Comprehensive quantification of monolignol-pathway enzymes in populus trichocarpa by protein cleavage isotope dilution mass spectrometry

Journal of Proteome Research

Volumn 11, Issue 6, 2012, Pages 3390-3404

  Shuford, Christopher M ^a   Li, Quanzi ^b   Sun, Ying Hsuan ^b   Chen, Hsi Chuan ^b   Wang, Jack ^b   Shi, Rui ^b   Sederoff, Ronald R ^b   Chiang, Vincent L ^b   Muddiman, David C ^a  

^a WM Keck FT ICR Mass Spectrometry Laboratory   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

filter aided sample preparation; isotope dilution mass spectrometry; monolignol biosynthesis; quantification; selected reaction monitoring

Indexed keywords

4 COUMARATE 3 HYROXYLASE; 4 COUMARATE COA LIGASE; CAFFEIC ACID 3 O METHYLTRANSFERASE; CAFFEOYL COA O METHYLTRANSFERASE; CINNAMATE 4 MONOOXYGENASE; CINNAMOYL COA REDUCTASE; CINNAMYL ALCOHOL DEHYDROGENASE; CONIFERALDEHYDE 5 HYDROXYLASE; HYDROXYCINNAMOYL TRANSFERASE; LIGNIN; METHYLTRANSFERASE; MONOLIGNOL; OXYGENASE; PEROXIDASE; PHENYLALANINE AMMONIUM LYASE; PLANT MEDICINAL PRODUCT; TRYPSIN; UNCLASSIFIED DRUG; PROTEOME; VEGETABLE PROTEIN;

ARTICLE; ASPEN; BIOSYNTHESIS; CHEMICAL MODIFICATION; CHEMICAL REACTION; CONTROLLED STUDY; ENZYME ASSAY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; POLYMERIZATION; POPULUS TRICHOCARPA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE ISOTOPE DILUTION MASS SPECTROMETRY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REACTION OPTIMIZATION; XYLEM; AMINO ACID SEQUENCE; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; ENZYMOLOGY; ISOTOPE LABELING; METABOLISM; MOLECULAR GENETICS; POPULUS; STANDARD; STANDARDS;

POPULUS TRICHOCARPA;

AMINO ACID SEQUENCE; BIOSYNTHETIC PATHWAYS; ISOTOPE LABELING; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; POPULUS; PROTEOME; REFERENCE STANDARDS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; XYLEM;

EID: 84861831985     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300205a     Document Type: Article

References (76)

1. Sarkanen, K. V.; Ludwig, C. H. Lignins: Occurrence, Formation, Structure and Reactions; John Wiley and Sons: New York, 1971.
2. Boerjan, W.; Ralph, J.; Baucher, M. Lignin Biosynthesis Annu. Rev. Plant Biol. 2003, 54, 519-546
3. Sjostrom, E. Wood Chemistry: Fundamentals and Applications; Ann Arbor Science Publishers: Ann Arbor, MI, 1993.
4. Talbot, J. M.; Yelle, D. J.; Nowick, J.; Treseder, K. K. Litter Decay Rates are Determined by Lignin Chemistry Biogeochemsitry 2012, 108 (1-3) 279-295
5. Hurst, H. M.; Burges, N. A. Lignin and Humic Acids. In Soil Biochemistry; McLaren, A. D.; Peterson, G. H., Eds.; Marcel Dekker Inc.: New York, 1967; Vol. 11, pp 260-286.
6. Vance, C. P.; Kirk, T. K.; Sherwood, R. T. Lignification as a Mechanism of Disease Resistance Annu. Rev. Phytopathol. 1980, 18, 259-288
7. Erikson, K., -E., L.; Blanchette, R. A.; Ander, P. Microbial and Enzymatic Degradation of Wood and Wood Components; Springer-Verlag: Berlin, Germany, 1990.
8. Koch, G. W.; Sillett, S. C.; Jennings, G. M.; Davis, S. D. The Limits to Tree Height Nature 2004, 428 (6985) 851-854
9. Schniewind, A. P.; Berndt, H. The Composite Nature of Wood; Marcel Dekker Inc.: New York, 1991.
10. Fry, W.; White, J. B. Big Trees; Stanford University Press: Standford, CA, 1938.
11. Biermann, C. J. Essentials of Pulping and Papermaking; Academic Press: San Diego, CA, 1993.
12. Jung, H. G.; Allen, M. S. Characteristics of Plant Cell Walls Affecting Intake and Digestibility of Forages by Ruminants J. Anim. Sci. 1995, 73 (9) 2774-2790
13. Chen, F.; Dixon, R. A. Lignin Modification Improves Fermentable Sugar Yields for Biofuel Nat. Biotechnol. 2007, 25 (7) 759-761
14. Tillman, D. A. Wood as an Energy Resource; Academic Press: New York, 1978.
15. B., M. S.; Samson, R.; Bransby, D.; Wiselogel, A. In Evaluating Physical, Chemical, and Energetic Properties of Perennial Grasses as Biofuels, Bioenergy '96-The Seventh National Bioenergy Conference: Partnerships to Develop and Apply Biomass Technologies, Nashville, TN, 1996; Oak Ridge National Laboratory: Nashville, TN, 1996; pp 1-8.
16. Novaes, E.; Kirst, M.; Chiang, V.; Winter-Sederoff, H.; Sederoff, R. Lignin and Biomass: A Negative Correlation for Wood Formation and Lignin Content in Trees Plant Physiol. 2010, 154 (2) 555-561
17. Ralph, J.; Ludnquist, K.; Brunow, G.; Lu, F.; Kim, H.; Schatz, P. F.; Marita, J. M.; Hatfield, R. D.; Ralph, S. A.; Christensen, J. H.; Boerjan, W. Lignins: Natural Polymers from Oxidative Coupling of 4-hyroxyphenylpropanoids Phytochem. Rev. 2004, 3 (1-2) 29-60
18. Higuchi, T. Lignin Biochemistry: Biosynthesis and Biodegradation Wood Sci. Technol. 1990, 24 (1) 23-63
19. Umezawa, T. The Cinnamate/Monolignol Pathway Phytochem. Rev. 2010, 9 (1) 1-17
20. Shi, R.; Sun, Y. H.; Li, Q. Z.; Heber, S.; Sederoff, R.; Chiang, V. L. Towards a Systems Approach for Lignin Biosynthesis in Populus trichocarpa: Transcript Abundance and Specificity of the Monolignol Biosynthetic Genes Plant Cell Physiol. 2010, 51 (1) 144-163
21. Dixon, R. A.; Chen, F.; Guo, D. J.; Parvathi, K. The Biosynthesis of Monolignols: A 'Metabolic Grid', or Independent Pathways to Guaiacyl and Syringyl Units? Phytochemistry 2001, 57 (7) 1069-1084
22. Higuchi, T. Pathways for Monolignol Biosynthesis via Metabolic Grids: Coniferyl Aldehyde 5-hyroxylase, a Possible Key Enzyme in Angiosperm Syringyl Lignin Biosynthesis Proc. Jpn. Acad., Ser. B 2003, 79 (8) 227-236
23. Freudenberg, K.; Neish, A. C. Constitution and Biosynthesis of Lignin; Springer Verlag: New York, NY, 1968.
24. Higuchi, T. Biosynthesis and Biodegradation of Wood Components; Academic Press: London, 1985.
25. Baucher, M.; Monties, B.; Van Montagu, M.; Boerjan, W. Biosynthesis and Genetic Engineering of Lignin Crit. Rev. Plant Sci. 1998, 17 (2) 125-197
26. Gion, J. M.; Lalanne, C.; Le Provost, G.; Ferry-Dumazet, H.; Paiva, J.; Chaumeil, P.; Frigerio, J. M.; Brach, J.; Barre, A.; de Daruvar, A.; Claverol, S.; Bonneu, M.; Sommerer, N.; Negroni, L.; Plomion, C. The Proteome of Maritime Pine Wood Forming Tissue Proteomics 2005, 5 (14) 3731-3751
27. Millar, D. J.; Whitelegge, J. P.; Bindschedler, L. V.; Rayon, C.; Boudet, A. M.; Rossignol, M.; Borderies, G.; Bolwell, G. P. The Cell Wall and Secretory Proteome of a Tobacco Cell Line Synthesizing Secondary Wall Proteomics 2009, 9 (9) 2355-2372
28. Raes, J.; Rohde, A.; Christensen, J. H.; Van de Peer, Y.; Boerjan, W. Genome-wide Characterization of the Lignification Toolbox in Arabidopsis Plant Physiol. 2003, 133 (3) 1051-1071
29. Lee, Y.; Chen, F.; Gallego-Giraldo, L.; Dixon, R. A.; Voit, E. O., Integrative Analysis of Transgenic Alfalfa (Medicago sativa L.) Suggests New Metabolic Control Mechanisms for Monolignol Biosynthesis. PloS Comput. Biol. 2011, 7, (5).
30. Tuskan, G. A.; DiFazio, S.; Jansson, S.; Bohlmann, J.; Grigoriev, I.; Hellsten, U.; Putnam, N.; Ralph, S.; Rombauts, S.; Salamov, A.; Schein, J.; Sterck, L.; Aerts, A.; Bhalerao, R. R.; Bhalerao, R. P.; Blaudez, D.; Boerjan, W.; Brun, A.; Brunner, A.; Busov, V.; Campbell, M.; Carlson, J.; Chalot, M.; Chapman, J.; Chen, G. L.; Cooper, D.; Coutinho, P. M.; Couturier, J.; Covert, S.; Cronk, Q.; Cunningham, R.; Davis, J.; Degroeve, S.; Dejardin, A.; Depamphilis, C.; Detter, J.; Dirks, B.; Dubchak, I.; Duplessis, S.; Ehlting, J.; Ellis, B.; Gendler, K.; Goodstein, D.; Gribskov, M.; Grimwood, J.; Groover, A.; Gunter, L.; Hamberger, B.; Heinze, B.; Helariutta, Y.; Henrissat, B.; Holligan, D.; Holt, R.; Huang, W.; Islam-Faridi, N.; Jones, S.; Jones-Rhoades, M.; Jorgensen, R.; Joshi, C.; Kangasjarvi, J.; Karlsson, J.; Kelleher, C.; Kirkpatrick, R.; Kirst, M.; Kohler, A.; Kalluri, U.; Larimer, F.; Leebens-Mack, J.; Leple, J. C.; Locascio, P.; Lou, Y.; Lucas, S.; Martin, F.; Montanini, B.; Napoli, C.; Nelson, D. R.; Nelson, C.; Nieminen, K.; Nilsson, O.; Pereda, V.; Peter, G.; Philippe, R.; Pilate, G.; Poliakov, A.; Razumovskaya, J.; Richardson, P.; Rinaldi, C.; Ritland, K.; Rouze, P.; Ryaboy, D.; Schmutz, J.; Schrader, J.; Segerman, B.; Shin, H.; Siddiqui, A.; Sterky, F.; Terry, A.; Tsai, C. J.; Uberbacher, E.; Unneberg, P.; Vahala, J.; Wall, K.; Wessler, S.; Yang, G.; Yin, T.; Douglas, C.; Marra, M.; Sandberg, G.; Van de Peer, Y.; Rokhsar, D. The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Science 2006, 313 (5793) 1596-1604
31. Barr, J. R.; Maggio, V. L.; Patterson, D. G.; Cooper, G. R.; Henderson, L. O.; Turner, W. E.; Smith, S. J.; Hannon, W. H.; Needham, L. L.; Sampson, E. J. Isotope Dilution Mass Spectrometric Quantification of Specific Proteins: Model Application with Apolipoprotein A-I Clin. Chem. 1996, 42 (10) 1676-1682
32. Gerber, S. A.; Rush, J.; Stemman, O.; Kirschner, M. W.; Gygi, S. P. Absolute Quantification of Proteins and Phosphoproteins from Cell Lysates by Tandem MS Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (12) 6940-6945
33. Barnidge, D. R.; Goodmanson, M. K.; Klee, G. G.; Muddiman, D. C. Absolute Quantification of the Model Biomarker Prostate-Specific Antigen in Serum by LC-MS/MS Using Protein Cleavage and Isotope Dilution Mass Spectrometry J. Proteome Res. 2004, 3 (3) 644-652
34. Brun, V.; Masselon, C.; Garin, J.; Dupuis, A. Isotope Dilution Strategies for Absolute Quantitative Proteomics J. Proteomics 2009, 72 (5) 740-749
35. Kuhn, E.; Wu, J.; Karl, J.; Liao, H.; Zolg, W.; Guild, B. Quantification of C-Reactive Protein in the Serum of Patients with Rheumatoid Arthritis Using Multiple Reaction Monitoring Mass Spectrometry and C-13-Labeled Peptide Standards Proteomics 2004, 4 (4) 1175-1186
36. Anderson, N. L.; Anderson, N. G.; Haines, L. R.; Hardie, D. B.; Olafson, R. W.; Pearson, T. W. Mass Spectrometric Quantitation of Peptides and Proteins Using Stable Isotope Standards and Capture by Anti-peptide Antibodies (SISCAPA) J. Proteome Res. 2004, 3 (2) 235-244
37. Anderson, L.; Hunter, C. L. Quantitative Mass Spectrometric Multiple Reaction Monitoring Assays for Major Plasma Proteins Mol. Cell. Proteomics 2006, 5 (4) 573-588
38. Williams, D. K.; Muddiman, D. C. Absolute Quantification of C-Reactive Protein in Human Plasma Derived from Patients with Epithelial Ovarian Cancer Utilizing Protein Cleavage Isotope Dilution Mass Spectrometry J. Proteome Res. 2009, 8 (2) 1085-1090
39. Keshishian, H.; Addona, T.; Burgess, M.; Kuhn, E.; Carr, S. A. Quantitative, Multiplexed Assays for Low Abundance Proteins in Plasma by Targeted Mass Spectrometry and Stable Isotope Dilution Mol. Cell. Proteomics 2007, 6 (12) 2212-2229
40. Kettenbach, A. N.; Rush, J.; Gerber, S. A. Absolute Quantification of Protein and Post-translational Modification Abundance with Stable Isotope-labeled Synthetic Peptides Nat. Protoc. 2011, 6 (2) 175-186
41. Schmidt, C.; Lenz, C.; Grote, M.; Luhrmann, R.; Urlaub, H. Determination of Protein Stoichiometry within Protein Complexes Using Absolute Quantification and Multiple Reaction Monitoring Anal. Chem. 2010, 82 (7) 2784-2796
42. Wienkoop, S.; Weckwerth, W. Relative and Absolute Quantitative Shotgun Proteomics: Targeting Low-abundance Proteins in Arabidopsis thaliana J. Exp. Bot. 2006, 57 (7) 1529-1535
43. Hu, X. T.; Owens, M. A. Multiplexed Protein Quantification in Maize Leaves by Liquid Chromatography Coupled with Tandem Mass Spectrometry: An Alternative Tool to Immunoassays for Target Protein Analysis in Genetically Engineered Crops J. Agric. Food Chem. 2011, 59 (8) 3551-3558
44. Lange, V.; Picotti, P.; Domon, B.; Aebersold, R. Selected Reaction Monitoring for Quantitative Proteomics: A Tutorial Mol. Syst. Biol. 2008, 4, 14
45. Chen, H.; Li, Q.; Shuford, C. M.; Liu, J.; Muddiman, D. C.; Sederoff, R. R.; Chiang, V. L. Membrane Protein Complexes Catalyze both 4- and 3-hydroxylation of Cinnamic Acid Derivatives in Monolignol Biosynthesis Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (52) 21253-21258
46. Urban, P.; Mignotte, C.; Kazmaier, M.; Delorme, F.; Pompon, D. Cloning, Yeast Expression, and Characterization of the Coupling of Two Distantly Related Arabidopsis thaliana NADPH-Cytochrome P450 Reductases with P450 CYP73A5 J. Biol. Chem. 1997, 272 (31) 19176-19186
47. Gietz, R. D.; Schiestl, R. H. High-efficiency Yeast Transformation Using the LiAc/SS Carrier DNA/PEG Method Nat. Protoc. 2007, 2 (1) 31-34
48. Scopes, R. K. Measurement of Protein by Spectrophotometry at 205-nm Anal. Biochem. 1974, 59 (1) 277-282
49. Shevchenko, A.; Tomas, H.; Havlis, J.; Olsen, J. V.; Mann, M. In-gel Digestion for Mass Spectrometric Characterization of Proteins and Proteomes Nat. Protoc. 2006, 1 (6) 2856-2860
50. Andrews, G. L.; Shuford, C. M.; Burnett, J. C.; Hawkridge, A. M.; Muddiman, D. C. Coupling of a Vented Column with Splitless nanoRPLC-ESI-MS for the Improved Separation and Detection of Brain Natriuretic Peptide-32 and its Proteolytic Peptides J. Chromatogr. B 2009, 877 (10) 948-954
51. Andrews, G. L.; Dean, R. A.; Hawkridge, A. M.; Muddiman, D. C. Improving Proteome Coverage on a LTQ-Orbitrap Using Design of Experiments J. Am. Soc. Mass Spectrom. 2011, 22 (4) 773-783
52. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal Sample Preparation Method for Proteome Analysis Nat. Methods 2009, 6 (5) 359-360
53. MacLean, B.; Tomazela, D. M.; Shulman, N.; Chambers, M.; Finney, G. L.; Frewen, B.; Kern, R.; Tabb, D. L.; Liebler, D. C.; MacCoss, M. J. Skyline: An Open Source Document Editor for Creating and Analyzing Targeted Proteomics Experiments Bioinformatics 2010, 26 (7) 966-968
54. Blom, N.; Gammeltoft, S.; Brunak, S. Sequence and Structure-based Prediction of Eukaryotic Protein Phosphorylation Sites J. Mol. Biol. 1999, 294 (5) 1351-1362
55. Blom, N.; Sicheritz-Ponten, T.; Gupta, R.; Gammeltoft, S.; Brunak, S. Prediction of Post-translational Glycosylation and Phosphorylation of Proteins from the Amino Acid Sequence Proteomics 2004, 4 (6) 1633-1649
56. de Graaf, E. L.; Altelaar, A. F. M.; van Breukelen, B.; Mohammed, S.; Heck, A. J. R. Improving SRM Assay Development: A Global Comparison between Triple Quadrupole, Ion Trap, and Higher Energy CID Peptide Fragmentation Spectra J. Proteome Res. 2011, 10 (9) 4334-4341
57. MacLean, B.; Tomazela, D. M.; Abbatiello, S. E.; Zhang, S. C.; Whiteaker, J. R.; Paulovich, A. G.; Carr, S. A.; MacCoss, M. J. Effect of Collision Energy Optimization on the Measurement of Peptides by Selected Reaction Monitoring (SRM) Mass Spectrometry Anal. Chem. 2010, 82 (24) 10116-10124
58. Sherman, J.; McKay, M. J.; Ashman, K.; Molloy, M. P. How specific is my SRM?: The issue of precursor and product ion redundancy Proteomics 2009, 9 (5) 1120-1123
59. Sauvage, F. L.; Gaulier, J. M.; Lachatre, G.; Marquet, P. Pitfalls and Prevention Strategies for Liquid Chromatography-Tandem Mass Spectrometry in the Selected Reaction-Monitoring Mode for Drug Analysis Clin. Chem. 2008, 54 (9) 1519-1527
60. de Zeeuw, R. A. Substance Identification: The Weak Link in Analytical Toxicology J. Chromatogr. B 2004, 811, 3-12
61. Kushnir, M. M.; Rockwood, A. L.; Nelson, G. J.; Yue, B. F.; Urry, F. M. Assessing Analytical Specificity in Quantitative Analysis Using Tandem Mass Spectrometry Clin. Biochem. 2005, 38 (4) 319-327
62. Harris, J. I. Effect of Urea on Trypsin and Alpha-chymotrypsin Nature 1956, 177 (4506) 471-473
63. Proc, J. L.; Kuzyk, M. A.; Hardie, D. B.; Yang, J.; Smith, D. S.; Jackson, A. M.; Parker, C. E.; Borchers, C. H. A Quantitative Study of the Effects of Chaotropic Agents, Surfactants, and Solvents on the Digestion Efficiency of Human Plasma Proteins by Trypsin J. Proteome Res. 2010, 9 (10) 5422-5437
64. Blonder, J.; Conrads, T. P.; Yu, L. R.; Terunuma, A.; Janini, G. M.; Issaq, H. J.; Vogel, J. C.; Veenstra, T. D. A Detergent- and Cyanogen Bromide-free Method for Integral Membrane Proteomics: Application to Halobacterium Purple Membranes and the Human Epidermal Membrane Proteome Proteomics 2004, 4 (1) 31-45
65. Li, F. M.; Schmerberg, C. M.; Ji, Q. C. Accelerated Tryptic Digestion of Proteins in Plasma for Absolute Quantitation Using a Protein Internal Standard by Liquid Chromatography/Tandem Mass Spectrometry Rapid Commun. Mass Spectrom. 2009, 23 (5) 729-732
66. Green, N. M.; Neurath, H. The Effects of Divalent Cations on Trypsin J. Biol. Chem. 1953, 204 (1) 379-390
67. Sipos, T.; Merkel, J. R. An Effect of Calcium Ions on Activity, Heat Stability, and Structure of Trypsin Biochemistry 1970, 9 (14) 2766-2775
68. Arsene, C. G.; Ohlendorf, R.; Burkitt, W.; Pritchard, C.; Henrion, A.; O'Connor, G.; Bunk, D. M.; Guttler, B. Protein Quantification by Isotope Dilution Mass Spectrometry of Proteolytic Fragments: Cleavage Rate and Accuracy Anal. Chem. 2008, 80 (11) 4154-4160
69. Eyers, C. E.; Lawless, C.; Wedge, D. C.; Lau, K. W.; Gaskell, S. J.; Hubbard, S. J. CONSeQuence: Prediction of Reference Peptides for Absolute Quantitative Proteomics Using Consensus Machine Learning Approaches Mol. Cell. Proteomics 2011, 10 (11) 12
70. Stergachis, A. B.; MacLean, B.; Lee, K.; Stamatoyannopoulos, J. A.; MacCoss, M. J. Rapid Empirical Discovery of Optimal Peptides for Targeted Proteomics Nature Methods 2011, 8 (12) 1041-1043
71. Fisher, R. A. Statistical Methods for Research Workers; Hafner Publishing Co.: New York, 1973.
72. Laundsby, R. G.; Weese, D. L. Straight Talk on Designing Experiments: An Introductory Text for Scientists and Engineers, 2 nd ed.; Launsby Consulting: CO, 1995.
73. Tamhane, A. C., Statistical Analysis of Designed Experiments: Theory and Application; John Wiley & Sons: NJ, 2009.
74. Riter, L. S.; Vitek, O.; Gooding, K. M.; Hodge, B. D.; Julian, R. K. Statistical Design of Experiments as a Tool in Mass Spectrometry J. Mass Spectrom. 2005, 40 (5) 565-579
75. Walker, S. H.; Papas, B. N.; Comins, D. L.; Muddiman, D. C. Interplay of Permanent Charge and Hydrophobicity in the Electrospray Ionization of Glycans Anal. Chem. 2010, 82 (15) 6636-6642
76. Barry, J. A.; Muddiman, D. C. Global Optimization of the Infrared Matrix-assisted Laser Desorption Electrospray Ionization (IR MALDESI) Source for Mass Spectrometry Using Statistical Design of Experiments Rapid Commun. Mass Spectrom. 2011, 25 (23) 3527-3536