Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper

Plant Cell

Volumn 24, Issue 4, 2012, Pages 1675-1690

  Choi, Du Seok ^a   Hwang, In Sun ^a,b   Hwang, Byung Kook ^a  

^a Korea University   (South Korea)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; CAPSICUM ANNUUM; HYALOPERONOSPORA; LYCOPERSICON ESCULENTUM; NICOTIANA BENTHAMIANA; PSEUDOMONAS SYRINGAE; XANTHOMONAS CAMPESTRIS;

EID: 84861709449     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.095869     Document Type: Article

References (77)

1. Barna, B., Ibenthal, W.D., and Heitefuss, R. (1989). Extracellular RNase activity in healthy and rust-infected wheat leaves. Physiol. Mol. Plant Pathol. 35: 151-160.
2. Breiteneder, H., Pettenburger, K., Bito, A., Valenta, R., Kraft, D., Rumpold, H., Scheiner, O., and Breitenbach, M. (1989). The gene coding for the major birch pollen allergen Betv1, is highly homologous to a pea disease resistance response gene. EMBO J. 8: 1935-1938.
3. Brodersen, P., Petersen, M., Pike, H.M., Olszak, B., Skov, S., Ødum, N., Jørgensen, L.B., Brown, R.E., and Mundy, J. (2002). Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16: 490-502.
4. Bufe, A., Spangfort, M.D., Kahlert, H., Schlaak, M., and Becker, W.-M. (1996). The major birch pollen allergen, Bet v 1, shows ribonuclease activity. Planta 199: 413-415.
5. Burch-Smith, T.M., Schiff, M., Caplan, J.L., Tsao, J., Czymmek, K., and Dinesh-Kumar, S.P. (2007). A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol. 5: e68.
6. Choi, D.S., and Hwang, B.K. (2011). Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 23: 823-842.
7. Choi, H.W., Lee, B.G., Kim, N.H., Park, Y., Lim, C.W., Song, H.K., and Hwang, B.K. (2008). A role for a menthone reductase in resistance against microbial pathogens in plants. Plant Physiol. 148: 383-401.
8. Choi, H.W., Kim, Y.J., and Hwang, B.K. (2011). The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity. Mol. Plant Microbe Interact. 24: 68-78.
9. Choi, H.W., Kim, Y.J., Lee, S.C., Hong, J.K., and Hwang, B.K. (2007). Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol. 145: 890-904.
10. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
11. Colditz, F., Niehaus, K., and Krajinski, F. (2007). Silencing of PR-10-like proteins in Medicago truncatula results in an antagonistic induction of other PR proteins and in an increased tolerance upon infection with the oomycete Aphanomyces euteiches. Planta 226: 57-71.
12. Dangl, J.L., Dietrich, R.A., and Richberg, M.H. (1996). Death don't have no mercy: Cell death programs in plant-microbe interactions. Plant Cell 8: 1793-1807.
13. Dangl, J.L., and Jones, J.D.G. (2001). Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
14. Do, H.M., Lee, S.C., Jung, H.W., Sohn, K.H., and Hwang, B.K. (2004). Differential expression and in situ localization of a pepper defensin (CADEF1) gene in response to pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Plant Sci. 166: 1297-1305.
15. Fujimoto, Y., Nagata, R., Fukasawa, H., Yano, K., Azuma, M., Iida, A., Sugimoto, S., Shudo, K., and Hashimoto, Y. (1998). Purification and cDNA cloning of cytokinin-specific binding protein from mung bean (Vigna radiata). Eur. J. Biochem. 258: 794-802.
16. Galiana, E., Bonnet, P., Conrod, S., Keller, H., Panabières, F., Ponchet, M., Poupet, A., and Ricci, P. (1997). RNase activity prevents the growth of a fungal pathogen in tobacco leaves and increases upon induction of systemic acquired resistance with elicitin. Plant Physiol. 115: 1557-1567.
17. Gao, Z., Chung, E.-H., Eitas, T.K., and Dangl, J.L. (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. USA 108: 7619-7624. Erratum. Proc. Natl. Acad. Sci. USA 108: 8915.
18. Gassmann, W., Hinsch, M.E., and Staskawicz, B.J. (1999). The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIRNBS- LRR family of disease-resistance genes. Plant J. 20: 265-277.
19. Gómez-Gómez, L., and Boller, T. (2000). FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagelin in Arabidopsis. Mol. Cell 5: 1003-1011.
20. Greenberg, J.T., and Yao, N. (2004). The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6: 201-211.
21. Gutierrez, J.R., Balmuth, A.L., Ntoukakis, V., Mucyn, T.S., Gimenez- Ibanez, S., Jones, A.M.E., and Rathjen, J.P. (2010). Prf immune complexes of tomato are oligomeric and contain multiple Pto-like kinases that diversify effector recognition. Plant J. 61: 507-518.
22. Hashimoto, M., Kisseleva, L., Sawa, S., Furukawa, T., Komatsu, S., and Koshiba, T. (2004). A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol. 45: 550-559.
23. Hodel, M.R., Corbett, A.H., and Hodel, A.E. (2001). Dissection of a nuclear localization signal. J. Biol. Chem. 276: 1317-1325.
24. Hwang, I.S., An, S.H., and Hwang, B.K. (2011). Pepper asparagine synthetase 1 (CaAS1) is required for plant nitrogen assimilation and defense responses to microbial pathogens. Plant J. 67: 749-762.
25. Hwang, I.S., and Hwang, B.K. (2011). The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Plant Physiol. 155: 447-463.
26. Jung, E.H., Jung, H.W., Lee, S.C., Han, S.W., Heu, S., and Hwang, B.K. (2004). Identification of a novel pathogen-induced gene encoding a leucine-rich repeat (LRR) protein expressed in phloem cells of Capsicum annuum. Biochim. Biophys. Acta 1676: 211-222.
27. Jung, H.W., and Hwang, B.K. (2007). The leucine-rich repeat (LRR) protein, CaLRR1, interacts with the hypersensitive induced reaction (HIR) protein, CaHIR1, and suppresses cell death induced by the CaHIR1 protein. Mol. Plant Pathol. 8: 503-514.
28. Jung, Y.-H., Lee, J.-H., Agrawal, G.K., Rakwal, R., Kim, J.-A., Shim, J.-K., Lee, S.-K., Jeon, J.-S., Koh, H.-J., Lee, Y.-H., Iwahashi, H., and Jwa, N.-S. (2005). The rice (Oryza sativa) blast lesion mimic mutant, blm, may confer resistance to blast pathogens by triggering multiple defense-associated signaling pathways. Plant Physiol. Biochem. 43: 397-406.
29. Jung, Y.H., et al. (2006). Differential expression of defense/stressrelated marker proteins in leaves of a unique rice blast lesion mimic mutant (blm). J. Proteome Res. 5: 2586-2598.
30. Kim, D.S., and Hwang, B.K. (2011). The pepper receptor-like cytoplasmic protein kinase CaPIK1 is involved in plant signaling of defense and cell-death responses. Plant J. 66: 642-655.
31. Kim, Y.J., and Hwang, B.K. (2000). Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiol. Plant. 108: 51-60.
32. Koistinen, K.M., Soininen, P., Venäläinen, T.A., Häyrinen, J., Laatikainen, R., Peräkylä, M., Tervahauta, A.I., and Kärenlampi, S.O. (2005). Birch PR-10c interacts with several biologically important ligands. Phytochemistry 66: 2524-2533.
33. Lacomme, C., and Santa Cruz, S. (1999). Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl. Acad. Sci. USA 96: 7956-7961.
34. Lee, D.H., Choi, H.W., and Hwang, B.K. (2011). The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response. Plant Physiol. 156: 2011-2025.
35. Lee, S.C., and Hwang, B.K. (2003). Identification of the pepper SAR8.2 gene as a molecular marker for pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Planta 216: 387-396.
36. Lee, S.C., Hwang, I.S., Choi, H.W., and Hwang, B.K. (2008). Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol. 148: 1004-1020.
37. Li, Y., Tessaro, M.J., Li, X., and Zhang, Y. (2010). Regulation of the expression of plant resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol. 153: 1425-1434.
38. Lim, J.H., Park, C.-J., Huh, S.U., Choi, L.M., Lee, G.J., Kim, Y.J., and Paek, K.-H. (2011). Capsicum annuum WRKYb transcription factor that binds to the CaPR-10 promoter functions as a positive regulator in innate immunity upon TMV infection. Biochem. Biophys. Res. Commun. 411: 613-619.
39. Liu, J.J., and Ekramoddoullah, A.K.M. (2006). The family 10 of plant pathogenesis-related proteins: Their structure, regulation, and function in response to biotic and abiotic stresses. Physiol. Mol. Plant Pathol. 68: 3-13.
40. Liu, Y.L., Schiff, M., and Dinesh-Kumar, S.P. (2002). Virus-induced gene silencing in tomato. Plant J. 31: 777-786.
41. Lo, S.-C.C., Hipskind, J.D., and Nicholson, R.L. (1999). cDNA cloning of a sorghum pathogenesis-related protein (PR-10) and differential expression of defense-related genes following inoculation with Cochliobolus heterostrophus or Colletotrichum sublineolum. Mol. Plant Microbe Interact. 12: 479-489.
42. Lorrain, S., Vailleau, F., Balagué, C., and Roby, D. (2003). Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8: 263-271.
43. Lusso, M., and Kuc, J. (1995). Increased activities of ribonuclease and protease after challenge in tobacco plants with induced systemic resistance. Physiol. Mol. Plant Pathol. 47: 419-428.
44. Markovic ́-Housley, Z., Degano, M., Lamba, D., von Roepenack- Lahaye, E., Clemens, S., Susani, M., Ferreira, F., Scheiner, O., and Breiteneder, H. (2003). Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier. J. Mol. Biol. 325: 123-133.
45. Martin, K., Steinberg, T.H., Cooley, L.A., Gee, K.R., Beechem, J.M., and Patton, W.F. (2003). Quantitative analysis of protein phosphorylation status and protein kinase activity on microarrays using a novel fluorescent phosphorylation sensor dye. Proteomics 3: 1244-1255.
46. Matton, D.P., and Brisson, N. (1989). Cloning, expression, and sequence conservation of pathogenesis-related gene transcripts of potato. Mol. Plant Microbe Interact. 2: 325-331.
47. McGee, J.D., Hamer, J.E., and Hodges, T.K. (2001). Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol. Plant Microbe Interact. 14: 877-886.
48. Melech-Bonfil, S., and Sessa, G. (2010). Tomato MAPKKK« is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J. 64: 379-391.
49. Michael Weaver, L., Swiderski, M.R., Li, Y., and Jones, J.D.G. (2006). The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant J. 47: 829-840.
50. Moffett, P., Farnham, G., Peart, J., and Baulcombe, D.C. (2002). Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21: 4511-4519.
51. Mogensen, J.E., Wimmer, R., Larsen, J.N., Spangfort, M.D., and Otzen, D.E. (2002). The major birch allergen, Bet v 1, shows affinity for a broad spectrum of physiological ligands. J. Biol. Chem. 277: 23684-23692.
52. Mohammadi, M., Anoop, V., Gleddie, S., and Harris, L.J. (2011). Proteomic profiling of two maize inbreds during early gibberella ear rot infection. Proteomics 11: 3675-3684.
53. Mosher, S., Moeder, W., Nishimura, N., Jikumaru, Y., Joo, S.H., Urquhart, W., Klessig, D.F., Kim, S.K., Nambara, E., and Yoshioka, K. (2010). The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol. 152: 1901-1913.
54. Park, C.J., Kim, K.J., Shin, R., Park, J.M., Shin, Y.C., and Paek, K.H. (2004). Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J. 37: 186-198.
55. Pontier, D., Godiard, L., Marco, Y., and Roby, D. (1994). hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J. 5: 507-521.
56. Pühringer, H., Moll, D., Hoffmann-Spmmergruber, K., Watillon, B., Katinger, H., and Laimer da Camara Machado, M. (2000). The promoter of apple Ypr 10 gene, encoding the major allerhen Mal d 1, is stress- and pathogen-inducible. Plant Sci. 152: 35-50.
57. Sheen, J., and He, P. (2007). Nuclear actions in innate immune signaling. Cell 128: 821-823.
58. Shen, Q.-H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Ülker, B., Somssich, I.E., and Schulze-Lefert, P. (2007). Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098-1103.
59. Shen, Q.-H., and Schulze-Lefert, P. (2007). Rumble in the nuclear jungle: Compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO J. 26: 4293-4301.
60. Shivakumar, P.D., Vasanthi, N.S., Shetty, H.S., and Smedegaard- Petersen, V. (2000). Ribonucleases in the seedlings of pearl millet and their involvement in resistance against downy mildew disease. Eur. J. Plant Pathol. 106: 825-836.
61. Slootweg, E., 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.
62. Somssich, I.E., Schmelzer, E., Bollmann, J., and Hahlbrock, K. (1986). Rapid activation by fungal elicitor of genes encoding "pathogenesis-related" proteins in cultured parsley cells. Proc. Natl. Acad. Sci. USA 83: 2427-2430.
63. Spoel, S.H., and Dong, X. (2008). Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3: 348-351.
64. Staehelin, L.A., and Driouich, A. (1997). Brefeldin A effects in plants (Are different Golgi responses caused by different sites of action?). Plant Physiol. 114: 401-403.
65. Tameling, W.I.L., Nooijen, C., Ludwig, N., Boter, M., Slootweg, E., Goverse, A., Shirasu, K., and Joosten, M.H.A.J. (2010). RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22: 4176-4194.
66. Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y., and Martin, G.B. (1996). Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274: 2060-2063.
67. Walter, M.H., Liu, J.W., Grand, C., Lamb, C.J., and Hess, D. (1990). Bean pathogenesis-related (PR) proteins deduced from elicitor-induced transcripts are members of a ubiquitous new class of conserved PR proteins including pollen allergens. Mol. Gen. Genet. 222: 353-360.
68. Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K., and Kudla, J. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
69. Wang, X., Goshe, M.B., Soderblom, E.J., Phinney, B.S., Kuchar, J.A., Li, J., Asami, T., Yoshida, S., Huber, S.C., and Clouse, S.D. (2005). Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell 17: 1685-1703.
70. Wang, Z.Y., Seto, H., Fujioka, S., Yoshida, S., and Chory, J. (2001). BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410: 380-383.
71. Warner, S.A.J., Scott, R., and Draper, J. (1992). Characterisation of a wound-induced transcript from the monocot asparagus that shares similarity with a class of intracellular pathogenesis-related (PR) proteins. Plant Mol. Biol. 19: 555-561.
72. Wirthmueller, L., Zhang, Y., Jones, J.D.G., and Parker, J.E. (2007). Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17: 2023-2029.
73. Yen, Y., and Green, P.J. (1991). Identification and properties of the major ribonucleases of Arabidopsis thaliana. Plant Physiol. 97: 1487-1493.
74. Zhang, H., Dong, S., Wang, M., Wang, W., Song, W., Dou, X., Zheng, X., and Zhang, Z. (2010). The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure. J. Exp. Bot. 61: 3799-3812.
75. Zhou, X.-J., Lu, S., Xu, Y.-H., Wang, J.-W., and Chen, X.-Y. (2002). A cotton cDNA (GaPR-10) encoding a pathogenesis-related 10 protein with in vitro ribonuclease activity. Plant Sci. 162: 629-636.
76. Ziadi, S., Poupard, P., Brisset, M.-n., Paulin, J.P., and Simoneau, P. (2001). Characterization in apple leaves of two subclasses of PR-10 transcripts inducible by acibenzolar-S-methyl, a functional analogue of salicylic acid. Physiol. Mol. Plant Pathol. 59: 33-43.
77. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D., Boller, T., and Felix, G. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.