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• W2128268951 abstract "Ethylene is an important plant hormone that regulates numerous cellular processes and stress responses. The mode of action of ethylene is both dose- and time-dependent. Protein phosphorylation plays a key role in ethylene signaling, which is mediated by the activities of ethylene receptors, constitutive triple response 1 (CTR1) kinase, and phosphatase. To address how ethylene alters the cellular protein phosphorylation profile in a time-dependent manner, differential and quantitative phosphoproteomics based on 15N stable isotope labeling in Arabidopsis was performed on both one-minute ethylene-treated Arabidopsis ethylene-overly-sensitive loss-of-function mutant rcn1-1, deficient in PP2A phosphatase activity, and a pair of long-term ethylene-treated wild-type and loss-of-function ethylene signaling ctr1-1 mutants, deficient in mitogen-activated kinase kinase kinase activity. In total, 1079 phosphopeptides were identified, among which 44 were novel. Several one-minute ethylene-regulated phosphoproteins were found from the rcn1-1. Bioinformatic analysis of the rcn1-1 phosphoproteome predicted nine phosphoproteins as the putative substrates for PP2A phosphatase. In addition, from CTR1 kinase-enhanced phosphosites, we also found putative CTR1 kinase substrates including plastid transcriptionally active protein and calcium-sensing receptor. These regulatory proteins are phosphorylated in the presence of ethylene. Analysis of ethylene-regulated phosphosites using the group-based prediction system with a protein–protein interaction filter revealed a total of 14 kinase–substrate relationships that may function in both CTR1 kinase- and PP2A phosphatase-mediated phosphor-relay pathways. Finally, several ethylene-regulated post-translational modification network models have been built using molecular systems biology tools. It is proposed that ethylene regulates the phosphorylation of arginine/serine-rich splicing factor 41, plasma membrane intrinsic protein 2A, light harvesting chlorophyll A/B binding protein 1.1, and flowering bHLH 3 proteins in a dual-and-opposing fashion. Ethylene is an important plant hormone that regulates numerous cellular processes and stress responses. The mode of action of ethylene is both dose- and time-dependent. Protein phosphorylation plays a key role in ethylene signaling, which is mediated by the activities of ethylene receptors, constitutive triple response 1 (CTR1) kinase, and phosphatase. To address how ethylene alters the cellular protein phosphorylation profile in a time-dependent manner, differential and quantitative phosphoproteomics based on 15N stable isotope labeling in Arabidopsis was performed on both one-minute ethylene-treated Arabidopsis ethylene-overly-sensitive loss-of-function mutant rcn1-1, deficient in PP2A phosphatase activity, and a pair of long-term ethylene-treated wild-type and loss-of-function ethylene signaling ctr1-1 mutants, deficient in mitogen-activated kinase kinase kinase activity. In total, 1079 phosphopeptides were identified, among which 44 were novel. Several one-minute ethylene-regulated phosphoproteins were found from the rcn1-1. Bioinformatic analysis of the rcn1-1 phosphoproteome predicted nine phosphoproteins as the putative substrates for PP2A phosphatase. In addition, from CTR1 kinase-enhanced phosphosites, we also found putative CTR1 kinase substrates including plastid transcriptionally active protein and calcium-sensing receptor. These regulatory proteins are phosphorylated in the presence of ethylene. Analysis of ethylene-regulated phosphosites using the group-based prediction system with a protein–protein interaction filter revealed a total of 14 kinase–substrate relationships that may function in both CTR1 kinase- and PP2A phosphatase-mediated phosphor-relay pathways. Finally, several ethylene-regulated post-translational modification network models have been built using molecular systems biology tools. It is proposed that ethylene regulates the phosphorylation of arginine/serine-rich splicing factor 41, plasma membrane intrinsic protein 2A, light harvesting chlorophyll A/B binding protein 1.1, and flowering bHLH 3 proteins in a dual-and-opposing fashion. Ethylene is a volatile plant hormone that regulates versatile molecular and physiological processes in higher plants (1Mattoo A.K. Suttle J.C. The Plant Hormone Ethylene. CRC Press, Boca Raton, FL1991Google Scholar). The perception of this gaseous two-carbon hormone is achieved by a group of membrane-associated dimeric ethylene receptors that resemble bacterial two-component signaling systems and are composed of hybrid histidine (or aspartic acid) kinases, a histidine-containing phosphor-transfer domain, and response regulators (2Chang C. Kwok S.F. Bleecker A.B. Meyerowitz E.M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.Science. 1993; 262: 539-544Crossref PubMed Google Scholar). These receptors are made of two membrane-bound protein subunits cross-linked at the N-terminal region through two disulfide bonds (3Schaller G.E. Ladd A.N. Lanahan M.B. Spanbauer J.M. Bleecker A.B. The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer.J. Biol. Chem. 1995; 270: 12526-12530Abstract Full Text Full Text PDF PubMed Scopus (193) Google Scholar). In Arabidopsis, there are five different ethylene receptor subunits: ethylene response 1, ethylene response 2, ethylene insensitive 4 (EIN4), 1The abbreviations used are:ACCaminocyclopropane-1-carboxylic acidACNacetonitrileCIPK1CBL-interacting protein kinase 1CTR1constitutive triple response 1eer1-1enhanced ethylene response 1EINethylene insensitiveFBH3flowering bHLH 3 proteinFDRfalse discovery rateGPSgroup-based prediction systemHMGhigh mobility groupIMACimmobilized metal-ion-affinity chromatographyiTRAQisobaric tag for relative and absolute quantitationLHCBlight harvetsting chlorophyll A/B binding proteinMAPKKKmitogen-activated protein kinase kinase kinasePIPplasma membrane intrinsic proteinPPIprotein–protein interactionPP2Aprotein phosphatase 2APTAC16plastic transcriptionally active 16PTMpost-translational modificationRCN1roots curl in naphthylphthalamic acid 1SILIA15N stable isotope labeling in ArabidopsisSTNstate transition. 1The abbreviations used are:ACCaminocyclopropane-1-carboxylic acidACNacetonitrileCIPK1CBL-interacting protein kinase 1CTR1constitutive triple response 1eer1-1enhanced ethylene response 1EINethylene insensitiveFBH3flowering bHLH 3 proteinFDRfalse discovery rateGPSgroup-based prediction systemHMGhigh mobility groupIMACimmobilized metal-ion-affinity chromatographyiTRAQisobaric tag for relative and absolute quantitationLHCBlight harvetsting chlorophyll A/B binding proteinMAPKKKmitogen-activated protein kinase kinase kinasePIPplasma membrane intrinsic proteinPPIprotein–protein interactionPP2Aprotein phosphatase 2APTAC16plastic transcriptionally active 16PTMpost-translational modificationRCN1roots curl in naphthylphthalamic acid 1SILIA15N stable isotope labeling in ArabidopsisSTNstate transition. ethylene response sensor 1, and ethylene response sensor 2, each of which is encoded by an ethylene receptor gene of unique DNA sequence and structure (4Hua J. Meyerowitz E.M. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana.Cell. 1998; 94: 261-271Abstract Full Text Full Text PDF PubMed Scopus (789) Google Scholar). Ethylene gas binds to a pair of cross-linked transmembrane domains in a receptor with the help of an incorporated copper ion (5Rodriguez F.I. Esch J.J. Hall A.E. Binder B.M. Schaller G.E. Bleecker A.B. A copper cofactor for the ethylene receptor ETR1 from Arabidopsis.Science. 1999; 283: 996-998Crossref PubMed Scopus (459) Google Scholar). The physical interaction of ethylene molecules with receptor complexes somehow induces inactivation of the negative regulation of another downstream signaling component, constitutive triple response 1 (CTR1) (AT5G03730) (6Kieber J.J. Rothenberg M. Roman G. Feldmann K.A. Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.Cell. 1993; 72: 427-441Abstract Full Text PDF PubMed Scopus (1392) Google Scholar). This ethylene-signaling component has been perceived as a Raf-like Ser/Thr protein kinase, a putative mitogen-activated protein kinase kinase kinase (MAPKKK) (6Kieber J.J. Rothenberg M. Roman G. Feldmann K.A. Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.Cell. 1993; 72: 427-441Abstract Full Text PDF PubMed Scopus (1392) Google Scholar, 7Gao Z. Chen Y.F. Randlett M.D. Zhao X.C. Findell J.L. Kieber J.J. Schaller G.E. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes.J. Biol. Chem. 2003; 278: 34725-34732Abstract Full Text Full Text PDF PubMed Scopus (244) Google Scholar), and its primary function in the ethylene signal-transduction pathway has been defined as a negative regulator of ethylene responses according to molecular genetic studies (8Kieber J.J. The ethylene response pathway in Arabidopsis.Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997; 48: 277-296Crossref PubMed Google Scholar). CRT1 physically interacts with both ethylene receptors (9Clark K.L. Larsen P.B. Wang X. Chang C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors.Proc. Natl. Acad. Sci. U.S.A. 1998; 95: 5401-5406Crossref PubMed Scopus (360) Google Scholar, 10Huang Y. Li H. Hutchison C.E. Laskey J. Kieber J.J. Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis.Plant J. 2003; 33: 221-233Crossref PubMed Scopus (257) Google Scholar) and a downstream positive regulator of ethylene response, EIN2 (11Qiao H. Shen Z. Huang S.S. Schmitz R.J. Urich M.A. Briggs S.P. Ecker J.R. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas.Science. 2012; 338: 390-393Crossref PubMed Scopus (285) Google Scholar, 12Ju 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. Chang C. 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. 2012; 109: 19486-19491Crossref PubMed Scopus (312) Google Scholar), and it directly inhibits the molecular function of EIN2 in ethylene signaling by phosphorylating EIN2 (12Ju 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. Chang C. 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. 2012; 109: 19486-19491Crossref PubMed Scopus (312) Google Scholar), which was identified as an endoplasmic reticulum (ER) membrane-localized natural resistance-associated macrophage protein homolog (13Alonso J.M. Hirayama T. Roman G. Nourizadeh S. Ecker J.R. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.Science. 1999; 284: 2148-2152Crossref PubMed Scopus (903) Google Scholar). When ethylene binds to ethylene receptors, the negative regulation of ethylene signaling output from CTR1 is reduced, dephosphorylation of EIN2 occurs, and the C terminus of EIN2 is subsequently cleaved from the putative metal ion channel and translocated into the nucleus to initiate the activation of transcriptional cascades for most ethylene-responsive gene expression (11Qiao H. Shen Z. Huang S.S. Schmitz R.J. Urich M.A. Briggs S.P. Ecker J.R. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas.Science. 2012; 338: 390-393Crossref PubMed Scopus (285) Google Scholar). The EIN2 C-terminus-activated EIN3 and ethylene insensitive 3-like 1 ethylene response transcription factors (14Chao Q. Rothenberg M. Solano R. Roman G. Terzaghi W. Ecker J.R. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins.Cell. 1997; 89: 1133-1144Abstract Full Text Full Text PDF PubMed Google Scholar, 15Guo H. Ecker J.R. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor.Cell. 2003; 115: 667-677Abstract Full Text Full Text PDF PubMed Scopus (604) Google Scholar, 16Potuschak T. Lechner E. Parmentier Y. Yanagisawa S. Grava S. Koncz C. Genschik P. EIN3-dependent regulation of plant ethylene hormone signaling by two arabidopsis F box proteins: EBF1 and EBF2.Cell. 2003; 115: 679-689Abstract Full Text Full Text PDF PubMed Scopus (493) Google Scholar) consequently orchestrate combinatorial control over the transcriptional activities of a large number of ethylene response factor proteins (17Ohme-Takagi M. Shinshi H. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element.Plant Cell. 1995; 7: 173-182Crossref PubMed Scopus (941) Google Scholar) that lead to plant ethylene responses. aminocyclopropane-1-carboxylic acid acetonitrile CBL-interacting protein kinase 1 constitutive triple response 1 enhanced ethylene response 1 ethylene insensitive flowering bHLH 3 protein false discovery rate group-based prediction system high mobility group immobilized metal-ion-affinity chromatography isobaric tag for relative and absolute quantitation light harvetsting chlorophyll A/B binding protein mitogen-activated protein kinase kinase kinase plasma membrane intrinsic protein protein–protein interaction protein phosphatase 2A plastic transcriptionally active 16 post-translational modification roots curl in naphthylphthalamic acid 1 15N stable isotope labeling in Arabidopsis state transition. aminocyclopropane-1-carboxylic acid acetonitrile CBL-interacting protein kinase 1 constitutive triple response 1 enhanced ethylene response 1 ethylene insensitive flowering bHLH 3 protein false discovery rate group-based prediction system high mobility group immobilized metal-ion-affinity chromatography isobaric tag for relative and absolute quantitation light harvetsting chlorophyll A/B binding protein mitogen-activated protein kinase kinase kinase plasma membrane intrinsic protein protein–protein interaction protein phosphatase 2A plastic transcriptionally active 16 post-translational modification roots curl in naphthylphthalamic acid 1 15N stable isotope labeling in Arabidopsis state transition. Given the established ethylene-signaling pathway, an emerging and pressing issue is how to deploy the current mechanistic paradigm of ethylene signaling to address diverse ethylene responses in plants (18Lin Z. Zhong S. Grierson D. Recent advances in ethylene research.J. Exp. Botany. 2009; 60: 3311-3336Crossref PubMed Scopus (0) Google Scholar, 19Zhao Q. Guo H.W. Paradigms and paradox in the ethylene signaling pathway and interaction network.Mol. Plant. 2011; 4: 626-634Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar). The mode of ethylene action is dose-dependent in Arabidopsis (20Lu B.W. Pei L.K. Chan W.K. Zhang H. Zhu G. Li J.Y. Li N. The dual effects of ethylene on the negative gravicurvature of arabidopsis inflorescence, an intriguing action model for the plant hormone ethylene.Chinese Sci. Bull. 2001; 46: 279-283Crossref Google Scholar, 21Madlung A. Behringer F.J. Lomax T.L. Ethylene plays multiple nonprimary roles in modulating the gravitropic response in tomato.Plant Physiol. 1999; 120: 897-906Crossref PubMed Google Scholar), and its response to ethylene is achieved over a wide range of concentrations (22Binder B.M. The ethylene receptors: complex perception for a simple gas.Plant Sci. 2008; 175: 8-17Crossref Scopus (0) Google Scholar). At lower concentrations, ethylene promotes both gravicurvature of inflorescence stem and elongation of etiolated seedlings of Arabidopsis (20Lu B.W. Pei L.K. Chan W.K. Zhang H. Zhu G. Li J.Y. Li N. The dual effects of ethylene on the negative gravicurvature of arabidopsis inflorescence, an intriguing action model for the plant hormone ethylene.Chinese Sci. Bull. 2001; 46: 279-283Crossref Google Scholar, 23Binder B.M. Mortimore L.A. Stepanova A.N. Ecker J.R. Bleecker A.B. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent.Plant Physiol. 2004; 136: 2921-2927Crossref PubMed Scopus (116) Google Scholar), whereas at higher concentrations it inhibits both gravicurvature and elongation of the etiolated seedlings (21Madlung A. Behringer F.J. Lomax T.L. Ethylene plays multiple nonprimary roles in modulating the gravitropic response in tomato.Plant Physiol. 1999; 120: 897-906Crossref PubMed Google Scholar, 23Binder B.M. Mortimore L.A. Stepanova A.N. Ecker J.R. Bleecker A.B. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent.Plant Physiol. 2004; 136: 2921-2927Crossref PubMed Scopus (116) Google Scholar). In addition, plant responses to ethylene are also time-dependent (20Lu B.W. Pei L.K. Chan W.K. Zhang H. Zhu G. Li J.Y. Li N. The dual effects of ethylene on the negative gravicurvature of arabidopsis inflorescence, an intriguing action model for the plant hormone ethylene.Chinese Sci. Bull. 2001; 46: 279-283Crossref Google Scholar, 23Binder B.M. Mortimore L.A. Stepanova A.N. Ecker J.R. Bleecker A.B. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent.Plant Physiol. 2004; 136: 2921-2927Crossref PubMed Scopus (116) Google Scholar, 24Lu B.W. Yu H.Y. Pei L.K. Wong M.Y. Li N. Prolonged exposure to ethylene stimulates the negative gravitropic responses of Arabidopsis inflorescence stems and hypocotyls.Funct. Plant Biol. 2002; 29: 987-997Crossref Google Scholar). A short-term exposure to ethylene inhibits gravicurvature of inflorescence stem in Arabidopsis, whereas a long-term pretreatment, regardless of the concentration of ethylene, stimulates gravicurvature (20Lu B.W. Pei L.K. Chan W.K. Zhang H. Zhu G. Li J.Y. Li N. The dual effects of ethylene on the negative gravicurvature of arabidopsis inflorescence, an intriguing action model for the plant hormone ethylene.Chinese Sci. Bull. 2001; 46: 279-283Crossref Google Scholar, 24Lu B.W. Yu H.Y. Pei L.K. Wong M.Y. Li N. Prolonged exposure to ethylene stimulates the negative gravitropic responses of Arabidopsis inflorescence stems and hypocotyls.Funct. Plant Biol. 2002; 29: 987-997Crossref Google Scholar). Such a dual-and-opposing effect of ethylene on the Arabidopsis shoot gravitropic response was also found in the regulation of flowering (25Zhu L. Liu D. Li Y. Li N. Functional phosphoproteomic analysis reveals that a serine-62-phosphorylated isoform of ethylene response factor110 is involved in Arabidopsis bolting.Plant Physiol. 2013; 161: 904-917Crossref PubMed Scopus (17) Google Scholar). The sophisticated mode of action of ethylene is typified by the fact that it delays bolting and both the ethylene receptor mutant etr1-1 and the receptor-interacting signaling component mutant ctr1-1 exhibit similar delayed-bolting phenotypes (26Achard P. Baghour M. Chapple A. Hedden P. Van Der Straeten D. Genschik P. Moritz T. Harberd N.P. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes.Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 6484-6489Crossref PubMed Scopus (0) Google Scholar, 27Ogawara T. Higashi K. Kamada H. Ezura H. Ethylene advances the transition from vegetative growth to flowering in Arabidopsis thaliana.J. Plant Physiol. 2003; 160: 1335-1340Crossref PubMed Scopus (57) Google Scholar). Attempts to address the diverse and complex phenomena related to ethylene responses with a transcriptomics approach have confirmed the existence of a difference in gene expression profiles between ethylene-treated wild-type Arabidopsis and the constitutive ethylene response mutant ctr1-1 (11Qiao H. Shen Z. Huang S.S. Schmitz R.J. Urich M.A. Briggs S.P. Ecker J.R. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas.Science. 2012; 338: 390-393Crossref PubMed Scopus (285) Google Scholar, 28De Paepe A. Vuylsteke M. Van Hummelen P. Zabeau M. Van Der Straeten D. Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis.Plant J. 2004; 39: 537-559Crossref PubMed Scopus (106) Google Scholar, 29Zhong G.Y. Burns J.K. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis.Plant Mol. Biol. 2003; 53: 117-131Crossref PubMed Scopus (125) Google Scholar). Molecular biological analysis has successfully classified ethylene-regulated genes into early- and late-induction groups (30Yang T. Poovaiah B.W. An early ethylene up-regulated gene encoding a calmodulin-binding protein involved in plant senescence and death.J. Biol. Chem. 2000; 275: 38467-38473Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar, 31Zegzouti H. Jones B. Frasse P. Marty C. Maitre B. Latch A. Pech J.C. Bouzayen M. Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display.Plant J. 1999; 18: 589-600Crossref PubMed Google Scholar). The integration of biochemical and cellular functions of each class of time-dependent gene products (i.e. either early or late ethylene-induced gene groups) should constitute separate yet overlapping molecular interaction matrices and networks to define diverse yet complex ethylene responses (32Li N. The dual-and-opposing-effect of ethylene on the negative gravitropism of Arabidopsis inflorescence stem and light-grown hypocotyls.Plant Sci. 2008; 175: 71-86Crossref Scopus (10) Google Scholar). Moreover, post-translational modification (PTM) has recently emerged as one of the important mechanisms regulating the complex plant ethylene responses (19Zhao Q. Guo H.W. Paradigms and paradox in the ethylene signaling pathway and interaction network.Mol. Plant. 2011; 4: 626-634Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar). One type of PTM involved in ethylene signaling is the ethylene-dependent and ubiquitin/26S proteasome-mediated protein degradation or stabilization of ethylene receptors and signaling components EIN2 and EIN3 (33Etheridge N. Chen Y.F. Schaller G.E. Dissecting the ethylene pathway of Arabidopsis.Brief. Funct. Genomic. Proteomic. 2005; 3: 372-381Crossref PubMed Scopus (20) Google Scholar, 34Kendrick M.D. Chang C. Ethylene signaling: new levels of complexity and regulation.Curr. Opin. Plant Biol. 2008; 11: 479-485Crossref PubMed Scopus (198) Google Scholar, 35Qiao H. Chang K.N. Yazaki J. Ecker J.R. Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis.Genes Dev. 2009; 23: 512-521Crossref PubMed Scopus (217) Google Scholar). The other type of PTM-mediated ethylene signaling is interconversion between the phosphorylation and dephosphorylation statuses of signaling components catalyzed by both kinases and phosphatases (11Qiao H. Shen Z. Huang S.S. Schmitz R.J. Urich M.A. Briggs S.P. Ecker J.R. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas.Science. 2012; 338: 390-393Crossref PubMed Scopus (285) Google Scholar, 12Ju 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. Chang C. 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. 2012; 109: 19486-19491Crossref PubMed Scopus (312) Google Scholar, 25Zhu L. Liu D. Li Y. Li N. Functional phosphoproteomic analysis reveals that a serine-62-phosphorylated isoform of ethylene response factor110 is involved in Arabidopsis bolting.Plant Physiol. 2013; 161: 904-917Crossref PubMed Scopus (17) Google Scholar, 33Etheridge N. Chen Y.F. Schaller G.E. Dissecting the ethylene pathway of Arabidopsis.Brief. Funct. Genomic. Proteomic. 2005; 3: 372-381Crossref PubMed Scopus (20) Google Scholar, 36Li Y. Shu Y. Peng C. Zhu L. Guo G. Li N. Absolute quantitation of isoforms of post-translationally modified proteins in transgenic organism.Mol. Cell. Proteomics. 2012; 11: 272-285Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, 37Yoo S.D. Cho Y.H. Tena G. Xiong Y. Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling.Nature. 2008; 451: 789-795Crossref PubMed Scopus (349) Google Scholar). Protein phosphor-relay has long been reported to participate in ethylene signaling events (2Chang C. Kwok S.F. Bleecker A.B. Meyerowitz E.M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.Science. 1993; 262: 539-544Crossref PubMed Google Scholar, 6Kieber J.J. Rothenberg M. Roman G. Feldmann K.A. Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.Cell. 1993; 72: 427-441Abstract Full Text PDF PubMed Scopus (1392) Google Scholar, 38Li H. Wong W.S. Zhu L. Guo H.W. Ecker J. Li N. Phosphoproteomic analysis of ethylene-regulated protein phosphorylation in etiolated seedlings of Arabidopsis mutant ein2 using two-dimensional separations coupled with a hybrid quadrupole time-of-flight mass spectrometer.Proteomics. 2009; 9: 1646-1661Crossref PubMed Scopus (65) Google Scholar, 39Moshkov I.E. Mur L.A. Novikova G.V. Smith A.R. Hall M.A. Ethylene regulates monomeric GTP-binding protein gene expression and activity in Arabidopsis.Plant Physiol. 2003; 131: 1705-1717Crossref PubMed Scopus (0) Google Scholar, 40Raz V. Fluhr R. Ethylene signal is transduced via protein phosphorylation events in plants.Plant Cell. 1993; 5: 523-530Crossref PubMed Scopus (0) Google Scholar). Many ethylene signaling components, including ethylene receptor family proteins and their downstream regulator CTR1, have kinase activities (7Gao Z. Chen Y.F. Randlett M.D. Zhao X.C. Findell J.L. Kieber J.J. Schaller G.E. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes.J. Biol. Chem. 2003; 278: 34725-34732Abstract Full Text Full Text PDF PubMed Scopus (244) Google Scholar, 34Kendrick M.D. Chang C. Ethylene signaling: new levels of complexity and regulation.Curr. Opin. Plant Biol. 2008; 11: 479-485Crossref PubMed Scopus (198) Google Scholar, 41Gamble R.L. Qu X. Schaller G.E. Mutational analysis of the ethylene receptor ETR1. Role of the histidine kinase domain in dominant ethylene insensitivity.Plant Physiol. 2002; 128: 1428-1438Crossref PubMed Scopus (118) Google Scholar, 42Wang W. Hall A.E. O'Malley R. Bleecker A.B. 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. 2003; 100: 352-357Crossref PubMed Scopus (187) Google Scholar), and there are at least two MAPK cascades involved in the regulation of ethylene signaling and the ethylene-regulated phosphorylation of EIN3 (37Yoo S.D. Cho Y.H. Tena G. Xiong Y. Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling.Nature. 2008; 451: 789-795Crossref PubMed Scopus (349) Google Scholar, 43Ouaked F. Rozhon W. Lecourieux D. Hirt H. A MAPK pathway mediates ethylene signaling in plants.EMBO J. 2003; 22: 1282-1288Crossref PubMed Scopus (209) Google Scholar). Phosphorylation/dephosphrylation of the ethylene response factor 110 protein has been found to be EIN2-independent (25Zhu L. Liu D. Li Y. Li N. Functional phosphoproteomic analysis reveals that a serine-62-phosphorylated isoform of ethylene response factor110 is involved in Arabidopsis bolting.Plant Physiol. 2013; 161: 904-917Crossref PubMed Scopus (17) Google Scholar, 36Li Y. Shu Y. Peng C. Zhu L. Guo G. Li N. Absolute quantitation of isoforms of post-translationally modified proteins in transgenic organism.Mol. Cell. Proteomics. 2012; 11: 272-285Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar). Thus, the diverse yet complex plant ethylene responses are actually consequences of the multifaceted and constant integration of ethylene signals mediated by both transcriptional activation cascades and PTM networks (i.e. protein phosphorylation/dephosphorylation, C-terminal cleavage, and ubiquitin/26S proteasome-mediated protein degradation). The key issue is, therefore, how the ethylene receptor–MAPKKK (including CTR1) complexes convert the binding of ethylene into a signal output in the form of kinase activities in a quantitative and substrate-specific manner (12Ju 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. Chang C. 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. 2012; 109: 19486-19491Crossref PubMed Scopus (312) Google Scholar, 22Binder B.M. The ethylene receptors: complex perception for a simple gas.Plant Sci. 2008; 175: 8-17Crossref Scopus (0) Google Scholar). The hypothesis that ethylene inactivates kinase activities of CTR1 has not been substantiated in vivo thus far. It is possible that the binding of ethylene to receptors may alter the substrate specificity of the putative CTR1 serine/threonine kinase. The isolation of an enhanced ethylene response 1 (eer1-1) mutant further complicated the study of the already intriguing ethylene signaling in Arabidopsis (44Larsen P.B. Chang C. The Arabidop" @default.
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• W2128268951 date "2013-12-01" @default.
• W2128268951 modified "2023-10-02" @default.
• W2128268951 title "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" @default.
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