Mutations in FLS2 Ser-938 Dissect Signaling Activation in FLS2-Mediated Arabidopsis Immunity

Cao, Yangrong; Aceti, David J.; Sabat, Grzegorz; Song, Junqi; Makino, Shin-ichi; Fox, Brian G.; Bent, Andrew F.

doi:10.1371/journal.ppat.1003313

Title: Mutations in FLS2 Ser-938 Dissect Signaling Activation in FLS2-Mediated Arabidopsis Immunity

Journal Article · Thu Apr 18 00:00:00 EDT 2013 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1003313· OSTI ID:1904701

Cao, Yangrong ^[1]; Aceti, David J. ^[1]; Sabat, Grzegorz ^[1]; Song, Junqi ^[1]; Makino, Shin-ichi ^[1]; Fox, Brian G. ^[1]; Bent, Andrew F. ^[1]

University of Wisconsin, Madison, WI (United States)

FLAGELLIN-SENSING 2 (FLS2) is a leucine-rich repeat/transmembrane domain/protein kinase (LRR-RLK) that is the plant receptor for bacterial flagellin or the flagellin-derived flg22 peptide. Previous work has shown that after flg22 binding, FLS2 releases BIK1 kinase and homologs and associates with BAK1 kinase, and that FLS2 kinase activity is critical for FLS2 function. However, the detailed mechanisms for activation of FLS2 signaling remain unclear. The present study initially identified multiple FLS2 in vitro phosphorylation sites and found that Serine-938 is important for FLS2 function in vivo. FLS2-mediated immune responses are abolished in transgenic plants expressing FLS2_S938A, while the acidic phosphomimic mutants FLS2_S938D and FLS2_S938E conferred responses similar to wild-type FLS2. FLS2-BAK1 association and FLS2-BIK1 disassociation after flg22 exposure still occur with FLS2_S938A, demonstrating that flg22-induced BIK1 release and BAK1 binding are not sufficient for FLS2 activity, and that Ser-938 controls other aspects of FLS2 activity. Purified BIK1 still phosphorylated purified FLS2_S938A and FLS2_S938D mutant kinase domains in vitro. Phosphorylation of BIK1 and homologs after flg22 exposure was disrupted in transgenic Arabidopsis thaliana plants expressing FLS2_S938A or FLS2_D997A (a kinase catalytic site mutant), but was normally induced in FLS2_S938D plants. BIK1 association with FLS2 required a kinase-active FLS2, but FLS2-BAK1 association did not. Hence FLS2-BIK1 dissociation and FLS2-BAK1 association are not sufficient for FLS2-mediated defense activation, but the proposed FLS2 phosphorylation site Ser-938 and FLS2 kinase activity are needed both for overall defense activation and for appropriate flg22-stimulated phosphorylation of BIK1 and homologs.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-02ER15342

OSTI ID:: 1904701

Journal Information:: PLoS Pathogens, Vol. 9, Issue 4; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays a role in brassinosteroid signaling and basal defense gene expression Oh, Man-Ho; Wang, Xiaofeng; Wu, Xia Proceedings of the National Academy of Sciences, Vol. 107, Issue 41 https://doi.org/10.1073/pnas.0915064107	journal	September 2010
Flagellin perception: a paradigm for innate immunity Gómez-Gómez, Lourdes; Boller, Thomas Trends in Plant Science, Vol. 7, Issue 6 https://doi.org/10.1016/S1360-1385(02)02261-6	journal	June 2002
A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity Lu, D.; Wu, S.; Gao, X. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0909705107	journal	December 2009
The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation Zhang, Wei; He, Sheng Yang; Assmann, Sarah M. The Plant Journal, Vol. 56, Issue 6 https://doi.org/10.1111/j.1365-313X.2008.03657.x	journal	December 2008
Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity Lu, D.; Lin, W.; Gao, X. Science, Vol. 332, Issue 6036 https://doi.org/10.1126/science.1204903	journal	June 2011
Nomenclature and Symbolism for Amino Acids and Peptides. Recommendations 1983 European Journal of Biochemistry, Vol. 138, Issue 1, p. 9-37 https://doi.org/10.1111/j.1432-1033.1984.tb07877.x	journal	January 1984
Structural Insights into the Autoactivation Mechanism of p21-Activated Protein Kinase Wang, Jue; Wu, Jia-Wei; Wang, Zhi-Xin Structure, Vol. 19, Issue 12 https://doi.org/10.1016/j.str.2011.10.013	journal	December 2011
Sequential Transphosphorylation of the BRI1/BAK1 Receptor Kinase Complex Impacts Early Events in Brassinosteroid Signaling Wang, Xiaofeng; Kota, Uma; He, Kai Developmental Cell, Vol. 15, Issue 2 https://doi.org/10.1016/j.devcel.2008.06.011	journal	August 2008
Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions Bent, Andrew F.; Mackey, David Annual Review of Phytopathology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.phyto.45.062806.094427	journal	September 2007
Regulation of Brassinosteroid Signaling by a GSK3/SHAGGY-Like Kinase Li, Jianming; Nam, Kyoung Hee Science, Vol. 295, Issue 5558 https://doi.org/10.1126/science.1065769	journal	February 2002
Probing the Arabidopsis Flagellin Receptor: FLS2-FLS2 Association and the Contributions of Specific Domains to Signaling Function Sun, Wenxian; Cao, Yangrong; Jansen Labby, Kristin The Plant Cell, Vol. 24, Issue 3 https://doi.org/10.1105/tpc.112.095919	journal	March 2012
Autophosphorylation profiling of Arabidopsis protein kinases using the cell-free system Nemoto, Keiichirou; Seto, Takuya; Takahashi, Hirotaka Phytochemistry, Vol. 72, Issue 10 https://doi.org/10.1016/j.phytochem.2011.02.029	journal	July 2011
Brassinosteroid signal transduction – choices of signals and receptors Wang, Zhi-Yong; He, Jun-Xian Trends in Plant Science, Vol. 9, Issue 2 https://doi.org/10.1016/j.tplants.2003.12.009	journal	February 2004
A Type I–Secreted, Sulfated Peptide Triggers XA21-Mediated Innate Immunity Lee, Sang-Won; Han, Sang-Wook; Sririyanum, Malinee Science, Vol. 326, Issue 5954 https://doi.org/10.1126/science.1173438	journal	November 2009
Phosphorylation-Dependent Differential Regulation of Plant Growth, Cell Death, and Innate Immunity by the Regulatory Receptor-Like Kinase BAK1 Schwessinger, Benjamin; Roux, Milena; Kadota, Yasuhiro PLoS Genetics, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pgen.1002046	journal	April 2011
Activation segment exchange: a common mechanism of kinase autophosphorylation? Oliver, Antony W.; Knapp, Stefan; Pearl, Laurence H. Trends in Biochemical Sciences, Vol. 32, Issue 8 https://doi.org/10.1016/j.tibs.2007.06.004	journal	August 2007
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 Song, W. -Y.; Wang, G. -L.; Chen, L. -L. Science, Vol. 270, Issue 5243 https://doi.org/10.1126/science.270.5243.1804	journal	December 1995
Identification and Mutational Analysis of Arabidopsis FLS2 Leucine-Rich Repeat Domain Residues That Contribute to Flagellin Perception Dunning, F. Mark; Sun, Wenxian; Jansen, Kristin L. The Plant Cell, Vol. 19, Issue 10 https://doi.org/10.1105/tpc.106.048801	journal	October 2007
A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors Boller, Thomas; Felix, Georg Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105346	journal	June 2009
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence Chinchilla, Delphine; Zipfel, Cyril; Robatzek, Silke Nature, Vol. 448, Issue 7152 https://doi.org/10.1038/nature05999	journal	July 2007
Identification and Functional Analysis of in Vivo Phosphorylation Sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 Receptor Kinase Wang, Xiaofeng; Goshe, Michael B.; Soderblom, Erik J. The Plant Cell, Vol. 17, Issue 6 https://doi.org/10.1105/tpc.105.031393	journal	May 2005
The Arabidopsis Leucine-Rich Repeat Receptor–Like Kinases BAK1/SERK3 and BKK1/SERK4 Are Required for Innate Immunity to Hemibiotrophic and Biotrophic Pathogens Roux, Milena; Schwessinger, Benjamin; Albrecht, Catherine The Plant Cell, Vol. 23, Issue 6 https://doi.org/10.1105/tpc.111.084301	journal	June 2011
Homomeric and heteromeric complexes among TGF-β and BMP receptors and their roles in signaling Ehrlich, Marcelo; Horbelt, Daniel; Marom, Barak Cellular Signalling, Vol. 23, Issue 9 https://doi.org/10.1016/j.cellsig.2011.04.004	journal	September 2011
Cell-Free Protein Synthesis Technology in NMR High-Throughput Structure Determination Makino, Shin-ichi; Goren, Michael A.; Fox, Brian G. Methods in Molecular Biology https://doi.org/10.1007/978-1-60327-331-2_12	book	January 2009
Differential innate immune signalling via Ca2+ sensor protein kinases Boudsocq, Marie; Willmann, Matthew R.; McCormack, Matthew Nature, Vol. 464, Issue 7287 https://doi.org/10.1038/nature08794	journal	February 2010
Asymmetric tyrosine kinase arrangements in activation or autophosphorylation of receptor tyrosine kinases Bae, Jae Hyun; Schlessinger, Joseph Molecules and Cells, Vol. 29, Issue 5 https://doi.org/10.1007/s10059-010-0080-5	journal	April 2010
Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses: Quantitative phosphoproteomics for signalling pathways Nühse, Thomas S.; Bottrill, Andrew R.; Jones, Alexandra M. E. The Plant Journal, Vol. 51, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03192.x	journal	July 2007
A Conserved Threonine Residue in the Juxtamembrane Domain of the XA21 Pattern Recognition Receptor Is Critical for Kinase Autophosphorylation and XA21-mediated Immunity Chen, Xuewei; Chern, Mawsheng; Canlas, Patrick E. Journal of Biological Chemistry, Vol. 285, Issue 14 https://doi.org/10.1074/jbc.M109.093427	journal	January 2010
Use of Phospho-Site Substitutions to Analyze the Biological Relevance of Phosphorylation Events in Regulatory Networks Dissmeyer, Nico; Schnittger, Arp Methods in Molecular Biology https://doi.org/10.1007/978-1-61779-264-9_6	book	January 2011
Pseudomonas syringae Effector AvrPto Blocks Innate Immunity by Targeting Receptor Kinases Xiang, Tingting; Zong, Na; Zou, Yan Current Biology, Vol. 18, Issue 1 https://doi.org/10.1016/j.cub.2007.12.020	journal	January 2008
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.199	journal	June 2007
Fls2 Gómez-Gómez, Lourdes; Boller, Thomas Molecular Cell, Vol. 5, Issue 6 https://doi.org/10.1016/S1097-2765(00)80265-8	journal	June 2000
Tomato Protein Kinase 1b Mediates Signaling of Plant Responses to Necrotrophic Fungi and Insect Herbivory AbuQamar, Synan; Chai, Mao-Feng; Luo, Hongli The Plant Cell, Vol. 20, Issue 7 https://doi.org/10.1105/tpc.108.059477	journal	July 2008
Brassinosteroid-Insensitive-1 Is a Ubiquitously Expressed Leucine-Rich Repeat Receptor Serine/Threonine Kinase Friedrichsen, Danielle M.; Joazeiro, Claudio A. P.; Li, Jianming Plant Physiology, Vol. 123, Issue 4 https://doi.org/10.1104/pp.123.4.1247	journal	August 2000
MAP kinase signalling cascade in Arabidopsis innate immunity Asai, Tsuneaki; Tena, Guillaume; Plotnikova, Joulia Nature, Vol. 415, Issue 6875 https://doi.org/10.1038/415977a	journal	February 2002
Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation Zipfel, Cyril; Kunze, Gernot; Chinchilla, Delphine Cell, Vol. 125, Issue 4 https://doi.org/10.1016/j.cell.2006.03.037	journal	May 2006
The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants Heese, A.; Hann, D. R.; Gimenez-Ibanez, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 29 https://doi.org/10.1073/pnas.0705306104	journal	July 2007
Both the Extracellular Leucine-Rich Repeat Domain and the Kinase Activity of FLS2 Are Required for Flagellin Binding and Signaling in Arabidopsis Gómez-Gómez, Lourdes; Bauer, Zsuzsa; Boller, Thomas The Plant Cell, Vol. 13, Issue 5 https://doi.org/10.1105/tpc.13.5.1155	journal	May 2001
Cell Signaling by Receptor Tyrosine Kinases Lemmon, Mark A.; Schlessinger, Joseph Cell, Vol. 141, Issue 7 https://doi.org/10.1016/j.cell.2010.06.011	journal	June 2010
Receptor-like Cytoplasmic Kinases Integrate Signaling from Multiple Plant Immune Receptors and Are Targeted by a Pseudomonas syringae Effector Zhang, Jie; Li, Wei; Xiang, Tingting Cell Host & Microbe, Vol. 7, Issue 4 https://doi.org/10.1016/j.chom.2010.03.007	journal	April 2010
Disruption of Poly(ADP-ribosyl)ation Mechanisms Alters Responses of Arabidopsis to Biotic Stress Adams-Phillips, Lori; Briggs, Amy G.; Bent, Andrew F. Plant Physiology, Vol. 152, Issue 1 https://doi.org/10.1104/pp.109.148049	journal	November 2009
Project management system for structural and functional proteomics: Sesame Zolnai, Zsolt; Lee, Peter T.; Li, Jing Journal of Structural and Functional Genomics, Vol. 4, Issue 1, p. 11-23 https://doi.org/10.1023/A:1024684404761	journal	January 2003
Structural Analysis of Pseudomonas syringae AvrPtoB Bound to Host BAK1 Reveals Two Similar Kinase-Interacting Domains in a Type III Effector Cheng, Wei; Munkvold, Kathy R.; Gao, Haishan Cell Host & Microbe, Vol. 10, Issue 6 https://doi.org/10.1016/j.chom.2011.10.013	journal	December 2011
Structural Modes of Stabilization of Permissive Phosphorylation Sites in Protein Kinases: Distinct Strategies in Ser/Thr and Tyr Kinases Krupa, A.; Preethi, G.; Srinivasan, N. Journal of Molecular Biology, Vol. 339, Issue 5 https://doi.org/10.1016/j.jmb.2004.04.043	journal	June 2004
Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis Oh, M. -H.; Wang, X.; Kota, U. Proceedings of the National Academy of Sciences, Vol. 106, Issue 2 https://doi.org/10.1073/pnas.0810249106	journal	January 2009
Deactivation of the Arabidopsis BRASSINOSTEROID INSENSITIVE 1 (BRI1) receptor kinase by autophosphorylation within the glycine-rich loop Oh, Man-Ho; Wang, Xiaofeng; Clouse, Steven D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1108321109	journal	December 2011
Phosphoproteomics of the Arabidopsis Plasma Membrane and a New Phosphorylation Site Database Nühse, Thomas S.; Stensballe, Allan; Jensen, Ole N. The Plant Cell, Vol. 16, Issue 9 https://doi.org/10.1105/tpc.104.023150	journal	August 2004
The insulin receptor: a prototype for dimeric, allosteric membrane receptors? De Meyts, Pierre Trends in Biochemical Sciences, Vol. 33, Issue 8 https://doi.org/10.1016/j.tibs.2008.06.003	journal	August 2008
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 Laluk, Kristin; Luo, Hongli; Chai, Maofeng The Plant Cell, Vol. 23, Issue 8 https://doi.org/10.1105/tpc.111.087122	journal	August 2011
Model for growth hormone receptor activation based on subunit rotation within a receptor dimer Brown, Richard J.; Adams, Julian J.; Pelekanos, Rebecca A. Nature Structural & Molecular Biology, Vol. 12, Issue 9 https://doi.org/10.1038/nsmb977	journal	August 2005
Allele-Specific Suppression of a Defective Brassinosteroid Receptor Reveals a Physiological Role of UGGT in ER Quality Control Jin, Hua; Yan, Zhenyan; Nam, Kyoung Hee Molecular Cell, Vol. 26, Issue 6 https://doi.org/10.1016/j.molcel.2007.05.015	journal	June 2007
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase Knighton, D.; Zheng, J.; Ten Eyck, L. Science, Vol. 253, Issue 5018 https://doi.org/10.1126/science.1862342	journal	July 1991
Plant and Animal Pathogen Recognition Receptors Signal through Non-RD Kinases Dardick, Christopher; Ronald, Pamela PLoS Pathogens, Vol. 2, Issue 1 https://doi.org/10.1371/journal.ppat.0020002	journal	January 2006
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi Journal of Bioscience and Bioengineering, Vol. 104, Issue 1 https://doi.org/10.1263/jbb.104.34	journal	July 2007
High efficiency single step production of expression plasmids from cDNA clones using the Flexi Vector cloning system Blommel, Paul G.; Martin, Peter A.; Wrobel, Russell L. Protein Expression and Purification, Vol. 47, Issue 2 https://doi.org/10.1016/j.pep.2005.11.007	journal	June 2006
BIK1 Function in Plant Growth and Defense Signaling Eckardt, Nancy A. The Plant Cell, Vol. 23, Issue 8 https://doi.org/10.1105/tpc.111.230811	journal	August 2011
BRI1/BAK1, a Receptor Kinase Pair Mediating Brassinosteroid Signaling Nam, Kyoung Hee; Li, Jianming Cell, Vol. 110, Issue 2 https://doi.org/10.1016/S0092-8674(02)00814-0	journal	July 2002
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis Robatzek, S. Genes & Development, Vol. 20, Issue 5 https://doi.org/10.1101/gad.366506	journal	March 2006
Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases Shiu, S. -H.; Bleecker, A. B. Proceedings of the National Academy of Sciences, Vol. 98, Issue 19 https://doi.org/10.1073/pnas.181141598	journal	August 2001
Autophosphorylation Induces Autoactivation and a Decrease in the Src Homology 2 Domain Accessibility of the Lyn Protein Kinase Sotirellis, Nikolaos; Johnson, Timothy M.; Hibbs, Margaret L. Journal of Biological Chemistry, Vol. 270, Issue 50 https://doi.org/10.1074/jbc.270.50.29773	journal	December 1995
Battling Immune Kinases in Plants Day, Brad; He, Sheng Yang Cell Host & Microbe, Vol. 7, Issue 4 https://doi.org/10.1016/j.chom.2010.04.003	journal	April 2010
Face-to-Face, Pak-to-Pak Malecka, Kimberly A.; Peterson, Jeffrey R. Structure, Vol. 19, Issue 12 https://doi.org/10.1016/j.str.2011.11.007	journal	December 2011
Innate Immunity: The Virtues of a Nonclonal System of Recognition Medzhitov, Ruslan; Janeway, Charles A. Cell, Vol. 91, Issue 3 https://doi.org/10.1016/s0092-8674(00)80412-2	journal	October 1997
Active and Inactive Protein Kinases: Structural Basis for Regulation Johnson, Louise N.; Noble, Martin E. M.; Owen, David J. Cell, Vol. 85, Issue 2 https://doi.org/10.1016/s0092-8674(00)81092-2	journal	April 1996
Rapid Heteromerization and Phosphorylation of Ligand-activated Plant Transmembrane Receptors and Their Associated Kinase BAK1 Schulze, Birgit; Mentzel, Tobias; Jehle, Anna K. Journal of Biological Chemistry, Vol. 285, Issue 13 https://doi.org/10.1074/jbc.m109.096842	journal	January 2010
Flagellin Is Not a Major Defense Elicitor in Ralstonia solanacearum Cells or Extracts Applied to Arabidopsis thaliana Pfund, Christine; Tans-Kersten, Julie; Dunning, F. Mark Molecular Plant-Microbe Interactions, Vol. 17, Issue 6 https://doi.org/10.1094/mpmi.2004.17.6.696	journal	June 2004
The Molecular Biology of Rice Shimamoto, Ko Science, Vol. 270, Issue 5243 https://doi.org/10.1126/science.270.5243.1772	journal	December 1995
Tyrosine phosphorylation in brassinosteroid signaling Oh, Man-Ho; Clouse, Steven D.; Huber, Steven C. Plant Signaling & Behavior, Vol. 4, Issue 12 https://doi.org/10.4161/psb.4.12.10046	journal	December 2009
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. Laluk, K. The Plant Cell https://doi.org/10.3410/f.13109956.14433054	dataset	August 2011

Cited By (8)

Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture Chen, Dongqin; Cao, Yangrong; Li, Hong Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02340-3	journal	December 2017
Sucrose-induced Receptor Kinase 1 is Modulated by an Interacting Kinase with Short Extracellular Domain* Wu, Xu Na; Chu, Liangcui; Xi, Lin Molecular & Cellular Proteomics, Vol. 18, Issue 8 https://doi.org/10.1074/mcp.ra119.001336	journal	August 2019
Behind the lines–actions of bacterial type III effector proteins in plant cells Büttner, Daniela FEMS Microbiology Reviews, Vol. 40, Issue 6 https://doi.org/10.1093/femsre/fuw026	journal	August 2016
Intracellular Ca2+ is important for flagellin-triggered defense in Arabidopsis and involves inositol polyphosphate signaling Ma, Yi; Zhao, Yichen; Berkowitz, Gerald A. Journal of Experimental Botany, Vol. 68, Issue 13 https://doi.org/10.1093/jxb/erx176	journal	June 2017
The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity Wang, Jing; Qu, Baoyuan; Dou, Shijuan BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0442-4	journal	February 2015
Physcomitrella patens Has Kinase-LRR R Gene Homologs and Interacting Proteins Tanigaki, Yusuke; Ito, Kenji; Obuchi, Yoshiyuki PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0095118	journal	April 2014
FLS2-BAK1 Extracellular Domain Interaction Sites Required for Defense Signaling Activation Koller, Teresa; Bent, Andrew F. PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0111185	journal	October 2014
SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato Huang, Shuhua; Nie, Shuming; Wang, Shufen International Journal of Molecular Sciences, Vol. 18, Issue 9 https://doi.org/10.3390/ijms18091966	journal	September 2017

Similar Records

FLS2-BAK1 Extracellular Domain Interaction Sites Required for Defense Signaling Activation

Journal Article · Thu Oct 30 00:00:00 EDT 2014 · PLoS ONE · OSTI ID:1904701

Koller, Teresa; Bent, Andrew F.

Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes

Journal Article · Fri Feb 10 00:00:00 EST 2017 · PLoS ONE · OSTI ID:1904701

Tunc-Ozdemir, Meral; Jones, Alan M.

Directed Evolution of FLS2 towards Novel Flagellin Peptide Recognition

Journal Article · Mon Jun 06 00:00:00 EDT 2016 · PLoS ONE · OSTI ID:1904701

Helft, Laura; Thompson, Mikayla; Bent, Andrew F.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
phosphorylation
Arabidopsis thaliana
genetically modified plants
protein kinases
seedings
flagellin
in vitro kinase assay
immune response

Title: Mutations in FLS2 Ser-938 Dissect Signaling Activation in FLS2-Mediated Arabidopsis Immunity

Citation Formats

References (70)

Cited By (8)

Similar Records

Related Subjects