Stable isotope metabolic labeling-based quantitative phosphoproteomic analysis of arabidopsis mutants reveals ethylene-regulated time-dependent phosphoproteins and putative substrates of constitutive triple response 1 kinase

Molecular and Cellular Proteomics

Volumn 12, Issue 12, 2013, Pages 3559-3582

  Yang, Zhu ^a   Guo, Guangyu ^a   Zhang, Manyu ^a   Liu, Claire Y ^a   Hu, Qin ^a   Lam, Henry ^a   Cheng, Han ^b   Xue, Yu ^b   Li, Jiayang ^c   Li, Ning ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE SERINE RICH SPLICING FACTOR 41; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR 3; BINDING PROTEIN 1.1; CALCIUM SENSING RECEPTOR; CELL PROTEIN; CHLOROPHYLL A; CHLOROPHYLL B; CONSTITUTIVE TRIPLE RESPONSE 1 KINASE; ETHYLENE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MUTANT PROTEIN; NITROGEN 15; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEOME; PLASMA MEMBRANE INTRINSIC PROTEIN 2A; PROTEIN KINASE; PROTEOME; RCN1 1 PROTEIN; REGULATOR PROTEIN; SERINE ARGININE RICH PROTEIN; STABLE ISOTOPE; UNCLASSIFIED DRUG;

ARABIDOPSIS; BINDING SITE; BIOINFORMATICS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE EXPRESSION; ISOTOPE LABELING; LIGHT HARVESTING SYSTEM; LOSS OF FUNCTION MUTATION; MEDIATOR; MOLECULAR BIOLOGY; NONHUMAN; PLASTID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; TRANSCRIPTION INITIATION;

ARABIDOPSIS;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM-BINDING PROTEINS; COMPUTATIONAL BIOLOGY; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; ISOTOPE LABELING; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MUTATION; NITROGEN ISOTOPES; PHOSPHOPROTEINS; PHOSPHORYLATION; PLANT GROWTH REGULATORS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN KINASES; PROTEIN PHOSPHATASE 2; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TIME FACTORS;

EID: 84890677480     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.031633     Document Type: Review

References (105)

1. Mattoo, A. K., and Suttle, J. C. (1991) The Plant Hormone Ethylene, CRC Press, Boca Raton, FL
2. Chang, C., Kwok, S. F., Bleecker, A. B., and Meyerowitz, E. M. (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to twocomponent regulators. Science 262, 539-544
3. Schaller, G. E., Ladd, A. N., Lanahan, M. B., Spanbauer, J. M., and Bleecker, A. B. (1995) The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer. J. Biol. Chem. 270, 12526-12530
4. Hua, J., and Meyerowitz, E. M. (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94, 261-271
5. Rodriguez, F. I., Esch, J. J., Hall, A. E., Binder, B. M., Schaller, G. E., and Bleecker, A. B. (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283, 996-998
6. Kieber, J. J., Rothenberg, M., Roman, G., Feldmann, K. A., and Ecker, J. R. (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427-441
7. Gao, Z., Chen, Y. F., Randlett, M. D., Zhao, X. C., Findell, J. L., Kieber, J. J., and Schaller, G. E. (2003) Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J. Biol. Chem. 278, 34725- 34732
8. Kieber, J. J. (1997) The ethylene response pathway in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 277-296
9. Clark, K. L., Larsen, P. B., Wang, X., and Chang, C. (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl. Acad. Sci. U.S.A. 95, 5401-5406
10. Huang, Y., Li, H., Hutchison, C. E., Laskey, J., and Kieber, J. J. (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J. 33, 221-233
11. Qiao, H., Shen, Z., Huang, S. S., Schmitz, R. J., Urich, M. A., Briggs, S. P., and Ecker, J. R. (2012) Processing and subcellular trafficking of ERtethered EIN2 control response to ethylene gas. Science 338, 390-393
12. Ju, C., Yoon, G. M., Shemansky, J. M., Lin, D. Y., Ying, Z. I., Chang, J., Garrett, W. M., Kessenbrock, M., Groth, G., Tucker, M. L., Cooper, B., Kieber, J. J., and Chang, C. (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 19486-19491
13. Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J. R. (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148-2152
14. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., and Ecker, J. R. (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133-1144
15. Guo, H., and Ecker, J. R. (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115, 667-677
16. Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C., and Genschik, P. (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two arabidopsis F box proteins: EBF1 and EBF2. Cell 115, 679-689
17. Ohme-Takagi, M., and Shinshi, H. (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7, 173-182
18. Lin, Z., Zhong, S., and Grierson, D. (2009) Recent advances in ethylene research. J. Exp. Botany 60, 3311-3336
19. Zhao, Q., and Guo, H. W. (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol. Plant 4, 626-634
20. Lu, B. W., Pei, L. K., Chan, W. K., Zhang, H., Zhu, G., Li, J. Y., and Li, N. (2001) The dual effects of ethylene on the negative gravicurvature of arabidopsis inflorescence, an intriguing action model for the plant hormone ethylene. Chinese Sci. Bull. 46, 279-283
21. Madlung, A., Behringer, F. J., and Lomax, T. L. (1999) Ethylene plays multiple nonprimary roles in modulating the gravitropic response in tomato. Plant Physiol. 120, 897-906
22. Binder, B. M. (2008) The ethylene receptors: complex perception for a simple gas. Plant Sci. 175, 8-17
23. Binder, B. M., Mortimore, L. A., Stepanova, A. N., Ecker, J. R., and Bleecker, A. B. (2004) Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent. Plant Physiol. 136, 2921-2927
24. Lu, B. W., Yu, H. Y., Pei, L. K., Wong, M. Y., and Li, N. (2002) Prolonged exposure to ethylene stimulates the negative gravitropic responses of Arabidopsis inflorescence stems and hypocotyls. Funct. Plant Biol. 29, 987-997
25. Zhu, L., Liu, D., Li, Y., and Li, N. (2013) Functional phosphoproteomic analysis reveals that a serine-62-phosphorylated isoform of ethylene response factor110 is involved in Arabidopsis bolting. Plant Physiol. 161, 904-917
26. Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D., Genschik, P., Moritz, T., and Harberd, N. P. (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc. Natl. Acad. Sci. U.S.A. 104, 6484-6489
27. Ogawara, T., Higashi, K., Kamada, H., and Ezura, H. (2003) Ethylene advances the transition from vegetative growth to flowering in Arabidopsis thaliana. J. Plant Physiol. 160, 1335-1340
28. De Paepe, A., Vuylsteke, M., Van Hummelen, P., Zabeau, M., and Van Der Straeten, D. (2004) Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J. 39, 537-559
29. Zhong, G. Y., and Burns, J. K. (2003) Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol. Biol. 53, 117-131
30. Yang, T., and Poovaiah, B. W. (2000) An early ethylene up-regulated gene encoding a calmodulin-binding protein involved in plant senescence and death. J. Biol. Chem. 275, 38467-38473
31. Zegzouti, H., Jones, B., Frasse, P., Marty, C., Maitre, B., Latch, A., Pech, J. C., and Bouzayen, M. (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening- related genes isolated by differential display. Plant J. 18, 589-600
32. Li, N. (2008) The dual-and-opposing-effect of ethylene on the negative gravitropism of Arabidopsis inflorescence stem and light-grown hypocotyls. Plant Sci. 175, 71-86
33. Etheridge, N., Chen, Y. F., and Schaller, G. E. (2005) Dissecting the ethylene pathway of Arabidopsis. Brief. Funct. Genomic. Proteomic. 3, 372-381
34. Kendrick, M. D., and Chang, C. (2008) Ethylene signaling: new levels of complexity and regulation. Curr. Opin. Plant Biol. 11, 479-485
35. Qiao, H., Chang, K. N., Yazaki, J., and Ecker, J. R. (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev. 23, 512-521
36. Li, Y., Shu, Y., Peng, C., Zhu, L., Guo, G., and Li, N. (2012) Absolute quantitation of isoforms of post-translationally modified proteins in transgenic organism. Mol. Cell. Proteomics 11, 272-285
37. Yoo, S. D., Cho, Y. H., Tena, G., Xiong, Y., and Sheen, J. (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451, 789-795
38. Li, H., Wong, W. S., Zhu, L., Guo, H. W., Ecker, J., and Li, N. (2009) Phosphoproteomic analysis of ethylene-regulated protein phosphorylation in etiolated seedlings of Arabidopsis mutant ein2 using twodimensional separations coupled with a hybrid quadrupole time-offlight mass spectrometer. Proteomics 9, 1646-1661
39. Moshkov, I. E., Mur, L. A., Novikova, G. V., Smith, A. R., and Hall, M. A. (2003) Ethylene regulates monomeric GTP-binding protein gene expression and activity in Arabidopsis. Plant Physiol. 131, 1705-1717
40. Raz, V., and Fluhr, R. (1993) Ethylene signal is transduced via protein phosphorylation events in plants. Plant Cell 5, 523-530
41. Gamble, R. L., Qu, X., and Schaller, G. E. (2002) Mutational analysis of the ethylene receptor ETR1. Role of the histidine kinase domain in dominant ethylene insensitivity. Plant Physiol. 128, 1428-1438
42. Wang, W., Hall, A. E., O'Malley, R., and Bleecker, A. B. (2003) Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc. Natl. Acad. Sci. U.S.A. 100, 352-357
43. Ouaked, F., Rozhon, W., Lecourieux, D., and Hirt, H. (2003) A MAPK pathway mediates ethylene signaling in plants. EMBO J. 22, 1282-1288
44. Larsen, P. B., and Chang, C. (2001) The Arabidopsis eer1 mutant has enhanced ethylene responses in the hypocotyl and stem. Plant Physiol. 125, 1061-1073
45. Larsen, P. B., and Cancel, J. D. (2003) Enhanced ethylene responsiveness in the Arabidopsis eer1 mutant results from a loss-of-function mutation in the protein phosphatase 2A A regulatory subunit, RCN1. Plant J. 34, 709-718
46. Mayer-Jaekel, R. E., and Hemmings, B. A. (1994) Protein phosphatase 2A-a "menage a trois." Trends Cell Biol. 4, 287-291
47. Garbers, C., DeLong, A., Deruere, J., Bernasconi, P., and Soll, D. (1996) A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J. 15, 2115-2124
48. Guo, G., and Li, N. (2011) Relative and accurate measurement of protein abundance using 15N stable isotope labeling in Arabidopsis (SILIA). Phytochemistry 72, 1028-1039
49. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
50. Goshe, M. B., Blonder, J., and Smith, R. D. (2003) Affinity labeling of highly hydrophobic integral membrane proteins for proteome-wide analysis. J. Proteome Res. 2, 153-161
51. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F., Gelb, M. H., and Aebersold, R. (1999) Quantitative analysis of complex protein mixtures using isotope- coded affinity tags. Nat. Biotechnol. 17, 994-999
52. Huttlin, E. L., Hegeman, A. D., Harms, A. C., and Sussman, M. R. (2007) Comparison of full versus partial metabolic labeling for quantitative proteomics analysis in Arabidopsis thaliana. Mol. Cell. Proteomics 6, 860-881
53. Ong, S. E., and Mann, M. (2005) Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262
54. Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., Purkayastha, S., Juhasz, P., Martin, S., Bartlet-Jones, M., He, F., Jacobson, A., and Pappin, D. J. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169
55. Whitelegge, J. P., Katz, J. E., Pihakari, K. A., Hale, R., Aguilera, R., Gomez, S. M., Faull, K. F., Vavilin, D., and Vermaas, W. (2004) Subtle modification of isotope ratio proteomics; an integrated strategy for expression proteomics. Phytochemistry 65, 1507-1515
56. Yao, X., Freas, A., Ramirez, J., Demirev, P. A., and Fenselau, C. (2001) Proteolytic 18O labeling for comparative proteomics: model studies with two serotypes of adenovirus. Anal. Chem. 73, 2836-2842
57. Washburn, M. P., Wolters, D., and Yates, J. R., 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247
58. Kline, K. G., and Sussman, M. R. (2010) Protein quantitation using isotope-assisted mass spectrometry. Annu. Rev. Biophys. 39, 291-308
59. Schulze, W. X., and Usadel, B. (2010) Quantitation in mass-spectrometrybased proteomics. Annu. Rev. Plant Biol. 61, 491-516
60. Xue, Y., Ren, J., Gao, X., Jin, C., Wen, L., and Yao, X. (2008) GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy. Mol. Cell. Proteomics 7, 1598-1608
61. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J., and Gygi, S. P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2, 43-50
62. Blanco, L., Mead, J. A., and Bessant, C. (2009) Comparison of novel decoy database designs for optimizing protein identification searches using ABRF sPRG2006 standard MS/MS data sets. J. Proteome Res. 8, 1782-1791
63. Choi, H., and Nesvizhskii, A. I. (2008) False discovery rates and related statistical concepts in mass spectrometry-based proteomics. J. Proteome Res. 7, 47-50
64. Tabb, D. L. (2008) What's driving false discovery rates? J. Proteome Res. 7, 45-46
65. Li, L., Kresh, J. A., Karabacak, N. M., Cobb, J. S., Agar, J. N., and Hong, P. (2008) A hierarchical algorithm for calculating the isotopic fine structures of molecules. J. Am. Soc. Mass Spectrom. 19, 1867-1874
66. Kline, K. G., Barrett-Wilt, G. A., and Sussman, M. R. (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc. Natl. Acad. Sci. U.S.A. 107, 15986-15991
67. Swarup, G., Cohen, S., and Garbers, D. L. (1982) Inhibition of membrane phosphotyrosyl-protein phosphatase activity by vanadate. Biochem Biophys. Res. Commun. 107, 1104-1109
68. Tsuboi, K. K., Wiener, G., and Hudson, P. B. (1957) Acid phosphatase. 7. Yeast phosphomonoesterase; isolation procedure and stability characteristics. J. Biol. Chem. 224, 621-635
69. Hanks, S. K., and Hunter, T. (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and clas-sification. FASEB J. 9, 576-596
70. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934
71. Breitkreutz, B. J., Stark, C., Reguly, T., Boucher, L., Breitkreutz, A., Livstone, M., Oughtred, R., Lackner, D. H., Bahler, J., Wood, V., Dolinski, K., and Tyers, M. (2008) The BioGRID Interaction Database: 2008 update. Nucleic Acids Res. 36, D637-D640
72. Salwinski, L., Miller, C. S., Smith, A. J., Pettit, F. K., Bowie, J. U., and Eisenberg, D. (2004) The Database of Interacting Proteins: 2004 update. Nucleic Acids Res. 32, D449-D451
73. Aranda, B., Achuthan, P., Alam-Faruque, Y., Armean, I., Bridge, A., Derow, C., Feuermann, M., Ghanbarian, A. T., Kerrien, S., Khadake, J., Kerssemakers, J., Leroy, C., Menden, M., Michaut, M., Montecchi-Palazzi, L., Neuhauser, S. N., Orchard, S., Perreau, V., Roechert, B., van Eijk, K., and Hermjakob, H. (2010) The IntAct molecular interaction database in 2010. Nucleic Acids Res. 38, D525-D531
74. Chatr-aryamontri, A., Ceol, A., Palazzi, L. M., Nardelli, G., Schneider, M. V., Castagnoli, L., and Cesareni, G. (2007) MINT: the Molecular INTeraction database. Nucleic Acids Res. 35, D572-D574
75. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., and von Mering, C. (2009) STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416
76. Guzman, P., and Ecker, J. R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523
77. Tsuchisaka, A., Yu, G., Jin, H., Alonso, J. M., Ecker, J. R., Zhang, X., Gao, S., and Theologis, A. (2009) A combinatorial interplay among the 1-aminocyclopropane- 1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183, 979-1003
78. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641
79. Herzog, F., Kahraman, A., Boehringer, D., Mak, R., Bracher, A., Walzthoeni, T., Leitner, A., Beck, M., Hartl, F. U., Ban, N., Malmstrom, L., and Aebersold, R. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 337, 1348-1352
80. Duby, G., and Boutry, M. (2009) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflugers Arch. 457, 645-655
81. Speth, C., Jaspert, N., Marcon, C., and Oecking, C. (2010) Regulation of the plant plasma membrane H+-ATPase by its C-terminal domain: what do we know for sure? Eur. J. Cell Biol. 89, 145-151
82. O'Neill, S. D., and Zheng, C. C. (1998) Abundance of mRNAs encoding HMG1/HMG2 class high-mobility-group DNA-binding proteins are differentially regulated in cotyledons of Pharbitis nil. Plant Mol. Biol. 37, 235-241
83. Wisniewski, J. R., Szewczuk, Z., Petry, I., Schwanbeck, R., and Renner, U. (1999) Constitutive phosphorylation of the acidic tails of the high mobility group 1 proteins by casein kinase 2 alters their conformation, stability, and DNA binding specificity. J. Biol. Chem. 274, 20116-20122
84. Young, N. L., Plazas-Mayorca, M. D., and Garcia, B. A. (2010) Systemswide proteomic characterization of combinatorial post-translational modification patterns. Expert Rev. Proteomics 7, 79-92
85. Ingelsson, B., and Vener, A. V. (2012) Phosphoproteomics of Arabidopsis chloroplasts reveals involvement of the STN7 kinase in phosphorylation of nucleoid protein pTAC16. FEBS Lett. 586, 1265-1271
86. Bellafiore, S., Barneche, F., Peltier, G., and Rochaix, J. D. (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892-895
87. Angel, T. E., Aryal, U. K., Hengel, S. M., Baker, E. S., Kelly, R. T., Robinson, E. W., and Smith, R. D. (2012) Mass spectrometry-based proteomics: existing capabilities and future directions. Chem. Soc. Rev. 41, 3912-3928
88. Domon, B., and Aebersold, R. (2010) Options and considerations when selecting a quantitative proteomics strategy. Nat. Biotechnol. 28, 710-721
89. He, Z., Yang, C., Guo, G., Li, N., and Yu, W. (2011) Motif-All: discovering all phosphorylation motifs. BMC Bioinformatics 12 Suppl 1, S22
90. Stemmer, C., Leeming, D. J., Franssen, L., Grimm, R., and Grasser, K. D. (2003) Phosphorylation of maize and Arabidopsis HMGB proteins by protein kinase CK2alpha. Biochemistry 42, 3503-3508
91. Brodersen, P., Petersen, M., Bjorn Nielsen, H., Zhu, S., Newman, M. A., Shokat, K. M., Rietz, S., Parker, J., and Mundy, J. (2006) Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47, 532-546
92. Bonhomme, L., Valot, B., Tardieu, F., and Zivy, M. (2012) Phosphoproteome dynamics upon changes in plant water status reveal early events associated with rapid growth adjustment in maize leaves. Mol. Cell. Proteomics 11, 957-972
93. Yu, Y., Yoon, S. O., Poulogiannis, G., Yang, Q., Ma, X. M., Villen, J., Kubica, N., Hoffman, G. R., Cantley, L. C., Gygi, S. P., and Blenis, J. (2011) Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332, 1322-1326
94. Kerk, D., Templeton, G., and Moorhead, G. B. (2008) Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol. 146, 351-367
95. An, F., Zhao, Q., Ji, Y., Li, W., Jiang, Z., Yu, X., Zhang, C., Han, Y., He, W., Liu, Y., Zhang, S., Ecker, J. R., and Guo, H. (2010) Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 22, 2384-2401
96. Johansson, I., Larsson, C., Ek, B., and Kjellbom, P. (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8, 1181-1191
97. Tornroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Neutze, R., and Kjellbom, P. (2006) Structural mechanism of plant aquaporin gating. Nature 439, 688-694
98. Johansson, I., Karlsson, M., Shukla, V. K., Chrispeels, M. J., Larsson, C., and Kjellbom, P. (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10, 451-459
99. Prak, S., Hem, S., Boudet, J., Viennois, G., Sommerer, N., Rossignol, M., Maurel, C., and Santoni, V. (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol. Cell. Proteomics 7, 1019-1030
100. Peret, B., Li, G., Zhao, J., Band, L. R., Voss, U., Postaire, O., Luu, D. T., Da Ines, O., Casimiro, I., Lucas, M., Wells, D. M., Lazzerini, L., Nacry, P., King, J. R., Jensen, O. E., Schaffner, A. R., Maurel, C., and Bennett, M. J. (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14, 991-998
101. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G. T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M. J. (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19, 2186-2196
102. Xu, Y. H., Liu, R., Yan, L., Liu, Z. Q., Jiang, S. C., Shen, Y. Y., Wang, X. F., and Zhang, D. P. (2012) Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. J. Exp. Bot. 63, 1095-1106
103. Cho, Y. H., Sheen, J., and Yoo, S. D. (2010) Low glucose uncouples hexokinase1-dependent sugar signaling from stress and defense hormone abscisic acid and C2H4 responses in Arabidopsis. Plant Physiol. 152, 1180-1182
104. Cho, Y. H., and Yoo, S. D. (2011) Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet. 7, e1001263
105. Ito, S., Song, Y. H., Josephson-Day, A. R., Miller, R. J., Breton, G., Olmstead, R. G., and Imaizumi, T. (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 3582-3587