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Defence responses of pepper (Capsicum annuum L.) infected with incompatible and compatible strains of Phytophthora capsici

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Abstract

In this study, we investigated the activities of β-1,3-glucanase and peroxidase enzymes in the leaves of pepper cultivar A3 infected with the incompatible strain PC and the compatible strain HX-9 of Phytophthora capsici. The activities of β-1,3-glucanase and peroxidase enzymes substantially increased in the incompatible interactions compared to the compatible interactions. We also analysed the expression patterns of four defence-related genes, including CABPR1, CABGLU, CAPO1 and CaRGA1, in the leaves and roots of pepper inoculated with different strains of P. capsici. All gene expression levels were higher in the leaves than in the roots. Markedly different expression patterns were observed between incompatible and compatible host-pathogen interactions. In the incompatible interactions, the expression levels of CABPR1, CABGLU and CAPO1 genes in leaves increased by a maximum of 17.2-, 13.2- and 20.5-fold at 24, 12 and 12 h, respectively, whereas the CaRGA1 gene expression level increased to a lesser degree, 6.0-fold at 24 h. However, in the compatible interactions, the expression levels of the four defence-related genes increased by a maximum of 11.2-, 8.6-, 7.9- and 2.0-fold at 48, 24, 48 and 72 h, respectively. Compared to the leaves, the expression levels of the four defence-related genes were much lower in the roots. The highest levels of mRNA were those of the CABPR1 gene, which increased 5.1-fold at 24 h in the incompatible and 3.2-fold at 48 h in the compatible interactions. The other three genes exhibited lower expression levels in the incompatible and compatible interactions. These results further confirmed that defence-related genes might be involved in the defence response of pepper to P. capsici attack.

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References

  • Abd EI-Rahman, S. S., Mazen, M. M., Heba, I. M., et al. (2012). Induction of defence related enzymes and phenolic compounds in lupin (Lupinus albus L.) and their effects on host resistance against Fusarium wilt. European Journal of Plant Pathology, 134, 105–116.

    Article  Google Scholar 

  • Ahl Goy, P., Felix, G., Matraux, J. P., et al. (1992). Resistance to disease in the hybrid Nicotiana glutinosa × Nicotiana clebney is associated with high constitutive levels of β-l, 3-glucanase, chitinase, peroxidase and polyphenoloxidase. Physiological and Molecular Plant Pathology, 41, 11–21.

    Article  Google Scholar 

  • Alcantara, T. P., & Bosland, P. W. (1994). An inexpensive disease screening technique for foliar blight of chile pepper seedlings. HortScience, 29, 1182–1183.

    Google Scholar 

  • Baker, B., Zamsryski, P., Staskaweiz, B., & Dinesh-Kumar, S. P. (1997). Signaling in plant-microbe interactions. Science, 272, 726–733.

    Article  Google Scholar 

  • Balasubramanian, V., Vashisht, D., Cletus, J., et al. (2012). Plant β-1, 3-glucanases: their biological functions and transgenic expression against phytopathogenic fungi. Biotechnology Letters, 34, 1983–1990.

    Article  PubMed  CAS  Google Scholar 

  • Barceló, A. R., Gómez Ros, L. V., Gabaldón, C., et al. (2004). Basic peroxidases: the gateway for lignin evolution ? Phytochemistry Reviews, 3, 61–78.

    Article  Google Scholar 

  • Beffa, R., Martin, H. V., & Pilet, P. E. (1990). In vitro oxidation of indoleacetic acid by soluble auxin-oxidases and peroxidases from maize roots. Plant Physiology, 94, 485–491.

    Article  PubMed  CAS  Google Scholar 

  • Boller, T. (1993). Antimicrobial functions of the plant hydrolases chitinase and β-1, 3-glucanase. In B. Fritig & M. Legrand (Eds.), Mechanisms of plant defence responses (pp. 391–400). Dordecht: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Boudet, A. M. (2000). Lignins and lignification: selected issues. Plant Physiology and Biochemistry, 38, 81–96.

    Article  CAS  Google Scholar 

  • Cao, Y., Ding, X., Cai, M., et al. (2007). Expression pattern of a rice disease resistance gene Xa3/Xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function. Genetics, 177, 523–533.

    Article  PubMed  CAS  Google Scholar 

  • Chen, C. W., Yang, Y. W., Lur, H. S., et al. (2006). A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant & Cell Physiology, 47, 1–13.

    Article  Google Scholar 

  • Chmielowska, J., Veloso, J., Gutierrez, J., et al. (2010). Cross-protection of pepper plants stressed by copper against a vascular pathogen is accompanied by the induction of a defence response. Plant Science, 178, 176–182.

    Article  CAS  Google Scholar 

  • Conrath, U., Thulke, O., Katz, V., et al. (2001). Priming as a mechanism in induced systemic resistance of plants. European Journal of Plant Pathology, 107, 113–119.

    Article  CAS  Google Scholar 

  • Conrath, U., Pieterse, M. J., & Mauch-Mani, B. (2002). Priming in plant-pathogen interactions. Trends in Plant Science, 7(5), 21–26.

    Article  Google Scholar 

  • Do, H. M., Hong, J. K., Jung, H. W., et al. (2003). Expression of peroxidase-like genes, H2O2 production, and peroxidase activity during the hypersensitive response to Xanthomonas campestris pv. vesicatoria in Capsicum annuum. Molecular Plant-Microbe Interactactions, 16, 196–205.

    Article  CAS  Google Scholar 

  • Dong, X., Mindrinos, M., Davis, K. R., & Ausubel, F. M. (1991). Induction of Arabidopsis defence genes by virulent and avirulent pseudomonas syringae strain and by a cloned avirulence gene. The Plant Cell, 3, 61–72.

    PubMed  CAS  Google Scholar 

  • Egea, C., Alcázar, M. D., & Candela, M. E. (1996). Capsidiol: its role in the resistance of Capsicum annuum to Phytophthora capsici. Physiologia Plantarum, 98, 737–742.

    Article  CAS  Google Scholar 

  • Egea, C., Dickinson, M. J., Candela, M., & Candela, M. E. (1999). β-1, 3-glucanase isozymes and genes in resistant and susceptible pepper (Capsicum annuum) cultivars infected with Phytophthora capsici. Physiologia Plantarum, 107, 312–318.

    Article  CAS  Google Scholar 

  • Egea, C., Ahmed, A. S., Candela, M., et al. (2001). Elicitation of peroxidase activity and lignin biosynthesis in pepper suspension cells by Phytophthora capsici. Journal of Plant Physiology, 158, 151–158.

    Article  CAS  Google Scholar 

  • Esra, K., Üstüna, A. S., \( {\mathop {\text{I}}\limits^. } \)slekb, C., et al. (2011). Defense responses in leaves of resistant and susceptible pepper (Capsicum annuum L.) cultivars infected with different inoculum concentrations of Phytophthora capsici Leon. Scientia Horticulturae, 128, 434–442.

  • Eyal, Y., Sagge, O., & Fluhr, R. (1992). Dark induced accumulation of a basic PR-1 transcript and a light requirement for its induction by ethylene. Plant Molecular Biology, 19(4), 589–599.

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Pavia, S. (1997). Host-Pathogen interactions in the root rot resistant Phytophthora capsici /Capsicum annuum resistant CM-334 pathosystem. Ph. D. Dissertation. New Mexico State University.

  • Fung, R. W. M., Wang, C. Y., Smith, D. L. et al. (2004). MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Science, 166, 711–719.

  • Gayoso, C., Pomar, F., Merino, F., et al. (2004). Oxidative metabolism and phenolic compounds in Capsicum annuum L. var. annuum infected by Phytophthora capsici Leon. Sci Hortic, 102, 1–13.

    Article  CAS  Google Scholar 

  • Gayoso, C., Martinez de ilarduya, O., Pomar, F., et al. (2007). Assessment of real-time PCR as a method for determining the presence of Verticillium dahliae in different Solanaceae cultivars. European Journal of Plant Pathology, 118, 199–209.

    Google Scholar 

  • Gheysen, G., & Fenoll, C. (2002). Gene expression in nematode feeding sites. Annual Review of Phytopathology, 40, 191–219.

    Article  PubMed  CAS  Google Scholar 

  • Gholizadeh, A., Kumar, M., Balasubrahmanyam, A., Sharma, S., et al. (2004). Antioxidant activity of antiviral proteins from Celosia cristata. J Plant Biochem Biotechnol, 13, 13–18.

    Article  CAS  Google Scholar 

  • Govindappa, M., Lokesh, S., Rai, V. R., et al. (2010). Induction of systemic resistance and management of safflower Macrophomina phaseolina root rot disease by biocontrol agents. Arch Phytopathol Plant Protect, 43, 26–40. doi:10.1080/03235400701652227.

    Article  CAS  Google Scholar 

  • Graham, M. Y., & Graham, T. L. (1991). Rapid accutnulation of anionic peroxidases and phenolic polymers in soybean cotyledon tissues following treatment with Phytophthiira megasperma f. sp. ghcinea wall glucan. Plant Physiology, 97, 1445–1455.

    Article  PubMed  CAS  Google Scholar 

  • Hong, J. K., & Hwang, B. K. (2005). Induction of enhanced disease resistance and oxidative stress tolerance by overexpression of pepper basic PR-1 gene in Arabidopsis. Physiologia Plantarum, 124, 267–277.

    Article  CAS  Google Scholar 

  • Huang, J. S., & Knopp, J. A. (1998). Involvement of nitric oxide in Ralstonia solanacearum-induced hypersensitive reaction in tobacco. In P. Prior, C. Allen, & J. Elphinstone (Eds.), Bacterial wilt disease: Molecular and ecological aspects (pp. 218–224). Berlin: INRA and Springer Editions.

    Chapter  Google Scholar 

  • Huang, Z., Yeakley, J. M., Garcia, E. W., et al. (2005). Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiology, 137, 1147–1159.

    Article  PubMed  CAS  Google Scholar 

  • Jebakumar, R. S., Anandaraj, M., & Sarma, Y. R. (2001). Induction of PR-proteins and defence related enzymes in black pepper due to inoculation with phytophthora capsici. Indian Phytopathol, 54, 23–28.

    CAS  Google Scholar 

  • Kauffmann, S., Legrand, M., Geoffroy, P., & Fritig, B. (1987). Biological function of pathogenesis-related proteins: four PR proteins of tobacco have β-1, 3-glucanase activity. EMBO Journal, 6, 3209–3212.

    PubMed  CAS  Google Scholar 

  • Kim, Y. J., & Hwang, B. K. (1994). Differential accumulation of β-1-3-glucanase and chitinase isoforms in pepper stems infected by compatible and incompatible isolates of Phytophthoracapsici. Physiological and Molecular Plant Pathology, 45, 195–209.

    Article  CAS  Google Scholar 

  • Kim, H. J., Nahm, S. H., Lee, H. R., et al. (2008). BAC-derived markers converted from RFLP linked to Phytophthora capsici resistance in pepper (Capsicum annuum L.). Theoretical and Applied Genetics, 118, 15–27.

    Article  PubMed  CAS  Google Scholar 

  • Koç, E., & Üstün, A. S. (2012). Influence of Phytophthora capsici L. inoculation on disease severity, necrosis length, peroxidase and catalase activity, and phenolic content of resistant and susceptible pepper (Capsicum annuum L.) plants. Turkish Journal of Biology, 36, 357–371.

    Google Scholar 

  • Kook Hwang, B., Sunwoo, J. Y., Kim, B. S., et al. (1997). Accumulation of β-1, 3-glucanase and chitinase isoforms, and salicylic acid in the DL-b-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. Physiological and Molecular Plant Pathology, 51, 305–322.

    Article  Google Scholar 

  • Kramer, L. C., Choudoir, M. J., Wielgus, S. M., et al. (2009). Correlation between transcript abundance of the RB gene and the level of the RB-mediated late blight resistance in potato. Mol Plant-Microbe Interact, 22, 447–455.

    Article  PubMed  CAS  Google Scholar 

  • Lamour, K. H., Stam, R., Jupe, J., et al. (2012). The oomycete broad-host-range pathogen Phytophthora capsici. Molecular Plant Pathology, 13, 329–337.

    Article  PubMed  Google Scholar 

  • Lee, Y. K., Hippe-Sanwald, S., Jung, H. W., et al. (2000). In situ localization of chitinase Mrna and protein in compatible and incompatible interactions of pepper stems with Phytophthora capsici. Physiological and Molecular Plant Pathology, 57, 111–121.

    Article  CAS  Google Scholar 

  • Marate, R., Guan, Z., Anandalakshmi, R., et al. (2004). Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Molecular Biology, 55, 501–520.

    Article  Google Scholar 

  • Mauch, F., Mauch-Mani, B., & Boller, T. (1988). Antifungal hydrolases in pea tissue.II. Inhibition of fungal growth by combinations of chitinase and β-1, 3-glucanase. Plant Physiology, 88, 936–942.

    Article  PubMed  CAS  Google Scholar 

  • Melillo, M. T., Leonetti, P., Bongiovanni, M., et al. (2006). Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root-knot nematode interactions. New Phytologist, 170, 501–512.

    Article  PubMed  CAS  Google Scholar 

  • Melo, G. A., Shimzu, M. M., & Mazzafera, P. (2006). Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry, 67, 277–285.

    Article  PubMed  CAS  Google Scholar 

  • Mérillon, J.M., Ramawat, K.G., et al. (2012). Pathogenesis Related Proteins in Plant Defence Response. Plant Defence: Biological Control, Springer Netherlands. 12, 379–403.

  • Mithöfer, A., Schulze, B., & Boland, W. (2004). Biotic and heavy metal stress response in plants: evidence for common signal. FEBS Letters, 566, 1–5.

    Article  PubMed  Google Scholar 

  • Nelson, N. (1994). A photometric adaption of the Somogyi method for the degradation of glucose. Journal of Biological Chemistry, 153, 375–380.

    Google Scholar 

  • Núñez-Pastrana, R., Arcos-Ortega, G. F., Souza-Perera, R. A., et al. (2011). Ethylene, but not salicylic acid or methyl jasmonate, induces a resistance response against Phytophthora capsici in Habanero pepper. European Journal of Plant Pathology, 131(4), 669–683.

    Article  Google Scholar 

  • Oelke, L. M., Bosland, P. W., & Steiner, R. (2003). Differentiation of race specific resistance to Phytophthora root rot and foliar blight in Capsicum annuum. Journal of the American Society for Horticultural Science, 128, 213–218.

    Google Scholar 

  • Ou, L. J., Dai, X., Zhang, Z. Q., et al. (2011). Responses of pepper to waterlogging stress. Photosynthetica, 49, 339–345.

    Article  CAS  Google Scholar 

  • Passardi, F., Cosio, C., Penel, C., et al. (2005). Peroxidases have more functions than army knife. Plant Cell Reports, 24, 255–265.

    Article  PubMed  CAS  Google Scholar 

  • Quirin, E. A., Ogundiwin, E. A., Prince, J. P., et al. (2005). Development of sequence characterized amplified region (SCAR) primers for the detection of Phyto.5.2, a major QTL for resistance to Phytophthora capsici Leon. in pepper. Theoretical and Applied Genetics, 110, 605–612.

    Article  PubMed  CAS  Google Scholar 

  • Requena, M. E., Egea-Gilabert, C., & Candela, M. E. (2005). Nitric oxide generation during the interaction with Phytophtora capsici of two Capsicum annuum varieties showing different degrees of sensitivity. Physiologia Plantarum, 124, 50–60.

    Article  CAS  Google Scholar 

  • Ristaino, J. B., & Johnston, S. A. (1999). Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease, 83, 1080–1089.

    Article  Google Scholar 

  • Rivera, M. E., Codina, J. C., Olea, F., et al. (2002). Differential expression of β-1, 3-glucanase in susceptible and resistant melon cultivars in response to infection by Sphaerotheca fusca. Physiological and Molecular Plant Pathology, 61, 257–265.

    Article  Google Scholar 

  • Saikia, R., Singh, B. P., Kumar, R., & Arora, D. K. (2005). Detection of pathogenesis related proteins chitinase and β-1,3 glucanase in induced chickpea. Current Science, 89, 659–663.

    CAS  Google Scholar 

  • Sarowar, S., Kim, Y. J., Kim, E. N., et al. (2005). Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Reports, 24, 216–224.

    Article  PubMed  CAS  Google Scholar 

  • Sarowar, S., Kim, Y. J., Kim, E. N., Kim, K. D., et al. (2006). Constitutive expression of two pathogenesis-related genes in tomato plants enhanced resistance to oomycete pathogen Phytophthora capsici. Plant Cell, Tissue Organ Culture, 86, 7–14.

    Article  CAS  Google Scholar 

  • Silvar, C., Merino, F., & Díaz, J. (2008). Differential activation of defence-related genes in different pepper cultivars infected with phytophthora capsici. Journal of Plant Physiology, 165, 1120–1124.

    Article  PubMed  CAS  Google Scholar 

  • Singh, R., Adholeya, A., & Mukerji, K. G. (2000). Mycorrhiza in control of soil borne pathogens. In K. G. Mukerji, B. P. Chamola, & J. Singh (Eds.), Mycorrhizal biology (pp. 173–196). New York: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Taheri, P. & Tarighi, S. (2012). The Role of Pathogenesis-Related Proteins in the Tomato-Rhizoctonia solani Interaction. Journal of Botany, article ID 137037, 6 pages.

  • Van Loon, L. C., & Van Strien, E. A. (1999). The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type protein. Physiology Molecular Plant Pathology, 55, 85–97.

    Article  Google Scholar 

  • Van Loon, L. C., Rep, M., & Pieterse, C. M. J. (2006). Significance of inducible defence-related proteins in infected plants. Annual Review of Phytopathology, 44, 135–162.

    Article  PubMed  Google Scholar 

  • Vercauteren, I., Van Der Schueren, E., Van Montagu, M., et al. (2001). Arabidopsis thaliana genes expressed in the early compatible interaction with root-knot nematodes. Molecular Plant-Microbe Interactactions, 14, 288–299.

    Article  CAS  Google Scholar 

  • Wan, H. J., Yuan, W., Ruan, M. Y., et al. (2011). Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L.). Biochemical and Biophysical Research Communications, 416, 24–30.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Z.-X., Yamanouchi, U., Katayose, Y., et al. (2001). Expression of the Pib rice-blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Molecular Biology, 47, 653–661.

    Article  PubMed  CAS  Google Scholar 

  • Williamson, V. M., & Hussey, R. S. (1996). Nematode pathogenesis and resistance in plants. The Plant Cell, 8, 1735–1745.

    PubMed  CAS  Google Scholar 

  • Yang, C., Guo, R., Jie, F., et al. (2007). Spatial analysis of Arabidopsis thaliana gene expression in response to Turnip mosaic virus infection. Molecular Plant-Microbe Interactactions, 20, 358–370.

    Article  CAS  Google Scholar 

  • Ye, X. S., Pan, S. Q., & Kuc, J. (1990). Activity, isoenzyme pattern and cellular localization of peroxidase as related to systemic resistance of tobaceo to blue mold (Peronospora tabacina) and to tobacco mosaic virus. Phytopathology, 80, 1295–1299.

    Article  CAS  Google Scholar 

  • Yeom, S. I., Baek, H. K., Oh, S. K., et al. (2011). Use of a secretion trap screen in pepper following Phytophthora capsici infection reveals novel functions of secreted plant proteins in modulating cell death. Molecular Plant-Microbe Interactactions, 24, 671–684.

    Article  CAS  Google Scholar 

  • Zhang, Y. L., Gong, Z. H., Li, D. W., et al. (2009). Identification of Phytophthora capsici in Shaanxi Province and screening of the Fungicides against Phytophthora blight of pepper. Acta Agriculturae Boreali-occidentalis Sinica, 5, 336–340.

    Google Scholar 

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Acknowledgments

This research was supported by the National Natural Science Foundation of China (No. 31272163), “The Twelfth Five-Year” Plan of National Science and Technology in Rural Areas (No.2011BAD12B03) and the Shaanxi Provincial Science and Technology Coordinating Innovative Engineering Project (2012KTCL02-09). Language help was provided by American Journal Experts (AJE).

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Wang, JE., Li, DW., Zhang, YL. et al. Defence responses of pepper (Capsicum annuum L.) infected with incompatible and compatible strains of Phytophthora capsici . Eur J Plant Pathol 136, 625–638 (2013). https://doi.org/10.1007/s10658-013-0193-8

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