Loss of Arabidopsis thaliana Dynamin-Related Protein 2B Reveals Separation of Innate Immune Signaling Pathways

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Smith, John M ^a,b   Leslie, Michelle E ^a,b   Robinson, Samuel J ^a,b   Korasick, David A ^a,b,d   Zhang, Tong ^a,b   Backues, Steven K ^c,e   Cornish, Peter V ^a   Koo, Abraham J ^a,b   Bednarek, Sebastian Y ^c   Heese, Antje ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d WASHINGTON UNIVERSITY   (United States)

^e EASTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; DYNAMIN; DYNAMIN RELATED PROTEIN 2B; FLAGELLIN; FLAGELLIN 22; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESPIRATORY BURST OXIDASE HOMOLOGUE D; SALICYLIC ACID; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; DRP2B PROTEIN, ARABIDOPSIS; FLS2 PROTEIN, ARABIDOPSIS; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN KINASE; RESPIRATORY BURST OXIDASE HOMOLOG D, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; CALCIUM CELL LEVEL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENDOCYTOSIS; IMMUNOBLOTTING; INNATE IMMUNITY; NONHUMAN; PROTEIN PHOSPHORYLATION; PSEUDOMONAS SYRINGAE; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ARABIDOPSIS; DEFICIENCY; GENETICS; IMMUNOLOGY; MUTATION; PHYSIOLOGY; PLANT IMMUNITY;

ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); EUKARYOTA; PSEUDOMONAS SYRINGAE PV. TOMATO;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLAGELLIN; GTP-BINDING PROTEINS; IMMUNITY, INNATE; MUTATION; NADPH OXIDASE; PLANT IMMUNITY; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 84919665924     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004578     Document Type: Article

References (98)

1. Macho Alberto P, Zipfel C, (2014) Plant PRRs and the Activation of Innate Immune Signaling. Molecular Cell 54: 263–272.
2. Boller T, Felix G, (2009) A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors. Annual Review of Plant Biology 60: 379–406.
3. Kumar H, Kawai T, Akira S, (2011) Pathogen Recognition by the Innate Immune System. International Reviews of Immunology 30: 16–34.
4. Bardy SL, Ng SYM, Jarrell KF, (2003) Prokaryotic motility structures. Microbiology 149: 295–304.
5. Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, et al. (2013) Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytologist 200: 847–860.
6. Robatzek S, Wirthmueller L, (2013) Mapping FLS2 function to structure: LRRs, kinase and its working bits. Protoplasma 250: 671–681.
7. Monaghan J, Zipfel C, (2012) Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology 15: 349–357.
8. Sun Y, Li L, Macho AP, Han Z, Hu Z, et al. (2013) Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex. Science 342: 624–628.
9. Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S, (2012) Spatio-Temporal Cellular Dynamics of the Arabidopsis Flagellin Receptor Reveal Activation Status-Dependent Endosomal Sorting. Plant Cell 24: 4205–4219.
10. Choi S-w, Tamaki T, Ebine K, Uemura T, Ueda T, et al. (2013) RABA Members Act in Distinct Steps of Subcellular Trafficking of the FLAGELLIN SENSING2 Receptor. Plant Cell 25: 1174–1187.
11. Lu D, Lin W, Gao X, Wu S, Cheng C, et al. (2011) Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity. Science 332: 1439–1442.
12. Robatzek S, Chinchilla D, Boller T, (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes & Development 20: 537–542.
13. Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A, (2014) Sensitivity to Flg22 Is Modulated by Ligand-Induced Degradation and de Novo Synthesis of the Endogenous Flagellin-Receptor FLAGELLIN-SENSING2. Plant Physiology 164: 440–454.
14. Spallek T, Beck M, Ben Khaled S, Salomon S, Bourdais G, et al. (2013) ESCRT-I Mediates FLS2 Endosomal Sorting and Plant Immunity. PLoS Genet 9: e1004035.
15. Nicaise V, Roux M, Zipfel C, (2009) Recent Advances in PAMP-Triggered Immunity against Bacteria: Pattern Recognition Receptors Watch over and Raise the Alarm. Plant Physiol 150: 1638–1647.
16. Tena G, Boudsocq M, Sheen J, (2011) Protein kinase signaling networks in plant innate immunity. Current Opinion in Plant Biology 14: 519–529.
17. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJR, Slijper M, et al. (2007) Quantitative Phosphoproteomics of Early Elicitor Signaling in Arabidopsis. Molecular & Cellular Proteomics 6: 1198–1214.
18. Nühse TS, Bottrill AR, Jones AME, Peck SC, (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant Journal 51: 931–940.
19. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, et al. (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464: 418–422.
20. Korasick DA, McMichael C, Walker KA, Anderson JC, Bednarek SY, et al. (2010) Novel Functions of Stomatal Cytokinesis-Defective 1 (SCD1) in Innate Immune Responses against Bacteria. Journal of Biological Chemistry 285: 23342–23350.
21. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F, (2009) Network Properties of Robust Immunity in Plants. PLoS Genet 5: e1000772.
22. Xu J, Xie J, Yan C, Zou X, Ren D, et al. (2014) A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. Plant Journal 77: 222–234.
23. Henty-Ridilla JL, Li J, Day B, Staiger CJ, (2014) ACTIN DEPOLYMERIZING FACTOR4 Regulates Actin Dynamics during Innate Immune Signaling in Arabidopsis. Plant Cell 26: 340–352.
24. Bednarek SY, Backues SK, (2010) Plant dynamin-related protein families DRP1 and DRP2 in plant development. Biochemical Society Transactions 038: 797–806.
25. Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G, et al. (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Molecular Biology 53: 261–265.
26. Backues SK, Korasick DA, Heese A, Bednarek SY, (2010) The Arabidopsis Dynamin-Related Protein2 Family Is Essential for Gametophyte Development. Plant Cell 22: 3218–3231.
27. Taylor N, (2011) A role for Arabidopsis dynamin related proteins DRP2A/B in endocytosis; DRP2 function is essential for plant growth. Plant Molecular Biology 76: 117–129.
28. Ferguson SM, De Camilli P, (2012) Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13: 75–88.
29. Pucadyil TJ, Schmid SL, (2009) Conserved Functions of Membrane Active GTPases in Coated Vesicle Formation. Science 325: 1217–1220.
30. Howes MT, Mayor S, Parton RG, (2010) Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis. Current Opinion in Cell Biology 22: 519–527.
31. Sandvig K, Pust S, Skotland T, van Deurs B, (2011) Clathrin-independent endocytosis: mechanisms and function. Current Opinion in Cell Biology 23: 413–420.
32. Fujimoto M, Arimura S-i, Nakazono M, Tsutsumi N, (2008) Arabidopsis dynamin-related protein DRP2B is co-localized with DRP1A on the leading edge of the forming cell plate. Plant Cell Rep 27: 1581–1586.
33. Fujimoto M, Arimura S-i, Ueda T, Takanashi H, Hayashi Y, et al. (2010) Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc Natl Acad Sci U S A 107: 6094–6099.
34. Xiong G, Li R, Qian Q, Song X, Liu X, et al. (2010) The rice dynamin-related protein DRP2B mediates membrane trafficking, and thereby plays a critical role in secondary cell wall cellulose biosynthesis. Plant Journal 64: 56–70.
35. Bandmann V, Homann U, (2012) Clathrin-independent endocytosis contributes to uptake of glucose into BY-2 protoplasts. Plant J 70: 578–584.
36. Li R, Liu P, Wan Y, Chen T, Wang Q, et al. (2012) A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24: 2105–2122 doi: 2110.1105/tpc.2112.095695. Epub 092012 May 095615
37. Hirano K, Kotake T, Kamihara K, Tsuna K, Aohara T, et al. (2010) Rice BRITTLE CULM 3 (BC3) encodes a classical dynamin OsDRP2B essential for proper secondary cell wall synthesis. Planta 232: 95–108.
38. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, et al. (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 104: 12217–12222.
39. Torres MA, Dangl JL, Jones JDG, (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99: 517–522.
40. Wildermuth MC, Dewdney J, Wu G, Ausubel FM, (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562–565.
41. Knight H, Trewavas AJ, Knight MR, (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489–503.
42. Smith J, Heese A, (2014) Rapid bioassay to measure early reactive oxygen species production in Arabidopsis leave tissue in response to living Pseudomonas syringae. Plant Methods 10: 6.
43. Tanaka K, Swanson SJ, Gilroy S, Stacey G, (2010) Extracellular Nucleotides Elicit Cytosolic Free Calcium Oscillations in Arabidopsis. Plant Physiology 154: 705–719.
44. Fan J, Crooks C, Lamb C, (2008) High-throughput quantitative luminescence assay of the growth in planta of Pseudomonas syringae chromosomally tagged with Photorhabdus luminescens luxCDABE. Plant Journal 53: 393–399.
45. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F, (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant Journal 53: 763–775.
46. Anderson JC, Bartels S, Besteiro MAG, Shahollari B, Ulm R, et al. (2011) Arabidopsis MAP Kinase Phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria. Plant Journal 67: 258–268.
47. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G, (2007) Identification of 118 Arabidopsis Transcription Factor and 30 Ubiquitin-Ligase Genes Responding to Chitin, a Plant-Defense Elicitor. Molecular Plant-Microbe Interactions 20: 900–911.
48. Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, et al. (2011) Callose Deposition: A Multifaceted Plant Defense Response. Molecular Plant-Microbe Interactions 24: 183–193.
49. Koo AJK, Cooke TF, Howe GA, (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc Natl Acad Sci U S A 108: 9298–9303.
50. Koo AJK, Gao X, Daniel Jones A, Howe GA, (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant Journal 59: 974–986.
51. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Meth 9: 676–682.
52. Hall M, Frank E, Holmes G, Pfahringer B, Reutemann P, et al. (2009) The WEKA data mining software: an update. SIGKDD Explor Newsl 11: 10–18.
53. Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, et al. (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci U S A 107: 14502–14507.
54. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497–500.
55. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant Journal 18: 265–276.
56. Zhang J, Shao F, Li Y, Cui H, Chen L, et al. (2007) A Pseudomonas syringae Effector Inactivates MAPKs to Suppress PAMP-Induced Immunity in Plants. Cell Host & Microbe 1: 175–185.
57. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D, (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant Journal 68: 100–113.
58. Li L, Li M, Yu L, Zhou Z, Liang X, et al. (2014) The FLS2-Associated Kinase BIK1 Directly Phosphorylates the NADPH Oxidase RbohD to Control Plant Immunity. Cell Host & Microbe 15: 329–338.
59. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, et al. (2011) Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis. Plant Cell 23: 1639–1653.
60. Munnik T, Nielsen E, (2011) Green light for polyphosphoinositide signals in plants. Current Opinion in Plant Biology 14: 489–497.
61. Wang J, Cai Y, Miao Y, Lam SK, Jiang L, (2009) Wortmannin induces homotypic fusion of plant prevacuolar compartments. Journal of Experimental Botany 60: 3075–3083.
62. Ito E, Fujimoto M, Ebine K, Uemura T, Ueda T, et al. (2012) Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging. Plant Journal 69: 204–216.
63. Banbury DN, Oakley JD, Sessions RB, Banting G, (2003) Tyrphostin A23 Inhibits Internalization of the Transferrin Receptor by Perturbing the Interaction between Tyrosine Motifs and the Medium Chain Subunit of the AP-2 Adaptor Complex. Journal of Biological Chemistry 278: 12022–12028.
64. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, et al. (2007) Clathrin-Mediated Constitutive Endocytosis of PIN Auxin Efflux Carriers in Arabidopsis. Current Biology 17: 520–527.
65. Irani NG, Di Rubbo S, Mylle E, Van den Begin J, Schneider-Pizoń J, et al. (2012) Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat Chem Biol 8: 583–589.
66. Konopka CA, Bednarek SY, (2008) Comparison of the Dynamics and Functional Redundancy of the Arabidopsis Dynamin-Related Isoforms DRP1A and DRP1C during Plant Development. Plant Physiol 147: 1590–1602.
67. Leborgne-Castel N, Lherminier J, Der C, Fromentin J, Houot V, et al. (2008) The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells. Plant Physiology 146: 1255–1266.
68. Ortiz-Zapater E, Soriano-Ortega E, Marcote MJ, Ortiz-Masiá D, Aniento F, (2006) Trafficking of the human transferrin receptor in plant cells: effects of tyrphostin A23 and brefeldin A. Plant Journal 48: 757–770.
69. Torres MA, Jones JDG, Dangl JL, (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37: 1130–1134.
70. Mansfield JW, (2009) From bacterial avirulence genes to effector functions via the hrp delivery system: an overview of 25 years of progress in our understanding of plant innate immunity. Molecular Plant Pathology 10: 721–734.
71. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, et al. (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 110: 8744–8749.
72. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, et al. (2014) Direct Regulation of the NADPH Oxidase RBOHD by the PRR-Associated Kinase BIK1 during Plant Immunity. Molecular Cell 54: 43–55.
73. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, et al. (2007) Calcium-Dependent Protein Kinases Regulate the Production of Reactive Oxygen Species by Potato NADPH Oxidase. Plant Cell 19: 1065–1080.
74. Curran A, Chang I-F, Chang C-L, Garg S, Miguel RM, et al. (2011) Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Front Plant Sci 2: 36.
75. Tsuda K, Mine A, Bethke G, Igarashi D, Botanga CJ, et al. (2013) Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana. PLoS Genet 9: e1004015.
76. Gangadharan A, Sreerekha M-V, Whitehill J, Ham JH, Mackey D, (2013) The Pseudomonas syringae pv. tomato Type III Effector HopM1 Suppresses Arabidopsis Defenses Independent of Suppressing Salicylic Acid Signaling and of Targeting AtMIN7. PLoS ONE 8: e82032.
77. Nomura K, Mecey C, Lee Y-N, Imboden LA, Chang JH, et al. (2011) Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc Natl Acad Sci U S A 108: 10774–10779.
78. Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, et al. (2011) Hierarchy and Roles of Pathogen-Associated Molecular Pattern-Induced Responses in Nicotiana benthamiana. Plant Physiology 156: 687–699.
79. Lu X, Tintor N, Mentzel T, Kombrink E, Boller T, et al. (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc Natl Acad Sci U S A 106: 22522–22527.
80. Falbel TG, Koch LM, Nadeau JA, Segui-Simarro JM, Sack FD, et al. (2003) SCD1 is required for cytokinesis and polarized cell expansion in Arabidopsis thaliana. Development 130: 4011–4024.
81. McMichael CM, Reynolds GD, Koch LM, Wang C, Jiang N, et al. (2013) Mediation of Clathrin-Dependent Trafficking during Cytokinesis and Cell Expansion by Arabidopsis STOMATAL CYTOKINESIS DEFECTIVE Proteins. Plant Cell 25: 3910–3925.
82. Beck M, Heard W, Mbengue M, Robatzek S, (2012) The INs and OUTs of pattern recognition receptors at the cell surface. Current Opinion in Plant Biology 15: 367–374.
83. Scita G, Di Fiore PP, (2010) The endocytic matrix. Nature 463: 464–473.
84. Sorkin A, von Zastrow M, (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10: 609–622.
85. Irani NG, Russinova E, (2009) Receptor endocytosis and signaling in plants. Current Opinion in Plant Biology 12: 653–659.
86. Kagan Jonathan C, (2012) Signaling Organelles of the Innate Immune System. Cell 151: 1168–1178.
87. McGettrick AF, O'Neill LAJ, (2010) Localisation and trafficking of Toll-like receptors: an important mode of regulation. Current Opinion in Immunology 22: 20–27.
88. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al. (2006) Dynasore, a Cell-Permeable Inhibitor of Dynamin. Developmental Cell 10: 839–850.
89. Husebye H, Halaas O, Stenmark H, Tunheim G, Sandanger O, et al. (2006) Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J 25: 683–692.
90. Wang Y, Yang Y, Liu X, Wang N, Cao H, et al. (2012) Inhibition of clathrin/dynamin-dependent internalization interferes with LPS-mediated TRAM–TRIF-dependent signaling pathway. Cellular Immunology 274: 121–129.
91. Parker D, Prince A, (2013) Epithelial Uptake of Flagella Initiates Proinflammatory Signaling. PLoS ONE 8: e59932.
92. Sharfman M, Bar M, Ehrlich M, Schuster S, Melech-Bonfil S, et al. (2011) Endosomal signaling of the tomato leucine-rich repeat receptor-like protein LeEix2. Plant Journal 68: 413–423.
93. Hao H, Fan L, Chen T, Li R, Li X, et al. (2014) Clathrin and Membrane Microdomains Cooperatively Regulate RbohD Dynamics and Activity in Arabidopsis. The Plant Cell Online 26: 1729–1745.
94. Kitakura S, Vanneste S, Robert S, Löfke C, Teichmann T, et al. (2011) Clathrin Mediates Endocytosis and Polar Distribution of PIN Auxin Transporters in Arabidopsis. Plant Cell 23: 1920–1931.
95. Lu D, Wu S, Gao X, Zhang Y, Shan L, et al. (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci U S A 107: 496–501.
96. Zhang J, Li W, Xiang T, Liu Z, Laluk K, et al. (2010) Receptor-like Cytoplasmic Kinases Integrate Signaling from Multiple Plant Immune Receptors and Are Targeted by a Pseudomonas syringae Effector. Cell Host & Microbe 7: 290–301.
97. Lin W, Li B, Lu D, Chen S, Zhu N, et al. (2014) Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc Natl Acad Sci U S A 111: 3632–3637.
98. Li W, Ahn I-P, Ning Y, Park C-H, Zeng L, et al. (2012) The U-Box/ARM E3 Ligase PUB13 Regulates Cell Death, Defense, and Flowering Time in Arabidopsis. Plant Physiology 159: 239–250.