Targeted quantitative analysis of a diurnal RuBisCO subunit expression and translation profile in Chlamydomonas reinhardtii introducing a novel Mass Western approach

Journal of Proteomics

Volumn 113, Issue , 2015, Pages 143-153

  Recuenco Muñoz, Luis ^a   Offre, Pierre ^a   Valledor, Luis ^a   Lyon, David ^a   Weckwerth, Wolfram ^a   Wienkoop, Stefanie ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

Chlamydomonas reinhardtii; Mass Western; Protein complex stoichiometry; RuBisCO; SRM; Targeted protein absolute quantification

Indexed keywords

HOLOENZYME; RIBULOSEBISPHOSPHATE CARBOXYLASE; SYNTHETIC PEPTIDE; CHLOROPLAST PROTEIN; RBCL PROTEIN, PLASTID;

ARTICLE; CHLAMYDOMONAS REINHARDTII; GENE EXPRESSION; LIGHT; LIGHT DARK CYCLE; MASS WESTERN; METHODOLOGY; NONHUMAN; OSCILLATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SUBUNIT; QUANTITATIVE ANALYSIS; STOICHIOMETRY; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; MASS SPECTROMETRY; PHOTOPERIODICITY; PHYSIOLOGY; PROCEDURES; PROTEOMICS;

CHLAMYDOMONAS REINHARDTII;

CHLAMYDOMONAS REINHARDTII; CHLOROPLAST PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; MASS SPECTROMETRY; PHOTOPERIOD; PROTEOMICS; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84908388827     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.09.026     Document Type: Article

References (60)

1. Barr J.R., Maggio V.L., Patterson D.G., Cooper G.R., Henderson L.O., Turner W.E., et al. Isotope dilution-mass spectrometric quantification of specific proteins: model application with apolipoprotein A-I. Clin Chem 1996, 42:1676-1682.
2. Barnidge D.R., Dratz E.a, Martin T., Bonilla L.E., Moran L.B., Lindall A. Absolute quantification of the G protein-coupled receptor rhodopsin by LC/MS/MS using proteolysis product peptides and synthetic peptide standards. Anal Chem 2003, 75:445-451.
3. Wienkoop S., Larrainzar E., Glinski M., Gonzalez E.M., Arrese-Igor C., Weckwerth W. Absolute quantification of Medicago truncatula sucrose synthase isoforms and N-metabolism enzymes in symbiotic root nodules and the detection of novel nodule phosphoproteins by mass spectrometry. J Exp Bot 2008, 59:3307-3315.
4. Wienkoop S., Weiss J., May P., Kempa S., Irgang S., Recuenco-Munoz L., et al. Targeted proteomics for Chlamydomonas reinhardtii combined with rapid subcellular protein fractionation, metabolomics and metabolic flux analyses. Mol Biosyst 2010, 6:1018-1031.
5. Lehmann U., Wienkoop S., Tschoep H., Weckwerth W. If the antibody fails-a Mass Western approach. Plant J 2008, 55:1039-1046.
6. Holzmann J., Pichler P., Madalinski M., Kurzbauer R., Mechtler K. Stoichiometry determination of the MP1-p14 complex using a novel and cost-efficient method to produce an equimolar mixture of standard peptides. Anal Chem 2009, 81:10254-10261.
7. Johnson X. Manipulating RuBisCO accumulation in the green alga, Chlamydomonas reinhardtii. Plant Mol Biol 2011, 76:397-405.
8. Feller U., Anders I., Mae T. Rubiscolytics: fate of RuBisCo after its enzymatic function in a cell is terminated. J Exp Bot 2008, 59:1615-1624.
9. Wostrikoff K., Stern D. RuBisCO large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc Natl Acad Sci U S A 2007, 104:6466-6471.
10. Khrebtukova I., Spreitzer R.J. Elimination of the Chlamydomonas gene family that encodes the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci U S A 1996, 93:13689-13693.
11. Mishkind M.L., Schmidt G.W. Posttranscriptional regulation of ribulose 1,5-bisphosphate carboxylase small subunit accumulation in Chlamydomonas reinhardtii. Plant Physiol 1983, 72:847-854.
12. Wang Z., Wang T. Dynamic proteomic analysis reveals diurnal homeostasis of key pathways in rice leaves. Proteomics 2011, 11:225-238.
13. Pilgrim M.L., McClung C.R. Differential involvement of the circadian clock in the expression of genes required for ribulose-1,5-bisphosphate carboxylase/oxygenase synthesis, assembly, and activation in Arabidopsis thaliana. Plant Physiol 1993, 103:553-564.
14. Winder T.L., Anderson J.C., Spalding M.H. Translational regulation of the large and small subunits of ribulose bisphosphate carboxylase/oxygenase during induction of the CO(2)-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 1992, 98:1409-1414.
15. Shapira M., Lers a, Heifetz P.B., Irihimovitz V., Osmond C.B., Gillham N.W., et al. Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress transiently suppresses synthesis of the RuBisCO LSU protein while enhancing synthesis of the PS II D1 protein. Plant Mol Biol 1997, 33:1001-1011.
16. Cohen I., Sapir Y., Shapira M. A conserved mechanism controls translation of RuBisCO large subunit in different photosynthetic organisms 1. Plant Physiol 2006, 141:1089-1097.
17. Genkov T., Spreitzer R.J. Highly conserved small subunit residues influence RuBisCO large subunit catalysis. J Biol Chem 2009, 284:30105-30112.
18. Merchant S.S., Prochnik S.E., Vallon O., Harris E.H., Karpowicz S.J., Witman G.B., et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318:245-250.
19. Chang R.L., Ghamsari L., Manichaikul A., Hom E.F.Y., Balaji S., Fu W., et al. Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism. Mol Syst Biol 2011, 7:518.
20. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
21. Olinares P.B.D., Ponnala L., Van Wijk K.J. Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry and hierarchical clustering. Mol Cell Biol 2010, 9:1594-1615.
22. Fiala G.J., Schamel W.W.a, Blumenthal B. Blue native polyacrylamide gel electrophoresis (BN-PAGE) for analysis of multiprotein complexes from cellular lysates. J Vis Exp 2011, 1-8.
23. Wienkoop S., Weckwerth W. Relative and absolute quantitative shotgun proteomics: targeting low-abundance proteins in Arabidopsis thaliana. J Exp Bot 2006, 57:1529-1535.
24. Tourna M., Freitag T.E., Prosser J.I. Stable isotope probing analysis of interactions between ammonia oxidizers. Appl Environ Microbiol 2010, 76:2468-2477.
25. Roze S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
26. Sun X., Weckwerth W. COVAIN: a toolbox for uni- and multivariate statistics, time-series and correlation network analysis and inverse estimation of the differential Jacobian from metabolomics covariance data. Metabolomics 2012, 8:81-93.
27. Lyon D., Weckwerth W., Wienkoop S. Mass Western for Absolute Quantification of Target Proteins and Considerations About the Instrument of Choice. Plant Proteomics Methods Protoc. Methods Mol. Biol. 2014, vol. 1072:199-208. Humana Press, Totowa, NJ. J.V. Jorrin-Novo, S. Komatsu, W. Weckwerth, S. Wienkoop (Eds.).
28. Millard P. The accumulation and storage of nitrogen by herbaceous plants. Plant Cell Environ 1988, 11:1365-1504.
29. Irving L.J., Robinson D. A dynamic model of RuBisCO turnover in cereal leaves. New Phytol 2006, 169:493-504.
30. Taylor T.C., Backlund a, Bjorhall K., Spreitzer R.J., Andersson I. First crystal structure of RuBisCO from a green alga, Chlamydomonas reinhardtii. J Biol Chem 2001, 276(48):159-164.
31. Peltier J.-B., Cai Y., Sun Q., Zabrouskov V., Giacomelli L., Rudella A., et al. The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 2006, 5:114-133.
32. Mastrobuoni G., Irgang S., Pietzke M., Aßmus H.E., Wenzel M., Schulze W.X., et al. Proteome dynamics and early salt stress response of the photosynthetic organism Chlamydomonas reinhardtii. BMC Genomics 2012, 13.
33. Ishihama Y., Oda Y., Tabata T., Sato T., Nagasu T., Rappsilber J., et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005, 4:1265-1272.
34. Zybailov B., Florens L., Washburn M. Quantitative shotgun proteomics using a protease with broad specificity and normalized spectral abundance factors. Mol Biosyst 2007, 3:354-360.
35. Larrainzar E., Wienkoop S., Scherling C., Kempa S., Ladrera R., Arrese-Igor C., et al. Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Mol Plant Microbe Interact 2009, 22:1565-1576.
36. Pratt J.M., Simpson D.M., Doherty M.K., Rivers J., Gaskell S.J., Beynon R.J. Multiplexed absolute quantification for proteomics using concatenated signature peptides encoded by QconCAT genes. Nat Protoc 2006, 1:1029-1043.
37. Aebersold R., Burlingame A.L., Bradshaw R.a. Western blots versus selected reaction monitoring assays: time to turn the tables?. Mol Cell Proteomics 2013, 12:2381-2382.
38. Makino A., Mae T., Ohira K. Colorimetric measurement of protein stained with Coomassie brilliant blue R on sodium dodecyl sulfate-polyacrylamide gel electrophoresis by eluting with formamide. Agric Biol Chem 1986, 50:1911-1912.
39. 2 and light in rice plants?. Plant Physiol 1997, 114:483-491.
40. Makino A., Osmond B. Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol 1991, 96:355-362.
41. Suzuki Y., Makino A., Mae T. Changes in the turnover of RuBisCO and levels of rbcL and rbcS in rice leaves from emergence to senescence. Plant Cell Environ 2001, 24:1353-1360.
42. Spreitzer R.J. Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys 2003, 414:141-149.
43. Van Lun M., van der Spoel D., Andersson I. Subunit interface dynamics in hexadecameric RuBisCO. J Mol Biol 2011, 411:1083-1098.
44. Tcherkez G.G.B., Farquhar G.D., Andrews T.J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci U S A 2006, 103:7246-7251.
45. Meyer M.T., Genkov T., Skepper J.N., Jouhet J., Mitchell M.C., Spreitzer R.J., et al. RuBisCO small-subunit α-helices control pyrenoid formation in Chlamydomonas. Proc Natl Acad Sci U S A 2012, 109:19474-19479.
46. Kawazoe R., Mahan K.M., Venghaus B.E., Carter M.L., Herrin D.L. Circadian regulation of chloroplast transcription in Chlamydomonas is accompanied by little or no fluctuation in RPOD levels or core RNAP activity. Mol Biol Rep 2012, 39:10565-10571.
47. Herrin D.L., Michaels A.S., Paul G.A. Regulation of genes encoding the large subunit of ribulose-l, 5-bisphosphate carboxylase and the photosystem II polypeptides D-1 and D-2 during the cell cycle of Chlamydomonas reinhardtii preparation of thylakoid membranes isolation of thylakoid membrane. J Cell Biol 1986, 103:1837-1845.
48. Salvadort M.L., Klein U., Bogorad L. Light-regulated and endogenous fluctuations of chloroplast transcript levels in Chlamydomonas. Regulation by transcription and RNA degradation. Plant J 1993, 3:213-219.
49. Choquet Y., Vallon O. Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie 2000, 82:615-634.
50. Kim J., Mullet J.E. A mechanism for light-induced translation of the rbcL mRNA encoding the large subunit of ribulose-1,5-bisphosphate carboxylase in barley chloroplasts. Plant Cell Physiol 2003, 44:491-499.
51. Nassoury N., Fritz L., Morse D. Circadian changes in ribulose-1,5-bisphosphate carboxylase/oxygenase distribution inside individual chloroplasts can account for the rhythm in dinoflagellate carbon fixation. Plant Cell 2001, 13:923-934.
52. Mitsuhashi W., Feller U. Effects of light and external solutes on the catabolism of nuclear-encoded stromal proteins in intact chloroplasts isolated from pea leaves. Plant Physiol 1992, 100:2100-2105.
53. Desimone M., Henke a, Wagner E. oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 1996, 111:789-796.
54. Ishida H., Nishimori Y., Sugisawa M., Makino a, Mae T. The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented into 37-kDa and 16-kDa polypeptides by active oxygen in the lysates of chloroplasts from primary leaves of wheat. Plant Cell Physiol 1997, 38:471-479.
55. Ishida H., Shimizu S., Makino a, Mae T. Light-dependent fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts isolated from wheat leaves. Planta 1998, 204:305-309.
56. Ishida H., Makino a, Mae T. Fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species occurs near Gly-329. J Biol Chem 1999, 274:5222-5226.
57. Foyer C.H. Stromal protein phosphorylation in spinach (Spinacia oleracea) chloroplasts. Biochem J 1985, 231:97-103.
58. Blowers A., Klein U., Ellmore G., Bogorad L. Functional in vivo analyses of the 3' flanking sequences of the Chlamydomonas chloroplast rbcL and psaB genes. Mol Gen Genet MGG 1993, 238:339-349.
59. Pang Q., Chen S., Dai S., Chen Y., Wang Y., Yan X. Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res 2010, 9:2584-2599.
60. Aranjuelo I., Molero G., Erice G., Christophe Avice J., Nogues S. Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). J Exp Bot 2011, 62:111-123.