Skip to main content
SpringerLink
Log in

Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Glaucophytes represent the first lineage of photosynthetic eukaryotes of primary endosymbiotic origin that diverged after plastid establishment. The muroplast of Cyanophora paradoxa represents a primitive plastid that resembles its cyanobacterial ancestor in pigment composition and the presence of a peptidoglycan wall. To attain insights into the evolutionary history of cyanobiont integration and plastid development, it would thus be highly desirable to obtain knowledge on the composition of the glaucophyte plastid proteome. Here, we provide the first proteomic analysis of the muroplast of C. paradoxa. Mass spectrometric analysis of the muroplast proteome identified 510 proteins with high confidence. The protein repertoire of the muroplast revealed novel paths for reduced carbon flow and export to the cytosol through a sugar phosphate transporter of chlamydial origin. We propose that C. paradoxa possesses a primordial plastid mirroring the situation in the early protoalga.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

MS:

Mass spectrometry

EGT:

Endosymbiotic gene transfer

TOC/TIC:

Translocon of the outer chloroplast membrane/translocon of the inner chloroplast membrane

PT:

Phosphate translocators

NST:

Nucleotide-sugar transporter

NTT:

Nucleoside triphosphate transporter

References

  • Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451

    Article  PubMed  Google Scholar 

  • Agrawal GK, Bourguignon J, Rolland N, Ephritikhine G, Ferro M, Jaquinod M, Alexiou KG, Chardot T, Chakraborty N, Jolivet P, Doonan JH, Rakwal R (2011) Plant organelle proteomics: collaborating for optimal cell function. Mass Spectrom Rev 30:772–853

    CAS  Google Scholar 

  • Baginsky S (2009) Plant proteomics: concepts, applications, and novel strategies for data interpretation. Mass Spectrom Rev 28:93–120

    Article  PubMed  CAS  Google Scholar 

  • Ball SG, Colleoni C, Cenci U, Raj JN, Tirtiaux C (2011) The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 62:1775–1801

    Article  PubMed  CAS  Google Scholar 

  • Ball SG, Subtil A, Bhattachrya D, Moustafa A, Weber APM, Gehre L, Colleoni C, Arias MC, Cenci U, Dauvillé D (2012) Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell (in press)

  • Becker B, Hoef-Emden K, Melkonian M (2008) Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol 8:203

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Black MT, Meyer D, Widger W, Cramer W (1987) Light-regulated methylation of chloroplast proteins. J Biol Chem 262:9803–9807

    PubMed  CAS  Google Scholar 

  • Block MA, Tewari AK, Albrieux C, Maréchal E, Joyard J (2003) The plant S-adenosyl-l-methionine: Mg-protoporphyrin IX methyltransferase is located in both envelope and thylakoid chloroplast membranes. Eur J Biochem 269:240–248

    Article  Google Scholar 

  • Borchert S, Harborth J, Schunemann D, Hoferichter P, Heldt HW (1993) Studies of the enzymatic capacities and transport-properties of pea root plastids. Plant Physiol 101:303–312

    PubMed  CAS  Google Scholar 

  • Bouvier F, Linka N, Isner JC, Mutterer J, Weber APM, Camara B (2006) Arabidopsis SAMT1 defines a plastid transporter regulating plastid biogenesis and plant development. Plant Cell 18:3088–3105

    Article  PubMed  CAS  Google Scholar 

  • Breuers FK, Brautigam A, Geimer S, Welzel UY, Stefano G, Renna L, Brandizzi F, Weber APM (2012) Dynamic remodeling of the plastid envelope membranes—a tool for chloroplast envelope in vivo localizations. Front Plant Sci 3:7

    Article  PubMed  Google Scholar 

  • Brinkman FSL, Blanchard JL, Cherkasov A, Av-Gay Y, Brunham RC, Fernandez RC, Finlay BB, Otto SP, Ouellette BFF, Keeling PJ, Rose AM, Hancock REW, Jones SJM (2002) Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res 12:1159–1167

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5:174–182

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12:R62–R64

    Article  PubMed  CAS  Google Scholar 

  • Cheng Z, Sattler S, Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2003) Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15:2343–2356

    Article  PubMed  CAS  Google Scholar 

  • Colleoni C, Linka M, Deschamps P, Handford MG, Dupree P, Weber APM, Ball SG (2010) Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol Biol Evol 27:2691–2701

    Article  PubMed  CAS  Google Scholar 

  • Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832

    PubMed  Google Scholar 

  • Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  PubMed  CAS  Google Scholar 

  • Deschamps P, Colleoni C, Nakamura Y, Suzuki E, Putaux JL, Buleon A, Haebel S, Ritte G, Steup M, Falcon LI, Moreira D, Loffelhardt W, Raj JN, Plancke C, d’Hulst C, Dauvillee D, Ball S (2008) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548

    Article  PubMed  CAS  Google Scholar 

  • Eastmond PJ, Rawsthorne S (2000) Coordinate changes in carbon partitioning and plastidial metabolism during the development of oilseed rape embryo. Plant Physiol 122:767–774

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt U, Grimm B, Hörtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56:1–14

    Article  PubMed  CAS  Google Scholar 

  • Enami I, Iwai M, Akiyama A, Suzuki T, Okumura A, Katoh T, Tada O, Ohta H, Shen JR (2003) Comparison of binding and functional properties of two extrinsic components, Cyt c550 and a 12 kDa protein, in cyanobacterial PSII with those in red algal PSII. Plant Cell Physiol 44:820–827

    Article  PubMed  CAS  Google Scholar 

  • Facchinelli F, Weber APM (2011) Frontiers: the metabolite transporters of the plastid envelope: an update. Front Plant Physiol 2:50

    CAS  Google Scholar 

  • Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Häusler RE, Flügge UI (1997) A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 9:453–462

    PubMed  CAS  Google Scholar 

  • Fliege R, Flügge UI, Werdan K, Heldt HW (1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim Biophys Acta 502:232–247

    Article  PubMed  CAS  Google Scholar 

  • Flügge UI, Heldt HW (1984) The phosphate-triose phosphate-phosphoglycerate translocator of the chloroplast. Trends Biochem Sci 9:530–533

    Article  Google Scholar 

  • Grefen C, Donald N, Hashimoto K, Kudla J, Schumacher K, Blatt MR (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J 64:355–365

    Article  PubMed  CAS  Google Scholar 

  • Herrmann KM (1995) The Shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7:907–919

    PubMed  CAS  Google Scholar 

  • Huang JL, Gogarten JP (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8(9):R109

    Article  Google Scholar 

  • Journet EP, Douce R (1985) Enzymic capacities of purified cauliflower bud plastids for lipid-synthesis and carbohydrate-metabolism. Plant Physiol 79:458–467

    Article  PubMed  CAS  Google Scholar 

  • Kaundal R, Saini R, Zhao PX (2010) Combining machine learning and homology-based approaches to accurately predict subcellular localization in Arabidopsis. Plant Physiol 154:36–54

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383–5392

    Article  PubMed  CAS  Google Scholar 

  • Koike H, Ikeda Y, Yusa F, Kashino Y, Satoh K (2007) Isolation and characterization of outer and inner envelope membranes of cyanelles from a glaucocystophyte, Cyanophora paradoxa. Photosynth Res 93:45–53

    Article  PubMed  CAS  Google Scholar 

  • Lamesch P, Berardini TZ, Li DH, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210

    Article  PubMed  CAS  Google Scholar 

  • Linka N, Weber APM (2010) Intracellular metabolite transporters in plants. Mol Plant 3:21–53

    Article  PubMed  CAS  Google Scholar 

  • Linka M, Jamai A, Weber AP (2008) Functional characterization of the plastidic phosphate translocator gene family from the thermo-acidophilic red alga Galdieria sulphuraria reveals specific adaptations of primary carbon partitioning in green plants and red algae. Plant Physiol 148:1487–1496

    Article  PubMed  CAS  Google Scholar 

  • Löffelhardt W, Haeseler A, Schleiff E, Margulis L, Hall J, McFall-Ngai M (2007) The β-barrel shaped polypeptide transporter, an old concept for precursor protein transfer across membranes, vol 44. Balaban, Rehovot, Israel, pp 33–42

    Google Scholar 

  • Marin B, Nowack EC, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:425–432

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  PubMed  CAS  Google Scholar 

  • McFadden G, Melkonian M (1986) Use of Hepes buffer for microalgal culture media and fixation for electron microscopy. Phycologia 25:551–557

    Article  CAS  Google Scholar 

  • Miernyk JA, Dennis DT (1992) A developmental analysis of the enolase Isozymes from Ricinus communis. Plant Physiol 99:748–750

    Article  PubMed  CAS  Google Scholar 

  • Mitra SK, Gantt JA, Ruby JF, Clouse SD, Goshe MB (2007) Membrane proteomic analysis of Arabidopsis thaliana using alternative solubilization techniques. J Proteome Res 6:1933–1950

    Article  PubMed  CAS  Google Scholar 

  • Moreira D, Le Guyader H, Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405:69–72

    Article  PubMed  CAS  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    Article  PubMed  Google Scholar 

  • Moustafa A, Reyes-Prieto A, Bhattacharya D (2008) Chlamydiae has contributed at least 55 genes to plantae with predominantly plastid functions. Plos One 3 e2205

  • Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646–4658

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge JB, Jaworski JG (1997) Regulation of fatty acid synthesis. Annu Rev Plant Biol 48:109–136

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Prabhakar V, Lottgert T, Gigolashvili T, Bell K, Flügge UI, Häusler RE (2009) Molecular and functional characterization of the plastid-localized phosphoenolpyruvate enolase (ENO1) from Arabidopsis thaliana. FEBS Lett 583:983–991

    Article  PubMed  CAS  Google Scholar 

  • Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, Schwacke R, Gross J, Blouin NA, Lane C (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843–847

    Article  PubMed  CAS  Google Scholar 

  • Qiu H, Yang EC, Bhattacharya D, Yoon HS (2012) Ancient gene paralogy may mislead inference of plastid phylogeny. Mol Biol Evol 29:3333–3343

    Article  PubMed  CAS  Google Scholar 

  • Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, Rebeille F, Douce R (2004) Methionine metabolism in plants—chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. J Biol Chem 279:22548–22557

    Article  PubMed  CAS  Google Scholar 

  • Robert V, Volokhina EB, Senf F, Bos MP, Van Gelder P, Tommassen J (2006) Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4:1984–1995

    Article  CAS  Google Scholar 

  • Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387

    Article  PubMed  CAS  Google Scholar 

  • Ruuska SA, Schwender J, Ohlrogge JB (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol 136:2700–2709

    Article  PubMed  CAS  Google Scholar 

  • Schenk H (1970) Nachweis einer lysozymempfindlichen Stützmembran der Endocyanellen von Cyanophora paradoxa (Korschikoff). Z Naturforsch 25b:656

  • Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6:1023–1027

    Article  PubMed  CAS  Google Scholar 

  • Schulze-Siebert D, Heineke D, Scharf H, Schultz G (1984) Pyruvate-derived amino acids in spinach chloroplasts: synthesis and regulation during photosynthetic carbon metabolism. Plant Physiol 76:465–471

    Article  PubMed  CAS  Google Scholar 

  • Schwöppe C, Winkler HH, Neuhaus HE (2002) Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp) and the glucose-6-phosphate sensor from Escherichia coli (UhpC). J Bacteriol 184:2108–2115

    Article  PubMed  Google Scholar 

  • Soll J, Kemmerling M, Schultz G (1980) Tocopherol and plastoquinone synthesis in spinach chloroplasts subfractions. Arch Biochem Biophys 204:544–550

    Article  PubMed  CAS  Google Scholar 

  • Steiner JM, Serrano A, Allmaier G, Jakowitsch J, Löffelhardt W (2000) Cytochrome c(6) from Cyanophora paradoxa—characterization of the protein and the cDNA of the precursor and import into isolated cyanelles. Eur J Biochem 267:4232–4241

    PubMed  CAS  Google Scholar 

  • Steiner JM, Löffelhardt W (2002) Protein import into cyanelles. Trends Plant Sci 7:72–77

    Google Scholar 

  • Steiner JM, Yusa F, Pompe JA, Löffelhardt W (2005) Homologous protein import machineries in chloroplasts and cyanelles. Plant J 44:646–652

    Article  PubMed  CAS  Google Scholar 

  • Stitt M, Ap Rees T (1979) Capacities of pea-chloroplasts to catalyze the oxidative pentose-phosphate pathway and glycolysis. Phytochemistry 18:1905–1911

    Article  CAS  Google Scholar 

  • Struyvé M, Moons M, Tommassen J (1991) Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218:141–148

    Article  PubMed  Google Scholar 

  • Thangaraj B, Ryan CM, Souda P, Krause K, Faull KF, Weber APM, Fromme P, Whitelegge JP (2010) Data-directed top-down Fourier-transform mass spectrometry of a large integral membrane protein complex: photosystem II from Galdieria sulphuraria. Proteomics 10:3644–3656

    Article  PubMed  CAS  Google Scholar 

  • Thornton LE, Ohkawa H, Roose JL, Kashino Y, Keren N, Pakrasi HB (2004) Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 16:2164–2175

    Article  PubMed  CAS  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  PubMed  CAS  Google Scholar 

  • Tusnady GE, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol 283:489–506

    Article  PubMed  CAS  Google Scholar 

  • Tyra HM, Linka M, Weber A, Bhattacharya D (2007) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8:R212

    Article  PubMed  Google Scholar 

  • Van Der Straeten D, Rodrigues-Pousada RA, Goodman HM, Van Montagu M (1991) Plant enolase: gene structure, expression, and evolution. Plant Cell 3:719–735

    PubMed  Google Scholar 

  • van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155:1578–1588

    Article  PubMed  Google Scholar 

  • Weber APM, Linka N (2011) Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62:53–77

    Article  PubMed  CAS  Google Scholar 

  • Weber APM, Oesterhelt C, Gross W, Brautigam A, Imboden LA, Krassovskaya I, Linka N, Truchina J, Schneidereit J, Voll H, Voll LM, Zimmermann M, Jamai A, Riekhof WR, Yu B, Garavito RM, Benning C (2004) EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55:17–32

    Article  PubMed  CAS  Google Scholar 

  • Weber APM, Linka M, Bhattacharya D (2006) Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot Cell 5:609–612

    Article  PubMed  CAS  Google Scholar 

  • Wolfe GR, Cunningham FX, Durnford D, Green BR, Gantt E (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367:566–568

    Article  CAS  Google Scholar 

  • Wunder T, Martin R, Löffelhardt W, Schleiff E, Steiner JM (2007) The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol Biol 7:236

    Article  PubMed  Google Scholar 

  • Yusa F, Steiner JM, Löffelhardt W (2008) Evolutionary conservation of dual Sec translocases in the cyanelles of Cyanophora paradoxa. BMC Evol Biol 8:304

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Work in the authors’ laboratories was supported by grants of the Deutsche Forschungsgemeinschaft (CRC TR1, projects B9 and C12). Additionally, we acknowledge Youlia Davidova for MS analysis.

Author information

Authors and Affiliations

  1. Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine-University, Universitätsstraße 1, 40225, Düsseldorf, Germany

    Fabio Facchinelli, Nina J. Ebert & Andreas P. M. Weber

  2. Lehrstuhl für Botanik, Department Biologie I, Ludwig-Maximilians-Universität, 82152, Planegg-Martinsried, Germany

    Mathias Pribil & Dario Leister

  3. Mass Spectrometry Unit, Department Biologie I, Ludwig-Maximilians-Universität, 82152, Planegg-Martinsried, Germany

    Mathias Pribil & Ulrike Oster

  4. Department of Ecology, Evolution, and Natural Resources and Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, 08901, USA

    Debashish Bhattacharya

Authors
  1. Fabio Facchinelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mathias Pribil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ulrike Oster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nina J. Ebert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Debashish Bhattacharya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dario Leister
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andreas P. M. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas P. M. Weber.

Additional information

A contribution to the Special Issue on Evolution and Biogenesis of Chloroplasts and Mitochondria.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 446kb)

Supplementary material 2 (JPEG 4.15mb)

Table S1 Protein identification for each sample and replicate (PDF 431 kb)

425_2012_1819_MOESM4_ESM.pdf

Table S2 Summary of the protein identifications with annotations based on blast2GO, TAIR and KEGG. For each protein identified the sequence, the number of predicted transmembrane domains (Tusnady and Simon 1998) and the number of assigned spectra for each replicate are indicated (PDF 672 kb)

Table S3 Subcellular localization prediction of the identified proteins by AtSubP (PDF 649 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1819-3

Keywords

Search

Navigation