Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29038514
PubMed Central
PMC5643376
DOI
10.1038/s41598-017-13575-x
PII: 10.1038/s41598-017-13575-x
Knihovny.cz E-zdroje
- MeSH
- Alveolata genetika fyziologie MeSH
- delece genu MeSH
- fotosyntéza genetika fyziologie MeSH
- fotosystém I - proteinový komplex genetika izolace a purifikace fyziologie MeSH
- fylogeneze MeSH
- hmotnostní spektrometrie MeSH
- molekulární evoluce MeSH
- superoxiddismutasa metabolismus MeSH
- tylakoidy metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fotosystém I - proteinový komplex MeSH
- superoxiddismutasa MeSH
In oxygenic photosynthesis the initial photochemical processes are carried out by photosystem I (PSI) and II (PSII). Although subunit composition varies between cyanobacterial and plastid photosystems, the core structures of PSI and PSII are conserved throughout photosynthetic eukaryotes. So far, the photosynthetic complexes have been characterised in only a small number of organisms. We performed in silico and biochemical studies to explore the organization and evolution of the photosynthetic apparatus in the chromerids Chromera velia and Vitrella brassicaformis, autotrophic relatives of apicomplexans. We catalogued the presence and location of genes coding for conserved subunits of the photosystems as well as cytochrome b6f and ATP synthase in chromerids and other phototrophs and performed a phylogenetic analysis. We then characterised the photosynthetic complexes of Chromera and Vitrella using 2D gels combined with mass-spectrometry and further analysed the purified Chromera PSI. Our data suggest that the photosynthetic apparatus of chromerids underwent unique structural changes. Both photosystems (as well as cytochrome b6f and ATP synthase) lost several canonical subunits, while PSI gained one superoxide dismutase (Vitrella) or two superoxide dismutases and several unknown proteins (Chromera) as new regular subunits. We discuss these results in light of the extraordinarily efficient photosynthetic processes described in Chromera.
Centre Algatech Institute of Microbiology Czech Academy of Sciences Třeboň Czech Republic
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Zobrazit více v PubMed
Rutherford AW, Faller P. Photosystem II: evolutionary perspectives. Philos. Trans. R. Soc. London B. 2003;358:245–253. doi: 10.1098/rstb.2002.1186. PubMed DOI PMC
Green BR. After the primary endosymbiosis: An update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth. Res. 2011;107:103–115. doi: 10.1007/s11120-010-9584-2. PubMed DOI
Nielson JAD, Durnford DG. Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth. Res. 2010;106:57–71. doi: 10.1007/s11120-010-9576-2. PubMed DOI
Alboresi A, et al. Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana. New Phytol. 2017;213:714–726. doi: 10.1111/nph.14156. PubMed DOI PMC
Dudkina NV, Folea IM, Boekema EJ. Towards structural and functional characterization of photosynthetic and mitochondrial supercomplexes. Micron. 2015;72:39–51. doi: 10.1016/j.micron.2015.03.002. PubMed DOI
Nagao R, et al. Purification and characterization of a stable oxygen-evolving Photosystem II complex from a marine centric diatom. Chaetoceros gracilis. Biochim. Biophys. Acta. 2010;1979:160–166. doi: 10.1016/j.bbabio.2009.09.008. PubMed DOI
Umena Y, Kawakami K, Shen J-R, Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature. 2011;473:55–60. doi: 10.1038/nature09913. PubMed DOI
Wei X, et al. Structure of spinach photosystem II-LCHII supercomplex at 3.2 Å resolution. Nature. 2016;534:69–74. doi: 10.1038/nature18020. PubMed DOI
Amunts A, Nelson N. Plant photosystem I design in the light of evolution. Structure. 2009;17:637–650. doi: 10.1016/j.str.2009.03.006. PubMed DOI
Grouneva I, Rokka A, Aro E-M. The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J. Proteome Res. 2011;10:5338–5353. doi: 10.1021/pr200600f. PubMed DOI
Grouneva I, et al. Phylogenetic viewpoints on regulation of light harvesting and electron transport in eukaryotic photosynthetic organisms. Planta. 2013;237:399–412. doi: 10.1007/s00425-012-1744-5. PubMed DOI
Basso S, et al. Characterization of the photosynthetic apparatus of the eustigmatophycean Nannochloropsis gaditana: Evidence of convergent evolution in the supramolecular organization of photosystem I. Biochim. Biophys. Acta. 2014;1837:306–314. doi: 10.1016/j.bbabio.2013.11.019. PubMed DOI
Yang H, Liu J, Wen X, Lu C. Molecular mechanism of photosystem I assembly in oxygenic organisms. Biochim. Biophys. Acta. 2015;1847:838–848. doi: 10.1016/j.bbabio.2014.12.011. PubMed DOI
Cavalier-Smith T. Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Euk. Microbiol. 1999;46:347–366. doi: 10.1111/j.1550-7408.1999.tb04614.x. PubMed DOI
Archibald JM. The puzzle of plastid evolution. Current Biology. 2009;19:R81–R88. doi: 10.1016/j.cub.2008.11.067. PubMed DOI
Keeling PJ. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant Biol. 2013;64:583–607. doi: 10.1146/annurev-arplant-050312-120144. PubMed DOI
Stiller JW. Toward an empirical framework for interpreting plastid evolution. J. Phycol. 2014;50:462–471. doi: 10.1111/jpy.12178. PubMed DOI
Archibald JM. Genomic perspectives on the birth and spread of plastids. Proc. Natl. Acad. Sci. USA. 2015;112:10147–10153. doi: 10.1073/pnas.1421374112. PubMed DOI PMC
Falkowski PG, et al. The evolution of modern eukaryotic phytoplankton. Science. 2004;305:354–360. doi: 10.1126/science.1095964. PubMed DOI
Petersen J, et al. Chromera velia, endosymbiosis and the Rhodoplex Hypothesis – plastid evolution in cryptophytes, alveolates, stramenopliles, and haptophytes (CASH lineages) Genome Biol. Evol. 2014;6:666–684. doi: 10.1093/gbe/evu043. PubMed DOI PMC
Martin W, Herrmann RG. Gene transfer from organelles to the nucleus: How much, what happens, and why? Plant Physiol. 1998;118:9–17. doi: 10.1104/pp.118.1.9. PubMed DOI PMC
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;24:54–62. doi: 10.1093/molbev/msl129. PubMed DOI
Janouškovec J, et al. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc. Natl. Acad. Sci. USA. 2015;112:10200–10207. doi: 10.1073/pnas.1423790112. PubMed DOI PMC
McFadden GI, Reith ME, Munholland J, Lang-Unnasch N. Plastid in human parasites. Nature. 1996;381:482. doi: 10.1038/381482a0. PubMed DOI
Köhler S, et al. A plastid of probable green algal origin in apicomplexan parasites. Science. 1997;275:1485–1489. doi: 10.1126/science.275.5305.1485. PubMed DOI
Oborník M, Janouškovec J, Chrudimský T, Lukeš J. Evolution of the apicoplast and its hosts: From heterotrophy to autotrophy and back again. Int. J. Parasitol. 2009;39:1–12. doi: 10.1016/j.ijpara.2008.07.010. PubMed DOI
Moore RB, et al. A photosynthetic alveolate closely related to apicomplexan parasites. Nature. 2008;451:959–963. doi: 10.1038/nature06635. PubMed DOI
Janouškovec J, Horák A, Oborník M, Lukeš J, Keeling PJ. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc. Natl. Acad. Sci. USA. 2010;107:10949–10954. doi: 10.1073/pnas.1003335107. PubMed DOI PMC
Oborník M, et al. Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist. 2012;163:306–323. doi: 10.1016/j.protis.2011.09.001. PubMed DOI
Cumbo VR, et al. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. Protist. 2013;164:237–244. doi: 10.1016/j.protis.2012.08.003. PubMed DOI
Janouškovec J, et al. Split photosystem protein, linear-mapping topology and growth of structural complexity in the plastid genome of Chromera velia. Mol. Biol. Evol. 2013;30:2447–2462. doi: 10.1093/molbev/mst144. PubMed DOI
Belgio E, et al. High photochemical trapping efficiency in Photosystem I from the red clade algae Chromera velia and Phaeodactylum tricornutum. Biochim. Biophys. Acta. 2017;1858:56–63. doi: 10.1016/j.bbabio.2016.10.002. PubMed DOI
Tichy J, et al. Light harvesting complexes of Chromera velia, photosynthetic relative of apicomplexan parasites. Biochim. Biophys. Acta. 2013;1827:723–729. doi: 10.1016/j.bbabio.2013.02.002. PubMed DOI
Pan H, Šlapeta J, Carter D, Chen M. Phylogenetic analysis of the light-harvesting system in Chromera velia. Photosynth. Res. 2012;111:19–28. doi: 10.1007/s11120-011-9710-9. PubMed DOI
Ševčíková T, et al. Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci. Rep. 2015;5:10134. doi: 10.1038/srep10134. PubMed DOI PMC
Quigg A, et al. Photosynthesis in Chromera velia represents a simple system with high efficiency. PLOS One. 2012;7:e47036. doi: 10.1371/journal.pone.0047036. PubMed DOI PMC
Kotabová E, et al. Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim. Biophys. Acta. 2014;1837:734–743. doi: 10.1016/j.bbabio.2014.01.012. PubMed DOI
Mann M, et al. Unusual features of the high light acclimation of Chromera velia. Photosynth. Res. 2014;122:159–169. doi: 10.1007/s11120-014-0019-3. PubMed DOI
Xu Q, et al. Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 1995;270:16243–16250. doi: 10.1074/jbc.270.27.16243. PubMed DOI
Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV. The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature. 2000;408:613–615. doi: 10.1038/35046121. PubMed DOI
Plöchinger M, et al. The low molecular weight protein PsaI stabilizes the light-harvesting complex II docking site of photosystem I. Plant. Physiol. 2016;172:450–463. doi: 10.1104/pp.16.00647. PubMed DOI PMC
Jensen PE, Gilpin M, Knoetzel J, Scheller HV. The PSI-K subunit of photosystem I is involved in the interaction between light-harvesting complex I and the photosystem I reaction center core. J. Biol. Chem. 2000;275:24701–24708. doi: 10.1074/jbc.M000550200. PubMed DOI
Durnford DG, et al. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 1999;48:59–68. doi: 10.1007/PL00006445. PubMed DOI
Hippler M, Drepper F, Farah J, Rochaix J-D. Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochem. 1997;36:6343–6349. doi: 10.1021/bi970082c. PubMed DOI
Haldrup A, Simpson DJ, Scheller HV. 2000. Down-regulation of the PSI-F subunit of photosystem I (PSI) in Arabidopsis thaliana. J. Biol. Chem. 2000;275:31211–31218. doi: 10.1074/jbc.M002933200. PubMed DOI
Hansson A, et al. Knock-out of the chloroplast-encoded PSI-J subunit of photosystem I in Nicotiana tabacum. FEBS J. 2007;274:1734–1746. doi: 10.1111/j.1742-4658.2007.05722.x. PubMed DOI
Boudreau E, Takahashi Y, Lemieux C, Turmel M, Rochaix J-D. The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 1997;16:6095–6104. doi: 10.1093/emboj/16.20.6095. PubMed DOI PMC
Ozawa S, et al. Biochemical and structural studies of the large Ycf4-Photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell. 2009;21:2424–2442. doi: 10.1105/tpc.108.063313. PubMed DOI PMC
Krech K, et al. The plastid genome-encoded Ycf4 protein functions as a nonessential assembly factor for photosystem I in higher plants. Plant Physiol. 2012;159:579–591. doi: 10.1104/pp.112.196642. PubMed DOI PMC
Künstner P, Guardiola A, Takahashi Y, Rochaix J-D. A mutant strain of Chlamydomonas reinhardtii lacking the chloroplast photosystem II psbI gene grows photoautotrophically. J. Biol. Chem. 1995;270:9651–9654. doi: 10.1074/jbc.270.16.9651. PubMed DOI
Schwenkert S, et al. PsbI affects the stability, function, and phosphorylation patterns of Photosystem II assemblies in tobacco. J. Biol. Chem. 2006;281:34227–34238. doi: 10.1074/jbc.M604888200. PubMed DOI
Kawakami K, et al. Roles of PsbI and PsbM in photosystem II dimer formation and stability studied by deletion mutagenesis and X-ray crystallography. Biochim. Biophys. Acta. 2011;1807:319–325. doi: 10.1016/j.bbabio.2010.12.013. PubMed DOI
Funk C. Functional analysis of the PsbX protein by deletion of the corresponding gene in Synechocystis sp. PCC 6803. Plant Mol. Biol. 2000;44:815–827. doi: 10.1023/A:1026764728846. PubMed DOI
Sugiura M, et al. Psb30 contributes to structurally stabilise the Photosystem II complex in the thermophilic cyanobacterium Thermosynechococcus elongatus. Biochim. Biophys. Acta. 2010;1797:1546–1554. doi: 10.1016/j.bbabio.2010.03.020. PubMed DOI
von Sydow L, et al. The PsbY protein of Arabidopsis Photosystem II is important for the redox control of cytochrome b559. Biochim. Biophys. Acta. 2016;1857:1524–1533. doi: 10.1016/j.bbabio.2016.05.004. PubMed DOI
Inoue-Kashino N, Kashino Y, Takahashi Y. Psb30 is a photosystem II reaction center subunit and is required for optimal growth in high light in Clamydomonas reinhardtii. J. Photochem. Photobiol. B. 2011;104:220–338. doi: 10.1016/j.jphotobiol.2011.01.024. PubMed DOI
Bína D, Gardian Z, Herbstová M, Litvín R. Modular antenna of photosystem I in secondary plastids of red algal origin: a Nannochloropsis oceanica case study. Photosynth. Res. 2017;131:255–266. doi: 10.1007/s11120-016-0315-1. PubMed DOI
Takahashi Y, et al. The chloroplastycf7 (petL) open reading frame of Chlamydomonas reinhardtii encodes a small functionally important subunit of the cytochrome b6f complex. EMBO J. 1996;15:3498–3506. PubMed PMC
Schneider D, Vokmer T, Rögner M. PetG and PetN, but not PetL, are essential subunits of the cytochrome b6f complex from Synechocystis PCC 6803. Res. Microbiol. 2007;158:45–50. doi: 10.1016/j.resmic.2006.10.002. PubMed DOI
Schwenkert S, et al. Role of the low-molecular-weigth subunits PetL, PetG, and PetN in assembly, stability, and dimerization of the cytochrome b6f complex in tobacco. Plant Physiol. 2007;144:1924–1935. doi: 10.1104/pp.107.100131. PubMed DOI PMC
Stroebel D, Choquet Y, Popot J–L, Picot D. An atypical haem in the cytochrome b6f complex. Nature. 2003;426:413–418. doi: 10.1038/nature02155. PubMed DOI
Hojka M, et al. Inducible repression of nuclear-encoded subunits of the cytochrome b6f complex in tobacco reveals an extraordinarily long lifetime of the complex. Plant Physiol. 2014;165:1632–1646. doi: 10.1104/pp.114.243741. PubMed DOI PMC
Schneider D, Berry S, Rich P, Seidler A, Rögner M. A regulatory role of the PetM subunit in a cyanobacterial cytochrome b6f complex. J. Biol. Chem. 2001;276:16780–16785. doi: 10.1074/jbc.M009503200. PubMed DOI
Hager M, Biehler K, Illerhaus J, Ruf S, Bock R. Targeted inactivation of the smallest plastid genome-encoded open reading frame reveals a novel and essential subunit of the cytochrome b6f complex. EMBO J. 1999;18:5634–5842. doi: 10.1093/emboj/18.21.5834. PubMed DOI PMC
Maiwald D, et al. Knock-out of the genes coding for the rieske protein and the ATP-synthase δ-subunit of Arabidopsis. Effects on photosynthesis, thylakoid protein composition, and nuclear chloroplast gene expression. Plant Physiol. 2013;133:191–202. doi: 10.1104/pp.103.024190. PubMed DOI PMC
Woo YH, et al. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife. 2015;4:e06974. doi: 10.7554/eLife.06974. PubMed DOI PMC
Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–90. doi: 10.1093/bioinformatics/btl446. PubMed DOI
Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25:2286–8. doi: 10.1093/bioinformatics/btp368. PubMed DOI
Bodył A. Do plastid-related characters support the Chromalveolate Hypothesis? J. Phycol. 2005;41:712–719. doi: 10.1111/j.1529-8817.2005.00091.x. DOI
Bodył A, Stiller JW, Mackiewicz P. Chromalveolate plastids: direct descent or multiple endosymbioses? Trends Ecol. Evol. 2009;24:119–121. doi: 10.1016/j.tree.2008.11.003. PubMed DOI
Baurain D, et al. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 2010;27:1698–1709. doi: 10.1093/molbev/msq059. PubMed DOI
Zimorski V, Ku C, Martin WF, Gould SB. Endosymbiotic theory for organelle origins. Curr. Opin. Microbiol. 2014;22:38–48. doi: 10.1016/j.mib.2014.09.008. PubMed DOI
Gile GH, Slamovits CH. Transcriptomic analysis reveals evidence for a cryptic plastid in the colpodellid Voromonas pontica, a close relative of chromerids and apicomplexan parasites. PLOS ONE. 2014;9:e96258. doi: 10.1371/journal.pone.0096258. PubMed DOI PMC
Gould SV, Maier U–G, Martin WF. Protein import and the origin of red complex plastids. Curr. Biol. 2015;25:R515–R521. doi: 10.1016/j.cub.2015.04.033. PubMed DOI
Danne JC, Gornik SG, MacRae JI, McConville MJ, Waller RF. Alveolate mitochondrial metabolic evolution: Dinoflagellates force reassessment of the role of parasitism as a driver of change in apicomplexans. Mol. Biol. Evol. 2012;30:123–139. doi: 10.1093/molbev/mss205. PubMed DOI
Pagliano C, Barera S, Chimirri F, Saracco G, Barber J. Comparison of the α and β isomeric forms of the detergent n-dodecyl-D-maltoside for solubilizing photosynthetic complexes from pea thylakoid membranes. Biochim. Biophys. Acta. 2012;1817:1506–1515. doi: 10.1016/j.bbabio.2011.11.001. PubMed DOI
Petersen TN, Brunak S, von Heihne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods. 2011;8:785–786. doi: 10.1038/nmeth.1701. PubMed DOI
Nielsen H, Engelbrecht J, Brunak S, von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997;10:1–6. doi: 10.1093/protein/10.1.1. PubMed DOI
Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequences. J. Mol. Biol. 2000;300:1005–1016. doi: 10.1006/jmbi.2000.3903. PubMed DOI
Gschloessl, B., Guermeur Y. & Cock J. M. HECTAR: A method to predict subcellular targeting in heterokonts. BMC Bioinformatics9, 393 (2008). PubMed PMC
Busch A, Hippler M. The structure and function of eukaryotic photosystem I. Biochim. Biophys. Acta. 2011;1807:864–877. doi: 10.1016/j.bbabio.2010.09.009. PubMed DOI
Miyake C. Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol. 2010;51:1951–1963. doi: 10.1093/pcp/pcq173. PubMed DOI
Yokono M, Takabayashi A, Akimoto S, Tanaka A. A megacomplex composed of both photosystem reaction centres in higher plants. Nat. Comm. 2015;6:6675. doi: 10.1038/ncomms7675. PubMed DOI
Yadav KNS, et al. Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH. Biochim. Biophys. Acta. 2017;1858:12–20. doi: 10.1016/j.bbabio.2016.10.006. PubMed DOI
Asada K. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999;50:601–639. doi: 10.1146/annurev.arplant.50.1.601. PubMed DOI
Sae-Tang P, et al. Overexpressed superoxide dismutase and catalase act synergistically to protect the repair of PSII during photoinhibition in Synechococcus elongatus PCC 7942. Plant Cell Physiol. 2016;57:1899–1907. doi: 10.1093/pcp/pcw110. PubMed DOI
Hirotsu N, Makino A, Ushio A, Mae T. Changes in thermal dissipation and the electron flow in the water–water cycle in rice grown under conditions of physiologically low temperature. Plant Cell Physiol. 2004;45:635–644. doi: 10.1093/pcp/pch075. PubMed DOI
Ogawa K, Kanematsu S, Takabe K, Asada K. Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection of immune-gold labelling after rapid freezing and substitution method. Plant Cell Physiol. 1995;36:565–573.
Myouga F, et al. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell. 2008;20:3148–3162. doi: 10.1105/tpc.108.061341. PubMed DOI PMC
Boucher IW, et al. The crystal structure of superoxide dismutase from Plasmodium falciparum. BMC Struct. Biol. 2006;6:20. doi: 10.1186/1472-6807-6-20. PubMed DOI PMC
Muñoz IG, Moran JF, Becana M, Montoya G. The crystal structure of an eukaryotic iron superoxide dismutase suggests intersubunit cooporation during catalysis. Prot. Sci. 2005;14:387–394. doi: 10.1110/ps.04979505. PubMed DOI PMC
Kořeny L, Sobotka R, Janouškovec J, Keeling PJ, Oborník M. Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell. 2011;23:3454–3462. doi: 10.1105/tpc.111.089102. PubMed DOI PMC
Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66. doi: 10.1093/nar/gkf436. PubMed DOI PMC
Kaňa R, et al. Violaxanthin inhibits nonphotochemical quenching in light-harvesting antenna of Chromera velia. FEBS Lett. 2016;590:1076–1085. doi: 10.1002/1873-3468.12130. PubMed DOI
Wittig I, Schägger H. Features and applications of blue-native and clear-native electrophoresis. Proteomics. 2008;8:3974–3990. doi: 10.1002/pmic.200800017. PubMed DOI
Kuo W, Huang C, Shih C, Jinn T. Cellular extract preparation for superoxide dismutase (SOD) activity assay. Bio Protoc. 2013;3:e811. doi: 10.21769/BioProtoc.811. DOI
Complex Endosymbioses I: From Primary to Complex Plastids, Serial Endosymbiotic Events
Organellar Evolution: A Path from Benefit to Dependence
Fatty Acid Biosynthesis in Chromerids
Isolation of plastids and mitochondria from Chromera velia
Characterization of Aminoacyl-tRNA Synthetases in Chromerids
Endosymbiotic Evolution of Algae, Secondary Heterotrophy and Parasitism
Antenna proton sensitivity determines photosynthetic light harvesting strategy