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Changes induced by the Pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana

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Abstract

We have analyzed the chloroplast proteome of Nicotiana benthamiana using two-dimensional gel electrophoresis and mass spectrometry followed by a database search. In order to improve the resolution of the two-dimensional electrophoresis gels, we have made separate maps for the low and the high pH range. At least 200 spots were detected. We identified 72 polypeptides, some being isoforms of different multiprotein families. In addition, changes in this chloroplast proteome induced by the infection with the Spanish strain of the Pepper mild mottle virus were investigated. Viral infection induced the down-regulation of several chloroplastidic proteins involved in both the photosynthetic electron-transport chain and the Benson–Calvin cycle.

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Abbreviations

2-DE:

Two-dimensional gel electrophoresis

CF1 :

ATP-ase coupling factor

CP:

Coat protein

Cyt. f:

Cytochrome f

FNR:

Ferredoxin-NADP+ reductase

GS:

Glutamine synthetase

Hsp70:

Heat-shock protein 70 kDa

IEF:

Isoelectrofocusing

Lhca:

Photosystem I chlorophyll a/b binding proteins

Lhcb:

Photosystem II chlorophyll a/b binding proteins

MALDI:

Matrix-assisted laser desorption/ionization

M r :

Relative molecular mass

MS:

Mass spectrometry

OEC:

Oxygen-evolving complex

PGK:

Phosphoglycerate kinase

pI:

Isoelectrical point

PMMoV-S:

Spanish strain of Pepper mild mottle virus

PRK:

Phosphoribulokinase

PsaC, PsaD and PsaE:

C, D and E proteins, respectively of the photosystem I core complex

PsbO, PsbP and PsbQ:

33, 24 and 16 kDa extrinsic proteins of the photosystem II oxygen-evolving complex

PSI:

Photosystem I

PSII:

Photosystem II

RbcL and RbcS:

Ribulose 1, 5 bisphosphate carboxylase oxygenase large and small subunits, respectively

RuBisCO:

Ribulose 1, 5 bisphosphate carboxylase oxygenase

Rca:

Ribulose 1, 5 bisphosphate carboxylase oxygenase activase

SBPase:

Sedoheptulose-1, 7-bisphosphatase

TOF/TOF:

Time-of-flight tandem mass spectrometry

References

  • Alonso E, García-Luque I, Ávila-Rincón MJ, Wicke B, Serra MT, Díaz-Ruiz JR (1989) A tobamovirus causing heavy losses in protected pepper crops in Spain. J Phytopathol 125:67–76

    Google Scholar 

  • Andaluz S, López-Millán AF, De Las Rivas J, Aro EM, Abadía J, Abadía A (2006) Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth Res 89:141–155

    CAS  PubMed  Google Scholar 

  • Anderson LE, Gibbons JT, Wang X (1996) Distribution of ten enzymes of carbon metabolism in pea (Pisum sativum) chloroplasts. Int J Plant Sci 157:525–538

    CAS  Google Scholar 

  • Aro EM, Soursa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamaki E (2005) Dynamics of photosystem II a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    CAS  PubMed  Google Scholar 

  • Bagginsky S, Gruissem W (2004) Chloroplast proteomics: potentials and challenges. J Exp Bot 400:1213–1220

    Google Scholar 

  • Banks FM, Driscoll SP, Parry MAJ, Lawlor DW, Knight JS, Gray JC, Paul MJ (1999) Decrease in phosphoribulokinase activity by antisense RNA in transgenic tobacco. Relationship between photosynthesis, growth and allocation at different nitrogen levels. Plant Physiol 119:1125–1136

    CAS  PubMed  Google Scholar 

  • Buchanan BB, Wilhelm G, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Biologist, Rockville

    Google Scholar 

  • Cánovas FM, Dumas-Gaudot E, Recorbet G, Jorrín JV, Mock H-P, Rossignol M (2004) Plant proteome analysis. Proteomics 4:285–298

    PubMed  Google Scholar 

  • Chaerle L, Pineda M, Romero-Aranda R, Van Der Straeten D, Barón M (2006) Robotized thermal and chlorophyll fluorescence imaging of pepper mild mottle virus infection in Nicotiana benthamiana. Plant Cell Physiol 47:1323–1336

    CAS  PubMed  Google Scholar 

  • Cheregi O, Sicora C, Kos PB, Nixon PJ, Vass I (2005) The FtsH protease is required for the repair of photosystem II in the cyanobacterium Synechocystis 6803 damaged by UV-B radiation. BMC Plant Biol 5: S8. (Meeting abstract)

  • Ciambella C, Roepstorff P, Aro EM, Zolla L (2005) A proteomics approach for investigation of photosynthetic apparatus in plants. Proteomics 5:746–757

    CAS  PubMed  Google Scholar 

  • Corbett JM, Dunn MJ, Posch A, Görg A (1994) Positional reproducibility of protein spots in two-dimensional polyacrylamide gel electrophoresis using immobilized pH gradient isoelectric focusing in the first dimension: an interlaboratory comparison. Electrophoresis 15:1205–1211

    CAS  PubMed  Google Scholar 

  • Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172

    CAS  PubMed  Google Scholar 

  • Curto M, Camafeita E, López JA, Maldonado AM, Rubiales D, Jorrín JV (2006) A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi). Proteomics 6:S163–S174

    PubMed  Google Scholar 

  • Díaz-Vivancos P, Clemente-Moreno M, Rubio M, Olmos E, García JA, Martínez-Gómez P, Hernández JA (2008) Alteration in the chloroplastic metabolism leads to ROS accumulation in pea plants in response to Plum pox virus. J Exp Bot 59:2147–2160

    PubMed  Google Scholar 

  • Feng L, Wag K, Li Y, Tan Y, Kong J, Li H, Li Y, Zhu Y (2007) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26:1635–1646

    CAS  PubMed  Google Scholar 

  • Ferro M, Salvi D, Riviére-Rolland H, Vermat T, Seigneurin-Berny D, Grunwald D, Garin J, Joyard J, Rolland N (2002) Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc Natl Acad Sci USA 99:11487–11492

    CAS  PubMed  Google Scholar 

  • Foyer CH, Harbinson J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense system in plants. CRC Press, Boca Raton

    Google Scholar 

  • Friso G, Giacomelli L, Ytterberg JA, Peltier JB, Rudella A, Sun Q, van Wijk KJ (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16:478–499

    CAS  PubMed  Google Scholar 

  • Giacomelli L, Rudella A, van Wijk KJ (2006) High light response of the thylakoid proteome in Arabidopsis wild type and the ascorbate-deficient mutant vtc2–2. A comparative proteomics study. Plant Physiol 141:685–701

    CAS  PubMed  Google Scholar 

  • Gontero B, Cárdenas ML, Ricard J (1988) A functional 5-enzyme complex of chloroplast involved in the Calvin cycle. Eur J Biochem 173:437–443

    CAS  PubMed  Google Scholar 

  • Görg A, Obermaier C, Boguth G, Harder A, Scheibe B, Wildgrupber R, Weiss W (2000) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21:1037–1053

    PubMed  Google Scholar 

  • Görlach J, Schmid J, Amrhein N (1993) The 33 kDa protein of the oxygen-evolving complex: a multi-gene family in tomato. Plant Cell Physiol 34:479–501

    Google Scholar 

  • Grzyb J, Malec P, Rumak I, Garstka M, Strzalka K (2008) Two isoforms of ferredoxin: NADP+ oxidoreductase from wheat leaves: purification and initial biochemical characterization. Photosynth Res 96:99–112

    CAS  PubMed  Google Scholar 

  • Haake V, Zrenner R, Sonnewald U, Stitt M (1998) A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J 14:147–157

    CAS  PubMed  Google Scholar 

  • Hajirezaei MR, Peisker M, Tschiersch H, Palatnik JF, Valle EM, Carrillo N, Sonnewald U (2002) Small changes in the activity of chloroplast NADP+-dependent ferredoxin reductase lead to impaired plant growth and restrict photosynthetic capacity of transgenic tobacco plants. Plant J 29:281–293

    CAS  PubMed  Google Scholar 

  • Haldrup A, Lunde C, Scheller HV (2003) Arabidopsis thaliana plants lacking the PSI-D subunit of photosystem I suffer photoinhibition, have unstable photosystem I complexes, and altered redox homeostasis in the chloroplast stroma. J Biol Chem 278:33276–33283

    CAS  PubMed  Google Scholar 

  • Hanke GT, Okutani S, Satomi Y, Takao T, Suzuki A, Hase T (2005) Multiple iso-proteins of FNR in Arabidopsis: evidence for different contributions to chloroplast function and nitrogen assimilation. Plant Cell Environ 28:1146–1157

    CAS  Google Scholar 

  • Harrison EP, Willingham NM, Lloyd JC, Raines CA (1998) Reduced sedoheptulosoe-1, 7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204:27–36

    CAS  Google Scholar 

  • Houtz RL, ARJr Portis (2003) The life of ribulose 1, 5-bisphosphate carboxylase/oxygenase—Posttranslational facts and mysteries. Arch Biochem Biophys 414:150–158

    CAS  PubMed  Google Scholar 

  • Hua SB, Dube SK, Barnett NM, Kung SD (1991a) Nucleotide sequence of a cDNA clone encoding 23 kDa polypeptide of the oxygen-evolving complex of photosystem II in tobacco, Nicotiana tabacum L. Plant Mol Biol 16:749–750

    CAS  PubMed  Google Scholar 

  • Hua SB, Dube SK, Barnett NM, Kung SD (1991b) Nucleotide sequence of gene oee2-A and its cDNA encoding 23 kDa polypeptide of the oxygen-evolving complex of photosystem II in tobacco. Plant Mol Biol 17:551–553

    CAS  PubMed  Google Scholar 

  • Hua SB, Dube SK, Kung SD (1993) Molecular evolutionary of the psbP gene family of the photosystem II oxygen-evolving complex in Nicotiana. Genome 36:483–488

    CAS  PubMed  Google Scholar 

  • Huber CG, Walcher W, Timperio A, Troiani S, Porceddu A, Zolla L (2004) Multidimensional proteomic analysis of photosynthetic membrane proteins by liquid extraction-ultracentrifugation-liquid chromatography-mass spectrometry. Proteomics 4:3909–3920

    CAS  PubMed  Google Scholar 

  • Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D (2004) Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J 37:839–852

    CAS  PubMed  Google Scholar 

  • Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B, Bender CL (2009) The phytotoxin coronatine induces light-dependent reactive oxygen species in tomato seedlings. New Phytol 181:147–160

    CAS  PubMed  Google Scholar 

  • Ishihara S, Yamamoto Y, Ifuku K, Sato F (2005) Functional analysis of four members of the PsbP family in photosystem II in Nicotiana tabacum using differential RANA interference. Plant Cell Physiol 46:1885–1893

    CAS  PubMed  Google Scholar 

  • Jebanathirajah JA, Coleman JR (1998) Association of carbonic anhydrase with a Calvin cycle enzyme complex in Nicotiana tabacum. Planta 204:177–182

    CAS  PubMed  Google Scholar 

  • Jones AME, Bennett MH, Mansfield JW, Grant M (2006) Analysis of the defence phosphoproteome of Arabidopsis thaliana using differential mass tagging. Proteomics 6:4155–4165

    CAS  PubMed  Google Scholar 

  • Jorrín JV, Maldonado AM, Castillejo MA (2007) Plant proteome analysis: a 2006 update. Proteomics 7:2947–2962

    PubMed  Google Scholar 

  • Jorrín JV, Maldonado AM, Echevarría-Zomeño S, Valledor L, Castillejo MA, Curto M, Valero J, Sghaier B, Donoso G, Redondo I (2009) Plant proteomics update (2007–2008): second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfil MIAPE standards, increase plant proteome coverage and expand biological knowledge. J Proteomics 72:285–314

    Google Scholar 

  • Kieselbach T, Hagman A, Andersson B, Schröder PW (2000) The thylakoid lumen of chloroplast. Isolation and characterization. J Biol Chem 273:6710–6716

    Google Scholar 

  • Kleffman T, Russenberger D, von Zychlinski A, Christopher W, Sjölander K, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14:354–362

    Google Scholar 

  • Koiwa H, Barb AW, Xiong L, Li F, McCully MG, Lee B, Sokolchik I, Zhu J, Gong Z, Reddy M, Sharkhuu A, Manabe Y, Yokoi S, Zhu JK, Bressan RA, Hasegawa PM (2002) C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signalling, growth, and development. Proc Nat Acad Sci 99:10893–10898

    CAS  PubMed  Google Scholar 

  • Laganowsky A, Gómez SM, Whitelegge JP, Nishio JN (2009) Hydroponics on a chip: analysis of the Fe deficient Arabidopsis thilakoid membrane proteome. J Proteomics 72:397–415

    CAS  PubMed  Google Scholar 

  • Lintala M, Allahverdiyeva Y, Kidron H, Piippo M, Battchikova N, Suorsa M, Rintamäki E, Salminen TA, Aro E-M, Mulo P (2007) Structural and functional characterization of ferredoxin-NADP+-oxidoreductase using knock-out mutants of Arabidopsis. Plant J 49:1041–1052

    CAS  PubMed  Google Scholar 

  • Masclaux-Daubresse C, Carrayol E, Valadier MH (2005) The two nitrogen mobilisation- and senescence-associated GS1 and GDH genes are controlled by C and N metabolites. Planta 221:580–588

    CAS  PubMed  Google Scholar 

  • Merkle TH, Krenz M, Wenng A, Schäfer E (1990) Nucleotide sequence and deduced amino acid sequence of a gene encoding the 23 kDa polypeptide of the oxygen-evolving complex from mustard (Sinapis alba L). Plant Mol Biol 14:889–890

    CAS  PubMed  Google Scholar 

  • Montesano M, Scheller HV, Wettstein R, Palva ET (2004) Down-regulation of photosystem I by Erwinia carotovora-derived elicitors correlates with H2O2 accumulation in chloroplasts of potato. Mol Plant Pathol 5:115–123

    CAS  Google Scholar 

  • Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F (2005) Functional dissection of two Arabidopsis PsbO2. FEBS J 272:2165–2175

    CAS  PubMed  Google Scholar 

  • Naver H, Haldrup A, Scheller HV (1999) Cosuppression of photosystem I subunit PSI-H in Arabidopsis thaliana. Efficient electron transfer and stability of photosystem I is dependent upon the PSI-H subunit. J Biol Che. 274:10784–10789

    CAS  Google Scholar 

  • Newton RP, Brenton AG, Smith CJ, Dudley E (2004) Plant proteome analysis by mass spectrometry: principles, problems, pitfalls and recent developments. Phytochemistry 65:1449–1485

    CAS  PubMed  Google Scholar 

  • Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357–363

    CAS  PubMed  Google Scholar 

  • Obokata J, Mikami K, Hayashida N, Nakamura M, Sugiera M (1993) Molecular heterogeneity of photosystem I. psaD, psaE, psaF, psaH and psaL are all present in isoforms in Nicotiana spp. Plant Physiol 102:1259–1267

    CAS  PubMed  Google Scholar 

  • Obokata J, Mikami K, Yamamoto Y, Hayashida N (1994) Microheterogeneity of PSI-E subunit of photosystem I in Nicotiana sylvestris. Plant Cell Physiol 35:203–209

    CAS  PubMed  Google Scholar 

  • Okutani S, Hanke GT, Satomi Y, Takao T, Kurisu G, Suzuki A, Hase T (2005) Three maize leaf ferredoxin:NADP(+) oxidoreductase vary in subchloroplast location, expression, and interaction with ferredoxin. Plant Physiol 139:1451–1459

    CAS  PubMed  Google Scholar 

  • Peltier JB, Friso G, Kalume ED, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplasts: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12:319–341

    CAS  PubMed  Google Scholar 

  • Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Söderberg L, Roepstorff P, von Heijne G, van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14:211–236

    CAS  PubMed  Google Scholar 

  • Peltier JB, Ytterberg JA, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279:49367–49383

    CAS  PubMed  Google Scholar 

  • Pérez-Bueno ML (2003) Photosystem II and viral infection: analysis of fluorescence imaging and regulation of the synthesis of the oxygen-evolving-complex proteins during pathogenesis. Ph. D. Thesis, Granada University, Spain

  • Pérez-Bueno ML, Rahoutei J, Sajnani C, García-Luque I, Barón M (2004) Proteomic analysis of the oxygen-evolving complex of photosystem II under biotic stress. Studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425

    PubMed  Google Scholar 

  • Pérez-Bueno ML, Ciscato M, vandeVen M, García-Luque I, Valcke R, Barón M (2006) Imaging viral infection. Studies on Nicotiana benthamiana plants infected with the pepper mild mottle tobamovirus. Photosynth Res 90:111–123

    PubMed  Google Scholar 

  • Phee B-K, Cho J-H, Park S, Jung JH, Lee Y-H, Jeong J-S, Bhoo SH, Hahn T-R (2004) Proteomic analysis of the response of Arabidopsis chloroplast proteins to high light stress. Proteomics 4:3560–3568

    CAS  PubMed  Google Scholar 

  • Pineda M, Gáspár L, Morales F, Szigeti Z, Barón M (2008a) Multicolour fluorescence imaging: a useful tool to visualise systemic viral infections in plants. Photochem Photobiol 84:1048–1060

    CAS  PubMed  Google Scholar 

  • Pineda M, Soukupová J, Matouš K, Nedbal L, Barón M (2008b) Conventional and combinatorial chlorophyll fluorescence imaging of tobamovirus-infected plants. Photosynthetica 46:441–451

    CAS  Google Scholar 

  • Rahoutei J, García-Luque I, Cremona V, Barón M (1998) Effect of tobamovirus infection on PSII complex of infected plants. In: Garab G (ed) Photosynthesis: from light to biosphere. Kluwer, Dordrecht

    Google Scholar 

  • Rahoutei J, García-Luque I, Barón M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plant 110:286–292

    CAS  Google Scholar 

  • Raines CA (2003) The Calvin cycle revisited. Photosynth Res 110:286–292

    Google Scholar 

  • Reche A, Lázaro JJ, Hermoso R, Chueca A, López Gorgé J (1997) Binding and activation of pea chloroplast fructosa-1, 6-biphosphatase by homologous thioredoxins m and f. Physiol Plantarum 101:463–470

    CAS  Google Scholar 

  • Rodríguez Andrés A, Lázaro JJ, Chueca A, Hermoso R, López Gorgé J (1987) Binding of photosynthetic fructose- 1, 6- bisphosphatase to chloroplast membranes. Plant Sci 52:41–48

    Google Scholar 

  • Rodríguez RE, Lodeyro A, Poli HO, Zurbriggen M, Peisker M, Palatnik JF, Tognetti VB, Tschiersch H, Hajirezaei MR, Valle EM, Carrillo N (2007) Transgenic tobacco plants overexpressing chloroplastic ferredoxin-NADP(H) reductase display normal rates of photosynthesis and increased tolerance to oxidative stress. Plant Physiol 143:639–649

    PubMed  Google Scholar 

  • Rokka A, Zhang L, Aro EM (2001) RuBisCO activase: an enzyme with a temperature-dependent dual function? Plant J 25:463–471

    CAS  PubMed  Google Scholar 

  • Rose JK, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733

    CAS  PubMed  Google Scholar 

  • Rossignol M (2001) Analysis of the plant proteome. Curr Opin Biotech 12:131–134

    CAS  PubMed  Google Scholar 

  • Rossignol M, Peltier J-B, Mock H-P, Matros A, Maldonado AM, Jorrín JV (2006) Plant proteome analysis: a 2004–2006 update. Proteomics 6:5529–5548

    CAS  PubMed  Google Scholar 

  • Sajnani C, Zurita JL, Roncel M, Ortega JM, Barón M, Ducruet J-M (2007) Changes in photosynthetic metabolism induced by tobamovirus inection in Nicotiana benthamiana studied in vivo by thermoluminescence. New Phytol 175:120–130

    CAS  PubMed  Google Scholar 

  • Sánchez de Jiménez E, Medrano L, Martínez-Barajas E (1995) RuBisCO-activase, a possible new member of the molecular chaperone family. Biochemistry 34:2826–2831

    PubMed  Google Scholar 

  • Schägger H, Cramer WA, von Jagow G (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217:220–230

    PubMed  Google Scholar 

  • Schevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 68:850–858

    Google Scholar 

  • Schroda M, Kropat J, Oster U, Rudiger W, Vallon O, Wollman FA, Beck CF (2001) Possible role for molecular chaperones in assembly and repair of photosystem II. Biochem Soc Trans 29:413–418

    CAS  PubMed  Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schöder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    CAS  PubMed  Google Scholar 

  • Schuster AM, Davies E (1983) Ribonucleic acid and protein metabolism in pea epicotyls. Plant Physiol 73:809–816

    CAS  PubMed  Google Scholar 

  • Sétif P, Fischer N, Lagoutte B, Bottin H, Rochaix J-D (2002) The ferredoxin docking site of photosystem I. Biochim Biophys Acta 1555:204–209

    PubMed  Google Scholar 

  • Steinberg TH, Jones LJ, Haugland RP, Singer VL (1996) SYPRO Orange and SYPRO Red Protein gel stains: one-step fluorescent staining of denaturing gels for detection of nanogram levels of protein. Anal Biochem 239:223–237

    CAS  PubMed  Google Scholar 

  • Suckau D, Resemann A, Schuerenberg M, Hufnagel P, Franzen J, Holle A (2003) A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal Bioanal Chem 376:952–965

    CAS  PubMed  Google Scholar 

  • Süss KH, Arkona C, Manteuffel R, Adler K (1993) Calvin cycle multienzyme complexes are bound to chloroplast thylakoid membranes of higher plants in situ. Proc Natl Acad Sci USA 90:5514–5518

    PubMed  Google Scholar 

  • Süss KH, Prokhorenko I, Adler K (1995) In situ association of Calvin cycle enzymes, ribulose-1, 5-bisphosphate carboxylase/oxygenase activase, ferredoxin-NADP+ reductase, and nitrite reductase with thylakoid and pyrenoid membranes of chlamydomonas reinhardtii chloroplasts as revealed by immunoelectron microscopy. Plant Physiol 107:1387–1397

    PubMed  Google Scholar 

  • Takahashi H, Ehara Y, Hirano H (1991) A protein in the oxygen-evolving complex in the chloroplasts is associated with symptom expression on tobacco leaves infected with cucumber mosaic virus strain Y. Plant Mol Biol 16:689–698

    CAS  PubMed  Google Scholar 

  • Tanaka M, Wakasugi T, Sugita M, Shinozaki K, Sugiura M (1986) Genes for the eight ribosomal proteins are clustered on the chloroplast genome of tobacco (Nicotiana tabacum): similarity to the S10 and spc operons of Escherichia coli. Proc Natl Acad Sci USA 83:6030–6034

    CAS  PubMed  Google Scholar 

  • Taylor NL, Tan Y-F, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteomics 72:367–378

    CAS  PubMed  Google Scholar 

  • Teixeira J, Pereira S, Cánovas F, Salema R (2005) Glutamine synthetase of potato (Solanum tuberosum L. cv. Desiree) plants: cell- and organ-specific roles in nitrogen assimilation and mobilization. J Exp Bot 56:663–671

    CAS  PubMed  Google Scholar 

  • Timperio AM, D’Amici GM, Barta C, Loreto F, Zolla L (2007) Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J Exp Bot 58:3695–3710

    CAS  PubMed  Google Scholar 

  • van Wijk KJ (2001) Challenges and prospects of plant proteomics. Plant Physiol 126:501–508

    PubMed  Google Scholar 

  • van Wijk KJ (2004) Plastid proteomics. Plant Physiol Biochem 42:963–977

    PubMed  Google Scholar 

  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    PubMed  Google Scholar 

  • Wales R, Nweman BJ, Pappin D, Gray JC (1989) The extrinsic 33 kDa polypeptide of the oxygen-evolving complex of photosystem II is a putative calcium-binding protein and is encoded by a multi-gene family in pea. Plant Mol Biol 12:439–451

    CAS  Google Scholar 

  • Whitelegge JP (2003) Thylakoid membrane proteomics. Photosynth Res 78:265–277

    CAS  PubMed  Google Scholar 

  • Wilson KA, McManus MT, Gordon ME, Jordan TW (2002) The proteomics of senescence in leaves of white clover, Trifolium repens L. Proteomics 2:1114–1122

    CAS  PubMed  Google Scholar 

  • Yamada S, Komori T, Hashimoto A, Kuwata S, Imaseki H, Kubo T (2000) Differential expression of plastidic aldolase genes in Nicotiana plants under salt stress. Plant Sci 54:61–69

    Google Scholar 

  • Yamamoto Y, Tsuji H, Obokata J (1993) Structure and expression of a nuclear gene for the PSI-D subunit of photosystem I in Nicotiana sylvestris. Plant Mol Biol 22:985–994

    CAS  PubMed  Google Scholar 

  • Yan JX, Wait R, Berkelman T, Harry RA, Westbrook JA, Wheeler CH, Dunn MJ (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray-mass spectrometry. Electrophoresis 21:3666–3672

    CAS  PubMed  Google Scholar 

  • Zaltsman A, Feder A, Adam Z (2005a) Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts—implications for thylakoid formation and photosystem II maintenance. Plant J 42:609–617

    CAS  PubMed  Google Scholar 

  • Zaltsman A, Ori N, Adam Z (2005b) Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17:2782–2790

    CAS  PubMed  Google Scholar 

  • Zhou W, Eudes F, Laroche A (2006) Identification of differentialy regulated proteins in response to a compatible interaction between the pathogen Fusarium graminearum and its host, Triticum aestivum. Proteomics 6:4599–4609

    CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by grants from the Spanish Government (BIO2004-04968-C02-02, BIO2007-67874-C02-02 and AGL2008-00214 to M.B.) and FEDER Funds. The authors are very grateful to Drs. Isabel García Luque and Maite Serra (Centro Investigaciones Biológicas, CSIC, Madrid) for providing all PMMoV solutions and antibodies against the viral-coat protein. In addition, they thank J.A. López, E. Camafeita and E. Calvo from the Proteomic Unit of the National Centre for Cardiovascular Research (Madrid, Spain) for the skilful assistance with the MALDI/TOF-TOF analysis and protein identification.

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Correspondence to M. Barón.

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Pineda, M and Sajnani, C, These authors have contributed equally to this work and are placed in alphabetical order.

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Pineda, M., Sajnani, C. & Barón, M. Changes induced by the Pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana . Photosynth Res 103, 31–45 (2010). https://doi.org/10.1007/s11120-009-9499-y

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  • DOI: https://doi.org/10.1007/s11120-009-9499-y

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