Current Genetics

, Volume 64, Issue 2, pp 365–387 | Cite as

Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists

  • Lucia Hadariová
  • Matej Vesteg
  • Vladimír Hampl
  • Juraj Krajčovič


Chloroplasts are generally known as eukaryotic organelles whose main function is photosynthesis. They perform other functions, however, such as synthesizing isoprenoids, fatty acids, heme, iron sulphur clusters and other essential compounds. In non-photosynthetic lineages that possess plastids, the chloroplast genomes have been reduced and most (or all) photosynthetic genes have been lost. Consequently, non-photosynthetic plastids have also been reduced structurally. Some of these non-photosynthetic or “cryptic” plastids were overlooked or unrecognized for decades. The number of complete plastid genome sequences and/or transcriptomes from non-photosynthetic taxa possessing plastids is rapidly increasing, thus allowing prediction of the functions of non-photosynthetic plastids in various eukaryotic lineages. In some non-photosynthetic eukaryotes with photosynthetic ancestors, no traces of plastid genomes or of plastids have been found, suggesting that they have lost the genomes or plastids completely. This review summarizes current knowledge of non-photosynthetic plastids, their genomes, structures and potential functions in free-living and parasitic plants, algae and protists. We introduce a model for the order of plastid gene losses which combines models proposed earlier for land plants with the patterns of gene retention and loss observed in protists. The rare cases of plastid genome loss and complete plastid loss are also discussed.


Non-photosynthetic plastids Plastid genome Plastid loss Essential metabolic pathways Parasitism 



Endosymbiotic gene transfer


Translocon of outer chloroplast membrane


Translocon of inner chloroplast membrane




Acetyl co-enzyme A


Acetyl-CoA carboxylase


Inverted repeat


Large single copy


Small single copy






Non-mevalonate isoprenoid biosynthesis pathway


Isopentenyl pyrophosphate


Fatty acid synthesis


Co-location for redox regulation



This work was supported by the Scientific Grant Agency of the Slovak Ministry of Education and the Academy of Sciences (Grant VEGA 1/0535/17), by project ITMS 26210120024 supported by the Research & Development Operational Programme funded by the ERDF, by the Czech Science foundation Project nr. 16-25280S, by the Ministry of Education, Youth and Sports of CR within the National Sustainability Program II (Project BIOCEV-FAR) LQ1604 and by the project ‘‘BIOCEV’’ (CZ.1.05/1.1.00/02.0109). We thank Dr. Heather Esson (Laboratory of Evolutionary Protistology, Institute of Parasitology, Biology Centre CAS, České Budějovice, Czech Republic) for language revision of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

294_2017_761_MOESM1_ESM.pdf (334 kb)
Online Resource 1 Characteristics of plastid genomes in organisms with non-photosynthetic plastids. Plastid genome sizes – "0 bp" indicates that there is probably no plastid genome present. Gene number includes only protein-coding genes. rRNA genes, tRNA genes, pseudogenes and orfs are not included. Number of photosynthetic genes comprises psa, psb, pet and rbcL genes. IRs (inverted repeats) –"Yes" indicates presence, "No" indicates absence, "Cryptic" indicates the possibility of IRs existence, "Secondary" indicates that original IRs have been lost and new ones have arisen secondarily. A question mark indicates the lack of data (PDF 334 KB)


  1. Abrahamsen MS, Templeton TJ, Enomoto S et al (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 16:441–445CrossRefGoogle Scholar
  2. Adam Z (2000) Chloroplast proteases: possible regulators of gene expression? Biochimie 82(6):647–654PubMedCrossRefGoogle Scholar
  3. Adl SM, Simpson AG, Lane CE et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59(5):429–514PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allen JF (1993) Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 165:609–631PubMedCrossRefGoogle Scholar
  5. Allen JF (2003) The function of genomes in bioenergetic organelles. Philos Trans R Soc Lond B Biol Sci 358(1429):19–38PubMedPubMedCentralCrossRefGoogle Scholar
  6. Allison LA, Simon LD, Maliga P (1996) Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J 15(11):2802PubMedPubMedCentralGoogle Scholar
  7. Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19(2):R81–R88PubMedCrossRefGoogle Scholar
  8. Archibald JM (2015) Genomic perspectives on the birth and spread of plastids. PNAS 112(33):10147–10153PubMedPubMedCentralCrossRefGoogle Scholar
  9. Archibald JM, Keeling PJ (2002) Recycled plastids: a ‘green movement’ in eukaryotic evolution. Trends Genet 18(11):577–584PubMedCrossRefGoogle Scholar
  10. Arisue N, Hashimoto T, Mitsui H et al (2012) The Plasmodium apicoplast genome: conserved structure and close relationship of P. ovale to rodent malaria parasites. Mol Biol Evol 29(9):2095–2099PubMedCrossRefGoogle Scholar
  11. Atteia A, van Lis R, Beale SI (2005) Enzymes of the heme biosynthetic pathway in the nonphotosynthetic alga Polytomella sp. Eukaryot Cell 4:2087–2097PubMedPubMedCentralCrossRefGoogle Scholar
  12. Barbrook AC, Howe CJ, Purton S (2006) Why are plastid genomes retained in nonphotosynthetic organisms? Trends Plant Sci 11:101–108PubMedCrossRefGoogle Scholar
  13. Barrett CF, Davis JI (2012) The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. Am J Bot 99:1513–1523PubMedCrossRefGoogle Scholar
  14. Barrett CF, Freudenstein JV (2008) Molecular evolution of rbcL in the mycoheterotrophic coralroot orchids (Corallorhiza Gagnebin, Orchidaceae). Mol Phylogen Evol 47:665–679CrossRefGoogle Scholar
  15. Barrett CF, Freudenstein JV, Li J et al (2014) Investigating the path of plastid genome degradation in an early-transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms. Mol Biol Evol 31:3095–3112PubMedCrossRefGoogle Scholar
  16. Baurain D, Brinkmann H, Petersen J et al (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 27(7):1698–1709PubMedCrossRefGoogle Scholar
  17. Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73CrossRefGoogle Scholar
  18. Becker B, Hoef-Emden K, Melkonian M (2008) Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol 8:203PubMedPubMedCentralCrossRefGoogle Scholar
  19. Belcher JH, Swale EMF (1976) Spumella elongata nov. comb.—a colourless flagellate from soil. Arch Protistenkd 118:215–220Google Scholar
  20. Bellot S, Renner SS (2016) The plastomes of two species in the endoparasite genus Pilostyles (Apodanthaceae) each retain just five or six possibly functional genes. Genome Biol Evol 8(1):189–201CrossRefGoogle Scholar
  21. Ben Ali A, De Baerea R, De Wachtera R, Van de Peer Y (2002) Evolutionary relationships among heterokont algae (the autotrophic stramenopiles) based on combined analyses of small and large subunit ribosomal RNA. Protist 153:123–132PubMedCrossRefGoogle Scholar
  22. Bidartondo MI, Bruns TD, Weiss M, Sérgio C, Read DJ (2003) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proc R Soc Lond B Biol Sci 270(1517):835–842CrossRefGoogle Scholar
  23. Bjorkholm P, Harish A, Hagstrom E, Ernst AM, Andersson SG (2015) Mitochondrial genomes are retained by selective constraints on protein targeting. Proc Natl Acad Sci USA 112:10154–10161PubMedPubMedCentralCrossRefGoogle Scholar
  24. Blouin NA, Lane CE (2012) Red algal parasites: models for a life history evolution that leaves photosynthesis behind again and again. Bioessays 34(3):226–235PubMedCrossRefGoogle Scholar
  25. Bodył A (1996) Is the origin of Astasia longa an example of the inheritance of acquired characteristics? Acta Protozool 35:87–94Google Scholar
  26. Bodył A, Mackiewicz P, Stiller JW (2010) Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol 12(4):639–649PubMedGoogle Scholar
  27. Bölter B, Soll J (2017) Ycf1/Tic214 is not essential for the accumulation of plastid proteins. Mol Plant 10(1):219–221PubMedCrossRefGoogle Scholar
  28. Borza T, Popescu CE, Lee RW (2005) Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryot Cell 4:253–261PubMedPubMedCentralCrossRefGoogle Scholar
  29. Braukmann T, Kuzmina M, Stefanović S (2013) Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss. J Exp Bot 64:977–989PubMedPubMedCentralCrossRefGoogle Scholar
  30. Brayton KA, Lau AO, Herndon DR et al (2007) Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 3(10):e148PubMedCentralCrossRefGoogle Scholar
  31. Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 6(5):a016147PubMedPubMedCentralCrossRefGoogle Scholar
  32. Cahoon AB, Cunningham KA, Stern DB (2003) The plastid clpP gene may not be essential for plant cell viability. Plant Cell Physiol 44(1):93–95PubMedCrossRefGoogle Scholar
  33. Cai X, Fuller AL, McDougald LR, Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46PubMedCrossRefGoogle Scholar
  34. Cai Z, Guisinger M, Kim HG et al (2008) Extensive reorganization of the plastid genome of Trifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novel DNA insertions. J Mol Evol 67(6):696–704PubMedCrossRefGoogle Scholar
  35. Callow JA, Callow ME, Evans LV (1979) Nutritional studies of the parasitic red alga Choreocolax polysiphoniae. New Phytol 83:451–462CrossRefGoogle Scholar
  36. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46(4):347–366PubMedCrossRefGoogle Scholar
  37. Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and the phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354PubMedCrossRefGoogle Scholar
  38. Cavalier-Smith T, Chao EE (2004) Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur J Protistol 40(3):185–212CrossRefGoogle Scholar
  39. Cavalier-Smith T, Lee JJ (1985) Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Eukaryot Microbiol 32(3):376–379Google Scholar
  40. Chesnick JM, Hooistra WH, Wellbrock U, Medlin LK (1997) Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). J Eukaryot Microbiol 44:314–320PubMedCrossRefGoogle Scholar
  41. Cinar HN, Qvarnstrom Y, Wei-Pridgeon Y et al (2016) Comparative sequence analysis of Cyclospora cayetanensis apicoplast genomes originating from diverse geographical regions. Parasit Vectors 9(1):611PubMedPubMedCentralCrossRefGoogle Scholar
  42. Clarke AK (1999) ATP-dependent Clp proteases in photosynthetic organisms—a cut above the rest! Ann Bot 83(6):593–599CrossRefGoogle Scholar
  43. Court GJ (1980) Photosynthesis and translocation studies of Laurencia spectabilis and its symbiont Janczewskia gardneri (Rhodophyceae). J Phycol 16:270–279CrossRefGoogle Scholar
  44. de Koning AP, Keeling PJ (2004) Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastid in a parasitic alga. Eukaryot Cell 3:1198–1205PubMedPubMedCentralCrossRefGoogle Scholar
  45. de Koning AP, Keeling PJ (2006) The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol 4:12PubMedPubMedCentralCrossRefGoogle Scholar
  46. de Vries J, Sousa FL, Bölter B, Soll J, Gould SB (2015) YCF1: a green TIC? Plant Cell 27(7):1827–1833PubMedPubMedCentralCrossRefGoogle Scholar
  47. de Vries J, Archibald JM, Gould SB (2017) The carboxy terminus of YCF1 contains a motif conserved throughout > 500 Myr of streptophyte evolution. Genome Biol Evol 9(2):473–479PubMedPubMedCentralCrossRefGoogle Scholar
  48. Delannoy E, Fijii S, Colas des Francs C, Brundett M, Small I (2011) Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol 28:2077–2086PubMedPubMedCentralCrossRefGoogle Scholar
  49. Delwiche CF, Palmer JD (1996) Rampant horizontal transfer and duplication of Rubisco genes in eubacteria and plastids. Mol Biol Evol 13(6):873–882PubMedCrossRefGoogle Scholar
  50. Deschamps P, Colleonic C, Nakamura Y et al (2008) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548PubMedCrossRefGoogle Scholar
  51. Deusch O, Landan G, Roettger M et al (2008) Genes of cyanobacterial origin in plant nuclear genomes point to heterocyst-forming plastid ancestor. Mol Biol Evol 25:748–761PubMedCrossRefGoogle Scholar
  52. do Vieira LN,·dos Anjos KG, Faoro H, Fraga HPdeF, Greco TM, Pedrosa FdeO, de Souza EM, Rogalski M, de Souza RF, Guerra MP (2016) Phylogenetic inference and SSR characterization of tropical woody bamboos tribe Bambuseae (Poaceae: Bambusoideae) based on complete plastid genome sequences. Curr Genet 62:443–453. doi: 10.1007/s00294-015-0549-z CrossRefGoogle Scholar
  53. Dodge JD (1969) Observations on the fine structure of the eyespot and associated organelles in the dinoflagellate Glenodinium foliaceum. J Cell Sci 5:479–93PubMedGoogle Scholar
  54. Domman D, Horn M, Embley TM, Williams TA (2015) Plastid establishment did not require a chlamydial partner. Nat Commun 6:6421. doi: 10.1038/ncomms7421 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Donaher N, Tanifuji G, Onodera NT et al (2009) The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate. Genome Biol Evol 1:439–448PubMedPubMedCentralCrossRefGoogle Scholar
  56. Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14(8):307–311PubMedCrossRefGoogle Scholar
  57. Dorrell RG, Gile G, McCallum Méheust R, Bapteste EP, Klinger CM, Brillet-Guéguen L, Freeman KD, Richter DJ, Bowler C (2017) Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. eLife 2017 6:e23717. doi: 10.7554/eLife.23717 Google Scholar
  58. Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350(6314):148–151PubMedCrossRefGoogle Scholar
  59. Facchinelli F, Colleoni C, Ball SG, Weber AP (2013) Chlamydia, cyanobiont, or host: Who was on top in the ménage à trois? Trends Plant Sci 18(12):673–679PubMedCrossRefGoogle Scholar
  60. Falkowski PG, Katz ME, Knoll AH et al (2004) The evolution of modern eukaryotic phytoplankton. Science 305(5682):354–360PubMedCrossRefGoogle Scholar
  61. Figueroa-Martinez F, Nedelcu AM, Smith DR, Reyes-Prieto A (2017a) The plastid genome of Polytoma uvella is the largest known among colorless algae and plants and reflects contrasting evolutionary paths to nonphotosynthetic lifestyles. Plant Physiol 173(2):932–943PubMedCrossRefGoogle Scholar
  62. Figueroa-Martinez F, Nedelcu AM, Reyes-Prieto A, Smith DR (2017b) The plastid genomes of nonphotosynthetic algae are not so small after all. Commun Integ Biol 10(1):e1283080CrossRefGoogle Scholar
  63. Funk HT, Berg S, Krupinska K, Maier UG, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7:45PubMedPubMedCentralCrossRefGoogle Scholar
  64. Gagat P, Bodyl A, Mackiewicz P (2013) How protein targeting to primary plastids via the endomembrane system could have evolved? A new hypothesis based on phylogenetic studies. Biol Direct 8(1):18PubMedPubMedCentralCrossRefGoogle Scholar
  65. Gaillard T, Madamet M, Tsombeng FF, Dormoi J, Pradines B (2016) Antibiotics in malaria therapy: which antibiotics except tetracyclines and macrolides may be used against malaria? Malar J 15(1):556PubMedPubMedCentralCrossRefGoogle Scholar
  66. Gardner MJ, Bishop R, Shah T et al (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309(5731):134–137PubMedCrossRefGoogle Scholar
  67. George B, Bhatt BS, Awasthi M, George B, Singh AK (2015) Comparative analysis of microsatellites in chloroplast genomes of lower and higher plants. Curr Genet 61:665–677PubMedCrossRefGoogle Scholar
  68. Gile GH, Slamovits CH (2014) Transcriptomic analysis reveals evidence for a cryptic plastid in the colpodellid Voromonas pontica, a close relative of chromerids and apicomplexan parasites. PloS one 9(5):e96258PubMedPubMedCentralCrossRefGoogle Scholar
  69. Gilson PR, Su V, Slamovits CH et al (2006) Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature’s smallest nucleus. Proc Natl Acad Sci 103(25):9566–9571PubMedPubMedCentralCrossRefGoogle Scholar
  70. Giovannoni S, Turner S, Olsen G et al (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592PubMedPubMedCentralCrossRefGoogle Scholar
  71. Gockel G, Hachtel W (2000) Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151:347–351PubMedCrossRefGoogle Scholar
  72. Gockel G, Hachtel W, Baier S et al (1994) Genes for chloroplast apparatus are conserved in the reduced 73-kb plastid DNA of the nonphotosynthetic euglenoid flagellate Astasia longa. Curr Genet 26:256–262PubMedCrossRefGoogle Scholar
  73. Goff LJ, Coleman AW (1995) Fate of parasite and host organelle DNA during cellular transformation of red algae by their parasites. Plant Cell 7(11):1899–1911PubMedPubMedCentralCrossRefGoogle Scholar
  74. Goff LJ, Zuccarello G (1994) The evolution of parasitism in red algae: Cellular interactions of adelphoparasites and their hosts. J Phycol 30:695–720CrossRefGoogle Scholar
  75. Gogniashvili M, Jinjikhadze T, Maisaia I, Akhalkatsi M, Adam Kotorashvili A, Kotaria N, Beridze T, Dudnikov AJ (2016) Complete chloroplast genomes of Aegilops tauschii Coss. and Ae. cylindrica Host sheds light on plasmon D evolution. Curr Genet 62:791–798. doi: 10.1007/s00294-016-0583-5 PubMedCrossRefGoogle Scholar
  76. Gornik SG, Cassin AM, MacRae JI et al (2015) Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proc Natl Acad Sci 112(18):5767–5772PubMedPubMedCentralCrossRefGoogle Scholar
  77. Graham SW, Lam VK, Merckx VS (2017) Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes. New Phytol 214(1):48–55Google Scholar
  78. Grant J, Tekle YI, Anderson OR, Patterson DJ, Katz LA (2009) Multigene evidence for the placement of a heterotrophic amoeboid lineage Leukarachnion sp. among photosynthetic stramenopiles. Protist 160(3):376–385PubMedCrossRefGoogle Scholar
  79. Grauvogel C, Reece KS, Brinkmann H, Petersen J (2007) Plastid isoprenoid metabolism in the oyster parasite Perkinsus marinus connects dinoflagellates and malaria pathogens-new impetus for studying alveolates. J Mol Evol 65:725–729PubMedCrossRefGoogle Scholar
  80. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283(5407):1476–1481PubMedCrossRefGoogle Scholar
  81. Green BR (2011) Chloroplast genomes of photosynthetic eukaryotes. Plant J 66(1):34–44PubMedCrossRefGoogle Scholar
  82. Gruzdev EV, Mardanov AV, Beletsky AV et al (2016) The complete chloroplast genome of parasitic flowering plant Monotropa hypopitys: extensive gene losses and size reduction. Mitochondrial DNA Part B Resour 1(1):212–213CrossRefGoogle Scholar
  83. Hackett JD, Maranda L, Yoon HS, Bhattacharya D (2003) Phylogenetic evidence for the cryptophyte origin of the plastid of Dinophysis (Dinophysiales, Dinophyceae). J Phycol 39:440–448CrossRefGoogle Scholar
  84. Hadariová L, Vesteg M, Birčák E, Schwartzbach SD, Krajčovič J (2017) An intact plastid genome is essential for the survival of colorless Euglena longa but not Euglena gracilis. Curr Genet 63(2):331–334PubMedCrossRefGoogle Scholar
  85. Hallick RB, Hong L, Drager RG et al (1993) Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res 21:3537–3544PubMedPubMedCentralCrossRefGoogle Scholar
  86. Harris ME, Meyer G, Vandergon T, Vandergon VO (2013) Loss of the acetyl-CoA carboxylase (accD) gene in Poales. Plant Mol Biol Report 31(1):21–31CrossRefGoogle Scholar
  87. Hehenberger E, Imanian B, Burki F, Keeling PJ (2014) Evidence for the retention of two evolutionary distinct plastids in dinoflagellates with diatom endosymbionts. Gen Biol Evol 6(9):2321–2334CrossRefGoogle Scholar
  88. Hoef-Emden K (2005) Multiply independent losses of photosynthesis and differing evolutionary in the genus Cryptomonas (Cryptophyceae): Combined phylogenetic analyses of DNA sequences of the nuclear and the nucleomorph ribosomal operons. J Mol Evol 60:183–195PubMedCrossRefGoogle Scholar
  89. Howe CJ, Smith AG (1991) Plants without chlorophyll. Nature 349:109CrossRefGoogle Scholar
  90. Hrdá Š, Fousek J, Szabová J, Hampl V, Vlček Č (2012) The plastid genome of Eutreptiella provides a window into the process of secondary endosymbiosis of plastid in euglenids. PLoS One 7(3):e33746PubMedPubMedCentralCrossRefGoogle Scholar
  91. Hu J, Bogorad L (1990) Maize chloroplast RNA polymerase: the 180-, 120-, and 38-kilodalton polypeptides are encoded in chloroplast genes. Proc Natl Acad Sci 87(4):1531–1535PubMedPubMedCentralCrossRefGoogle Scholar
  92. Hu J, Troxler RF, Bogorad L (1991) Maize chloroplast RNA polymerase: the 78-kilodalton polypeptide is encoded by the plastid rpoC1 gene. Nucleic Acids Res 19(12):3431–3434PubMedPubMedCentralCrossRefGoogle Scholar
  93. Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422(6927):72PubMedCrossRefGoogle Scholar
  94. Huang Y, He L, Hu J et al (2015) Characterization and annotation of Babesia orientalis apicoplast genome. Parasites vectors 8(1):543PubMedPubMedCentralCrossRefGoogle Scholar
  95. Imura T, Sato S, Sato Y et al (2014) The apicoplast genome of Leucocytozoon caulleryi, a pathogenic apicomplexan parasite of the chicken. Parasitol Res 113(3):823–828PubMedCrossRefGoogle Scholar
  96. Janouškovec J, Tikhonenkov DV, Burki F et al (2015) Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc Natl Acad Sci 112(33):10200–10207PubMedPubMedCentralCrossRefGoogle Scholar
  97. Janouškovec J, Gavelis GS, Burki F et al (2017) Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proc Natl Acad Sci 114(2):E171–E180PubMedCrossRefGoogle Scholar
  98. Kamikawa R, Tanifuji G, Ishikawa SA et al (2015a) Proposal of a twin-arginine translocator system-mediated constraint against loss of ATP synthase genes from nonphotosynthetic plastid genomes. Mol Biol Evol 32:2598–2604PubMedCrossRefGoogle Scholar
  99. Kamikawa R, Yubuki N, Yoshida M et al (2015b) Multiple losses of photosynthesis in Nitzschia (Bacillariophyceae). Phycol Res 63(1):19–28CrossRefGoogle Scholar
  100. Kamikawa R, Moog D, Zauner S et al (2017) A non-photosynthetic diatom reveals early steps of reductive evolution in plastids. Mol Biol Evol 34(9):2355–2366Google Scholar
  101. Karnkowska A, Vacek V, Zubáčová Z et al (2016) A eukaryote without a mitochondrial organelle. Curr Biol 26(10):1274–1284PubMedCrossRefGoogle Scholar
  102. Katayama H, Ogihara Y (1996) Phylogenetic affinities of the grasses to other monocots as revealed by molecular analysis of chloroplast DNA. Curr Genet 29(6):572–581PubMedCrossRefGoogle Scholar
  103. Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607PubMedCrossRefGoogle Scholar
  104. Kikuchi S, Bédard J, Hirano M et al (2013) Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339(6119):571–574PubMedCrossRefGoogle Scholar
  105. Kleffmann T, Russenberger D, von Zychlinski A et al (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14(5):354–362PubMedCrossRefGoogle Scholar
  106. Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138PubMedCrossRefGoogle Scholar
  107. Klinger CM, Nisbet RE, Ouologuem DT, Roos DS, Dacks JB (2013) Cryptic organelle homology in apicomplexan parasites: insights from evolutionary cell biology. Curr Opin Microbiol 16(4):424–431PubMedPubMedCentralCrossRefGoogle Scholar
  108. Klinger CM, Karnkowska A, Herman EK, Hampl V, Dacks JB (2016) Phylogeny and evolution. In: Molecular parasitology. Springer, Vienna, pp 383–408CrossRefGoogle Scholar
  109. 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 Genom 267(4):492–497CrossRefGoogle Scholar
  110. Kohzuma K, Froehlich JE, Davis GA, Temple JA, Minhas D, Dhingra A, Cruz JA, Kramer DM (2017) The role of light–dark regulation of the chloroplast ATP synthase. Front Plant Sci 8:1248. doi: 10.3389/fpls.2017.01248 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Kong W, Yang J (2016) The complete chloroplast genome sequence of Morus mongolica and a comparative analysis within the Fabidae clade. Curr Genet 62:165–172. doi: 10.1007/s00294-015-0507-9 PubMedCrossRefGoogle Scholar
  112. Krajčovič J, Ebringer L, Schwartzbach SD (2002) Reversion of endosymbiosis? The case of bleaching in Euglena. In: Systems J, Seckbach (eds) Symbiosis: mechanism and model. Kluwer Academic Publishers, Dordrecht, pp 185–206Google Scholar
  113. Krajčovič J, Vesteg M, Schwartzbach SD (2015) Euglenoid flagellates: a multifaceted biotechnology platform. J Biotechnol 202:135–145PubMedCrossRefGoogle Scholar
  114. Krause K (2008) From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121PubMedCrossRefGoogle Scholar
  115. Ku C, Nelson-Sathi S, Roettger M et al (2015) Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes. Proc Natl Acad Sci 112(33):10139–10146PubMedPubMedCentralCrossRefGoogle Scholar
  116. Kugrens P, West JA (1973) The ultrastructure of an alloparasitic red alga Choreocolax polysiphoniae. Phycol 12(3–4):175–186CrossRefGoogle Scholar
  117. Lam VKY, Gomez MS, Graham SW (2015) The highly reduced plastome of mycoheterotrophis Sciaphila (Triuridaceae) is colinear with its green relatives and is under strong purifying selection. Genome Biol Evol 7:2220–2236PubMedPubMedCentralCrossRefGoogle Scholar
  118. Leger MM, Kolisko M, Kamikawa R et al (2017) Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes. Nat Ecol Evol 1:0092PubMedPubMedCentralCrossRefGoogle Scholar
  119. Li X, Zhang TC, Qiao Q et al (2013) Complete chloroplast genome sequence of holoparasite Cistanche deserticola (Orobanchaceae) reveals gene loss and horizontal gene transfer from its host Haloxylon ammodendron (Chenopodiaceae). PloS one 8(3):e58747PubMedPubMedCentralCrossRefGoogle Scholar
  120. Lim GS, Barrett CF, Pang CC, Davis JI (2016) Drastic reduction of plastome size in the mycoheterotrophic Thismia tentaculata relative to that of its autotrophic relative Tacca chantrieri. Am J Bot 103(6):1129–1137PubMedCrossRefGoogle Scholar
  121. Lister DL, Bateman JM, Purton S, Howe CJ (2003) DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316:33–38PubMedCrossRefGoogle Scholar
  122. Logacheva MD, Schelkunov MI, Penin AA (2011) Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol Evol 3:1296–1303PubMedPubMedCentralCrossRefGoogle Scholar
  123. Logacheva MD, Schelkunov MI, Nuraliev MS, Samigullin TH, Penin AA (2014) The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements. Genome Biol Evol 6(1):238–246PubMedPubMedCentralCrossRefGoogle Scholar
  124. Logacheva MD, Schelkunov MI, Shtratnikova VY, Matveeva MV, Penin AA (2016) Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives. Sci Rep 6:30042PubMedPubMedCentralCrossRefGoogle Scholar
  125. Lynch M, Marinov GK (2017) Membranes, energetics, and evolution across the prokaryote-eukaryote divide. eLife 6:e20437PubMedPubMedCentralCrossRefGoogle Scholar
  126. Mackiewicz P, Bodył A, Gagat P (2012) Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theory Biosci 131(1):1–18PubMedCrossRefGoogle Scholar
  127. Maier UG, Douglas SE, Cavalier-Smith T (2000) The nucleomorph genomes of cryptophytes and chlorarachniophytes. Protist 151(2):103–109PubMedCrossRefGoogle Scholar
  128. Maier UG, Zauner S, Hempel F (2015) Protein import into complex plastids: cellular organization of higher complexity. Eur J Cell Biol 94(7):340–348PubMedCrossRefGoogle Scholar
  129. Makiuchi T, Nozaki T (2014) Highly divergent mitochondrion-related organelles in anaerobic parasitic protozoa. Biochimie 100:3–17PubMedCrossRefGoogle Scholar
  130. Marin B (2004) Origin and fate of chloroplasts in the euglenoida. Protist 155:13–14PubMedCrossRefGoogle Scholar
  131. Marin B, Palm A, Klingberg M, Melkonian M (2003) Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparison and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154:99–145PubMedCrossRefGoogle Scholar
  132. Marin B, Nowack CM, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:425–432PubMedCrossRefGoogle Scholar
  133. Martin M, Sabater B (2010) Plastid ndh genes in plant evolution. Plant Physiol Biochem 48:636–645PubMedCrossRefGoogle Scholar
  134. Martin W, Stoebe B, Goremykin V et al (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165PubMedCrossRefGoogle Scholar
  135. Matsuzaki M, Kuroiwa H, Kuroiwa T, Kita K, Nozaki H (2008) A cryptic algal group unveiled: a plastid biosynthesis pathway in the oyster parasite Perkinsus marinus. Mol Biol Evol 25:1167–1179PubMedCrossRefGoogle Scholar
  136. McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37(6):951–959CrossRefGoogle Scholar
  137. McFadden GI, Yeh E (2017) The apicoplast: now you see it, now you don’t. Int J Parasitol 47(2):137–144PubMedCrossRefGoogle Scholar
  138. McNeal JR, Arumugunathan K, Kuehl JV, Boore JL, dePamphilis CV (2007) Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biol 5:55PubMedPubMedCentralCrossRefGoogle Scholar
  139. Merckx V, Freudenstein JV (2010) Evolution of mycoheterotrophy in plants: a phylogenetic perspective. New Phytol 185(3):605–609PubMedCrossRefGoogle Scholar
  140. Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604 (English translation In: Martin W, Kowallik KV (1999) Eur J Phycol 34:287–295)Google Scholar
  141. Miziorko HM, Lorimer GH (1983) Ribulose-1, 5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem 52(1):507–535PubMedCrossRefGoogle Scholar
  142. Molina J, Hazzouri KM, Nickrent D et al (2014) Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). Mol Biol Evol 31:793–803PubMedPubMedCentralCrossRefGoogle Scholar
  143. Moore CE, Archibald JM (2009) Nucleomorph genomes. Annu Rev Genet 43:251–264PubMedCrossRefGoogle Scholar
  144. Morse D, Salois P, Markovic P, Hastings JW (1995) A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268(5217):1622PubMedCrossRefGoogle Scholar
  145. Moustafa A, Reyes-Prieto A, Bhattacharya D (2008) Chlamydiae have contributed at least 55 genes to Plantae with predominantly plastid functions. PloS One 3:e2205PubMedPubMedCentralCrossRefGoogle Scholar
  146. Mukherjee A, Sadhukhan GC (2016) Anti-malarial drug design by targeting Apicoplasts: new perspectives. J Pharmacopunct 19(1):7CrossRefGoogle Scholar
  147. Müller M, Mentel M, van Hellemond JJ et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76(2):444–495PubMedPubMedCentralCrossRefGoogle Scholar
  148. Müllner AN, Angeler DG, Samuel R, Linton EW, Triemer RE (2001) Phylogenetic analysis of phagotrophic, phototrophic and osmotrophic euglenoids by using the nuclear 18S rDNA sequence. Int J Syst Evol Microbiol 51:783–791PubMedCrossRefGoogle Scholar
  149. Muñoz-Gómez SA, Mejía-Franco FG, Durnin K et al (2017) The new red algal subphylum Proteorhodophytina comprises the largest and most divergent plastid genomes known. Curr Biol 27(11):1677–1684Google Scholar
  150. Nakai M (2015a) The TIC complex uncovered: the alternative view on the molecular mechanism of protein translocation across the inner envelope membrane of chloroplasts. Biochim Biophys Acta Bioenerget 1847(9):957–967CrossRefGoogle Scholar
  151. Nakai M (2015b) YCF1: a green TIC: response to the de Vries et al. Commentary. Plant Cell 27:1834–1838PubMedPubMedCentralCrossRefGoogle Scholar
  152. Nass MMK, Nass S (1963) Intramitochondrial fibers with DNA characteristics. II. Enzymatic and other hydrolytic treatments. J Cell Biol 19:613–629PubMedPubMedCentralCrossRefGoogle Scholar
  153. Naumann J, Salomo K, Der JP et al (2013) Single-copy nuclear genes place haustorial Hydnoraceae within Piperales and reveal a cretaceous origin of multiple parasitic angiosperm lineages. PLoS One 8(11):e79204PubMedPubMedCentralCrossRefGoogle Scholar
  154. Naumann J, Der JP, Wafula EK et al (2016) Detecting and characterizing the highly divergent plastid genome of the nonphotosynthetic parasitic plant Hydnora visseri (Hydnoraceae). Genome Biol Evol 8(2):345–363PubMedPubMedCentralCrossRefGoogle Scholar
  155. Nowack EC (2014) Paulinella chromatophora-rethinking the transition from endosymbiont to organelle. Acta Societ Botanicorum Poloniae 83(4)Google Scholar
  156. Nowack EC, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci 109(14):5340–5345PubMedPubMedCentralCrossRefGoogle Scholar
  157. Nowack EC, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18(6):410–418PubMedCrossRefGoogle Scholar
  158. Oborník M, Green BR (2005) Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol 22:2343–2353PubMedCrossRefGoogle Scholar
  159. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7(7):957PubMedPubMedCentralCrossRefGoogle Scholar
  160. Parfrey LW, Lahr DJ, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci 108(33):13624–13629PubMedPubMedCentralCrossRefGoogle Scholar
  161. Petersen J, Ludewig AK, Michael V et al (2014) Chromera velia, endosymbioses and the rhodoplex hypothesis—plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol 6(3):666–684PubMedPubMedCentralCrossRefGoogle Scholar
  162. Pombert JF, Blouin NA, Lane C, Boucias D, Keeling PJ (2014) A lack of parasitic reduction in the obligate parasitic green alga Helicosporidium. PLoS Genet 10(5):e1004355PubMedPubMedCentralCrossRefGoogle Scholar
  163. Ponce-Toledo RI, Deschamps P, López-García P et al (2017) An early-branching freshwater cyanobacterium at the origin of plastids. Curr Biol 27(3):386–391PubMedPubMedCentralCrossRefGoogle Scholar
  164. Popot JL, de Vitry C (1990) On the microassembly of integral membrane proteins. Annu Rev Biophys Biophys Chem 19:369–403PubMedCrossRefGoogle Scholar
  165. Ralph SA, van Dooren G, Waller R et al (2004) Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2:203–216PubMedCrossRefGoogle Scholar
  166. Ris H, Plaut W (1962) Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 13:383–391PubMedPubMedCentralCrossRefGoogle Scholar
  167. Robledo JAF, Caler E, Matsuzaki M et al (2011) The search for the missing link: a relic plastid in Perkinsus? Int J Parasitol 41(12):1217–1229CrossRefGoogle Scholar
  168. Rockwell NC, Lagarias JC, Bhattacharya D (2014) Primary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes. Front Ecol Evol 2(66). doi: 10.3389/fevo.2014.00066
  169. Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell (3):539–553Google Scholar
  170. Ruiz-Nieto JE, Aguirre-Mancilla CL, Acosta-Gallegos JA et al (2015) Photosynthesis and chloroplast genes are involved in water-use efficiency in common bean. Plant Physiol Biochem 86:166–173PubMedCrossRefGoogle Scholar
  171. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14(3):225IN1–274IN6CrossRefGoogle Scholar
  172. Salomaki ED, Lane CE (2014) Are all red algal parasites cut from the same cloth? Acta Societ Botanicorum Poloniae 83(4):369–375CrossRefGoogle Scholar
  173. Salomaki ED, Nickles KR, Lane CE (2015) The ghost plastid of Choreocolax polysiphoniae. J Phycol 51(2):217–221PubMedCrossRefGoogle Scholar
  174. Samigullin TH, Logacheva MD, Penin AA, Vallejo-Roman CM (2016) Complete plastid genome of the recent holoparasite Lathraea squamaria reveals earliest stages of plastome reduction in Orobanchaceae. PLoS One 11:e0150718PubMedPubMedCentralCrossRefGoogle Scholar
  175. Sánchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF (2007) Plastid genes in a non-photosynthetic dinoflagellate. Protist 158:105–117PubMedCrossRefGoogle Scholar
  176. Sasaki Y, Nagano Y (2004) Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotech Biochem 68(6):1175–1184CrossRefGoogle Scholar
  177. Schelkunov MI, Shtratnikova VY, Nuraliev MS et al (2015) Exploring the limits for reduction of plastid genomes: a case study of the mycoheterotrophic orchids Epipogium aphyllum and Epipogium roseum. Genome Biol Evol 7:1179–1191PubMedPubMedCentralCrossRefGoogle Scholar
  178. Schleiff E, Becker T (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat Rev Mol Cell Biol 12(1):48–59PubMedCrossRefGoogle Scholar
  179. Schnepf E, Elbrächter M (1988) Cryptophycean-like double membrane-bound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: evolutionary, phylogenetic and toxicological implications. Plant Biol 101(2):96–203Google Scholar
  180. Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y (2004) Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432:779–782PubMedCrossRefGoogle Scholar
  181. Seeber F, Soldati-Favre D (2010) Metabolic pathways in the apicoplast of apicomplexa. Int Rev Cell Mol Biol 281:161–228PubMedCrossRefGoogle Scholar
  182. Sekiguchi H, Moriya M, Nakayama T, Inouye I (2002) Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyophyceae). Protist 153:157–167PubMedCrossRefGoogle Scholar
  183. Sheiner L, Striepen B (2013) Protein sorting in complex plastids. Biochim Biophys Acta (BBA) Mol Cell Res 1833(2):352–359CrossRefGoogle Scholar
  184. Shiina T, Tsunoyama Y, Nakahira Y, Khan MS (2005) Plastid RNA polymerases, promoters, and transcription regulators in higher plants. Int Rev Cytol 244:1–68PubMedCrossRefGoogle Scholar
  185. Sickmann A, Reinders J, Wagner Y et al (2003) The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci 100(23):13207–13212PubMedPubMedCentralCrossRefGoogle Scholar
  186. Slamovits CH, Keeling PJ (2008) Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Mol Biol Evol 25(7):1297–1306PubMedCrossRefGoogle Scholar
  187. Smith DR, Asmail SR (2014) Next-generation sequencing data suggest that certain nonphotosynthetic green plants have lost their plastid genomes. New Phytol 204:7–11PubMedCrossRefGoogle Scholar
  188. Smith DR, Lee RW (2014) A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol 164:1812–1819PubMedPubMedCentralCrossRefGoogle Scholar
  189. Smith AC, Purton S (2002) The transcriptional apparatus of plastids. Eur J Phycol 37:301–311CrossRefGoogle Scholar
  190. Smith DR, Hua J, Lee RW (2010) Evolution of linear mitochondrial DNA in three known lineages of Polytomella. Curr Genet 56:427–438PubMedCrossRefGoogle Scholar
  191. Smith DR, Crosby K, Lee RW (2011) Correlation between nuclear plastid DNA abundance and plastid number supports the limited transfer window hypothesis. Genome Biol Evol 3:365–371PubMedPubMedCentralCrossRefGoogle Scholar
  192. Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci 100(15):8828–8833PubMedPubMedCentralCrossRefGoogle Scholar
  193. Stelter K, El-Sayed NM, Seeber F (2007) The expression of a plant-type ferredoxin redox system provides molecular evidence for a plastid in the early dinoflagellate Perkinsus marinus. Protist 158:119–130PubMedCrossRefGoogle Scholar
  194. Stiller JW (2014) Toward an empirical framework for interpreting plastid evolution. J Phycol 50(3):462–471PubMedCrossRefGoogle Scholar
  195. Takishita K, Koike K, Maruyama T, Ogata T (2002) Molecular evidence for plastid robbery (Kleptoplastidy) in Dinophysis, a dinoflagellate causing diarrhetic shellfish poisoning. Protist 153:293–302PubMedCrossRefGoogle Scholar
  196. Tanifuji G, Onodera NT, Wheeler TJ et al (2011) Complete nucleomorph genome sequence of the nonphotosynthetic alga Cryptomonas paramecium reveals a core nucleomorph gene set. Genome Biol Evol 3:44–54PubMedCrossRefGoogle Scholar
  197. Teles-Grilo ML, Tato-Costa J, Duarte SM et al (2007) Is there a plastid in Perkinsus atlanticus (Phylum Perkinsozoa)? Eur J Protistol 43(2):163–167PubMedCrossRefGoogle Scholar
  198. Templeton TJ, Enomoto S, Chen W-J et al (2010) A genome-sequence survey for Ascogregarina taiwanensis supports evolutionary affiliation but metabolic diversity between a gregarine and Cryptosporidium. Mol Biol Evol 27:235–248PubMedCrossRefGoogle Scholar
  199. Tengs T, Dahlberg OJ, Shalchian-Tabrizi K et al (2000) Phylogenetic analyses indicate that the 19′ hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol 17(5):718–729PubMedCrossRefGoogle Scholar
  200. Terashima M, Specht M, Hippler M (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57(3):151–168PubMedCrossRefGoogle Scholar
  201. Toso MA, Omoto CK (2007) Gregarina niphandrodes may lack both a plastid genome and organelle. J Eukaryot Microbiol 54(1):66–72PubMedCrossRefGoogle Scholar
  202. Triemer RE, Linton E, Shin W et al (2006) Phylogeny of the Euglenales based upon combined SSU and LSU rDNA sequence comparisons and description of Discoplastis gen. nov. (Euglenophyta). J Phycol 42:731–740CrossRefGoogle Scholar
  203. Vernon D, Gutell RR, Cannone JJ, Rumpf RW, Birky CW (2001) Accelerated evolution of functional plastid rRNA and elongational factor genes due to reduced protein synthetic load after the loss of photosynthesis in the chlorophyte alga Polytoma. Mol Biol Evol 18:1810–1822PubMedCrossRefGoogle Scholar
  204. Vesteg M, Vacula R, Krajčovič J (2009) On the origin of chloroplasts, import mechanisms of chloroplast-targeted proteins, and loss of photosynthetic ability. Folia Microbiol 54:303–321CrossRefGoogle Scholar
  205. Waller RF, Keeling PJ, Donald RGK et al (1998) Nuclear encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Cell Biol 95:12352–12357Google Scholar
  206. Wallin IE (1927) Symbionticism and the origin of species. Bailliere, Tindall and Cox 171, LondonGoogle Scholar
  207. Watanabe MM, Suda S, Inouya I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. et sp. nov. (Gymnodinaiales, Dinophyta), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont. J Phycol 26(4):741–751CrossRefGoogle Scholar
  208. Whitney SM, Shaw DC, Yellowlees D (1995) Evidence that Some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the $\alpha $-proteobacteria. Proc R Soc Lond B Biol Sci 259(1356):271–275CrossRefGoogle Scholar
  209. Wicke S, Müller KF, dePamphilis CW, Quandt D, Wickett NJ, Zhang Y, Renner SS, Schneeweiss GM (2013) Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. Plant Cell 25:3711–3725PubMedPubMedCentralCrossRefGoogle Scholar
  210. Wicke S, Müller KF, Quandt D, Bellot S, Schneeweiss GM (2016) Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants. Proc Natl Acad Sci USA 113(32):9045–9050Google Scholar
  211. Wickett NJ, Zhang Y, Hansen SK et al (2008) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25:393–401PubMedCrossRefGoogle Scholar
  212. Williams BA, Keeling PJ (2003) Cryptic organelles in parasitic protists and fungi. Adv Parasitol 54:9–68PubMedCrossRefGoogle Scholar
  213. Wilson RJM (2004) Plastid functions in the Apicomplexa. Protist 155:11–12PubMedCrossRefGoogle Scholar
  214. Wilson RJM (2005) Parasite plastids: approaching the endgame. Biol Rev Camb Philos Soc 80:129–153PubMedCrossRefGoogle Scholar
  215. Wilson RJM, Williamson DH (1997) Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev 61:1–16PubMedPubMedCentralGoogle Scholar
  216. Wilson RJM, Denny PW, Preiser PR et al (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261:155–172PubMedCrossRefGoogle Scholar
  217. Wolfe A, de Pamphilis CW (1998) The effect of relaxed functional constraints on the photosynthetic gene rbcL in photosynthetic and nonphotosynthetic parasitic plants. Mol Biol Evol 15:1243–1258PubMedCrossRefGoogle Scholar
  218. Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652PubMedPubMedCentralCrossRefGoogle Scholar
  219. Yamada N, Sym SD, Horiguchi T (2017) Identification of highly divergent diatom-derived chloroplasts in dinoflagellates, including a description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae). Mol Biol Evol 34:1335–1351PubMedCrossRefGoogle Scholar
  220. Yan D, Wang Y, Murakami T et al (2015) Auxenochlorella protothecoides and Prototheca wickerhamii plastid genome sequences give insight into the origins of non-photosynthetic algae. Sci Rep 5:14465PubMedPubMedCentralCrossRefGoogle Scholar
  221. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447PubMedPubMedCentralCrossRefGoogle Scholar
  222. Yeh E, DeRisi JL (2011) Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol 9(8):e1001138PubMedPubMedCentralCrossRefGoogle Scholar
  223. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21(5):809–818PubMedCrossRefGoogle Scholar
  224. Yoon HS, Reyes-Prieto A, Melkonian M, Bhattacharya D (2006) Minimal plastid evolution in the Paulinella endosymbiont. Curr Biol 16:R670-R672CrossRefGoogle Scholar
  225. Yubuki N, Nakayama T, Inouye I (2008) A unique life cycle and perennation in a colorless chrysophyte Spumella sp. J Phycol 44(1):164–172PubMedCrossRefGoogle Scholar
  226. Záhonová K, Füssy Z, Oborník M, Eliáš M, Yurchenko V (2016) RuBisCO in non-photosynthetic alga Euglena longa: divergent features, transcriptomic analysis and regulation of complex formation. PLoS One 11(7):e0158790PubMedPubMedCentralCrossRefGoogle Scholar
  227. Zhu G, Marchewka MJ, Keithly JS (2000) Cryptosporidium parvum appears to lack a plastid genome. Microbiol 146:315–321CrossRefGoogle Scholar
  228. Zíková A, Hampl V, Paris Z, Týč J, Lukeš J (2016) Aerobic mitochondria of parasitic protists: diverse genomes and complex functions. Mol Biochem Parasitol 209(1):46–57PubMedCrossRefGoogle Scholar
  229. Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin 22C:38–48Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Lucia Hadariová
    • 1
  • Matej Vesteg
    • 2
  • Vladimír Hampl
    • 1
  • Juraj Krajčovič
    • 3
  1. 1.Department of Parasitology, Faculty of ScienceCharles UniversityPragueCzechia
  2. 2.Department of Biology and Ecology, Faculty of Natural SciencesMatej Bel UniversityBanská BystricaSlovakia
  3. 3.Department of Biology, Faculty of Natural SciencesUniversity of ss. Cyril and MethodiusTrnavaSlovakia

Personalised recommendations