Pepper pathogenesis-related protein 4c is a plasma membrane-localized cysteine protease inhibitor that is required for plant cell death and defense signaling

Plant Journal

Volumn 81, Issue 1, 2015, Pages 81-94

  Kim, Nak Hyun ^a   Hwang, Byung Kook ^a  

^a Korea University   (South Korea)

Author keywords

CaPR4c; Capsicum annuum; cell death; pepper; protease inhibitor; Xanthomonas campestris pv. vesicatoria; Xcv

Indexed keywords

AMINO ACIDS; CELL DEATH; CELL MEMBRANES; ESCHERICHIA COLI; GENE EXPRESSION; PEPTIDES; PLANT CELL CULTURE; PLANTS (BOTANY); RECOMBINANT PROTEINS;

CAPR4C; CAPSICUM ANNUUM; PEPPER; PROTEASE INHIBITOR; XANTHOMONAS CAMPESTRIS PV. VESICATORIA; XCV;

CELL SIGNALING;

ARABIDOPSIS; CAPSICUM ANNUUM; ESCHERICHIA COLI; HYALOPERONOSPORA; PSEUDOMONAS SYRINGAE PV. TOMATO; XANTHOMONAS CAMPESTRIS PV. VESICATORIA;

CYSTEINE PROTEINASE INHIBITOR; MEMBRANE PROTEIN; VEGETABLE PROTEIN;

ARABIDOPSIS; CELL DEATH; CELL MEMBRANE; CYTOLOGY; DISEASE RESISTANCE; GENETICS; IMMUNOLOGY; METABOLISM; PEPPER; PHYSIOLOGY; PLANT CELL; PLANT LEAF; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; XANTHOMONAS CAMPESTRIS;

ARABIDOPSIS; CAPSICUM; CELL DEATH; CELL MEMBRANE; CYSTEINE PROTEINASE INHIBITORS; DISEASE RESISTANCE; MEMBRANE PROTEINS; PLANT CELLS; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; XANTHOMONAS CAMPESTRIS;

EID: 84920262382     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12709     Document Type: Article

References (64)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and, Lipman, D.J., (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
2. 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.
3. Bertini, L., Cascone, A., Tucci, M., D'Amore, R., Di Berardino, I., Buonocore, V., Caporale, C., and, Caruso, C., (2006) Molecular and functional analysis of new members of the wheat PR4 gene family. Biol. Chem. 387, 1101-1111.
4. Boller, T., and, 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.
5. Boller, T., and, He, S.Y., (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 324, 742-744.
6. Broekaert, I., Lee, H.I., Kush, A., Chua, N.H., and, Raikhel, N., (1990) Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis). Proc. Natl Acad. Sci. USA, 87, 7633-7637.
7. Caporale, C., Di Berardino, I., Leonardi, L., Bertini, L., Cascone, A., Buonocore, V., and, Caruso, C., (2004) Wheat pathogenesis-related proteins of class 4 have ribonuclease activity. FEBS Lett. 575, 71-76.
8. Chavez, M.I., Vila-Perello, M., Canada, F.J., Andreu, D., and, Jimenez-Barbero, J., (2010) Effect of a serine-to-aspartate replacement on the recognition of chitin oligosaccharides by truncated hevein. A 3D view by using NMR. Carbohydr. Res. 345, 1461-1468.
9. Chichkova, N.V., Kim, S.H., Titova, E.S., Kalkum, M., Morozov, V.S., Rubtsov, Y.P., Kalinina, N.O., Taliansky, M.E., and, Vartapetian, A.B., (2004) A plant caspase-like protease activated during the hypersensitive response. Plant Cell, 16, 157-171.
10. 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.
11. 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.
12. Choi, D.S., Hwang, I.S., and, Hwang, B.K., (2012) Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper. Plant Cell, 24, 1675-1690.
13. 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.
14. Coll, N.S., Epple, P., and, Dangl, J.L., (2011) Programmed cell death in the plant immune system. Cell Death Differ. 18, 1247-1256.
15. Coppinger, P., Repetti, P.P., Day, B., Dahlbeck, D., Mehlert, A., and, Staskawicz, B.J., (2004) Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant J. 40, 225-237.
16. 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.
17. +-ATPase in plant-microbe interactions. Mol. Plant, 4, 416-427.
18. Friedrich, L., Moyer, M., Ward, E., and, Ryals, J., (1991) Pathogenesis-related protein 4 is structurally homologous to the carboxy-terminal domains of hevein, Win-1 and Win-2. Mol. Gen. Genet. 230, 113-119.
19. Gay, C., Collins, J., and, Gebicki, J.M., (1999) Hydroperoxide assay with the ferric-xylenol orange complex. Anal. Biochem. 273, 149-155.
20. Ha, S.D., Martins, A., Khazaie, K., Han, J., Chan, B.M., and, Kim, S.O., (2008) Cathepsin B is involved in the trafficking of TNF-alpha-containing vesicles to the plasma membrane in macrophages. J. Immunol. 181, 690-697.
21. Hao, L., Goodwin, P.H., and, Hsiang, T., (2007) Expression of a metacaspase gene of Nicotiana benthamiana after inoculation with Colletotrichum destructivum or Pseudomonas syringae pv. tomato, and the effect of silencing the gene on the host response. Plant Cell Rep. 26, 1879-1888.
22. Hoeberichts, F.A., ten Have, A., and, Woltering, E.J., (2003) A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta, 217, 517-522.
23. van der Hoorn, R.A.L., (2008) Plant proteases: from phenotypes to molecular mechanisms. Annu. Rev. Plant Biol. 59, 191-223.
24. Hwang, I.S., and, Hwang, B.K., (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol. 152, 948-967.
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. Hwang, I.S., Choi, D.S., Kim, N.H., Kim, D.S., and, Hwang, B.K., (2014) Pathogenesis-related protein 4b interacts with leucine-rich repeat protein 1 to suppress PR4b-triggered cell death and defense response in pepper. Plant J. 77, 521-533.
27. Jounai, N., Kobiyama, K., Takeshita, F., and, Ishii, K.J., (2013) Recognition of damage-associated molecular patterns related to nucleic acids during inflammation and vaccination. Front Cell. Infect. Microbiol. 2, 168.
28. Jung, H.W., and, Hwang, B.K., (2000) Isolation, partial sequencing, and expression of pathogenesis-related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. vesicatoria. Mol. Plant Microbe Interact. 13, 136-142.
29. 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.
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, N.H., Choi, H.W., and, Hwang, B.K., (2010) Xanthomonas campestris pv. vesicatoria effector AvrBsT induces cell death in pepper, but suppresses defense responses in tomato. Mol. Plant Microbe Interact. 23, 1069-1082.
32. Lam, E., Kato, N., and, Lawton, M., (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature, 411, 848-853.
33. Lamb, C., and, Dixon, R.A., (1997) The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
34. Laskowski, M. Jr, and, Kato, I., (1980) Protein inhibitors of proteinases. Annu. Rev. Biochem. 49, 593-626.
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. Leister, R.T., Dahlbeck, D., Day, B., Li, Y., Chesnokova, O., and, Staskawicz, B.J., (2005) Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell, 17, 1268-1278.
37. Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R., and, Lamb, C., (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427-437.
38. Li, X., Xia, B., Jiang, Y., Wu, Q., Wang, C., He, L., Peng, F., and, Wang, R., (2010) A new pathogenesis-related protein, LrPR4, from Lycoris radiata, and its antifungal activity against Magnaporthe grisea. Mol. Biol. Rep. 37, 995-1001.
39. Linthorst, H.J., Danhash, N., Brederode, F.T., Van Kan, J.A., De Wit, P.J., and, Bol, J.F., (1991) Tobacco and tomato PR proteins homologous to win and pro-hevein lack the "hevein" domain. Mol. Plant Microbe Interact. 4, 586-592.
40. Liu, Y., Schiff, M., and, Dinesh-Kumar, S.P., (2002) Virus-induced gene silencing in tomato. Plant J. 31, 777-786.
41. van Loon, L.C., Rep, M., and, Pieterse, C.M.J., (2006) Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135-162.
42. Lu, H.C., Lin, J.H., Chua, A.C., Chung, T.Y., Tsai, I.C., Tzen, J.T., and, Chou, W.M., (2012) Cloning and expression of pathogenesis-related protein 4 from jelly fig (Ficus awkeotsang Makino) achenes associated with ribonuclease, chitinase and anti-fungal activities. Plant Physiol. Biochem. 56, 1-13.
43. Ludvigsen, S., and, Poulsen, F.M., (1992) Three-dimensional structure in solution of Barwin, a protein from barley seed. Biochemistry, 31, 8783-8789.
44. Mosolov, V.V., and, Valueva, T.A., (2005) Proteinase inhibitors and their function in plants: a review. Prikl. Biokhim. Mikrobiol. 41, 261-282.
45. Nelson, B.K., Cai, X., and, Nebenfuhr, A., (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
46. 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.
47. Ponstein, A.S., Bres-Vloemans, S.A., Sela-Buurlage, M.B., van den Elzen, P.J.M., Melchers, L.S., and, Cornelissen, B.J.C., (1994) A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity. Plant Physiol. 104, 109-118.
48. Romer, P., Hahn, S., Jordan, T., Strauss, T., Bonas, U., and, Lahaye, T., (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science, 318, 645-648.
49. Serveau, C., Juliano, L., Bernard, P., Moreau, T., Mayer, R., and, Gauthier, F., (1994) New substrates of papain, based on the conserved sequence of natural inhibitors of the cystatin family. Biochimie, 76, 153-158.
50. Shin, R., Lee, G.J., Park, C.J., Kim, T.Y., You, J.S., Nam, Y.W., and, Paek, K.H., (2001) Isolation of pepper mRNAs differentially expressed during the hypersensitive response to tobacco mosaic virus and characterization of a proteinase inhibitor gene. Plant Sci. 161, 727-737.
51. 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.
52. Skopelitis, D.S., Paranychianakis, N.V., Paschalidis, K.A., Pliakonis, E.D., Delis, I.D., Yakoumakis, D.I., Kouvarakis, A., Papadakis, A.K., Stephanou, E.G., and, Roubelakis-Angelakis, K.A., (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell, 18, 2767-2781.
53. Solomon, M., Belenghi, B., Delledonne, M., Menachem, E., and, Levine, A., (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell, 11, 431-444.
54. Stanford, A., Bevan, M., and, Northcote, D., (1989) Differential expression within a family of novel wound-induced genes in potato. Mol. Gen. Genet. 215, 200-208.
55. Svensson, B., Svendsen, I., Hojrup, P., Roepstorff, P., Ludvigsen, S., and, Poulsen, F.M., (1992) Primary structure of Barwin: a barley seed protein closely related to the C-terminal domain of proteins encoded by wound-induced plant genes. Biochemistry, 31, 8767-8770.
56. Torres, M.A., Jones, J.D.G., and, Dangl, J.L., (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378.
57. Van Breusegem, F., and, Dat, J.F., (2006) Reactive oxygen species in plant cell death. Plant Physiol. 141, 384-390.
58. Vorhölter, F.J., Wiggerich, H.G., Scheidle, H., Sidhu, V.K., Mrozek, K., Küster, H., Pühler, A., and, Niehaus, K., (2012) Involvement of bacterial TonB-dependent signaling in the generation of an oligogalacturonide damage-associated molecular pattern from plant cell walls exposed to Xanthomonas campestris pv. campestris pectate lyases. BMC Microbiol. 12, 239.
59. Wan, H., Lee, K.S., Kim, B.Y., Zou, F.M., Yoon, H.J., Je, H.J., Li, J., and, Jin, B.R., (2013) A spider-derived Kunitz-type serine protease inhibitor that acts as a plasmin inhibitor and an elastase inhibitor. PLoS ONE, 8, e53343.
60. Wang, N., Xiao, B., and, Xiong, L., (2011) Identification of a cluster of PR4-like genes involved in stress responses in rice. J. Plant Physiol. 168, 2212-2224.
61. Xu, Q., and, Zhang, L., (2009) Plant caspase-like proteases in plant programmed cell death. Plant Signal. Behav. 4, 902-904.
62. Yamaguchi, Y., and, Huffaker, A., (2011) Endogenous peptide elicitors in higher plants. Curr. Opin. Plant Biol. 14, 351-357.
63. Yen, Y., and, Green, P.J., (1991) Identification and properties of the major ribonucleases of Arabidopsis thaliana. Plant Physiol. 97, 1487-1493.
64. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.