholar 

  • Gardner MJ, Feagin JE, Moore DJ, Rangachari K, Williamson DH, Wilson RJ (1993) Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. Nucleic Acids Res 21:1067–1071

    Article  PubMed  CAS  Google Scholar 

  • Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR, Bateman A (2009) Rfam: updates to the RNA families database. Nucleic Acids Res 37:D136–D140

    Article  PubMed  CAS  Google Scholar 

  • Glockner G, Rosenthal A, Valentin K (2000) The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol 51:382–390

    PubMed  CAS  Google Scholar 

  • Gockel G, Hachtel W (2000) Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151:347–351

    Article  PubMed  CAS  Google Scholar 

  • Gogarten JP, Hilario E (2006) Inteins, introns, and homing endonucleases: recent revelations about the life cycle of parasitic genetic elements. BMC Evol Biol 6:94

    Article  PubMed  CAS  Google Scholar 

  • Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix JD (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65:135–143

    Article  PubMed  CAS  Google Scholar 

  • Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517

    Article  PubMed  CAS  Google Scholar 

  • Graham LE, Wilcox LW (2000) Algae. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Gray MW (2010) Rethinking plastid evolution. EMBO Rep 11:562–563

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Guillou L et al (2004) Diversity of picoplanktonic prasinophytes assessed by direct nuclear SSU rDNA sequencing of environmental samples and novel isolates retrieved from oceanic and coastal marine ecosystems. Protist 155:193–214

    Article  PubMed  CAS  Google Scholar 

  • Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T, Bhattacharya D (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol 14:213–218

    PubMed  CAS  Google Scholar 

  • Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rummele SE, Bhattacharya D (2007) Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol 24:1702–1713

    Article  PubMed  CAS  Google Scholar 

  • Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, de Oliveira MC (2004) Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. J Mol Evol 59:464–477

    Article  PubMed  CAS  Google Scholar 

  • Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A, Orsat B, Spielmann A, Stutz E (1993) Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res 21:3537–3544

    Article  PubMed  CAS  Google Scholar 

  • Hempel F, Felsner G, Maier UG (2010) New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms. Mol Microbiol 76:793–801

    Article  PubMed  CAS  Google Scholar 

  • Howe CJ, Nisbet RE, Barbrook AC (2008) The remarkable chloroplast genome of dinoflagellates. J Exp Bot 59:1035–1045

    Article  PubMed  CAS  Google Scholar 

  • Imanian B, Pombert JF, Keeling PJ (2010) The complete plastid genomes of the two ‘dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum. PLoS One 5:e10711

    Article  PubMed  CAS  Google Scholar 

  • Jacobs J, Glanz S, Bunse-Grassmann A, Kruse O, Kuck U (2010) RNA trans-splicing: identification of components of a putative chloroplast spliceosome. Eur J Cell Biol 89:932–939

    Article  PubMed  CAS  Google Scholar 

  • Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ (2010) A common red algal origin of the ­apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107:10949–10954

    Article  PubMed  Google Scholar 

  • Jansen RK, Raubeson LA, Boore JL, de Pamphilis CW, Chumley TW, Haberle RC, Wyman SK, Alverson AJ, Peery R, Herman SJ, Fourcade HM, Kuehl JV, McNeal JR, Leebens-Mack J, Cui L (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Methods Enzymol 395:348–384

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50:539–570

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ (2009) Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 56:1–8

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 365:729–748

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ, Deane JA, Hink-Schauer C, Douglas SE, Maier UG, McFadden GI (1999) The secondary endosymbiont of the cryptomonad Guillardia theta contains alpha-, beta-, and gamma-tubulin genes. Mol Biol Evol 16:1308–1313

    Article  PubMed  CAS  Google Scholar 

  • Kessler F, Schnell D (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr Opin Cell Biol 21:494–500

    Article  PubMed  CAS  Google Scholar 

  • Khan H, Parks N, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM (2007) Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol Biol Evol 24:1832–1842

    Article  PubMed  CAS  Google Scholar 

  • Knauf U, Hachtel W (2002) The genes encoding subunits of ATP synthase are conserved in the reduced plastid genome of the heterotrophic alga Prototheca wickerhamii. Mol Genet Genomics 267:492–497

    Article  PubMed  CAS  Google Scholar 

  • Kohler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJ, Palmer JD, Roos DS (1997) A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485–1489

    Article  PubMed  CAS  Google Scholar 

  • Kovacs-Bogdan E, Soll J, Bolter B (2010) Protein import into chloroplasts: the Tic complex and its regulation. Biochim Biophys Acta 1803:740–747

    Article  PubMed  CAS  Google Scholar 

  • Kowallik KV, Stoeb B, Schaffran I, Kroth-Pancic P, Freier U (1995) The chloroplast genome of a chlorophyll a+c-containing alga, Odontella sinenesis. Plant Mol Biol Rep 13:336–342

    Article  CAS  Google Scholar 

  • Laatsch T, Zauner S, Stoebe-Maier B, Kowallik KV, Maier UG (2004) Plastid-derived single gene minicircles of the dinoflagellate Ceratium horridum are localized in the nucleus. Mol Biol Evol 21:1318–1322

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, Burger G, O’Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493–497

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, Laforest MJ, Burger G (2007) Mitochondrial introns: a critical view. Trends Genet 23:119–125

    Article  PubMed  CAS  Google Scholar 

  • Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21:1095–1109

    Article  PubMed  CAS  Google Scholar 

  • Lartillot N, Philippe H (2008) Improvement of molecular phylogenetic inference and the phylogeny of Bilateria. Philos Trans R Soc Lond B Biol Sci 363:1463–1472

    Article  PubMed  Google Scholar 

  • Lartillot N, Brinkmann H, Philippe H (2007) Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol 7(Suppl 1):S4

    Article  PubMed  CAS  Google Scholar 

  • Le Corguille G, Pearson G, Valente M, Viegas C, Gschloessl B, Corre E, Bailly X, Peters AF, Jubin C, Vacherie B, Cock JM, Leblanc C (2009) Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol 9:253

    Article  PubMed  CAS  Google Scholar 

  • Le Gall L, Saunders GW (2007) A nuclear phylogeny of the Florideophyceae (Rhodophyta) inferred from combined EF2, small subunit and large subunit ribosomal DNA: establishing the new red algal subclass Corallinophycidae. Mol Phylogenet Evol 43:1118–1130

    Article  PubMed  CAS  Google Scholar 

  • Lehman RL, Manhart JR (1997) A preliminary comparison of restriction fragment patterns in the genus Caulerpa (Chlorophyta) and the unique structure of the chloroplast genome of Caulerpa sertularioides. J Phycol 33:1055–1062

    Article  CAS  Google Scholar 

  • Lemieux C, Otis C, Turmel M (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 Biol 5:2

    Article  PubMed  CAS  Google Scholar 

  • Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556

    Article  PubMed  Google Scholar 

  • Li HM, Chiu CC (2010) Protein transport into chloroplasts. Annu Rev Plant Biol 61:157–180

    Article  PubMed  CAS  Google Scholar 

  • Ling F, Shibata T (2004) Mhr1p-dependent concatemeric mitochondrial DNA formation for generating yeast mitochondrial homoplasmic cells. Mol Biol Cell 15:310–322

    Article  PubMed  CAS  Google Scholar 

  • Liu XQ (2000) Protein-splicing intein: genetic mobility, origin, and evolution. Annu Rev Genet 34:61–76

    Article  PubMed  CAS  Google Scholar 

  • Löffelhardt W, Bohnert HJ (1994) Structure and function of the cyanelle genome. Int Rev Cytol 151:29–65

    Article  PubMed  Google Scholar 

  • Lu F, Xu W, Tian C, Wang G, Niu J, Pan G, Hu S (2010) The Bryopsis hypnoides plastid genome: multimeric forms and complete nucleotide sequence. PLoS One 6:e14663

    Article  CAS  Google Scholar 

  • Ma Y, Jakowitsch J, Deusch O, Henze K, Martin W, Löffelhardt W (2009) Transketolase from Cyanophora paradoxa: in vitro import into cyanelles and pea chloroplasts and a complex history of a gene often, but not always, transferred in the context of secondary endosymbiosis. J Eukaryot Microbiol 56:568–576

    Article  PubMed  CAS  Google Scholar 

  • Manhart JR, Hoshaw RW, Palmer JD (1990) Unique chloroplast genome in Spirogyra maxima (Chlorophyta) revealed by physical and gene mapping. J Phycol 26:490–494

    Article  CAS  Google Scholar 

  • Manhart JR, Kelly K, Dudock BS, Palmer JD (1989) Unusual characteristics of Codium fragile chloroplast DNA revealed by physical and gene mapping. Mol Gen Genet 216:417–421

    Article  PubMed  CAS  Google Scholar 

  • Marin B, Melkonina M (2010) Molecular phylogeny and classification of the Mamiellophyceae class. nov (Chlorophyta) based on sequence comparisons of the nuclear- and plastid-encoded rRNA operons. Protist 161:304–336

    Article  PubMed  CAS  Google Scholar 

  • Mattox KR, Stewart KD (1984) Classification of the green algae: a concept based on comparative ecology. In: Irvine DEG, John DM (eds) The systematics of the green algae. Academic Press, London, pp 29–72

    Google Scholar 

  • Maul JE et al. (2002) The Chlamydomonas reinhardtti plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659–2679

    Article  PubMed  CAS  Google Scholar 

  • McFadden GI (1999) Plastids and protein targeting. J Eukaryot Microbiol 46:339–346

    Article  PubMed  CAS  Google Scholar 

  • McFadden GI (2010) The apicoplast. Protoplasma. 248:641–650

    Google Scholar 

  • McFadden GI, Waller RF (1997) Plastids in parasites of humans. Bioessays 19:1033–1040

    Article  PubMed  CAS  Google Scholar 

  • Minge MA, Shalchian-Tabrizi K, Torresen OK, Takishita K, Probert I, Inagaki Y, Klaveness D, Jakobsen KS (2010) A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evol Biol 10:191

    Article  PubMed  CAS  Google Scholar 

  • Moore CE, Archibald JM (2009) Nucleomorph genomes. Annu Rev Genet 43:251–264

    Article  PubMed  CAS  Google Scholar 

  • Moreira D, Philippe H (2001) Sure facts and open questions about the origin and evolution of photosynthetic plastids. Res Microbiol 152:771–780

    Article  PubMed  CAS  Google Scholar 

  • Nassoury N, Cappadocia M, Morse D (2003) Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci 116:2867–2874

    Article  PubMed  CAS  Google Scholar 

  • Obornik M, Van de Peer Y, Hypsa V, Frickey T, Slapeta JR, Meyer A, Lukes J (2002) Phylogenetic analyses suggest lateral gene transfer from the mitochondrion to the apicoplast. Gene 285:109–118

    Article  PubMed  CAS  Google Scholar 

  • O’Brien EA, Zhang Y, Wang E, Marie V, Badejoko W, Lang BF, Burger G (2009) GOBASE: an organelle genome database. Nucleic Acids Res 37:D946–D950

    Article  PubMed  CAS  Google Scholar 

  • Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin IT, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77

    Article  PubMed  CAS  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2001) Mitochondrial DNA from the liverwort Marchantia polymorpha: ­circularly permuted linear molecules, head-to-tail concatemers, and a 5’ protein. J Mol Biol 310:549–562

    Article  PubMed  CAS  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2004) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335:953–970

    Article  PubMed  CAS  Google Scholar 

  • Ong HC, Wilhelm SW, Gobler CJ, Bullerjahn G, Jacobs MA, McKay J, Sims EH, Gillett WG, Zhou Y, Haugen E, Rocap G, Cattolico RA (2010) Analysis of the complete chloroplast genome sequences of two members of the Pelagophyceae: Aureococcus anophagefferens and Aureoumbra lagunensis. J Phycol 46:602–615

    Article  CAS  Google Scholar 

  • Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics 277:427–439

    Article  PubMed  CAS  Google Scholar 

  • Parfrey LW, Grant J, Tekle YI, Lasek-Nesselquist E, Morrison HG, Sogin ML, Patterson DJ, Katz LA (2010) Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Syst Biol 59:518–533

    Article  PubMed  Google Scholar 

  • Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. Bioessays 29:1048–1058

    Article  PubMed  CAS  Google Scholar 

  • Patron NJ, Waller RF, Archibald JM, Keeling PJ (2005) Complex protein targeting to dinoflagellate plastids. J Mol Biol 348:1015–1024

    Article  PubMed  CAS  Google Scholar 

  • Patterson DJ (1989) Stramenopiles: chromophyte from a protistan perspective. In: Green JC, Leadbeater ESC, Diver WL (eds) The chromophyte algae: problems and perspectives. Clarendon, Oxford, pp 357–379

    Google Scholar 

  • Pfanzagl B, Zenker A, Pittenauer E, Allmaier G, Martinez-Torrecuadrada J, Schmid ER, De Pedro MA, Löffelhardt W (1996) Primary structure of cyanelle peptidoglycan of Cyanophora paradoxa: a prokaryotic cell wall as part of an organelle envelope. J Bacteriol 178:332–339

    PubMed  CAS  Google Scholar 

  • Philippe H, Delsuc F, Brinkmann H, Lartillot N (2005) Phylogenomics. Annu Rev Ecol Evol Syst 36:541–562

    Article  Google Scholar 

  • Pombert JF, Keeling PJ (2010) The mitochon­drial genome of the entomoparasitic green alga Helicosporidium. PLoS One 5:e8954

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pombert JF, Otis C, Lemieux C, Turmel M (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. Mol Biol Evol 21:922–935

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Reith ME, Munholland J (1995) Complete nucleotide sequence of the Porphyra pupurea chloroplast. Plant Mol Biol Rep 13:333–335

    Article  CAS  Google Scholar 

  • Reyes-Prieto A, Bhattacharya D (2007) Phylogeny of nuclear-encoded plastid-targeted proteins supports an early divergence of glaucophytes within Plantae. Mol Biol Evol 24:2358–2361

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Prieto A, Weber AP, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168

    Article  PubMed  CAS  Google Scholar 

  • Rivier C, Goldschmidt-Clermont M, Rochaix JD (2001) Identification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 20:1765–1773

    Article  PubMed  CAS  Google Scholar 

  • Robbens S, Derelle E, Ferraz C, Wuyts J, Moreau H, Van de Peer Y (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

    Article  PubMed  CAS  Google Scholar 

  • Rochaix JD (1996) Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol Biol 32:327–341

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, Bohnert HJ, Philippe H, Lang BF (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15:1325–1330

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Ezpeleta N, Brinkmann H, Burger G, Roger AJ, Gray MW, Philippe H, Lang BF (2007a) Toward resolving the eukaryotic tree: the phylogenetic positions of jakobids and cercozoans. Curr Biol 17:1420–1425

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Ezpeleta N, Brinkmann H, Roure B, Lartillot N, Lang BF, Philippe H (2007b) Detecting and overcoming systematic errors in genome-scale phylogenies. Syst Biol 56:389–399

    Article  PubMed  CAS  Google Scholar 

  • Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ (2007) The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol 24:54–62

    Article  PubMed  CAS  Google Scholar 

  • Rosenblad MA, Samuelsson T (2004) Identification of chloroplast signal recognition particle RNA genes. Plant Cell Physiol 45:1633–1639

    Article  PubMed  CAS  Google Scholar 

  • Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR (2008) Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci USA 105:17867–17871

    Article  PubMed  CAS  Google Scholar 

  • Sanchez Puerta MV, Bachvaroff TR, Delwiche CF (2005) The complete plastid genome sequence of the haptophyte Emiliania huxleyi: a comparison to other plastid genomes. DNA Res 12:151–156

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Puerta MV, Bachvaroff TR, Delwiche CF (2007) Sorting wheat from chaff in multi-gene analyses of chlorophyll c-containing plastids. Mol Phylogenet Evol 44:885–897

    Article  PubMed  CAS  Google Scholar 

  • Schunemann D (2004) Structure and function of the chloroplast signal recognition particle. Curr Genet 44:295–304

    Article  PubMed  CAS  Google Scholar 

  • Shevelev EL, Bryant DA, Löffelhardt W, Bohnert HJ (1995) Ribonuclease-P RNA gene of the plastid chromosome from Cyanophora paradoxa. DNA Res 2:231–234

    Article  PubMed  CAS  Google Scholar 

  • Shoup S, Lewis LA (2003) Polyphyletic origin of parallel basal bodies in swimming cells of chlorophycean green algae (Chlorophyta). J Phycol 39:789–796

    Article  CAS  Google Scholar 

  • Sluiman HJ (1985) A cladistic evaluation of the lower and higher green plants (Viridiplantae). Plant Syst Evol 149:217–232

    Article  Google Scholar 

  • Smith DR, Lee RW (2009) The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genomics 10:132

    Article  PubMed  CAS  Google Scholar 

  • Smith DR, Lee RW (2010) Low nucleotide diversity for the expanded organelle and nuclear genomes of Volvox carteri supports the mutational-hazard hypothesis. Mol Biol Evol 27:2244–2256

    Article  PubMed  CAS  Google Scholar 

  • Smith DR, Lee RW, Cushman JC, Magnuson JK, Tran D, Polle JE (2010) The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA. BMC Plant Biol 10:83

    Article  PubMed  CAS  Google Scholar 

  • Stiller JW, Huang J, Ding Q, Tian J, Goodwillie C (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genomics 10:484

    Article  PubMed  CAS  Google Scholar 

  • Stoebe B, Maier UG (2002) One, two, three: nature’s tool box for building plastids. Protoplasma 219:123–130

    Article  PubMed  Google Scholar 

  • Strittmatter P, Soll J, Bolter B (2010) The chloroplast protein import machinery: a review. Methods Mol Biol 619:307–321

    Article  PubMed  CAS  Google Scholar 

  • Tanaka T, Fukuda Y, Yoshino T, Maeda Y, Muto M, Matsumoto M, Mayama S, Matsunaga T (2011) High-throughput pyrosequencing of the chloroplast genome of a highly neutral-lipid-producing marine pennate diatom, Fistulifera sp. strain JPCC DA0580. Photosynth Res 109:223–229

    Google Scholar 

  • Turmel M, Otis C, Lemieux C (1999) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96:10248–10253

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2002) The complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants. Mol Biol Evol 19:24–38

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324–1338

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2007) An unexpectedly large and loosely packed mitochondrial genome in the charophycean green alga Chlorokybus atmophyticus. BMC Genomics 8:137

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Turmel M, Gagnon MC, O’Kelly CJ, Otis C, Lemieux C (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. Mol Biol Evol 26:631–648

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2009b) 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

    Article  PubMed  CAS  Google Scholar 

  • van Dooren GG, Schwartzbach SD, Osafune T, McFadden GI (2001) Translocation of proteins across the multiple membranes of complex plastids. Biochim Biophys Acta 1541:34–53

    Article  PubMed  Google Scholar 

  • Verbruggen H, Maggs CA, Saunders GW, Le Gall L, Yoon HS, De Clerck O (2010) Data mining approach identifies research priorities and data requirements for resolving the red algal tree of life. BMC Evol Biol 10:16

    Article  PubMed  CAS  Google Scholar 

  • Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (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 USA 94:5967–5972

    Article  PubMed  CAS  Google Scholar 

  • Wastl J, Maier UG (2000) Transport of proteins into cryptomonads complex plastids. J Biol Chem 275:23194–23198

    Article  PubMed  CAS  Google Scholar 

  • Wastl J, Duin EC, Iuzzolino L, Dorner W, Link T, Hoffmann S, Sticht H, Dau H, Lingelbach K, Maier UG (2000) Eukaryotically encoded and chloroplast-located rubredoxin is associated with photosystem II. J Biol Chem 275:30058–30063

    Article  PubMed  CAS  Google Scholar 

  • Williamson DH, Gardner MJ, Preiser P, Moore DJ, Rangachari K, Wilson RJ (1994) The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol Gen Genet 243:249–252

    PubMed  CAS  Google Scholar 

  • Wilson RJ, Williamson DH (1997) Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev 61:1–16

    PubMed  CAS  Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1991) Ins and outs of plastid genome evolution. Curr Opin Genet Dev 1:523–529

    Article  PubMed  CAS  Google Scholar 

  • Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255

    Article  PubMed  CAS  Google Scholar 

  • Yamada T (1991) Repetitive sequence-mediated rearrangements in Chlorella ellipsoidea chloroplast DNA – completion of nucleotide-sequence of the large inverted repeat. Curr Genet 19:139–147

    Article  PubMed  CAS  Google Scholar 

  • Yamada T, Shimaji M (1987) Splitting of the ribosomal-RNA operon on chloroplast DNA from Chlorella ellipsoidea. Mol Gen Genet 208:377–383

    Article  CAS  Google Scholar 

  • Zhang Z, Green BR, Cavalier-Smith T (1999) Single gene circles in dinoflagellate chloroplast genomes. Nature 400:155–159

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Cavalier-Smith T, Green BR (2002) Evolution of dinoflagellate unigenic minicircles and the partially concerted divergence of their putative replicon origins. Mol Biol Evol 19:489–500

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. G. Burger (Université de Montréal, Montreal, Canada) for insightful discussion and comments on the manuscript. This work was supported by the Canadian Research Chair Program and the Natural Sciences and Engineering Research Council (NSERC; 194560–2011) of Canada.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. Franz Lang .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Lang, B.F., Nedelcu, A.M. (2012). Plastid Genomes of Algae. In: Bock, R., Knoop, V. (eds) Genomics of Chloroplasts and Mitochondria. Advances in Photosynthesis and Respiration, vol 35. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2920-9_3

Download citation

Publish with us

Policies and ethics