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PMID: 19423572 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism.

Molecular & cellular proteomics : MCP ·Vol. 8 ·No. 8 ·2009-08-00 ·Pages 1789-1810

Zybailov B, Friso G, Kim J, Rudella A, Rodríguez VR, Asakura Y, Sun Q, van Wijk KJ

Abstract

The clpr2-1 mutant is delayed in development due to reduction of the chloroplast ClpPR protease complex. To understand the role of Clp proteases in plastid biogenesis and homeostasis, leaf proteomes of young seedlings of clpr2-1 and wild type were compared using large scale mass spectrometry-based quantification using an LTQ-Orbitrap and spectral counting with significance determined by G-tests. Virtually only chloroplast-localized proteins were significantly affected, indicating that the molecular phenotype was confined to the chloroplast. A comparative chloroplast stromal proteome analysis of fully developed plants was used to complement the data set. Chloroplast unfoldase ClpB3 was strongly up-regulated in both young and mature leaves, suggesting widespread and persistent protein folding stress. The importance of ClpB3 in the clp2-1 mutant was demonstrated by the observation that a CLPR2 and CLPB3 double mutant was seedling-lethal. The observed up-regulation of chloroplast chaperones and protein sorting components further illustrated destabilization of protein homeostasis. Delayed rRNA processing and up-regulation of a chloroplast DEAD box RNA helicase and polynucleotide phosphorylase, but no significant change in accumulation of ribosomal subunits, suggested a bottleneck in ribosome assembly or RNA metabolism. Strong up-regulation of a chloroplast translational regulator TypA/BipA GTPase suggested a specific response in plastid gene expression to the distorted homeostasis. The stromal proteases PreP1,2 were up-regulated, likely constituting compensation for reduced Clp protease activity and possibly shared substrates between the ClpP and PreP protease systems. The thylakoid photosynthetic apparatus was decreased in the seedlings, whereas several structural thylakoid-associated plastoglobular proteins were strongly up-regulated. Two thylakoid-associated reductases involved in isoprenoid and chlorophyll synthesis were up-regulated reflecting feedback from rate-limiting photosynthetic electron transport. We discuss the quantitative proteomics data and the role of Clp proteolysis using a "systems view" of chloroplast homeostasis and metabolism and provide testable hypotheses and putative substrates to further determine the significance of Clp-driven proteolysis.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/chemistry,genetics,metabolism Blotting, Western Chloroplasts/enzymology Electrophoresis, Polyacrylamide Gel Endopeptidase Clp/chemistry,genetics,metabolism Feedback, Physiological Gene Expression Regulation, Plant Homeostasis Mass Spectrometry/methods Mutation Plant Leaves/genetics,metabolism Protein Folding Proteomics/methods Seedlings/genetics,metabolism
Chemicals
APG6 protein, Arabidopsis Arabidopsis Proteins Endopeptidase Clp
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Zybailov Boris
Department of Plant Biology, Cornell University, Ithaca, New York 14853, USA.
Friso Giulia
Kim Jitae
Rudella Andrea
Rodríguez Verenice Ramírez
Asakura Yukari
Sun Qi
van Wijk Klaas J
References (114)
114 references, click to expand
  1. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome.
    PLoS One. 2008 Apr 23;3(4):e1994 PMID: 18431481
  2. The plastid clpP1 protease gene is essential for plant development.
    Nature. 2003 Sep 4;425(6953):86-9 PMID: 12955146
  3. The chloroplast clpP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco.
    Plant Cell Physiol. 2001 Mar;42(3):264-73 PMID: 11266577
  4. Stable isotope-coded proteomic mass spectrometry.
    Curr Opin Biotechnol. 2003 Feb;14(1):101-9 PMID: 12566009
  5. Transport of proteins into chloroplasts. Partial purification of a thylakoidal processing peptidase involved in plastocyanin biogenesis.
    J Biol Chem. 1987 Dec 5;262(34):16386-90 PMID: 3316219
  6. Protein disaggregation by the AAA+ chaperone ClpB involves partial threading of looped polypeptide segments.
    Nat Struct Mol Biol. 2008 Jun;15(6):641-50 PMID: 18488042
  7. Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG.
    FEBS Lett. 2006 Mar 6;580(6):1547-52 PMID: 16480720
  8. Advances in quantitative proteomics via stable isotope tagging and mass spectrometry.
    Curr Opin Biotechnol. 2003 Feb;14(1):110-8 PMID: 12566010
  9. Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis.
    Plant Cell. 2006 Jul;18(7):1704-21 PMID: 16766689
  10. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants.
    Plant Cell. 2001 Jul;13(7):1499-510 PMID: 11449047
  11. Mechanisms of protein import into thylakoids of chloroplasts.
    Biol Chem. 2007 Sep;388(9):907-15 PMID: 17696774
  12. Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis.
    Plant Cell. 2007 Apr;19(4):1347-61 PMID: 17449806
  13. Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12765-70 PMID: 15304652
  14. Interorganellar communication.
    Curr Opin Plant Biol. 2007 Dec;10(6):600-6 PMID: 17719262
  15. The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts.
    Curr Genet. 2002 Aug;41(5):291-310 PMID: 12185496
  16. A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis.
    Plant Physiol. 2004 Nov;136(3):3605-15 PMID: 15516497
  17. ClpS, a substrate modulator of the ClpAP machine.
    Mol Cell. 2002 Mar;9(3):673-83 PMID: 11931773
  18. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae.
    J Proteome Res. 2006 Sep;5(9):2339-47 PMID: 16944946
  19. Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress.
    J Exp Bot. 2008;59(15):4133-43 PMID: 18940932
  20. Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana.
    J Biol Chem. 2001 May 11;276(19):16318-27 PMID: 11278690
  21. Chaperone activity of recombinant maize chloroplast protein synthesis elongation factor, EF-Tu.
    Eur J Biochem. 2004 Sep;271(18):3684-92 PMID: 15355346
  22. Complete maturation of the plastid protein translocation channel requires a type I signal peptidase.
    J Cell Biol. 2005 Nov 7;171(3):425-30 PMID: 16275749
  23. Protein trafficking to plastids: one theme, many variations.
    Biochem J. 2008 Jul 1;413(1):15-28 PMID: 18537794
  24. Quantitative proteomics of a chloroplast SRP54 sorting mutant and its genetic interactions with CLPC1 in Arabidopsis.
    Plant Physiol. 2008 Sep;148(1):156-75 PMID: 18633119
  25. Molecular chaperones and protein folding in plants.
    Plant Mol Biol. 1996 Oct;32(1-2):191-222 PMID: 8980480
  26. RNR1, a 3'-5' exoribonuclease belonging to the RNR superfamily, catalyzes 3' maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana.
    Nucleic Acids Res. 2005 May 12;33(8):2751-63 PMID: 15891117
  27. Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase
    Plant Physiol. 1999 Jul;120(3):695-704 PMID: 10398704
  28. The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants.
    Plant Cell. 2007 Apr;19(4):1313-28 PMID: 17416734
  29. A chloroplast processing enzyme functions as the general stromal processing peptidase.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7463-8 PMID: 9636172
  30. Molecular studies of CtpA, the carboxyl-terminal processing protease for the D1 protein of the photosystem II reaction center in higher plants.
    J Biol Chem. 1996 Sep 6;271(36):21848-52 PMID: 8702985
  31. Polynucleotide phosphorylase and the archaeal exosome as poly(A)-polymerases.
    Biochim Biophys Acta. 2008 Apr;1779(4):247-55 PMID: 18177749
  32. SsTypA1, a chloroplast-specific TypA/BipA-type GTPase from the halophytic plant Suaeda salsa, plays a role in oxidative stress tolerance.
    Plant Cell Environ. 2008 Jul;31(7):982-94 PMID: 18373622
  33. PNPase activity determines the efficiency of mRNA 3'-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts.
    EMBO J. 2002 Dec 16;21(24):6905-14 PMID: 12486011
  34. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
    Plant J. 2004 Mar;37(6):914-39 PMID: 14996223
  35. In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import.
    Plant J. 2005 Feb;41(3):412-28 PMID: 15659100
  36. Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis.
    Plant Mol Biol. 2004 Jul;55(4):595-606 PMID: 15604703
  37. Variegation mutants and mechanisms of chloroplast biogenesis.
    Plant Cell Environ. 2007 Mar;30(3):350-365 PMID: 17263779
  38. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):2053-8 PMID: 11172074
  39. Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase.
    Plant J. 2007 Mar;49(5):800-9 PMID: 17291312
  40. The molecular chaperone Hsp104--a molecular machine for protein disaggregation.
    J Struct Biol. 2006 Oct;156(1):139-48 PMID: 16563798
  41. Protein degradation machineries in plastids.
    Annu Rev Plant Biol. 2006;57:599-621 PMID: 16669775
  42. Metabolic compartmentation of plastid prenyllipid biosynthesis--evidence for the involvement of a multifunctional geranylgeranyl reductase.
    Eur J Biochem. 1998 Jan 15;251(1-2):413-7 PMID: 9492312
  43. Plastoglobules: versatile lipoprotein particles in plastids.
    Trends Plant Sci. 2007 Jun;12(6):260-6 PMID: 17499005
  44. Signals from chloroplasts converge to regulate nuclear gene expression.
    Science. 2007 May 4;316(5825):715-9 PMID: 17395793
  45. Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease.
    Plant J. 2000 May;22(4):303-13 PMID: 10849347
  46. DEAD-box RNA helicases in Escherichia coli.
    Nucleic Acids Res. 2006;34(15):4189-97 PMID: 16935881
  47. The plastidial MEP pathway: unified nomenclature and resources.
    Trends Plant Sci. 2008 Dec;13(12):619-23 PMID: 18948055
  48. The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii.
    Plant Physiol. 2001 May;126(1):421-33 PMID: 11351104
  49. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts.
    Mol Cell Biol. 2001 Aug;21(16):5408-16 PMID: 11463823
  50. A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts.
    Proc Natl Acad Sci U S A. 2008 Oct 21;105(42):16386-91 PMID: 18845687
  51. Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b(6)f complex.
    Plant Cell. 2000 Jan;12(1):137-50 PMID: 10634913
  52. A nuclear-encoded ClpP subunit of the chloroplast ATP-dependent Clp protease is essential for early development in Arabidopsis thaliana.
    Planta. 2006 Oct;224(5):1103-15 PMID: 16705403
  53. Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature.
    Plant Physiol. 2001 Apr;125(4):1912-8 PMID: 11299370
  54. Turnover of endogenous SsrA-tagged proteins mediated by ATP-dependent proteases in Escherichia coli.
    J Biol Chem. 2008 Aug 22;283(34):22918-29 PMID: 18550539
  55. Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts.
    Curr Opin Plant Biol. 2006 Jun;9(3):234-40 PMID: 16603408
  56. Mass spectrometry and protein analysis.
    Science. 2006 Apr 14;312(5771):212-7 PMID: 16614208
  57. Dead-box proteins: a family affair--active and passive players in RNP-remodeling.
    Nucleic Acids Res. 2006;34(15):4168-80 PMID: 16936318
  58. An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development.
    Plant Mol Biol. 2007 Jan;63(1):85-96 PMID: 17009084
  59. Protein N-terminal methionine excision.
    Cell Mol Life Sci. 2004 Jun;61(12):1455-74 PMID: 15197470
  60. Function of ROC4 in the efficient repair of photodamaged photosystem II in Arabidopsis.
    Photochem Photobiol. 2008 Nov-Dec;84(6):1343-8 PMID: 19067955
  61. The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts.
    Mol Cell Proteomics. 2006 Jan;5(1):114-33 PMID: 16207701
  62. Comparison of label-free methods for quantifying human proteins by shotgun proteomics.
    Mol Cell Proteomics. 2005 Oct;4(10):1487-502 PMID: 15979981
  63. Catalysis, subcellular localization, expression and evolution of the targeting peptides degrading protease, AtPreP2.
    Plant Cell Physiol. 2005 Jun;46(6):985-96 PMID: 15827031
  64. Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells.
    Plant J. 2000 Oct;24(2):241-52 PMID: 11069698
  65. Plants need their vitamins too.
    Curr Opin Plant Biol. 2007 Jun;10(3):266-75 PMID: 17434786
  66. Identification and characterization of SppA, a novel light-inducible chloroplast protease complex associated with thylakoid membranes.
    J Biol Chem. 2001 Sep 7;276(36):33645-51 PMID: 11443110
  67. Arabidopsis tic110 is essential for the assembly and function of the protein import machinery of plastids.
    Plant Cell. 2005 May;17(5):1482-96 PMID: 15829604
  68. The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles.
    Genes Cells. 2002 Aug;7(8):769-80 PMID: 12167156
  69. An Arabidopsis mutant defective in the plastid general protein import apparatus.
    Science. 1998 Oct 2;282(5386):100-3 PMID: 9756470
  70. Genetics of the biogenesis and dynamics of the photosynthetic machinery in eukaryotes.
    Plant Cell. 2004 Jul;16(7):1650-60 PMID: 15235122
  71. Recycling or regulation? The role of amino-terminal modifying enzymes.
    Curr Opin Plant Biol. 2006 Jun;9(3):227-33 PMID: 16597508
  72. Consequences of membrane protein overexpression in Escherichia coli.
    Mol Cell Proteomics. 2007 Sep;6(9):1527-50 PMID: 17446557
  73. A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids.
    Plant Cell. 2008 May;20(5):1303-15 PMID: 18469163
  74. Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis.
    Plant Cell. 2008 Jul;20(7):1786-804 PMID: 18599582
  75. The tmRNA system for translational surveillance and ribosome rescue.
    Annu Rev Biochem. 2007;76:101-24 PMID: 17291191
  76. PPDB, the Plant Proteomics Database at Cornell.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D969-74 PMID: 18832363
  77. Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content.
    Plant Physiol. 2004 Dec;136(4):4114-26 PMID: 15563614
  78. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation.
    Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15178-83 PMID: 18818314
  79. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
    Anal Chem. 1996 Mar 1;68(5):850-8 PMID: 8779443
  80. The Hsp90 chaperone machinery.
    J Biol Chem. 2008 Jul 4;283(27):18473-7 PMID: 18442971
  81. A model for random sampling and estimation of relative protein abundance in shotgun proteomics.
    Anal Chem. 2004 Jul 15;76(14):4193-201 PMID: 15253663
  82. Measurement of protein using bicinchoninic acid.
    Anal Biochem. 1985 Oct;150(1):76-85 PMID: 3843705
  83. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13732-7 PMID: 10570141
  84. Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis.
    Plant Cell. 2006 Oct;18(10):2635-49 PMID: 16980539
  85. Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry.
    J Mass Spectrom. 1999 Feb;34(2):105-16 PMID: 10093212
  86. Protein profiling with cleavable isotope-coded affinity tag (cICAT) reagents: the yeast salinity stress response.
    Mol Cell Proteomics. 2003 Nov;2(11):1198-204 PMID: 14506205
  87. The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90.
    Plant J. 2003 Jan;33(1):107-18 PMID: 12943545
  88. The diurnal metabolism of leaf starch.
    Biochem J. 2007 Jan 1;401(1):13-28 PMID: 17150041
  89. The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15184-9 PMID: 18818313
  90. The structure of YqeH. An AtNOS1/AtNOA1 ortholog that couples GTP hydrolysis to molecular recognition.
    J Biol Chem. 2008 Nov 21;283(47):32968-76 PMID: 18801747
  91. The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis.
    Plant Cell. 2007 Mar;19(3):1039-47 PMID: 17351117
  92. The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of the plastid ribosomal RNAs and is essential for chloroplast differentiation.
    Plant Mol Biol. 2003 Mar;51(5):651-63 PMID: 12678554
  93. Two novel mitochondrial and chloroplastic targeting-peptide-degrading peptidasomes in A. thaliana, AtPreP1 and AtPreP2.
    Biol Chem. 2006 Oct-Nov;387(10-11):1441-7 PMID: 17081117
  94. Targeting of nucleus-encoded proteins to chloroplasts in plants.
    New Phytol. 2008 Jul;179(2):257-285 PMID: 19086173
  95. A dedicated translation factor controls the synthesis of the global regulator Fis.
    EMBO J. 2004 Aug 18;23(16):3375-85 PMID: 15297874
  96. Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence.
    Plant Physiol. 2006 Jun;141(2):776-92 PMID: 16603661
  97. Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question.
    Cell Mol Life Sci. 2002 Oct;59(10):1607-16 PMID: 12475170
  98. Heat-stress induced synthesis of chloroplast protein synthesis elongation factor (EF-Tu) in a heat-tolerant maize line.
    Planta. 2001 Feb;212(3):359-66 PMID: 11289600
  99. The Arabidopsis thaliana type I Isopentenyl Diphosphate Isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis.
    Plant Cell. 2008 Mar;20(3):677-96 PMID: 18319397
  100. An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response.
    Plant J. 2006 Oct;48(2):249-60 PMID: 16995899
  101. Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis.
    Biochem J. 2009 Jan 1;417(1):257-68 PMID: 18754756
  102. Two novel targeting peptide degrading proteases, PrePs, in mitochondria and chloroplasts, so similar and still different.
    J Mol Biol. 2005 Jun 17;349(4):847-60 PMID: 15893767
  103. Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import.
    Plant J. 2007 Apr;50(2):364-79 PMID: 17376159
  104. Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications.
    J Biol Chem. 2004 Feb 6;279(6):4768-81 PMID: 14593120
  105. Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system.
    Plant Physiol. 2004 Aug;135(4):2379-91 PMID: 15326282
  106. Isolation of chloroplast proteins from Arabidopsis thaliana for proteome analysis.
    Methods Mol Biol. 2007;355:43-8 PMID: 17093301
  107. The Mg-chelatase H subunit is an abscisic acid receptor.
    Nature. 2006 Oct 19;443(7113):823-6 PMID: 17051210
  108. EGY1 encodes a membrane-associated and ATP-independent metalloprotease that is required for chloroplast development.
    Plant J. 2005 Feb;41(3):364-75 PMID: 15659096
  109. Support for a potential role of E. coli oligopeptidase A in protein degradation.
    Biochem Biophys Res Commun. 2007 Aug 3;359(3):486-90 PMID: 17553460
  110. Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling.
    Anal Chem. 2005 Oct 1;77(19):6218-24 PMID: 16194081
  111. Quantitative mass spectrometry in proteomics: a critical review.
    Anal Bioanal Chem. 2007 Oct;389(4):1017-31 PMID: 17668192
  112. The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development.
    Plant J. 2007 Jan;49(1):115-27 PMID: 17144892
  113. Cloning and characterization of chloroplast and cytosolic forms of cyclophilin from Arabidopsis thaliana.
    J Biol Chem. 1994 Mar 18;269(11):7863-8 PMID: 8132503
  114. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation.
    Nat Biotechnol. 2007 Jan;25(1):117-24 PMID: 17187058
Article Info
Journal
Molecular & cellular proteomics : MCP
Abbr.
Mol Cell Proteomics
ISSN
1535-9484
DOI
10.1074/mcp.M900104-MCP200
Published
2009-08-00
Pages
1789-1810
Language
English
Region
United States
NLM ID
101125647
PMCID
PMC2722778
Subset
IM
External Links
PubMed source DOI: 10.1074/mcp.M900104-MCP200 PMC Full Text View journal details
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