Bifurcation of Arabidopsis NLR Immune Signaling via Ca2+-Dependent Protein Kinases

PLoS Pathogens

Volumn 9, Issue 1, 2013, Pages

  Gao, Xiquan ^a   Chen, Xin ^a   Lin, Wenwei ^a   Chen, Sixue ^b   Lu, Dongping ^a   Niu, Yajie ^c   Li, Lei ^c   Cheng, Cheng ^a   McCormack, Matthew ^c   Sheen, Jen ^c   Shan, Libo ^a   He, Ping ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; LEUCINE RICH REPEAT PROTEIN; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WRKY TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE ACTIVATION; IMMUNE RESPONSE; IMMUNE RESPONSE GENE; MOLECULAR GENETICS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VECTOR CONTROL; WESTERN BLOTTING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DEATH; DISEASE RESISTANCE; FOCAL ADHESION KINASE 2; GENE EXPRESSION REGULATION, PLANT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 84875075249     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003127     Document Type: Article

References (60)

1. Boller T, Felix G, (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
2. Tena G, Boudsocq M, Sheen J, (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14: 519-529.
3. Dodds PN, Rathjen JP, (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548.
4. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
5. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
6. Collier SM, Moffett P, (2009) NB-LRRs work a "bait and switch" on pathogens. Trends Plant Sci 14: 521-529.
7. Spoel SH, Dong X, (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12: 89-100.
8. Eitas TK, Dangl JL, (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13: 472-477.
9. Elmore JM, Lin ZJ, Coaker G, (2011) Plant NB-LRR signaling: upstreams and downstreams. Curr Opin Plant Biol 14: 365-371.
10. DeYoung BJ, Innes RW, (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7: 1243-1249.
11. Maekawa T, Kufer TA, Schulze-Lefert P, (2011) NLR functions in plant and animal immune systems: so far and yet so close. Nat Immunol 12: 817-826.
12. Davis BK, Wen H, Ting JP, (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 29: 707-735.
13. Chung EH, da Cunha L, Wu AJ, Gao Z, Cherkis K, et al. (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: 125-136.
14. Liu J, Elmore JM, Lin ZJ, Coaker G, (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: 137-146.
15. Axtell MJ, Staskawicz BJ, (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
16. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL, (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
17. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098-1103.
18. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, et al. (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5: e68.
19. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, et al. (2011) Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334: 1401-1404.
20. Bhattacharjee S, Halane MK, Kim SH, Gassmann W, (2011) Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334: 1405-1408.
21. Gao Z, Chung EH, Eitas TK, Dangl JL, (2011) Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. Proc Natl Acad Sci U S A 108: 7619-7624.
22. Slootweg E, Roosien J, Spiridon LN, Petrescu AJ, Tameling W, et al. (2010) Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains. Plant Cell 22: 4195-4215.
23. Tameling WI, Nooijen C, Ludwig N, Boter M, Slootweg E, et al. (2010) RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22: 4176-4194.
24. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, et al. (2007) Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19: 1081-1095.
25. Grant M, Brown I, Adams S, Knight M, Ainslie A, et al. (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23: 441-450.
26. Ma W, Smigel A, Tsai YC, Braam J, Berkowitz GA, (2008) Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 148: 818-828.
27. Cheng SH, Willmann MR, Chen HC, Sheen J, (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129: 469-485.
28. Luan S, (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14: 37-42.
29. Harper JF, Harmon A, (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6: 555-566.
30. Romeis T, Ludwig AA, Martin R, Jones JD, (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. Embo J 20: 5556-5567.
31. Romeis T, Piedras P, Jones JD, (2000) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12: 803-816.
32. 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.
33. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, et al. (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464: 418-422.
34. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, et al. (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282: 32338-48.
35. Blume B, Nurnberger T, Nass N, Scheel D, (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12: 1425-1440.
36. Zimmermann S, Nurnberger T, Frachisse JM, Wirtz W, Guern J, et al. (1997) Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci U S A 94: 2751-2755.
37. He P, Shan L, Lin NC, Martin GB, Kemmerling B, et al. (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563-575.
38. Wu Y, Wood MD, Tao Y, Katagiri F, (2003) Direct delivery of bacterial avirulence proteins into resistant Arabidopsis protoplasts leads to hypersensitive cell death. Plant J 33: 131-137.
39. Ritter C, Dangl JL, (1996) Interference between Two Specific Pathogen Recognition Events Mediated by Distinct Plant Disease Resistance Genes. Plant Cell 8: 251-257.
40. Eitas TK, Nimchuk ZL, Dangl JL, (2008) Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB. Proc Natl Acad Sci U S A 105: 6475-6480.
41. Kim MG, Geng X, Lee SY, Mackey D, (2009) The Pseudomonas syringae type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2. Plant J 57: 645-653.
42. Delledonne M, Xia Y, Dixon RA, Lamb C, (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585-588.
43. Dong J, Chen C, Chen Z, (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51: 21-37.
44. Rushton PJ, Somssich IE, Ringler P, Shen QJ, (2010) WRKY transcription factors. Trends Plant Sci 15: 247-258.
45. Torres MA, Dangl JL, Jones JD, (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.
46. Chen L, Zhang L, Yu D, (2010) Wounding-induced WRKY8 is involved in basal defense in Arabidopsis. Mol Plant Microbe Interact 23: 558-565.
47. Xing DH, Lai ZB, Zheng ZY, Vinod KM, Fan BF, et al. (2008) Stress- and pathogen-induced Arabidopsis WRKY48 is a transcriptional activator that represses plant basal defense. Mol Plant 1: 459-470.
48. Bernoux M, Ellis JG, Dodds PN, (2011) New insights in plant immunity signaling activation. Curr Opin Plant Biol 14: 512-518.
49. Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F, et al. (2010) Arabidopsis type I metacaspases control cell death. Science 330: 1393-1397.
50. Lecourieux D, Ranjeva R, Pugin A, (2006) Calcium in plant defence-signalling pathways. New Phytol 171: 249-269.
51. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, et al. (2000) The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A 97: 9323-9328.
52. Balague C, Lin B, Alcon C, Flottes G, Malmstrom S, et al. (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15: 365-379.
53. Jurkowski GI, Smith RK Jr, Yu IC, Ham JH, Sharma SB, et al. (2004) Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the "defense, no death" phenotype. Mol Plant Microbe Interact 17: 511-520.
54. Journot-Catalino N, Somssich IE, Roby D, Kroj T, (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18: 3289-3302.
55. Tsuda K, Katagiri F, (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13: 459-465.
56. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, et al. (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci U S A 102: 10736-10741.
57. Lu D, Wu S, He P, Shan L, (2010) Phosphorylation of receptor-like cytoplasmic kinases by bacterial flagellin. Plant Signal Behav 5Epub ahead of print.
58. Avila J, Gregory OG, Su D, Deeter TA, Chen S, et al. (2012) The beta-subunit of the SnRK1 complex is phosphorylated by the plant cell death suppressor Adi3. Plant Physiol 159: 1277-1290.
59. ThordalChristensen H, Zhang ZG, Wei YD, Collinge DB, (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant Journal 11: 1187-1194.
60. Sheen J, (1993) Protein phosphatase activity is required for light-inducible gene expression in maize. EMBO J 12: 3497-3505.