Quantitative Proteomics Reveals Dynamic Changes in the Plasma Membrane During Arabidopsis Immune Signaling

Dodds, 2010, Plant immunity: Towards an integrated view of plant-pathogen interactions, Nat. Rev. Genet, 11, 539, 10.1038/nrg2812 Boller, 2009, A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors, Annu. Rev. Plant Biol, 60, 379, 10.1146/annurev.arplant.57.032905.105346 Block, 2011, Plant targets for Pseudomonas syringae type III effectors: Virulence targets or guarded decoys?, Curr. Opin. Microbiol, 14, 39, 10.1016/j.mib.2010.12.011 Mackey, 2002, RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis, Cell, 108, 743, 10.1016/S0092-8674(02)00661-X Mackey, 2003, Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance, Cell, 112, 379, 10.1016/S0092-8674(03)00040-0 Axtell, 2003, Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4, Cell, 112, 369, 10.1016/S0092-8674(03)00036-9 Kim, 2005, Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis, Cell, 121, 749, 10.1016/j.cell.2005.03.025 Liu, 2009, RIN4 functions with the plasma membrane H+-ATPase to regulate stomatal apertures during pathogen attack, PLoS Biol, 7, e1000139, 10.1371/journal.pbio.1000139 Nimchuk, 2000, Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae, Cell, 101, 353, 10.1016/S0092-8674(00)80846-6 Wilton, 2010, The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence, Proc. Natl. Acad. Sci. U.S.A, 107, 2349, 10.1073/pnas.0904739107 Chung, 2011, Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants, Cell Host Microbe, 9, 125, 10.1016/j.chom.2011.01.009 Liu, 2011, A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor, Cell Host Microbe, 9, 137, 10.1016/j.chom.2011.01.010 Tsuda, 2010, Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity, Curr. Opin. Plant Biol, 13, 459, 10.1016/j.pbi.2010.04.006 Nühse, 2007, Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses, Plant J, 51, 931, 10.1111/j.1365-313X.2007.03192.x Benschop, 2007, Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis, Mol. Cell. Proteomics, 6, 1198, 10.1074/mcp.M600429-MCP200 Keinath, 2010, PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity, J. Biol. Chem, 285, 39140, 10.1074/jbc.M110.160531 Lu, 2011, Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity, Science, 332, 1439, 10.1126/science.1204903 Jones, 2004, Specific changes in the Arabidopsis proteome in response to bacterial challenge: Differentiating basal and R-gene mediated resistance, Phytochemistry, 65, 1805, 10.1016/j.phytochem.2004.04.005 Widjaja, 2009, Combining subproteome enrichment and Rubisco depletion enables identification of low abundance proteins differentially regulated during plant defense, Proteomics, 9, 138, 10.1002/pmic.200800293 Caplan, 2009, Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants, Cell Host Microbe, 6, 457, 10.1016/j.chom.2009.10.005 Bednarek, 2010, Not a peripheral issue: Secretion in plant-microbe interactions, Curr. Opin. Plant Biol, 13, 378, 10.1016/j.pbi.2010.05.002 Hatsugai, 2009, A novel membrane fusion-mediated plant immunity against bacterial pathogens, Genes Dev, 23, 2496, 10.1101/gad.1825209 McNellis, 1998, Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell death, Plant J, 14, 247, 10.1046/j.1365-313X.1998.00106.x Larsson, 1994, Isolation of highly purified plant plasma membranes and separation of inside-out and right-side-out vesicles, Methods Enzymol, Vol. 228, 451, 10.1016/0076-6879(94)28046-0 Johansson, 1995, Brij 58, a polyoxyethylene acyl ether, creates membrane vesicles of uniform sidedness: A new tool to obtain inside-out (cytoplasmic side-out) plasma membrane vesicles, Plant J, 7, 165, 10.1046/j.1365-313X.1995.07010165.x Wessel, 1984, A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids, Anal. Biochem, 138, 141, 10.1016/0003-2697(84)90782-6 Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 Shevchenko, 2006, In-gel digestion for mass spectrometric characterization of proteins and proteomes, Nat. Protoc, 1, 2856, 10.1038/nprot.2006.468 Alvarado, 2010, A comparative study of in-gel digestions using microwave and pressure-accelerated technologies, J. Biomol. Tech, 21, 148 Craig, 2004, TANDEM: Matching proteins with tandem mass spectra, Bioinformatics, 20, 1466, 10.1093/bioinformatics/bth092 Käll, 2008, Assigning significance to peptides identified by tandem mass spectrometry using decoy databases, J. Proteome Res, 7, 29, 10.1021/pr700600n Keller, 2002, Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search, Anal. Chem, 74, 5383, 10.1021/ac025747h Zhang, 2010, Refinements to label free proteome quantitation: How to deal with peptides shared by multiple proteins, Anal. Chem, 82, 2272, 10.1021/ac9023999 Liao, 2011, Proteomic characterization of human milk whey proteins during a twelve-month lactation period, J. Proteome Res, 10, 1746, 10.1021/pr101028k Choi, 2008, Significance analysis of spectral count data in label-free shotgun proteomics, Mol. Cell. Proteomics, 7, 2373, 10.1074/mcp.M800203-MCP200 Huang, 2009, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat. Protoc, 4, 44, 10.1038/nprot.2008.211 Morsomme, 1998, Single point mutations distributed in 10 soluble and membrane regions of the Nicotiana plumbaginifolia plasma membrane PMA2 H+-ATPase activate the enzyme and modify the structure of the C-terminal region, J. Biol. Chem, 273, 34837, 10.1074/jbc.273.52.34837 Dávila-Aponte, 2003, Two chloroplastic protein translocation components, Tic110 and Toc75, are conserved in different plastid types from multiple plant species, Plant Mol. Biol, 51, 175, 10.1023/A:1021190319786 Lingard, 2009, Peroxisome-associated matrix protein degradation in Arabidopsis, Proc. Natl. Acad. Sci. U.S.A, 106, 4561, 10.1073/pnas.0811329106 Antosiewicz, 1995, Cellular localization of the Ca2+ binding TCH3 protein of Arabidopsis, Plant J, 8, 623, 10.1046/j.1365-313X.1995.08050623.x La Camera, 2005, A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis, Plant J, 44, 810, 10.1111/j.1365-313X.2005.02578.x Nühse, 2003, A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin, J. Biol. Chem, 278, 45248, 10.1074/jbc.M307443200 Gassmann, 2009, Quantifying Western blots: Pitfalls of densitometry, Electrophoresis, 30, 1845, 10.1002/elps.200800720 Kunkel, 1993, RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2, Plant Cell, 5, 865 Coaker, 2005, Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin, Science, 308, 548, 10.1126/science.1108633 Chisholm, 2005, Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2, Proc. Natl. Acad. Sci. U.S.A, 102, 2087, 10.1073/pnas.0409468102 Larsson, 1987, Preparation of high-purity plasma membranes, Methods Enzymol, Vol. 148, 558, 10.1016/0076-6879(87)48054-3 Heazlewood, 2007, SUBA: The Arabidopsis Subcellular Database, Nucleic Acids Res, 35, D213, 10.1093/nar/gkl863 Nelson, 2006, A quantitative analysis of Arabidopsis plasma membrane using trypsin-catalyzed 18O labeling, Mol. Cell. Proteomics, 5, 1382, 10.1074/mcp.M500414-MCP200 Lundgren, 2010, Role of spectral counting in quantitative proteomics, Expert Rev. Proteomics, 7, 39, 10.1586/epr.09.69 Liu, 2004, A model for random sampling and estimation of relative protein abundance in shotgun proteomics, Anal. Chem, 76, 4193, 10.1021/ac0498563 De Michele, 2009, Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures, Plant Physiol, 150, 217, 10.1104/pp.108.133397 Bolton, 2009, Primary metabolism and plant defense: Fuel for the fire, Mol. Plant-Microbe Interact, 22, 487, 10.1094/MPMI-22-5-0487 Tsuji, 1992, Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae, Plant Physiol, 98, 1304, 10.1104/pp.98.4.1304 Schuhegger, 2006, CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis, Plant Physiol, 141, 1248, 10.1104/pp.106.082024 Millet, 2010, Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns, Plant Cell, 22, 973, 10.1105/tpc.109.069658 Nafisi, 2007, Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis, Plant Cell, 19, 2039, 10.1105/tpc.107.051383 Su, 2011, Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana, Plant Cell, 23, 364, 10.1105/tpc.110.079145 Glawischnig, 2007, Camalexin, Phytochemistry, 68, 401, 10.1016/j.phytochem.2006.12.005 Wang, 2004, Lipid signaling, Curr. Opin. Plant Biol, 7, 329, 10.1016/j.pbi.2004.03.012 Andersson, 2006, Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana, Plant J, 47, 947, 10.1111/j.1365-313X.2006.02844.x Zhang, 2009, Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis, Plant Cell, 21, 2357, 10.1105/tpc.108.062992 Kirik, 2009, SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT, Proc. Natl. Acad. Sci. U.S.A, 106, 20532, 10.1073/pnas.0903859106 Kwon, 2008, Co-option of a default secretory pathway for plant immune responses, Nature, 451, 835, 10.1038/nature06545 Pajonk, 2008, Activity determinants and functional specialization of Arabidopsis PEN1 syntaxin in innate immunity, J. Biol. Chem, 283, 26974, 10.1074/jbc.M805236200 Roje, 2006, S-Adenosyl-l-methionine: Beyond the universal methyl group donor, Phytochemistry, 67, 1686, 10.1016/j.phytochem.2006.04.019 Liu, 2008, Ethylene signaling is required for the acceleration of cell death induced by the activation of AtMEK5 in Arabidopsis, Cell Res, 18, 422, 10.1038/cr.2008.29 Brutus, 2010, A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides, Proc. Natl. Acad. Sci. U.S.A, 107, 9452, 10.1073/pnas.1000675107 Laluk, 2011, Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis, Plant Cell, Vol. 23, 2831, 10.1105/tpc.111.087122 Chen, 2004, Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis, Plant Mol. Biol, 56, 271, 10.1007/s11103-004-3381-2 Acharya, 2007, Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae, Plant J, 50, 488, 10.1111/j.1365-313X.2007.03064.x Kim, 2005, The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation, Proc. Natl. Acad. Sci. U.S.A, 102, 6496, 10.1073/pnas.0500792102 Bak, 2001, The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis, Plant Physiol, 127, 108, 10.1104/pp.127.1.108 Naur, 2003, CYP83A1 and CYP83B1, Two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis, Plant Physiol, 133, 63, 10.1104/pp.102.019240 Chen, 2007, Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology, Proc. Natl. Acad. Sci. U.S.A, 104, 20131, 10.1073/pnas.0704901104 Truman, 2010, Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds, Plant Physiol, 152, 1562, 10.1104/pp.109.152173 Mur, 2008, The hypersensitive response: The centenary is upon us but how much do we know?, J. Exp. Bot, 59, 501, 10.1093/jxb/erm239 Fu, 2009, Estimating accuracy of RNA-Seq and microarrays with proteomics, BMC Genomics, 10, 161, 10.1186/1471-2164-10-161 Lorrain, 2003, Lesion mimic mutants: Keys for deciphering cell death and defense pathways in plants?, Trends Plant Sci, 8, 263, 10.1016/S1360-1385(03)00108-0 Veronese, 2006, The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens, Plant Cell, 18, 257, 10.1105/tpc.105.035576 Pogány, 2009, Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-alternaria pathosystem, Plant Physiol, 151, 1459, 10.1104/pp.109.141994 Torres, 2005, Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana, Nat. Genet, 37, 1130, 10.1038/ng1639 Gao, 2009, Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis, Cell Host Microbe, 6, 34, 10.1016/j.chom.2009.05.019 Jambunathan, 2001, A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance, Plant Cell, 13, 2225, 10.1105/tpc.010226 Yang, 2006, The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis, Plant J, 45, 166, 10.1111/j.1365-313X.2005.02585.x Cheng, 2011, Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation, Proc. Natl. Acad. Sci. U.S.A, Vol. 108, 14694, 10.1073/pnas.1105685108