Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

Paweł Mackiewicz, Przemysław Gagat

Abstract


One of the key evolutionary events on the scale of the biosphere was an endosymbiosis between a heterotrophic eukaryote and a cyanobacterium, resulting in a primary plastid. Such an organelle is characteristic of three eukaryotic lineages, glaucophytes, red algae and green plants. The three groups are usually united under the common name Archaeplastida or Plantae in modern taxonomic classifications, which indicates they are considered monophyletic. The methods generally used to verify this monophyly are phylogenetic analyses. In this article we review up-to-date results of such analyses and discussed their inconsistencies. Although phylogenies of plastid genes suggest a single primary endosymbiosis, which is assumed to mean a common origin of the Archaeplastida, different phylogenetic trees based on nuclear markers show monophyly, paraphyly, polyphyly or unresolved topologies of Archaeplastida hosts. The difficulties in reconstructing host cell relationships could result from stochastic and systematic biases in data sets, including different substitution rates and patterns, gene paralogy and horizontal/endosymbiotic gene transfer into eukaryotic lineages, which attract Archaeplastida in phylogenetic trees. Based on results to date, it is neither possible to confirm nor refute alternative evolutionary scenarios to a single primary endosymbiosis. Nevertheless, if trees supporting monophyly are considered, relationships inferred among Archaeplastida lineages can be discussed. Phylogenetic analyses based on nuclear genes clearly show the earlier divergence of glaucophytes from red algae and green plants. Plastid genes suggest a more complicated history, but at least some studies are congruent with this concept. Additional research involving more representatives of glaucophytes and many understudied lineages of Eukaryota can improve inferring phylogenetic relationships related to the Archaeplastida. In addition, alternative approaches not directly dependent on phylogenetic methods should be developed.

Keywords


Archaeplastida; Glaucophyta; monophyly; phylogenomics; phylogenetic analyses; primary plastid; Rhodophyta; Viridiplantae

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References


Delwiche CF, Timme RE. Plants. Curr Biol. 2011;21(11):R417–R422. http://dx.doi.org/10.1016/j.cub.2011.04.021

Schenk HE. Glaucocystophytes. In: Encyclopedia of life sciences. Chichester: John Wiley & Sons; 2001. http://dx.doi.org/10.1038/npg.els.0003061

Thomas DN. Seaweeds. London: Natural History Museum; 2002.

Lewis LA, McCourt RM. Green algae and the origin of land plants. Am J Bot. 2004;91(10):1535–1556. http://dx.doi.org/10.3732/ajb.91.10.1535

Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol. 2005;52(5):399–451. http://dx.doi.org/10.1111/j.1550-7408.2005.00053.x

Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, et al. The revised classification of eukaryotes. J Eukaryot Microbiol. 2012;59(5):429–514. http://dx.doi.org/10.1111/j.1550-7408.2012.00644.x

Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, et al. The tree of eukaryotes. Trends Ecol Evol. 2005;20(12):670–676. http://dx.doi.org/10.1016/j.tree.2005.09.005

Gould SB, Waller RF, McFadden GI. Plastid evolution. Ann Rev Plant Biol. 2008;59(1):491–517. http://dx.doi.org/10.1146/annurev.arplant.59.032607.092915

Keeling PJ. The endosymbiotic origin, diversification and fate of plastids. Phil Trans R Soc Lond B. 2010;365(1541):729–748. http://dx.doi.org/10.1098/rstb.2009.0103

Reyes-Prieto A, Weber APM, Bhattacharya D. The origin and establishment of the plastid in algae and plants. Annu Rev Genet. 2007;41(1):147–168. http://dx.doi.org/10.1146/annurev.genet.41.110306.130134

Stoebe B, Kowallik KV. Gene-cluster analysis in chloroplast genomics. Trends Genet. 1999;15(9):344–347. http://dx.doi.org/10.1016/S0168-9525(99)01815-6

Stoebe B, Martin W, Kowallik KV. Distribution and nomenclature of protein-coding genes in 12 sequenced chloroplast genomes. Plant Mol Biol Rep. 1998;16(3):243–255. http://dx.doi.org/10.1023/A:1007568326120

Besendahl A, Qiu YL, Lee J, Palmer JD, Bhattacharya D. The cyanobacterial origin and vertical transmission of the plastid tRNA(Leu) group-I intron. Curr Genet. 2000;37(1):12–23.

Pfanzagl B, Zenker A, Pittenauer E, Allmaier G, Martinez-Torrecuadrada J, Schmid ER, et al. Primary structure of cyanelle peptidoglycan of Cyanophora paradoxa: a prokaryotic cell wall as part of an organelle envelope. J Bacteriol. 1996;178(2):332–339.

Burey SC, Fathi-Nejad S, Poroyko V, Steiner JM, Löffelhardt W, Bohnert HJ. The central body of the cyanelles of Cyanophora paradoxa: a eukaryotic carboxysome? Can J Bot. 2005;83(7):758–764. http://dx.doi.org/10.1139/b05-060

Kies L, Kremer BP. Phylum Glaucocystophyta. In: Margulis L, editor. Handbook of protoctista. Boston, MA: Jones and Bartlett Publishers; 1990. p. 152–166.

Archibald JM. The puzzle of plastid evolution. Curr Biol. 2009;19(2):R81–R88. http://dx.doi.org/10.1016/j.cub.2008.11.067

Bodył A, Stiller JW, Mackiewicz P. Chromalveolate plastids: direct descent or multiple endosymbioses? Trends Ecol Evol. 2009;24(3):119–121. http://dx.doi.org/10.1016/j.tree.2008.11.003

Yusa F, Steiner JM, Loffelhardt W. Evolutionary conservation of dual Sec translocases in the cyanelles of Cyanophora paradoxa. BMC Evol Biol. 2008;8(1):304. http://dx.doi.org/10.1186/1471-2148-8-304

Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science. 2012;335(6070):843–847. http://dx.doi.org/10.1126/science.1213561

Chan CX, Gross J, Yoon HS, Bhattacharya D. Plastid origin and evolution: new models provide insights into old problems. Plant Physiol. 2011;155(4):1552–1560. http://dx.doi.org/10.1104/pp.111.173500

McFadden GI, van Dooren GG. Evolution: red algal genome affirms a common origin of all plastids. Curr Biol. 2004;14(13):R514–R516. http://dx.doi.org/10.1016/j.cub.2004.06.041

Reyes-Prieto A, Bhattacharya D. Phylogeny of Calvin cycle enzymes supports Plantae monophyly. Mol Phylogenet Evol. 2007;45(1):384–391. http://dx.doi.org/10.1016/j.ympev.2007.02.026

Cavalier-Smith T, Lee JJ. Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Eukaryot Microbiol. 1985;32(3):376–379. http://dx.doi.org/10.1111/j.1550-7408.1985.tb04031.x

Cavalier-Smith T. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 2000;5(4):174–182. http://dx.doi.org/10.1016/S1360-1385(00)01598-3

Cavalier-Smith T. The origins of plastids. Bot J Linn Soc. 1982;17(3):289–306. http://dx.doi.org/10.1111/j.1095-8312.1982.tb02023.x

Palmer JD. The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol. 2003;39(1):4–12. http://dx.doi.org/10.1046/j.1529-8817.2003.02185.x

Howe C, Barbrook A, Nisbet RE, Lockhart P, Larkum AW. The origin of plastids. Philos Trans R Soc Lond B Biol Sci. 2008;363(1504):2675–2685. http://dx.doi.org/10.1098/rstb.2008.0050

Nozaki H. A new scenario of plastid evolution: plastid primary endosymbiosis before the divergence of the “Plantae”, emended. J Plant Res. 2005;118(4):247–255. http://dx.doi.org/10.1007/s10265-005-0219-1

Larkum AWD, Lockhart PJ, Howe CJ. Shopping for plastids. Trends Plant Sci. 2007;12(5):189–195. http://dx.doi.org/10.1016/j.tplants.2007.03.011

Nozaki H, Maruyama S, Matsuzaki M, Nakada T, Kato S, Misawa K. Phylogenetic positions of Glaucophyta, green plants (Archaeplastida) and Haptophyta (Chromalveolata) as deduced from slowly evolving nuclear genes. Mol Phylogenet Evol. 2009;53(3):872–880. http://dx.doi.org/10.1016/j.ympev.2009.08.015

Stiller JW, Reel DC, Johnson JC. A single origin of plastids revisited: convergent evolution in organellar genome content. J Phycol. 2003;39(1):95–105. http://dx.doi.org/10.1046/j.1529-8817.2003.02070.x

Stiller JW, Hall BD. The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci USA. 1997;94(9):4520–4525.

Douglas SE, Turner S. Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. J Mol Evol. 1991;33(3):267–273. http://dx.doi.org/10.1007/BF02100678

Giovannoni SJ, Wood N, Huss V. Molecular phylogeny of oxygenic cells and organelles based on small-subunit ribosomal RNA sequences. In: Lewin RA, editor. Origins of plastids. New York, NY: Chapman and Hall; 1993. p. 159–170. http://dx.doi.org/10.1007/978-1-4615-2818-0_10

Olsen GJ, Woese CR, Overbeek R. The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol. 1994;176(1):1–6.

Marin B, Nowack EC, Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis. Protist. 2005;156(4):425–432. http://dx.doi.org/10.1016/j.protis.2005.09.001

Ochoa de Alda JAG, Esteban R, Diago ML, Houmard J. The plastid ancestor originated among one of the major cyanobacterial lineages. Nat Commun. 2014;5:4937. http://dx.doi.org/10.1038/ncomms5937

Delwiche C. Phylogenetic analysis of tufa sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol. 1995;4(2):110–128. http://dx.doi.org/10.1006/mpev.1995.1012

Morden CW, Delwiche CF, Kuhsel M, Palmer JD. Gene phylogenies and the endosymbiotic origin of plastids. Biosystems. 1992;28(1–3):75–90. http://dx.doi.org/10.1016/0303-2647(92)90010-V

Palmer JD, Delwiche CF. The origin and evolution of plastids and their genomes. In: Soltis DE, Soltis PS, Doyle JJ, editors. Molecular systematics of plants II. Boston, MA: Kluwer Academic Publishers; 1998. p. 375–409. http://dx.doi.org/10.1007/978-1-4615-5419-6_13

Ohta N, Sato N, Nozaki H, Kuroiwa T. Analysis of the cluster of ribosomal protein genes in the plastid genome of a unicellular red alga Cyanidioschyzon merolae: translocation of the str cluster as an early event in the rhodophyte-chromophyte lineage of plastid evolution. J Mol Evol. 1997;45(6):688–695. http://dx.doi.org/10.1007/PL00006273

Adachi J, Waddell PJ, Martin W, Hasegawa M. Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J Mol Evol. 2000;50(4):348–358.

Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol. 2004;21(5):809–818. http://dx.doi.org/10.1093/molbev/msh075

Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, et al. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol. 2005;15(14):1325–1330. http://dx.doi.org/10.1016/j.cub.2005.06.040

Deschamps P, Moreira D. Signal conflicts in the phylogeny of the primary photosynthetic eukaryotes. Mol Biol Evol. 2009;26(12):2745–2753. http://dx.doi.org/10.1093/molbev/msp189

Criscuolo A, Gribaldo S. Large-scale phylogenomic analyses indicate a deep origin of primary plastids within cyanobacteria. Mol Biol Evol. 2011;28(11):3019–3032. http://dx.doi.org/10.1093/molbev/msr108

Li B, Lopes JS, Foster PG, Embley TM, Cox CJ. Compositional biases among synonymous substitutions cause conflict between gene and protein trees for plastid origins. Mol Biol Evol. 2014;31(7):1697–1709. http://dx.doi.org/10.1093/molbev/msu105

Chu KH, Qi J, Yu ZG, Anh V. Origin and phylogeny of chloroplasts revealed by a simple correlation analysis of complete genomes. Mol Biol Evol. 2003;21(1):200–206. http://dx.doi.org/10.1093/molbev/msh002

Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA. 2013;110(3):1053–1058. http://dx.doi.org/10.1073/pnas.1217107110

Marin B, Nowack EC, Glöckner G, Melkonian M. The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like γ-proteobacterium. BMC Evol Biol. 2007;7(1):85. http://dx.doi.org/10.1186/1471-2148-7-85

Sogin ML. The phylogenetic significance of sequence diversity and length variations in eukaryotic small subunit ribosomal RNA coding regions. In: Warren L, Koprowski H, editors. New perspectives on evolution. New York, NY: Wiley-Liss; 1991. p. 175–188. (Wistar symposium series; vol 4).

Sogin ML, Elwood HJ, Gunderson JH. Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA. 1986;83(5):1383–1387.

Bhattacharya D, Medlin L. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J Phycol. 1995;31(4):489–498. http://dx.doi.org/10.1111/j.1529-8817.1995.tb02542.x

Bhattacharya D, Helmchen T, Bibeau C, Melkonian M. Comparisons of nuclear-encoded small-subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Mol Biol Evol. 1995;12(3):415–420.

van de Peer Y, Rensing SA, Maier UG, de Wachter R. Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc Natl Acad Sci USA. 1996;93(15):7732–7736.

van de Peer Y, de Wachter R. Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J Mol Evol. 1997;45(6):619–630.

van de Peer Y, Baldauf SL, Doolittle WF, Meyer A. An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol. 2000;51(6):565–576.

Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol. 2002;52(2):297–354.

Cavalier-Smith T. Only six kingdoms of life. Proc Biol Sci. 2004;271(1545):1251–1262. http://dx.doi.org/10.1098/rspb.2004.2705

Okamoto N, Inouye I. The katablepharids are a distant sister group of the Cryptophyta: a proposal for Katablepharidophyta divisio nova/kathablepharida phylum novum based on SSU rDNA and beta-tubulin phylogeny. Protist. 2005;156(2):163–179. http://dx.doi.org/10.1016/j.protis.2004.12.003

Cuvelier ML, Ortiz A, Kim E, Moehlig H, Richardson DE, Heidelberg JF, et al. Widespread distribution of a unique marine protistan lineage. Environ Microbiol. 2008;10(6):1621–1634. http://dx.doi.org/10.1111/j.1462-2920.2008.01580.x

Ishida K, Inagaki Y, Sakaguchi M, Oiwa A, Kai A, Suzuki M, et al. Comprehensive SSU rRNA phylogeny of eukaryota. Endocytobiosis Cell Res. 2010;20:81–88.

Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, Wilson WH, et al. Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science. 2011;332(6030):714–717. http://dx.doi.org/10.1126/science.1203163

Seenivasan R, Sausen N, Medlin LK, Melkonian M. Picomonas judraskeda gen. et sp. nov.: the first identified member of the Picozoa phylum nov., a widespread group of Picoeukaryotes, formerly known as “picobiliphytes”. PLoS ONE. 2013;8(3):e59565. http://dx.doi.org/10.1371/journal.pone.0059565

Moreira D, von der Heyden S, Bass D, López-García P, Chao E, Cavalier-Smith T. Global eukaryote phylogeny: combined small- and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol Phylogenet Evol. 2007;44(1):255–266. http://dx.doi.org/10.1016/j.ympev.2006.11.001

Zhao S, Burki F, Brate J, Keeling PJ, Klaveness D, Shalchian-Tabrizi K. Collodictyon – an ancient lineage in the tree of eukaryotes. Mol Biol Evol. 2012;29(6):1557–1568. http://dx.doi.org/10.1093/molbev/mss001

Yabuki A, Inagaki Y, Ishida K. Palpitomonas bilix gen. et sp. nov.: a novel deep-branching heterotroph possibly related to Archaeplastida or Hacrobia. Protist. 2010;161(4):523–538. http://dx.doi.org/10.1016/j.protis.2010.03.001

Kim E, Simpson AGB, Graham LE. Evolutionary relationships of apusomonads inferred from taxon-rich analyses of 6 nuclear encoded genes. Mol Biol Evol. 2006;23(12):2455–2466. http://dx.doi.org/10.1093/molbev/msl120

Bhattacharya D, Weber K. The actin gene of the glaucocystophyte Cyanophora paradoxa: analysis of the coding region and introns, and an actin phylogeny of eukaryotes. Curr Genet. 1997;31(5):439–446.

Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science. 2000;290(5493):972–977. http://dx.doi.org/10.1126/science.290.5493.972

Lartillot N. A bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol. 2004;21(6):1095–1109. http://dx.doi.org/10.1093/molbev/msh112

Rodríguez-Ezpeleta N, Brinkmann H, Roure B, Lartillot N, Lang BF, Philippe H. Detecting and overcoming systematic errors in genome-scale phylogenies. Syst Biol. 2007;56(3):389–399. http://dx.doi.org/10.1080/10635150701397643

Reeb VC, Peglar MT, Yoon HS, Bai JR, Wu M, Shiu P, et al. Interrelationships of chromalveolates within a broadly sampled tree of photosynthetic protists. Mol Phylogenet Evol. 2009;53(1):202–211. http://dx.doi.org/10.1016/j.ympev.2009.04.012

Nikolaev SI, Berney C, Fahrni JF, Bolivar I, Polet S, Mylnikov AP, et al. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc Natl Acad Sci USA. 2004;101(21):8066–8071. http://dx.doi.org/10.1073/pnas.0308602101

Yoon HS, Grant J, Tekle YI, Wu M, Chaon BC, Cole JC, et al. Broadly sampled multigene trees of eukaryotes. BMC Evol Biol. 2008;8(1):14. http://dx.doi.org/10.1186/1471-2148-8-14

Parfrey LW, Grant J, Tekle YI, Lasek-Nesselquist E, Morrison HG, Sogin ML, et al. Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Syst Biol. 2010;59(5):518–533. http://dx.doi.org/10.1093/sysbio/syq037

Kim E, Graham LE. EEF2 analysis challenges the monophyly of Archaeplastida and Chromalveolata. PLoS ONE. 2008;3(7):e2621. http://dx.doi.org/10.1371/journal.pone.0002621

Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AGB, et al. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci USA. 2009;106(10):3859–3864. http://dx.doi.org/10.1073/pnas.0807880106

Cavalier-Smith T, Chao EE, Snell EA, Berney C, Fiore-Donno AM, Lewis R. Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa. Mol Phylogenet Evol. 2014;81:71–85. http://dx.doi.org/10.1016/j.ympev.2014.08.012

Burki F, Okamoto N, Pombert JF, Keeling PJ. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc Biol Sci. 2012;279(1736):2246–2254. http://dx.doi.org/10.1098/rspb.2011.2301

Tekle YI, Grant J, Anderson OR, Nerad TA, Cole JC, Patterson DJ, et al. Phylogenetic placement of diverse amoebae inferred from multigene analyses and assessment of clade stability within “Amoebozoa” upon removal of varying rate classes of SSU-rDNA. Mol Phylogenet Evol. 2008;47(1):339–352. http://dx.doi.org/10.1016/j.ympev.2007.11.015

Nozaki H, Matsuzaki M, Takahara M, Misumi O, Kuroiwa H, Hasegawa M, et al. The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. J Mol Evol. 2003;56(4):485–497. http://dx.doi.org/10.1007/s00239-002-2419-9

Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rummele SE, Bhattacharya D. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol. 2007;24(8):1702–1713. http://dx.doi.org/10.1093/molbev/msm089

Burki F, Shalchian-Tabrizi K, Pawlowski J. Phylogenomics reveals a new “megagroup” including most photosynthetic eukaryotes. Biol Lett. 2008;4(4):366–369. http://dx.doi.org/10.1098/rsbl.2008.0224

Burki F, Inagaki Y, Brate J, Archibald JM, Keeling PJ, Cavalier-Smith T, et al. Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, telonemia and centroheliozoa, are related to photosynthetic chromalveolates. Genome Biol Evol. 2009;1:231–238. http://dx.doi.org/10.1093/gbe/evp022

Yabuki A, Kamikawa R, Ishikawa SA, Kolisko M, Kim E, Tanabe AS, et al. Palpitomonas bilix represents a basal cryptist lineage: insight into the character evolution in Cryptista. Sci Rep. 2014;4:4641. http://dx.doi.org/10.1038/srep04641

Zhao S, Shalchian-Tabrizi K, Klaveness D. Sulcozoa revealed as a paraphyletic group in mitochondrial phylogenomics. Mol Phylogenet Evol. 2013;69(3):462–468. http://dx.doi.org/10.1016/j.ympev.2013.08.005

Jackson CJ, Reyes-Prieto A. The mitochondrial genomes of the Glaucophytes Gloeochaete wittrockiana and Cyanoptyche gloeocystis: multilocus phylogenetics suggests a monophyletic archaeplastida. Genome Biol Evol. 2014;6(10):2774–2785. http://dx.doi.org/10.1093/gbe/evu218

Stiller JW, Riley J, Hall BD. Are red algae plants? A critical evaluation of three key molecular data sets. J Mol Evol. 2001;52(6):527–539. http://dx.doi.org/10.1007/s002390010183

Roger AJ, Hug LA. The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Philos Trans R Soc Lond B Biol Sci. 2006;361(1470):1039–1054. http://dx.doi.org/10.1098/rstb.2006.1845

Delsuc F, Brinkmann H, Philippe H. Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet. 2005;6(5):361–375. http://dx.doi.org/10.1038/nrg1603

Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang BF, Simpson AGB, et al. Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc Biol Sci. 2013;280(1769):20131755. http://dx.doi.org/10.1098/rspb.2013.1755

Felsenstein J. Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool. 1978;27(4):401. http://dx.doi.org/10.2307/2412923

Stiller JW, Harrell L. The largest subunit of RNA polymerase II from the Glaucocystophyta: functional constraint and short-branch exclusion in deep eukaryotic phylogeny. BMC Evol Biol. 2005;5(1):71. http://dx.doi.org/10.1186/1471-2148-5-71

Roure B, Baurain D, Philippe H. Impact of missing data on phylogenies inferred from empirical phylogenomic data sets. Mol Biol Evol. 2013;30(1):197–214. http://dx.doi.org/10.1093/molbev/mss208

Philippe H, Snell EA, Bapteste E, Lopez P, Holland PW, Casane D. Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol Biol Evol. 2004;21(9):1740–1752. http://dx.doi.org/10.1093/molbev/msh182

Nozaki H, Iseki M, Hasegawa M, Misawa K, Nakada T, Sasaki N, et al. Phylogeny of primary photosynthetic eukaryotes as deduced from slowly evolving nuclear genes. Mol Biol Evol. 2007;24(8):1592–1595. http://dx.doi.org/10.1093/molbev/msm091

Inagaki Y, Nakajima Y, Sato M, Sakaguchi M, Hashimoto T. Gene sampling can bias multi-gene phylogenetic inferences: the relationship between red algae and green plants as a case study. Mol Biol Evol. 2009;26(5):1171–1178. http://dx.doi.org/10.1093/molbev/msp036

Brinkmann H, van der Giezen M, Zhou Y, de Raucourt GP, Philippe H. An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Syst Biol. 2005;54(5):743–757. http://dx.doi.org/10.1080/10635150500234609

Susko E, Roger AJ. On reduced amino acid alphabets for phylogenetic inference. Mol Biol Evol. 2007;24(9):2139–2150. http://dx.doi.org/10.1093/molbev/msm144

Tuffley C, Steel M. Modeling the covarion hypothesis of nucleotide substitution. Math Biosci. 1998;147(1):63–91. http://dx.doi.org/10.1016/S0025-5564(97)00081-3

Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, et al. Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol. 2011;21(4):328–333. http://dx.doi.org/10.1016/j.cub.2011.01.037

Maddison WP. Gene trees in species trees. Syst Biol. 1997;46(3):523–536. http://dx.doi.org/10.1093/sysbio/46.3.523

Page R. From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Mol Phylogenet Evol. 1997;7(2):231–240. http://dx.doi.org/10.1006/mpev.1996.0390

Chan CX, Bhattacharya D. Analysis of horizontal genetic transfer in red algae in the post-genomics age. Mob Genet Elem. 2013;3(6):e27669. http://dx.doi.org/10.4161/mge.27669

Chan CX, Bhattacharya D, Reyes-Prieto A. Endosymbiotic and horizontal gene transfer in microbial eukaryotes: impacts on cell evolution and the tree of life. Mob Genet Elem. 2012;2(2):101–105. http://dx.doi.org/10.4161/mge.20110

Huang J, Yue J. Horizontal gene transfer in the evolution of photosynthetic eukaryotes: HGT in plants. J Syst Evol. 2013;51(1):13–29. http://dx.doi.org/10.1111/j.1759-6831.2012.00237.x

Schönknecht G, Weber APM, Lercher MJ. Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays. 2014;36(1):9–20. http://dx.doi.org/10.1002/bies.201300095

Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 2008;9(8):605–618. http://dx.doi.org/10.1038/nrg2386

Keeling PJ. Role of horizontal gene transfer in the evolution of photosynthetic eukaryotes and their plastids. In: Gogarten MB, Gogarten JP, Olendzenski LC, editors. Horizontal gene transfer. Totowa, NJ: Humana Press; 2009. p. 501–515. (vol 532). http://dx.doi.org/10.1007/978-1-60327-853-9_29

Richardson AO, Palmer JD. Horizontal gene transfer in plants. J Exp Bot. 2006;58(1):1–9. http://dx.doi.org/10.1093/jxb/erl148

Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA. 2004;101(51):17747–17752. http://dx.doi.org/10.1073/pnas.0408336102

Bergthorsson U, Adams KL, Thomason B, Palmer JD. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature. 2003;424(6945):197–201. http://dx.doi.org/10.1038/nature01743

Woloszynska M, Bocer T, Mackiewicz P, Janska H. A fragment of chloroplast DNA was transferred horizontally, probably from non-eudicots, to mitochondrial genome of Phaseolus. Plant Mol Biol. 2004;56(5):811–820. http://dx.doi.org/10.1007/s11103-004-5183-y

Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 2004;5(2):123–135. http://dx.doi.org/10.1038/nrg1271

Kleine T, Maier UG, Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol. 2009;60(1):115–138. http://dx.doi.org/10.1146/annurev.arplant.043008.092119

Lane CE, Archibald JM. The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol Evol. 2008;23(5):268–275. http://dx.doi.org/10.1016/j.tree.2008.02.004

Leigh JW, Susko E, Baumgartner M, Roger AJ. Testing congruence in phylogenomic analysis. Syst Biol. 2008;57(1):104–115. http://dx.doi.org/10.1080/10635150801910436

Stiller JW. Experimental design and statistical rigor in phylogenomics of horizontal and endosymbiotic gene transfer. BMC Evol Biol. 2011;11(1):259. http://dx.doi.org/10.1186/1471-2148-11-259

Andersson JO, Roger AJ. A cyanobacterial gene in nonphotosynthetic protists – an early chloroplast acquisition in eukaryotes? Curr Biol. 2002;12(2):115–119.

Cavalier-Smith T. The origin, losses and gains of chloroplasts. In: Lewin RA, editor. Origins of plastids. New York, NY: Chapman and Hall; 1993. p. 291–348.

Dorrell RG, Smith AG. Do red and green make brown?: perspectives on plastid acquisitions within chromalveolates. Eukaryot Cell. 2011;10(7):856–868. http://dx.doi.org/10.1128/EC.00326-10

Vesteg M, Vacula R, Krajčovič J. On the origin of chloroplasts, import mechanisms of chloroplast-targeted proteins, and loss of photosynthetic ability – review. Folia Microbiol Praha. 2009;54(4):303–321. http://dx.doi.org/10.1007/s12223-009-0048-z

Krause K. From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet. 2008;54(3):111–121. http://dx.doi.org/10.1007/s00294-008-0208-8

Borza T, Popescu CE, Lee RW. Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryot Cell. 2005;4(2):253–261. http://dx.doi.org/10.1128/EC.4.2.253-261.2005

Mazumdar J, Wilson EH, Masek K, Hunter CA, Striepen B. Apicoplast fatty acid synthesis is essential for organelle biogenesis and parasite survival in Toxoplasma gondii. Proc Natl Acad Sci USA. 2006;103(35):13192–13197. http://dx.doi.org/10.1073/pnas.0603391103

Bodył A, Mackiewicz P, Gagat P. Organelle evolution: Paulinella breaks a paradigm. Curr Biol. 2012;22(9):R304–R306. http://dx.doi.org/10.1016/j.cub.2012.03.020

Gagat P, Bodył A, Mackiewicz P, Stiller JW. Tertiary plastid endosymbioses in dinoflagellates. In: Löffelhardt W, editor. Endosymbiosis. Vienna: Springer; 2014. p. 233–290. http://dx.doi.org/10.1007/978-3-7091-1303-5_13

Kies L, Kremer BP. Function of cyanelles in the tecamoeba Paulinella chromatophora. Naturewissenschaften. 1979;66:578–579.

Bodył A, Mackiewicz P, Stiller JW. The intracellular cyanobacteria of Paulinella chromatophora: endosymbionts or organelles? Trends Microbiol. 2007;15(7):295–296. http://dx.doi.org/10.1016/j.tim.2007.05.002

Nowack ECM, Melkonian M, Glöckner G. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol. 2008;18(6):410–418. http://dx.doi.org/10.1016/j.cub.2008.02.051

Reyes-Prieto A, Yoon HS, Moustafa A, Yang EC, Andersen RA, Boo SM, et al. Differential gene retention in plastids of common recent origin. Mol Biol Evol. 2010;27(7):1530–1537. http://dx.doi.org/10.1093/molbev/msq032

Nowack ECM, Vogel H, Groth M, Grossman AR, Melkonian M, Glockner G. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol Biol Evol. 2011;28(1):407–422. http://dx.doi.org/10.1093/molbev/msq209

Nakayama T, Ishida K. Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr Biol. 2009;19(7):R284–R285. http://dx.doi.org/10.1016/j.cub.2009.02.043

Nowack ECM, Grossman AR. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci USA. 2012;109(14):5340–5345. http://dx.doi.org/10.1073/pnas.1118800109

Mackiewicz P, Bodył A, Gagat P. Protein import into the photosynthetic organelles of Paulinella chromatophora and its implications for primary plastid endosymbiosis. Symbiosis. 2012;58(1–3):99–107. http://dx.doi.org/10.1007/s13199-012-0202-2

Mackiewicz P, Bodył A, Gagat P. Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora. Theory Biosci. 2012;131(1):1–18. http://dx.doi.org/10.1007/s12064-011-0147-7

Bodył A, Mackiewicz P, Stiller JW. Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol. 2009;12:639–649. http://dx.doi.org/10.1111/j.1438-8677.2009.00264.x

Carpenter EJ, Foster RA. Marine cyanobacterial symbioses. In: Rai AN, Bergman B, Rasmussen U, editors. Cyanobacteria in symbiosis. Dordrecht: Kluwer Academic Publishers; 2002. p. 11–17. http://dx.doi.org/10.1007/0-306-48005-0_2

Raven JA. Evolution of cyanobacterial symbioses. In: Rai AN, Bergman B, Rasmussen U, editors. Cyanobacteria in symbiosis. Dordrecht: Kluwer Academic Publishers; 2002. p. 329–346. http://dx.doi.org/10.1007/0-306-48005-0_16

Kneip C, Lockhart P, Voß C, Maier UG. Nitrogen fixation in eukaryotes – new models for symbiosis. BMC Evol Biol. 2007;7(1):55. http://dx.doi.org/10.1186/1471-2148-7-55

Kneip C, Voβ C, Lockhart PJ, Maier UG. The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution. BMC Evol Biol. 2008;8(1):30. http://dx.doi.org/10.1186/1471-2148-8-30

Rogers M, Keeling PJ. Lateral transfer and recompartmentalization of Calvin cycle enzymes of plants and algae. J Mol Evol. 2004;58(4):367–375. http://dx.doi.org/10.1007/s00239-003-2558-7

Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E, Green BR. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J Mol Evol. 1999;48(1):59–68.

Rissler HM, Durnford DG. Isolation of a novel carotenoid-rich protein in Cyanophora paradoxa that is immunologically related to the light-harvesting complexes of photosynthetic eukaryotes. Plant Cell Physiol. 2005;46(3):416–424. http://dx.doi.org/10.1093/pcp/pci054

Plancke C, Colleoni C, Deschamps P, Dauvillee D, Nakamura Y, Haebel S, et al. Pathway of cytosolic starch synthesis in the model glaucophyte Cyanophora paradoxa. Eukaryot Cell. 2008;7(2):247–257. http://dx.doi.org/10.1128/EC.00373-07

Deschamps P, Haferkamp I, d’Hulst C, Neuhaus HE, Ball SG. The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci. 2008;13(11):574–582. http://dx.doi.org/10.1016/j.tplants.2008.08.009

Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buleon A, et al. Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol. 2008;25(3):536–548. http://dx.doi.org/10.1093/molbev/msm280

Ball S, Colleoni C, Cenci U, Raj JN, Tirtiaux C. The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot. 2011;62(6):1775–1801. http://dx.doi.org/10.1093/jxb/erq411

Cavalier-Smith T. Eukaryote kingdoms: seven or nine? Biosystems. 1981;14(3–4):461–481.

Delwiche CF, Palmer JD. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol. 1996;13(6):873–882.

Shibata M, Kashino Y, Satoh K, Koike H. Isolation and characterization of oxygen-evolving thylakoid membranes and photosystem II particles from a glaucocystophyte, Cyanophora paradoxa. Plant Cell Physiol. 2001;42(7):733–741. http://dx.doi.org/10.1093/pcp/pce092

Koike H, Shibata M, Yasutomi K, Kashino Y, Satoh K. Identification of photosystem I components from a glaucocystophyte, Cyanophora paradoxa: the PsaD protein has an N-terminal stretch homologous to higher plants. Photosynth Res. 2000;65(3):207–217. http://dx.doi.org/10.1023/A:1010734912776

Machida M, Takechi K, Sato H, Chung SJ, Kuroiwa H, Takio S, et al. Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc Natl Acad Sci USA. 2006;103(17):6753–6758. http://dx.doi.org/10.1073/pnas.0510693103

Takano H, Takechi K. Plastid peptidoglycan. Biochim Biophys Acta. 2010;1800(2):144–151. http://dx.doi.org/10.1016/j.bbagen.2009.07.020

Lockhart PJ, Howe CJ, Bryant DA, Beanland TJ, Larkum AWD. Substitutional bias confounds inference of cyanelle origins from sequence data. J Mol Evol. 1992;34(2):153–162. http://dx.doi.org/10.1007/BF00182392

Lockhart PJ, Penny D, Hendy MD, Howe CJ, Beanland TJ, Larkum AWD. Controversy on chloroplast origins. FEBS Lett. 1992;301(2):127–131. http://dx.doi.org/10.1016/0014-5793(92)81231-A

Okamoto N, Chantangsi C, Horák A, Leander BS, Keeling PJ. Molecular phylogeny and description of the novel katablepharid Roombia truncata gen. et sp. nov., and establishment of the hacrobia taxon nov. PLoS ONE. 2009;4(9):e7080. http://dx.doi.org/10.1371/journal.pone.0007080

Burki F, Shalchian-Tabrizi K, Minge M, Skjæveland Å, Nikolaev SI, Jakobsen KS, et al. Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE. 2007;2(8):e790. http://dx.doi.org/10.1371/journal.pone.0000790

Turner S, Pryer KM, Miao VP, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol. 1999;46(4):327–338.

Reyes-Prieto A, Bhattacharya D. Phylogeny of nuclear-encoded plastid-targeted proteins supports an early divergence of glaucophytes within Plantae. Mol Biol Evol. 2007;24(11):2358–2361. http://dx.doi.org/10.1093/molbev/msm186

Qiu H, Yang EC, Bhattacharya D, Yoon HS. Ancient gene paralogy may mislead inference of plastid phylogeny. Mol Biol Evol. 2012;29(11):3333–3343. http://dx.doi.org/10.1093/molbev/mss137

Helmchen TA, Bhattacharya D, Melkonian M. Analyses of ribosomal RNA sequences from glaucocystophyte cyanelles provide new insights into the evolutionary relationships of plastids. J Mol Evol. 1995;41(2):203–210.

Yoon HS, Hackett JD, van Dolah FM, Nosenko T, Lidie KL, Bhattacharya D. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol Biol Evol. 2005;22(5):1299–1308. http://dx.doi.org/10.1093/molbev/msi118

Yoon HS, Nakayama T, Reyes-Prieto A, Andersen RA, Boo SM, Ishida K, et al. A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol Biol. 2009;9(1):98. http://dx.doi.org/10.1186/1471-2148-9-98

Falcón LI, Magallón S, Castillo A. Dating the cyanobacterial ancestor of the chloroplast. ISME J. 2010;4(6):777–783. http://dx.doi.org/10.1038/ismej.2010.2

Auch AF, Henz SR, Holland BR, Göker M. Genome BLAST distance phylogenies inferred from whole plastid and whole mitochondrion genome sequences. BMC Bioinformatics. 2006;7(1):350. http://dx.doi.org/10.1186/1471-2105-7-350

Nozaki H, Ohta N, Matsuzaki M, Misumi O, Kuroiwa T. Phylogeny of plastids based on cladistic analysis of gene loss inferred from complete plastid genome sequences. J Mol Evol. 2003;57(4):377–382. http://dx.doi.org/10.1007/s00239-003-2486-6

Sanchez-Puerta MV, Bachvaroff TR, Delwiche CF. Sorting wheat from chaff in multi-gene analyses of chlorophyll c-containing plastids. Mol Phylogenet Evol. 2007;44(2):885–897. http://dx.doi.org/10.1016/j.ympev.2007.03.003

de Las Rivas J. Comparative analysis of chloroplast genomes: functional annotation, genome-based phylogeny, and deduced evolutionary patterns. Genome Res. 2002;12(4):567–583. http://dx.doi.org/10.1101/gr.209402

Rodríguez-Ezpeleta N, Brinkmann H, Burger G, Roger AJ, Gray MW, Philippe H, et al. Toward resolving the eukaryotic tree: the phylogenetic positions of jakobids and cercozoans. Curr Biol. 2007;17(16):1420–1425. http://dx.doi.org/10.1016/j.cub.2007.07.036

Lopez P, Casane D, Philippe H. Heterotachy, an important process of protein evolution. Mol Biol Evol. 2002;19(1):1–7.

Vogl C, Badger J, Kearney P, Li M, Clegg M, Jiang T. Probabilistic analysis indicates discordant gene trees in chloroplast evolution. J Mol Evol. 2003;56(3):330–340. http://dx.doi.org/10.1007/s00239-002-2404-3

Ane C. Covarion structure in plastid genome evolution: a new statistical test. Mol Biol Evol. 2005;22(4):914–924. http://dx.doi.org/10.1093/molbev/msi076

Whelan S, Blackburne BP, Spencer M. Phylogenetic substitution models for detecting heterotachy during plastid evolution. Mol Biol Evol. 2011;28(1):449–458. http://dx.doi.org/10.1093/molbev/msq215

Lockhart PJ, Steel MA, Barbrook AC, Huson DH, Charleston MA, Howe CJ. A covariotide model explains apparent phylogenetic structure of oxygenic photosynthetic lineages. Mol Biol Evol. 1998;15(9):1183–1188.

Lockhart P, Steel M. A tale of two processes. Syst Biol. 2005;54(6):948–951. http://dx.doi.org/10.1080/10635150500234682

Lockhart P. Heterotachy and tree building: a case study with plastids and eubacteria. Mol Biol Evol. 2005;23(1):40–45. http://dx.doi.org/10.1093/molbev/msj005

Rice DW, Palmer JD. An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol. 2006;4(1):31. http://dx.doi.org/10.1186/1741-7007-4-31

Mackiewicz P, Bodył A, Moszczyński K. The case of horizontal gene transfer from bacteria to the peculiar dinoflagellate plastid genome. Mob Genet Elem. 2013;3(4):e25845. http://dx.doi.org/10.4161/mge.25845

Moszczynski K, Mackiewicz P, Bodyl A. Evidence for horizontal gene transfer from bacteroidetes bacteria to dinoflagellate minicircles. Mol Biol Evol. 2012;29(3):887–892. http://dx.doi.org/10.1093/molbev/msr276

Bachvaroff TR, Sanchez-Puerta MV, Delwiche CF. Chlorophyll c-containing plastid relationships based on analyses of a multigene data set with all four chromalveolate lineages. Mol Biol Evol. 2005;22(9):1772–1782. http://dx.doi.org/10.1093/molbev/msi172

Cuvelier ML, Allen AE, Monier A, McCrow JP, Messie M, Tringe SG, et al. Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc Natl Acad Sci USA. 2010;107(33):14679–14684. http://dx.doi.org/10.1073/pnas.1001665107

Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, de Oliveira MC. 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. 2004;59(4):464–477. http://dx.doi.org/10.1007/s00239-004-2638-3

Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA. 2010;107(24):10949–10954. http://dx.doi.org/10.1073/pnas.1003335107

Janouškovec J, Horák A, Barott KL, Rohwer FL, Keeling PJ. Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr Biol. 2012;22(13):R518–R519. http://dx.doi.org/10.1016/j.cub.2012.04.047

Khan H, Parks N, Kozera C, Curtis BA, Parsons BJ, Bowman S, et al. 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. 2007;24(8):1832–1842. http://dx.doi.org/10.1093/molbev/msm101

Kim E, Harrison JW, Sudek S, Jones MDM, Wilcox HM, Richards TA, et al. Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life. Proc Natl Acad Sci USA. 2011;108(4):1496–1500. http://dx.doi.org/10.1073/pnas.1013337108

Le Corguillé G, Pearson G, Valente M, Viegas C, Gschloessl B, Corre E, et al. Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol. 2009;9(1):253. http://dx.doi.org/10.1186/1471-2148-9-253

Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. 1998;393(6681):162–165. http://dx.doi.org/10.1038/30234

Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, et al. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA. 2002;99(19):12246–12251. http://dx.doi.org/10.1073/pnas.182432999

Nelissen B, van de Peer Y, Wilmotte A, de Wachter R. An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. Mol Biol Evol. 1995;12(6):1166–1173.

Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, et al. Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 2003;10(2):67–77. http://dx.doi.org/10.1093/dnares/10.2.67

Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ. The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol. 2007;24(1):54–62. http://dx.doi.org/10.1093/molbev/msl129

Sato N. Origin and evolution of plastids: genomic view on the unification and diversity of plastids. In: Wise RR, Hoober JK, editors. The structure and function of plastids. Dordrecht: Springer; 2006. p. 75–102. (Advances in photosynthesis and respiration). http://dx.doi.org/10.1007/978-1-4020-4061-0_4

Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF, et al. Phylogenetic analyses indicate that the 19’Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol. 2000;17(5):718–729.

Wang Y, Joly S, Morse D. Phylogeny of dinoflagellate plastid genes recently transferred to the nucleus supports a common ancestry with red algal plastid genes. J Mol Evol. 2008;66(2):175–184. http://dx.doi.org/10.1007/s00239-008-9070-z

Baurain D, Brinkmann H, Petersen J, Rodriguez-Ezpeleta N, Stechmann A, Demoulin V, et al. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol. 2010;27(7):1698–1709. http://dx.doi.org/10.1093/molbev/msq059

Minge MA, Silberman JD, Orr RJ, Cavalier-Smith T, Shalchian-Tabrizi K, Burki F, et al. Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proc Biol Sci. 2009;276(1657):597–604. http://dx.doi.org/10.1098/rspb.2008.1358

Moreira D, Le Guyader H, Philippe H. The origin of red algae and the evolution of chloroplasts. Nature. 2000;405(6782):69–72. http://dx.doi.org/10.1038/35011054

Patron NJ, Inagaki Y, Keeling PJ. Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr Biol. 2007;17(10):887–891. http://dx.doi.org/10.1016/j.cub.2007.03.069

Tekle YI, Grant J, Cole JC, Nerad TA, Anderson OR, Patterson DJ, et al. A multigene analysis of Corallomyxa tenera sp. nov. suggests its membership in a clade that includes Gromia, Haplosporidia and Foraminifera. Protist. 2007;158(4):457–472. http://dx.doi.org/10.1016/j.protis.2007.05.002

Tekle YI, Parfrey LW, Katz LA. Molecular data are transforming hypotheses on the origin and diversification of eukaryotes. Bioscience. 2009;59(6):471–481. http://dx.doi.org/10.1525/bio.2009.59.6.5




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