DOI QR코드

DOI QR Code

Functional Characterization of PR-1 Protein, β-1,3-Glucanase and Chitinase Genes During Defense Response to Biotic and Abiotic Stresses in Capsicum annuum

  • Hong, Jeum-Kyu (Division of Bioscience and Technology, College of Life and Environmental Science, Korea University) ;
  • Hwang, Byung-Kook (Division of Bioscience and Technology, College of Life and Environmental Science, Korea University)
  • Published : 2005.09.01

Abstract

Spatial and temporal expression of pathogenesis-related (PR) gene and proteins has been recognized as inducible defense response in pepper plants. Gene expression and/or protein accumulation of PR-1, $\beta-1,3-glucanase$ and chitinase was predominantly found in pepper plants during the inoculations by Xanthomonas campestris pv. vesicatoria, Phytophthora capsici and Colletotrichum coccodes. PR-1 and chitinase genes were also induced in pepper plants in response to environmental stresses, such as high salinity and drought. PR-1 and chitinase gene expressions by biotic and abiotic stresses were regulated by their own promoter regions containing several stress-related cis-acting elements. Overexpression of pepper PR-1 or chitinase genes in heterogeneous transgenic plants showed enhanced disease resistance as well as environmental stress tolerances. In this review, we focused on the putative function of pepper PR-1, $\beta-1,3-glucanase$ and chitinase proteins and/or genes at the biochemical, molecular and cytological aspects.

Keywords

References

  1. A-H-Mackerness, S., John, C. F., Jordan, B. and Thomas, B. 2001. Early signaling components in ultraviolet-B responses:distinct roles for different reactive species and nitric oxide. FEBS Lett. 489:237-242 https://doi.org/10.1016/S0014-5793(01)02103-2
  2. Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D. and Shinozaki K. 1997. Role of arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 10: 1859-1868
  3. Alexander, D., Goodman, R. M., Gut-Rella, M., Glascock, C., Weymann, K., Friedrich, L., Madoz, D., Ahl-goy, P., Luntz, T., Ward, E. and Ryals, J. 1993. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-regulated la. Proc. Natl. Acad. Sci. U.S.A. 90:7327-7331
  4. Apel, K. and Hirt, H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373-99 https://doi.org/10.1146/annurev.arplant.55.031903.141701
  5. Apse, M. P. and Blumwald, E. 2002. Engineering salt tolerance in plants. Curr. Opin. Biotechnol. 13:146-150 https://doi.org/10.1016/S0958-1669(02)00298-7
  6. Breda, C., Sallaud, C., EI-Turk, J., Buffard, D., de Kozak, I., Esnault, R. and Kondorosi, A. 1996. Defense reaction in Medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles. Mol. Plant-Microbe Interact. 9:713-719 https://doi.org/10.1094/MPMI-9-0713
  7. Broglie, K., Chet, I., Holliday, M., Cressman, R., Biddle, P., Knowlton, S., Mauvais, C. J. and Broglie, R. 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254:1194-1197 https://doi.org/10.1126/science.254.5035.1194
  8. Chen, R. D., Yu, L. X., Greer, A. F., Cheriti, H. and Tabaeizadeh, Z. 1994. Isolation of an osmotic stress- and abscisic acid-induced gene encoding an acidic endochitinase from Lycoper-sicon chilense. Mol. Gen. Genet. 245: 195-202
  9. Cherif, M., Benhamou, N. and Belanger, R. 1992. Occurrence of cellulose and chitin in the hyphal walls of Pythium ultimum: a comparative study with other plant pathogenic fungi. Can. J. Microbiol. 39:213-222 https://doi.org/10.1139/m93-030
  10. Constabel, C. P. and Brisson, N. 1995. Stigma- and vascular-specific expression of the PR-10a gene of potato: a novel pattern of expression of a pathogenesis-related gene. Mol. Plant-Microbe Interact. 8:104-113 https://doi.org/10.1094/MPMI-8-0104
  11. Cutt. J. R., Harpster, M. H., Dixon, D. C., Carr, J. P., Dunsmuir, P. and Klessig, D. F. 1989. Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. Virology 173:89-97 https://doi.org/10.1016/0042-6822(89)90224-9
  12. Daugrois, J. H., Lafiette, C., Barthe, J. P. and Touze, A. 1990. Induction of $\beta$-I ,3-glucanase and chitinase activity in compatible and incompatible interactions between Colletotrichum linthemuthianum and bean cultivars. J. Phytopathol. 130:225-234 https://doi.org/10.1111/j.1439-0434.1990.tb01171.x
  13. Do, H. M., Hong, J. K., Jung, H. W., Ham, J. H. and Hwang, B. K. 2003. Expression of peroxidase-like genes, $H_2O_2$ production and peroxidase activity during the hypersensitive response to Xanthomonas campestris pv. vesicatoria in Capsicum annuum. Mol. Plant-Microbe Interact. 16:196-205 https://doi.org/10.1094/MPMI.2003.16.3.196
  14. Ernst, D., Schraudner, M., Langebartels, C. and Sandermann, H. Jr. 1992. Ozone-induced changes of mRNA levels of $\beta$-I ,3-glucanase, chitinase and 'pathogenesis-related' protein 1b in tobacco plants. Plant Mol. Biol. 20:673-682 https://doi.org/10.1007/BF00046452
  15. Eulgem, T., Rushton, P. J., Robatzek, S. and Somssich, I. E. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5:199-206 https://doi.org/10.1016/S1360-1385(00)01600-9
  16. Eulgem, T., Rushton, P. J., Schmelzer, E., Hahlbrock, K. and Somssich, I. E. 1999. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J. 18:4689-4699 https://doi.org/10.1093/emboj/18.17.4689
  17. Eyal, Y., Meller, Y., Lev-Yadan, S. and Fluhr, R. 1993. A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. Plant J. 4:225-234 https://doi.org/10.1046/j.1365-313X.1993.04020225.x
  18. Finkelstein, R. R., Gampala, S. S. L. and Rock, C. D. 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell S15-S45
  19. Hoegen, E., Stromberg, A., Pihlgren, U. and Kombrink, E. 2002. Primary structure and tissue-specific expression of the pathogenesis-related protein PR-1b in potato. Mol. Plant Pathol. 3:329-345 https://doi.org/10.1046/j.1364-3703.2002.00126.x
  20. Hong, J. K. and Hwang, B. K. 1998. Influence of inoculum density, wetness duration, plant age, inoculation method, and cultivar resistance on infection of pepper plants by Colletotrichum coccodes. Plant Dis. 82: 1079-1083 https://doi.org/10.1094/PDIS.1998.82.10.1079
  21. Hong, J. K and Hwang, B. K. 2002. Induction by pathogen, salt and drought of a basic class II chitinase mRNA and in situ localization in pepper (Capsicum annuum). Physiol. Plant. 114:549-558 https://doi.org/10.1034/j.1399-3054.2002.1140407.x
  22. Hong, J. K., Jung, H. W., Kim, Y. J. and Hwang, B. K. 2000. Pepper gene encoding a basic class II chitinase is inducible by pathogen and ethephon. Plant Sci. 159:39-49 https://doi.org/10.1016/S0168-9452(00)00312-5
  23. Hong, J. K. and Hwang, B. K. 2005a. Induction of enhanced disease resistance and oxidative stress tolerance by overexpression of pepper basic PR-1 gene in Arabidopsis. Physiol. Plant. 124:267-277 https://doi.org/10.1111/j.1399-3054.2005.00515.x
  24. Hong, J. K. and Hwang, B. K. 2005b. Promoter activation of pepper class II basic chitinase gene, CAChi2, and enhanced bacterial disease resistance and osmotic stress tolerance in the CAChi2-overexpressing Arabidopsis. Planta (in press)
  25. Hong, J. K., Lee, S. C. and Hwang, B. K. 2005. Activation of pepper basic PR-1 gene promoter during defense signaling to pathogen, abiotic and environmental stresses. Gene 356: 169-180 https://doi.org/10.1016/j.gene.2005.04.030
  26. Hwang, B. K. 2001. Cytology, physiology and molecular genetics of resistance to Phytophthora blight in pepper plants. Plant Pathol. J. 17:9-21
  27. Hwang, B. K., Sunwoo, J. Y., Kim, Y. J. and Kim, B. S. 1997. Accumulation of $\beta$-1, 3-glucanase and chitinase isoforms, and salicylic acid in the DL-$\beta$-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. Physiol. Mol. Plant Pathol. 51:305-322 https://doi.org/10.1006/pmpp.1997.0119
  28. Jacinto, J., McGurl, B., Franceschi, V., Delano-Freier, J. and Ryan, C. A. 1997. Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the $\beta$-glucuronidase gene in transgenic tomato plants. Planta 203 :406-412 https://doi.org/10.1007/s004250050207
  29. Jung, H. W and Hwang, B. K. 2000a. Isolation, partial sequencing, and expressing of pathogenesis-related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. vesicatoria. Mol. Plant-Microbe Interact. 13:136-142 https://doi.org/10.1094/MPMI.2000.13.1.136
  30. Jung, H. W. and Hwang, B. K. 2000b. Pepper gene encoding a basic $\beta$-1 ,3-glucanase is differentially expressed in pepper tissues upon pathogen infection and ethephon or methyl jasmonate. Plant Sci. 159:97-106 https://doi.org/10.1016/S0168-9452(00)00334-4
  31. Keen, N. T. and Yoshikawa, M. 1983. $\beta$-1,3-Endoglucanase from soybean releases elicitor-active carbohydrates from fungus cell wall. Plant Physiol. 71:460-465 https://doi.org/10.1104/pp.71.3.460
  32. Kim, Y. J. and Hwang, B. K. 1994. Differential accumulation of $\beta$-1 ,3-glucanase and chitinase isoforms in pepper stems infected by compatible and incompatible isolates of Phytophthora capsici. Physiol. Mol. Plant Pathol. 45: 195-209 https://doi.org/10.1016/S0885-5765(05)80077-3
  33. Kim, Y. J. and Hwang, B. K. 1996. Purification, N-terminal amino acid sequencing and antifungal activity of chitinases from pepper stems treated with mercuric chloride. Physiol. Mol. Plant Pathol. 48:417-432 https://doi.org/10.1006/pmpp.1996.0033
  34. Kim, Y. J. and Hwang, B. K. 1997. Isolation of a basic 34 kiloDalton $\beta$-1 ,3-glucanase with inhibitory against Phytophthora capsici from pepper stems. Physiol. Mol. Plant Pathol. 50: 103-115 https://doi.org/10.1006/pmpp.1996.0073
  35. 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 https://doi.org/10.1034/j.1399-3054.2000.108001051x./
  36. Kuzniak, E. and Sklodowska, M. 2005. Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta (in press)
  37. Lee, S. C. and Hwang, B. K. 2005. Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221 :790-800 https://doi.org/10.1007/s00425-005-1488-6
  38. Lee, Y. K. and Hwang, B. K. 1996. Differential induction and accumulation of $\beta$-1 ,3-glucanase and chitinase isoforms in the intercellular space and leaf tissues of pepper by Xanthomonas campestris pv. vesicatoria. J. Phytopathol. 144:79-87 https://doi.org/10.1111/j.1439-0434.1996.tb01493.x
  39. Lee, Y. K., Hippe-Sanwald, S., Jung, H. W., Hong, J. K., Hause, B. and Hwang, B. K. 2000a. In situ localization of chitinase mRNA and protein in compatible and incompatible interactions of pepper stems with Phytophthora capsici. Physiol. Mol. Plant Pathol. 57: 111-121 https://doi.org/10.1006/pmpp.2000.0290
  40. Lee, Y. K., Hippe-Sanwald, S., Lee, S. C., Hohenberg, H. and Hwang, B. K. 2000b. In situ localization of PR-1 mRNA and PR-1 protein in compatible and incompatible interactions of pepper stems with Phytophthora capsici. Protoplasma 211:64-75 https://doi.org/10.1007/BF01279900
  41. Linthorst, H. J. M., Meuwissen, R. L. J., Kauffinann, S. and Bol, J. F. 1989. Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus infection. Plant Cell 1:285-291 https://doi.org/10.1105/tpc.1.3.285
  42. Mauch, F., Mauch-Mani B. and Boller, T. 1988. Antifungal hydrolases in pea tissue. Plant Physiol. 88:936-942 https://doi.org/10.1104/pp.88.3.936
  43. Metraux, J. P., Streit, L. and Staub, T. 1988. A pathogenesis-related protein in cucumber is a chitinase. Physiol. Mol. Plant Pathol. 33:1-9 https://doi.org/10.1016/0885-5765(88)90038-0
  44. Mithofer, A., Schulze, B. and Boland, W. 2004. Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett. 566:1-5 https://doi.org/10.1016/j.febslet.2004.04.011
  45. Niderman, T., Genetet, I., Bruyere, T, Gees, R., Stintzi, A., Legrand, M., Fritig, B. and Mosinger, E. 1995. Pathogenesisrelated PR-1 proteins are antifungal. Plant Physiol. 108: 17-27 https://doi.org/10.1104/pp.108.1.17
  46. Nielsen, K. K., Mikkelsen, J. D., Kragh, K. M. and Bojsen, K. 1993. An acidic class III chitinase in sugar beet: Induction by Cercospora beticola, characterization, and expression in transgenic tobacco plants. Mol. Plant-Microbe Interact. 6:495-506 https://doi.org/10.1094/MPMI-6-495
  47. Pasqualini, S., Piccioni, C., Reale, L., Ederli, L., Torre, G. D. and Ferranti, F. 2003. Ozone-induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation. Plant Physiol. 133:1122-1134 https://doi.org/10.1104/pp.103.026591
  48. Punja, Z. K. and Zhang, Y. Y. 1993. Plant chitinases and their roles in resistance to fungal diseases. J. Nematol. 25:526-540
  49. Rauscher, M., Adam, A. L., Wirtz, S., Guggenheim, R., Mendgen, K. and Deising, H. B. 1999. PR-1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. Plant J. 19:625-633 https://doi.org/10.1046/j.1365-313x.1999.00545.x
  50. Sarowar, S., Kim, Y. J., Kim, E. N., Kim, K. D., Hwang, B. K., Islam, R. and Shin, J. S. 2005. Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses Plant Cell Rep. 24:216-224 https://doi.org/10.1007/s00299-005-0928-x
  51. Sela-Buurlage, M. B., Ponstein, A. S., Bres-Vloemans, S. A., Melchers, L. S., Van den Elzen, P. J. M. and Cornelissen, B. J. C. 1993. Only specific tobacco (Nicotiana tabacum) chitinases and $\beta$-1 ,3-glucanases exhibit antifungal activity. Plant Physiol. 101:857-863 https://doi.org/10.1104/pp.101.3.857
  52. Shinozaki, K., Yamaguchi-Shinozaki, K. and Seki, M. 2003. Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6:410-417 https://doi.org/10.1016/S1369-5266(03)00092-X
  53. Sietsma, J. H., Everleigh, D. E. and Haskins, R. H. 1969. Cell wall composition and protoplast formation of some oomycete species. Biochem. Biophys. Acta 184:306-317 https://doi.org/10.1016/0304-4165(69)90033-6
  54. Sutoh, K. and Yamauchi, D. 2003. Two Cis-acting elements necessary and sufficient for giberellin-upregulated proteinase expression in rice seeds. Plant J. 34:635-645 https://doi.org/10.1046/j.1365-313X.2003.01753.x
  55. Takeuchi, Y., Yoshikawa, M., Takeba, G., Kunisuke, T., Shibata, D. and Horino, O. 1990. Molecular cloning and ethylene induction of mRNA encoding a phytoalexin elicitor-releasing factor, $\beta$-1 ,3-endoglucanase, in soybean. Plant Physiol. 93:673-682 https://doi.org/10.1104/pp.93.2.673
  56. van Kan, J. A., Joosten, M. H., Wagemakers, C. A., van den Berg-Velthuis, G. C. and de Wit, P. J. 1992. Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladospoium fulvum. Plant Mol. Biol. 20:513-527 https://doi.org/10.1007/BF00040610
  57. van Loon, L. C. and van Strien, E. A. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55:85-97 https://doi.org/10.1006/pmpp.1999.0213
  58. Wu, H., Michler, C. H., LaRussa, L. and Davis, J. M. 1999. The pine Pschi4 promoter directs wound-induced transcription. Plant Sci. 142:199-207 https://doi.org/10.1016/S0168-9452(99)00009-6
  59. Wubben, J. P., Joosten, M. H. A. J., Van Kan, J. A. L. and De Wit, P. J. G M. 1992. Subcellular localization of plant chitinase and 1,3-$\beta$-glucanases in Cladosporium fulvum (syn. Fulvia fulva)infected tomato leaves. Physiol. Mol. Plant Pathol. 41:23-32 https://doi.org/10.1016/0885-5765(92)90046-X

Cited by

  1. A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants vol.31, pp.4, 2009, https://doi.org/10.1007/s10529-008-9880-5
  2. Molecular mechanism of salicylic acid-induced abiotic stress tolerance in higher plants vol.36, pp.9, 2014, https://doi.org/10.1007/s11738-014-1603-z
  3. Identification and functional expression of the pepper pathogen-induced gene, CAPIP2, involved in disease resistance and drought and salt stress tolerance vol.62, pp.1-2, 2006, https://doi.org/10.1007/s11103-006-9010-5
  4. Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses vol.224, pp.5, 2006, https://doi.org/10.1007/s00425-006-0302-4
  5. The promoter of the pepper pathogen-induced membrane protein gene CaPIMP1 mediates environmental stress responses in plants vol.229, pp.2, 2009, https://doi.org/10.1007/s00425-008-0824-z
  6. A Bacterial–Fungal Metaproteomic Analysis Enlightens an Intriguing Multicomponent Interaction in the Rhizosphere ofLactuca sativa vol.11, pp.4, 2012, https://doi.org/10.1021/pr201204v
  7. Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance vol.61, pp.6, 2006, https://doi.org/10.1007/s11103-006-0057-0
  8. Role of a novel pathogen-induced pepper C3–H–C4 type RING-finger protein gene, CaRFP1, in disease susceptibility and osmotic stress tolerance vol.63, pp.4, 2007, https://doi.org/10.1007/s11103-006-9110-2
  9. Function of a novel GDSL-type pepper lipase gene, CaGLIP1, in disease susceptibility and abiotic stress tolerance vol.227, pp.3, 2008, https://doi.org/10.1007/s00425-007-0637-5
  10. Systemic Acquired Resistance of Pepper to Microbial Pathogens 2011, https://doi.org/10.1111/j.1439-0434.2010.01781.x