The Glaucophyta: the blue-green plants in a nutshell

Christopher Jackson, Susan Clayden, Adrian Reyes-Prieto

Abstract


The Glaucophyta is one of the three major lineages of photosynthetic eukaryotes, together with viridiplants and red algae, united in the presumed monophyletic supergroup Archaeplastida. Glaucophytes constitute a key algal lineage to investigate both the origin of primary plastids and the evolution of algae and plants. Glaucophyte plastids possess exceptional characteristics retained from their cyanobacterial ancestor: phycobilisome antennas, a vestigial peptidoglycan wall, and carboxysome-like bodies. These latter two traits are unique among the Archaeplastida and have been suggested as evidence that the glaucophytes diverged earliest during the diversification of this supergroup. Our knowledge of glaucophytes is limited compared to viridiplants and red algae, and this has restricted our capacity to untangle the early evolution of the Archaeplastida. However, in recent years novel genomic and functional data are increasing our understanding of glaucophyte biology. Diverse comparative studies using information from the nuclear genome of Cyanophora paradoxa and recent transcriptomic data from other glaucophyte species provide support for the common origin of Archaeplastida. Molecular and ultrastructural studies have revealed previously unrecognized diversity in the genera Cyanophora and Glaucocystis. Overall, a series of recent findings are modifying our perspective of glaucophyte diversity and providing fresh approaches to investigate the basic biology of this rare algal group in detail.

Keywords


Glaucophyta; Cyanophora; Archaeplastida; primary plastids; cyanelle

Full Text:

PDF

References


Skuja H. Glaucophyta. In: Melchior H, Werdermann E, editors. A. Engler’s Syllabus der Pflanzenfamilien. Berlin: Borntraeger; 1954. p. 56–57.

Kies L, Kremer BP. Typification of the Glaucocystophyta. Taxon. 1986;35(1):128–133. http://dx.doi.org/10.2307/1221049

Cavalier-Smith T. Eukaryote kingdoms: seven or nine? Biosystems. 1981;14(3–4):461–481. http://dx.doi.org/10.1016/0303-2647(81)90050-2

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

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

Burki F, Inagaki Y, Bråte 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

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

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

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

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

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

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. Plastid endosymbiosis, genome evolution and the origin of green plants. Trends Plant Sci. 2007;12(9):391–396. http://dx.doi.org/10.1016/j.tplants.2007.08.002

Parfrey LW, Barbero E, Lasser E, Dunthorn M, Bhattacharya D, Patterson DJ, et al. Evaluating support for the current classification of eukaryotic diversity. PLoS Genet. 2006;2(12):e220. http://dx.doi.org/10.1371/journal.pgen.0020220

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

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

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

Mackiewicz P, Gagat P. Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus? Acta Soc Bot Pol. 2014;83(4):263–280. http://dx.doi.org/10.5586/asbp.2014.044

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

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

Ball SG, Subtil A, Bhattacharya D, Moustafa A, Weber APM, Gehre L, et al. Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell. 2013;25(1):7–21. http://dx.doi.org/10.1105/tpc.112.101329

Elias M. The guanine nucleotide exchange factors Sec2 and PRONE: candidate synapomorphies for the Opisthokonta and the Archaeplastida. Mol Biol Evol. 2008;25(8):1526–1529. http://dx.doi.org/10.1093/molbev/msn113

Cavalier-Smith T. The origins of plastids. Biol 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

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

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

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

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

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

Reyes-Prieto A, Moustafa A. Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterial enzymes. Sci Rep. 2012;2:955. http://dx.doi.org/10.1038/srep00955

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

Steiner JM, Yusa F, Pompe JA, Löffelhardt W. Homologous protein import machineries in chloroplasts and cyanelles. Plant J. 2005;44(4):646–652. http://dx.doi.org/10.1111/j.1365-313X.2005.02559.x

Linka N, Hurka H, Lang BF, Burger G, Winkler HH, Stamme C, et al. Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene. 2003;306:27–35. http://dx.doi.org/10.1016/S0378-1119(03)00429-3

Stiller JW. Toward an empirical framework for interpreting plastid evolution. J Phycol. 2014;50(3):462–471. http://dx.doi.org/10.1111/jpy.12178

Kim E, Maruyama S. A contemplation on the secondary origin of green algal and plant plastids. Acta Soc Bot Pol. 2014;83(4):331–336. http://dx.doi.org/10.5586/asbp.2014.040

Smith DR, Jackson CJ, Reyes-Prieto A. Nucleotide substitution analyses of the glaucophyte Cyanophora suggest an ancestrally lower mutation rate in plastid vs mitochondrial DNA for the Archaeplastida. Mol Phylogenet Evol. 2014;79:380–384. http://dx.doi.org/10.1016/j.ympev.2014.07.001

Chong J, Jackson C, Kim JI, Yoon HS, Reyes-Prieto A. Molecular markers from different genomic compartments reveal cryptic diversity within glaucophyte species. Mol Phylogenet Evol. 2014;76C:181–188. http://dx.doi.org/10.1016/j.ympev.2014.03.019

Takahashi T, Sato M, Toyooka K, Matsuzaki R, Kawafune K, Kawamura M, et al. Five Cyanophora (Cyanophorales, Glaucophyta) species delineated based on morphological and molecular data. J Phycol. 2014;50(6):1058–1069. http://dx.doi.org/10.1111/jpy.12236

Watanabe M, Sato M, Kondo K, Narikawa R, Ikeuchi M. Phycobilisome model with novel skeleton-like structures in a glaucocystophyte Cyanophora paradoxa. Biochim Biophys Acta. 2012;1817(8):1428–1435. http://dx.doi.org/10.1016/j.bbabio.2011.11.013

Facchinelli F, Pribil M, Oster U, Ebert NJ, Bhattacharya D, Leister D, et al. Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis. Planta. 2013;237(2):637–651. http://dx.doi.org/10.1007/s00425-012-1819-3

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

Watanabe M, Kubota H, Wada H, Narikawa R, Ikeuchi M. Novel supercomplex organization of photosystem I in Anabaena and Cyanophora paradoxa. Plant Cell Physiol. 2011;52(1):162–168. http://dx.doi.org/10.1093/pcp/pcq183

Gross J, Wajid S, Price DC, Zelzion E, Li J, Chan CX, et al. Evidence for widespread exonic small RNAs in the glaucophyte alga Cyanophora paradoxa. PLoS One. 2013;8(7):e67669. http://dx.doi.org/10.1371/journal.pone.0067669

Duanmu D, Bachy C, Sudek S, Wong CH, Jimenez V, Rockwell NC, et al. Marine algae and land plants share conserved phytochrome signaling systems. Proc Natl Acad Sci USA. 2014;11(44):15827–15832. http://dx.doi.org/10.1073/pnas.1416751111

Rockwell NC, Duanmu D, Martin SS, Bachy C, Price DC, Bhattacharya D, et al. Eukaryotic algal phytochromes span the visible spectrum. Proc Natl Acad Sci USA. 2014;111(10):3871–3876. http://dx.doi.org/10.1073/pnas.1401871111

Bhattacharya D, Schmidt HA. Division Glaucocystophyta. In: Bhattacharya D, editor. Origins of algae and their plastids. Plant systematics and evolution – supplement 11. Vienna: Springer Verlag; 1997. p. 139–148. http://dx.doi.org/10.1007/978-3-7091-6542-3_7

Yang Y, Maruyama S, Sekimoto H, Sakayama H, Nozaki H. An extended phylogenetic analysis reveals ancient origin of “non-green” phosphoribulokinase genes from two lineages of “green” secondary photosynthetic eukaryotes: Euglenophyta and Chlorarachniophyta. BMC Res Notes. 2011;4:330. http://dx.doi.org/10.1186/1756-0500-4-330

Marin B, Klingberg M, Melkonian M. Phylogenetic relationships among the Cryptophyta: analyses of nuclear-encoded SSU rRNA sequences support the monophyly of extant plastid-containing lineages. Protist. 1998;149(3):265–276. http://dx.doi.org/10.1016/S1434-4610(98)70033-1

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

Pascher A. Studien über Symbiosen. I. Über einige Endosymbiosen von Blaualgen in Einzellern. Jahrb Wss Bot. 1929;71:286–462.

Schenk HEA. Cyanophora paradoxa: anagenetic model or missing link of plastid evolution. Endocytobiosis Cell Res. 1994;10:87–106.

Chapman DJ. The pigments of the symbiotic algae (cyanomes) of Cyanophora paradoxa and Glaucocystis nostochinearum and two Rhodophyceae, Porphyridium aerugineum and Asteroeytis ramosa. Arch fur Mikrobiol. 1966;55:17–25. http://dx.doi.org/10.1007/BF00409152

Hall W. T, Claus G. Ultrastructural studies on the blue-green algal symbiont in Cyanophora paradoxa Korschikoff. J Cell Biol. 1963;19:551–563. http://dx.doi.org/10.1083/jcb.19.3.551

Herdman M, Stanier RY. The cyanelle: chloroplast or endosymbiotic prokaryote? FEMS Microbiol Lett. 1977;1(1):7–11. http://dx.doi.org/10.1111/j.1574-6968.1977.tb00568.x

Kies L. Zur systematischen Einordnung von Cyanophora paradoxa, Gloeochaete wittrockiana und Glaucocystis nostochinearum. Ber Dtsch Bot Ges. 1979;92(1):445–454. http://dx.doi.org/10.1111/j.1438-8677.1979.tb03291.x

Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR. Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol. 1988;170(8):3584–3592.

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

Stirewalt VL, Michalowski CB, Löffelhardt W, Bohnert HJ, Bryant DA. Nucleotide sequence of the cyanelle genome from Cyanophora paradoxa. Plant Mol Biol Report. 1995;13(4):327–332. http://dx.doi.org/10.1007/BF02669186

Löffelhardt W, Bohnert HJ. The cyanelle (muroplast) of Cyanophora paradoxa: a paradigm for endosymbiotic organelle evolution. In: Seckbach J, editor. Symbiosis. Mechanisms and model systems. Cellular origin, Life in extreme habitats and astrobiology. Volume 4. Dordrecht: Kluwer Academic Publishers; 2001. p. 111–130. http://dx.doi.org/10.1007/0-306-48173-1_7

Fathinejad S, Steiner JM, Reipert S, Marchetti M, Allmaier G, Burey SC, et al. A carboxysomal carbon-concentrating mechanism in the cyanelles of the “coelacanth” of the algal world, Cyanophora paradoxa? Physiol Plant. 2008;133(1):27–32. http://dx.doi.org/10.1111/j.1399-3054.2007.01030.x

Steiner JM, Löffelhardt W. The photosynthetic apparatus of the living fossil, Cyanophora paradoxa. In: Peschek GA, Obinger C, Renger G, editors. Bioenergetic processes of cyanobacteria. Dordrecht: Springer Netherlands; 2011. p. 71–87. http://dx.doi.org/10.1007/978-94-007-0388-9_2

Bhattacharya D, Price DC, Gross J, Chan CX, Steiner JM, Löffelhardt W. Analysis of the genome of Cyanophora paradoxa: an algal model for understanding primary endosymbiosis. In: Löffelhardt W, editor. Endosymbiosis. Vienna: Springer; 2014. p. 135–148. http://dx.doi.org/10.1007/978-3-7091-1303-5_7

Lauterborn R. Protozoenstudien II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süsswassers mit blaugrünen chromatophorenartigen Einschlüssen. Zeitschrift für wissenschaftliche Zool. 1895;59:537–544.

Kies L. Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamöbe mit blau-grünen Endosymbionten (Cyanellen). Protoplasma. 1974;80(1–3):69–89. http://dx.doi.org/10.1007/BF01666352

Marin B, Nowack ECM, 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

Mignot JP, Joyon L, Pringsheim EG. Quelques Particularités Structurales de Cyanophora paradoxa Korsch., Protozoaire Flagellé. J Protozool. 1969;16(1):138–145. http://dx.doi.org/10.1111/j.1550-7408.1969.tb02245.x

Thompson A. The flagella of Cyanophora paradoxa Korsch. S Afr J Bot. 1973;39:35–39.

Kugrens P, Clay BL, Meyer CJ, Lee RE. Ultrastructure and description of Cyanophora biloba, sp. nov., with additional observations on C. paradoxa (Glaucophyta). J Phycol. 1999;35(4):844–854. http://dx.doi.org/10.1046/j.1529-8817.1999.3540844.x

Viola R, Nyvall P, Pedersén M. The unique features of starch metabolism in red algae. Proc Biol Sci. 2001;268(1474):1417–1422. http://dx.doi.org/10.1098/rspb.2001.1644

Plancke C, Colleoni C, Deschamps P, Dauvillée 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

Nomura T, Nakayama N, Murata T, Akazawa T. Biosynthesis of starch in chloroplasts. Plant Physiol. 1967;42(3):327–332. http://dx.doi.org/10.1104/pp.42.3.327

Tester RF, Karkalas J, Qi X. Starch – composition, fine structure and architecture. J Cereal Sci. 2004;39(2):151–165. http://dx.doi.org/10.1016/j.jcs.2003.12.001

Shimonaga T, Fujiwara S, Kaneko M, Izumo A, Nihei S, Francisco PB, et al. Variation in storage alpha-polyglucans of red algae: amylose and semi-amylopectin types in Porphyridium and glycogen type in Cyanidium. Mar Biotechnol. 2007;9(2):192–202. http://dx.doi.org/10.1007/s10126-006-6104-7

Hindak F, Hindakova A. Chalarodora azurea Pascher 1929 – a rare glaucophyte found in the peat-bog Klin (Orava, Northern Slovakia). In: Wołowski K, Kaczmarska I, Ehrman JM, Wojtal AZ, editors. Current advances in algal taxonomy and its applications: phylogenetic, ecological and applied perspective. Kraków: Institute of Botany, Polish Academy of Sciences; 2012. p. 53–60.

Willison JH, Brown RM. Cell wall structure and deposition in Glaucocystis. J Cell Biol. 1978;77(1):103–119. http://dx.doi.org/10.1083/jcb.77.1.103

Schnepf E, Koch W, Deichgraber G. Zur Cytologie und taxonomischen Einordnung von Glaucocystis. Arch Mikrobiol. 1966;55(2):149–174. http://dx.doi.org/10.1007/BF00418636

Kies L. Ultrastructure of Cyanoptyche gloeocystis f. dispersa (Glaucocystophyceae). Plant Syst Evol. 1989;164(1–4):65–73. http://dx.doi.org/10.1007/BF00940430

Lagerheim G. Bidrag till Sveriges algflora. Öfversigt af Kongl. Vetenskaps-Akademiens Förhandlingar. 1883;40(2):37–78.

Korshikov A. Protistologische Beobachtungen. I Cyanophora paradoxa n. g. et sp. Russ Arch Protistol. 1924;3:57–74.

Reddy TBK, Thomas AD, Stamatis D, Bertsch J, Isbandi M, Jansson J, et al. The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Res. 2014; 43:D1099–D1106. http://dx.doi.org/10.1093/nar/gku950

Collén J, Porcel B, Carré W, Ball SG, Chaparro C, Tonon T, et al. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA. 2013;110(13):5247–5252. http://dx.doi.org/10.1073/pnas.1221259110

Schönknecht G, Chen WH, Ternes CM, Barbier GG, Shrestha RP, Stanke M, et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science. 2013;339(6124):1207–1210. http://dx.doi.org/10.1126/science.1231707

Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, et al. The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One. 2013;8(3):e57122. http://dx.doi.org/10.1371/journal.pone.0057122

Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N, Ball S, et al. Genome of the red alga Porphyridium purpureum. Nat Commun. 2013;4:1941. http://dx.doi.org/10.1038/ncomms2931

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

Gross J, Bhattacharya D. Mitochondrial and plastid evolution in eukaryotes: an outsiders’ perspective Nat Rev Genet. 2009;10(7):495–505. http://dx.doi.org/10.1038/nrg2610

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. Weighing the evidence for a single origin of plastids. J Phycol. 2003;39(6):1283–1285. http://doi.wiley.com/10.1111/j.0022-3646.2003.03-084.x

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

Suzuki K, Miyagishima SY. Eukaryotic and eubacterial contributions to the establishment of plastid proteome estimated by large-scale phylogenetic analyses. Mol Biol Evol. 2010;27(3):581–590. http://dx.doi.org/10.1093/molbev/msp273

Qiu H, Price DC, Weber APM, Facchinelli F, Yoon HS, Bhattacharya D. Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci. 2013;18(12):680–687. http://dx.doi.org/10.1016/j.tplants.2013.09.007

Huang J, Gogarten JP. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 2007;8(6):R99. http://dx.doi.org/10.1186/gb-2007-8-6-r99

Moustafa A, Reyes-Prieto A, Bhattacharya D. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS One. 2008;3(5):e2205. http://dx.doi.org/10.1371/journal.pone.0002205

Deschamps P. Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates? Acta Soc Bot Pol. 2014;83(4):291–302. http://dx.doi.org/10.5586/asbp.2014.048

Facchinelli F, Colleoni C, Ball SG, Weber APM. Chlamydia, cyanobiont, or host: who was on top in the ménage à trois? Trends Plant Sci. 2013;18(12):673–679. http://dx.doi.org/10.1016/j.tplants.2013.09.006

Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, et al. Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol. 2013;5(1):31–44. http://dx.doi.org/10.1093/gbe/evs117

Flinner N, Ellenrieder L, Stiller SB, Becker T, Schleiff E, Mirus O. Mdm10 is an ancient eukaryotic porin co-occurring with the ERMES complex. Biochim Biophys Acta. 2013;1833(12):3314–3325. http://dx.doi.org/10.1016/j.bbamcr.2013.10.006

Cai X, Wang X, Clapham DE. Early evolution of the eukaryotic Ca2+ signaling machinery: conservation of the CatSper channel complex. Mol Biol Evol. 2014;31(10):2735–2740. http://dx.doi.org/10.1093/molbev/msu218

Petrželková R, Eliáš M. Contrasting patterns in the evolution of the Rab GTPase family in Archaeplastida. Acta Soc Bot Pol. 2014;83(4):303–315. http://dx.doi.org/10.5586/asbp.2014.052

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

Reyes-Prieto A, Hackett JD, Soares MB, Bonaldo MF, Bhattacharya D. Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr Biol. 2006;16(23):2320–2325. http://dx.doi.org/10.1016/j.cub.2006.09.063

Moustafa A, Bhattacharya D. PhyloSort: a user-friendly phylogenetic sorting tool and its application to estimating the cyanobacterial contribution to the nuclear genome of Chlamydomonas. BMC Evol Biol. 2008;8:6. http://dx.doi.org/10.1186/1471-2148-8-6

Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, et al. Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol. 2008;25(4):748–761. http://dx.doi.org/10.1093/molbev/msn022

Sato N, Ishikawa M, Fujiwara M, Sonoike K. Mass identification of chloroplast proteins of endosymbiont origin by phylogenetic profiling based on organism-optimized homologous protein groups. Genome Inform. 2005;16(2):56–68.

Lang BF, Nedelcu AM. Plastid genomes of algae. In Bock R, Knoop V, editors. Genomics of chloroplasts and mitochondria. Advances in photosynthesis and respiration series. Volume 35. Dordrecht: Springer Netherlands; 2012. p. 59–87. http://dx.doi.org/10.1007/978-94-007-2920-9_3

DePriest MS, Bhattacharya D, López-Bautista JM. The plastid genome of the red macroalga Grateloupia taiwanensis (Halymeniaceae). PLoS One. 2013;8(7):e68246. http://dx.doi.org/10.1371/journal.pone.0068246

Wang L, Mao Y, Kong F, Li G, Ma F, Zhang B, et al. Complete sequence and analysis of plastid genomes of two economically important red algae: Pyropia haitanensis and Pyropia yezoensis. PLoS One. 2013;8(5):e65902. http://dx.doi.org/10.1371/journal.pone.0065902

Tajima N, Sato S, Maruyama F, Kurokawa K, Ohta H, Tabata S, et al. Analysis of the complete plastid genome of the unicellular red alga Porphyridium purpureum. J Plant Res. 2014;127(3):389–397. http://dx.doi.org/10.1007/s10265-014-0627-1

Grossman AR, Talbot L, Egelhoff T. Biosynthesis of phycobilisome polypeptides of Porphyridium aerugineum and Cyanophora paradoxa. In: Year book Carnegie Institution of Washington. Washington, DC: Carnegie Institution of Washington; 1983. p. 112–116.

Steiner JM, Pompe JA, Löffelhardt W. Characterization of apcC, the nuclear gene for the phycobilisome core linker polypeptide L(c)(7.8) from the glaucocystophyte alga Cyanophora paradoxa. Import of the precursor into isolated cyanelles and integration of the mature protein into intact phycobilisomes. Curr Genet. 2003;44(3):132–137. http://dx.doi.org/10.1007/s00294-003-0433-0

Tomitani A, Okada K, Miyashita H, Matthijs HC, Ohno T, Tanaka A. Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature. 1999;400(6740):159–162. http://dx.doi.org/10.1038/22101

David L, Marx A, Adir N. High-resolution crystal structures of trimeric and rod phycocyanin. J Mol Biol. 2011;405(1):201–213. http://dx.doi.org/10.1016/j.jmb.2010.10.036

Engelken J, Brinkmann H, Adamska I. Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol Biol. 2010;10:233. http://dx.doi.org/10.1186/1471-2148-10-233

Umate P. Genome-wide analysis of the family of light-harvesting chlorophyll a/b-binding proteins in Arabidopsis and rice. Plant Signal Behav. 2010;5(12):1537–1542. http://dx.doi.org/10.4161/psb.5.12.13410

Montané MH, Kloppstech K. The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene. 2000;258(1–2):1–8. http://dx.doi.org/10.1016/S0378-1119(00)00413-3

Koziol AG, Borza T, Ishida KI, Keeling P, Lee RW, Durnford DG. Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol. 2007;143(4):1802–1816. http://dx.doi.org/10.1104/pp.106.092536

van Heijenoort J. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology. 2001;11(3):25R–36R. http://dx.doi.org/10.1093/glycob/11.3.25R

Vollmer W, Blanot D, de Pedro MA. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 2008;32(2):149–167. http://dx.doi.org/10.1111/j.1574-6976.2007.00094.x

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.

Pfanzagl B, Allmaier G, Schmid ER, de Pedro MA, Löffelhardt W. N-acetylputrescine as a characteristic constituent of cyanelle peptidoglycan in glaucocystophyte algae. J Bacteriol. 1996;178(23):6994–6997.

Schwartzbach SD, Osafune T, Löffelhardt W. Protein import into cyanelles and complex chloroplasts. Plant Mol Biol. 1998;38(1–2):247–263. http://dx.doi.org/10.1023/A:1006029919283

Plaimauer B, Pfanzagl B, Berenguer J, de Pedro MA, Löffelhardt W. Subcellular distribution of enzymes involved in the biosynthesis of cyanelle murein in the protist Cyanophora paradoxa. FEBS Lett. 1991;284(2):169–172. http://dx.doi.org/10.1016/0014-5793(91)80677-U

Iino M, Hashimoto H. Intermediate features of cyanelle division of Cyanophora paradoxa (Glaucocystophyta) between cyanobacterial and plastid division. J Phycol. 2003;39(3):561–569. http://dx.doi.org/10.1046/j.1529-8817.2003.02132.x

Berenguer J, Rojo F, de Pedro MA, Pfanzagl B, Löffelhardt W. Penicillin-binding proteins in the cyanelles of Cyanophora paradoxa, a eukaryotic photoautotroph sensitive to β-lactam antibiotics. FEBS Lett. 1987;224(2):401–405. http://dx.doi.org/10.1016/0014-5793(87)80492-1

Kies L. The effect of penicillin on the morphology and ultrastructure of Cyanophora, Gloeochaete and Glaucocystis (Glaucocystophyceae) and their cyanelles. Endocytobiosis Cell Res. 1988;5:361–372.

Sato M, Nishikawa T, Kajitani H, Kawano S. Conserved relationship between FtsZ and peptidoglycan in the cyanelles of Cyanophora paradoxa similar to that in bacterial cell division. Planta. 2007;227(1):177–187. http://dx.doi.org/10.1007/s00425-007-0605-0

Miyagishima SY, Takahara M, Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T. Plastid division is driven by a complex mechanism that involves differential transition of the bacterial and eukaryotic division rings. Plant Cell. 2001;13(10):2257–68. http://dx.doi.org/10.1105/tpc.010185

Miyagishima S, Kabeya Y, Sugita C, Sugita M, Fujiwara T. DipM is required for peptidoglycan hydrolysis during chloroplast division. BMC Plant Biol. 2014;14:57. http://dx.doi.org/10.1186/1471-2229-14-57

Kies L. Untersuchungen zur Feinstruktur und taxonomischen Einordnung von Gloeochaete wittrockiana, einer apoplastidalen capsalen Alge mit blaugrünen Endosymbionten (Cyanellen). Protoplasma. 1976;87(4):419–446. http://dx.doi.org/10.1007/BF01624010

Mangeney E, Gibbs SP. Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in the cyanelles of Cyanophora paradoxa and Glaucocystis nostochinearum. Eur J Cell Biol. 1987;43(1):65–70. http://dx.doi.org/10.1104/pp.84.4.1028

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

Giordano M, Beardall J, Raven JA. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol. 2005;56:99–131. http://dx.doi.org/10.1146/annurev.arplant.56.032604.144052

Burey SC, Poroyko V, Ergen ZN, Fathi-Nejad S, Schüller C, Ohnishi N, et al. Acclimation to low [CO2] by an inorganic carbon-concentrating mechanism in Cyanophora paradoxa. Plant Cell Environ. 2007;30(11):1422–1435. http://dx.doi.org/10.1111/j.1365-3040.2007.01715.x

Raven JA. Carboxysomes and peptidoglycan walls of cyanelles: possible physiological functions. Eur J Phycol. 2003;38(1):47–53. http://dx.doi.org/10.1080/0967026031000096245

Börner G V, Mörl M, Janke A, Pääbo S. RNA editing changes the identity of a mitochondrial tRNA in marsupials. EMBO J. 1996;15(21):5949–5957.

Valach M, Burger G, Gray MW, Lang BF. Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res. 2014;42(22):13764–13777. http://dx.doi.org/10.1093/nar/gku1266

Verbruggen H, Maggs CA, Saunders GW, Le Gall L, Yoon HS, de Clerck O. Data mining approach identifies research priorities and data requirements for resolving the red algal tree of life. BMC Evol Biol. 2010;10:16. http://dx.doi.org/10.1186/1471-2148-10-16

Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, et al. Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 2012;31(1):1–46. http://dx.doi.org/10.1080/07352689.2011.615705




DOI: https://doi.org/10.5586/asbp.2015.020

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society