A novel peroxidase CanPOD gene of pepper is involved in defense responses to Phytophtora capsici infection as well as abiotic stress tolerance

International Journal of Molecular Sciences

Volumn 14, Issue 2, 2013, Pages 3158-3177

  Wang, Jun E ^a   Liu, Ke Ke ^b   Li, Da Wei ^a   Zhang, Ying Li ^a   Zhao, Qian ^a   He, Yu Mei ^a   Gong, Zhen Hui ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b HENAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Abiotic stress; Pepper; Peroxidase; Phytophtora capsici; Virus induce gene silencing (VIGS)

Indexed keywords

PEROXIDASE;

3' UNTRANSLATED REGION; ABIOTIC STRESS; APOPTOSIS; ARACHIS; ARTICLE; BIOTIC STRESS; CANPOD GENE; CATHARANTHUS ROSEUS; CULTIVAR; DETOXIFICATION; ENDOPLASMIC RETICULUM; ENZYME ASSAY; GENE EXPRESSION; GENE SILENCING; GOSSYPIUM HIRSUTUM; GRAPE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PEPPER; PHYLOGENY; PHYTOPHTORA CAPSICI INFECTION; PLANT DISEASE; PLANT GENE; PLANT GENETICS; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; RUBIA CORDIFOLIA; SEQUENCE ANALYSIS; SOYBEAN; SWEET POTATO; TOBACCO; UPREGULATION; VITIS;

EID: 84875085465     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14023158     Document Type: Article

References (54)

1. Lamour, K.H.; Stam, R.; Jupe, J.; Huitema, E. The oomycete broad-host-range pathogen Phytophthora capsici. Mol. Plant Pathol. 2012, 13, 329-337.
2. Jones, J.D.G.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323-329.
3. Sarowar, S.; Kim, E.N.; Kim, Y.J.; Ok, K.D.; Kim, K.D.; Hwang, B.K.; Shin, J.S. Overexpression of a pepper ascorbate peroxidase-like 1 gene in tobacco plants enhances tolerance to oxidative stress and pathogens. Plant Sci. 2005, 1, 55-63.
4. Dang, F.F.; Wang, Y.N.; Yu, L.; Eulgem, T.; Lai, Y.; Liu, Z.Q.; Wang, X.; Qiu, A.L.; Zhang, T.X.; Lin, J.; et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ. 2012, doi:10.1111/pce.12011.
5. Passardi, F.; Penel, C.; Dunand, C. Performing the paradoxical: How plant peroxidases modify the cell wall. Trends Plant Sci. 2004, 11, 534-540.
6. Tognolli, M.; Penel, C.; Greppin, H.; Simon, P. Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 2002, 288, 129-138.
7. Welinder, K.G.; Justesen, A.F.; Inger, V.H.; Kjærsgård, I.V.H.; Jensen, R.B.; Rasmussen, S.K.; Jespersen, H.M.; Duroux, L. Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur. J. Biochem. 2002, 269, 6063-6381.
8. Hiraga, S.; Sasaki, K.; Ito, H.; Ohashi, Y.; Matsui, H. A large family of class III plant peroxidases. Plant Cell Physiol. 2001, 42, 462-468.
9. Valerio, L.; Meyer, M.D.; Penel, C.; Dunand, C. Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry 2004, 65, 1331-1342.
10. Kim, S.S.; Choi, S.Y.; Park, J.H.; Lee, D.J. Regulation of the activity of Korean radish cationic peroxidase promoter during dedifferentiation and differentiation. Plant Physiol. Biochem. 2004, 42, 763-772.
11. Bae, H.; Roberts, D.P.; Lim, H.S.; Strem, M.D.; Park, S.C.; Ryu, C.M.; Melnick, R.L.; Bailey, B.A. Endophytic trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol. Plant-Microbe Interact. 2011, 24, 336-351.
12. Passardi, F.; Cosio, C.; Penel, C.; Dunand, C. Peroxidases have more functions than a Swiss army knife. Plant Cell Rep. 2005, 24, 255-265.
13. Veloso, J.; Díaz, J. Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici, and induces the expression of defence genes. Plant Pathol. 2012, 61, 281-288.
14. Choi, H.W.; Kim, Y.J.; Lee, S.C.; Hong, J.K.; Hwang, B.K. Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol. 2007, 145, 890-904.
15. Bae, E.K.; Lee, H.; Lee, J.S.; Noh, E.W.; Jo, J. Molecular cloning of a peroxidase gene from poplar and its expression in response to stress. Tree Physiol. 2006, 26, 1405-1412.
16. Hiraga, S.; Yamamoto, K. Diverse expression profiles of 21 rice peroxidase genes. FEBS Lett. 2000, 471, 245-250.
17. Ito, H.; Hiraga, S.; Tsugawa, H.; Matsui, H.; Honma, M.; Otsuki, Y.; Murakami, T.; Ohashi, Y. Xylem-specific expression of wound-inducible rice peroxidase genes in transgenic plants. Plant Sci. 2000, 155, 85-100.
18. Kim, K.Y.; Kwon, H.K.; Kwon, S.Y.; Lee, H.S.; Hur, Y.; Bang, J.W.; Choi, K.S.; Kwak, S.S. Differential expression of four sweet potato peroxidase genes in response to abscisic acid and ethephon. Phytochemistry 2000, 54, 19-22.
19. Yoshida, K.; Kaothien, P.; Matsui, T.; Kawaoka, A.; Shinmyo, A. Molecular biology and application of plant Peroxidase genes. Appl. Microbiol. Biot. 2003, 60, 665-670.
20. Park, S.Y.; Ryu, S.H.; Kwon, S.Y.; Lee, H.S.; Kim, J.G.; Kwak, S.S. Differential expression of six novel peroxidase cDNAs from cell cultures of sweetpotato in response to stress. Mol. Genet. Genomics 2003, 269, 542-552.
21. Matin, M.N.; Pandeya, D.; Baek, K.H.; Lee, D.S.; Lee, J.H.; Kang, H.; Kang, S.G. Phenotypic and genotypic analysis of rice lesion mimic mutants. Plant Pathology J. 2010, 26, 159-169.
22. Sang, M.K.; Kim, J.G.; Kim, K.D. Biocontrol activity and induction of systemic resistance in pepper by compost water extracts against Phytophthora capsici. Phytopathology 2010, 100, 774-783.
23. Sang, M.K.; Kim, K.D. Biocontrol activity and primed systemic resistance by compost water extracts against anthracnoses of pepper and cucumber. Phytopathology 2011, 101, 732-740.
24. Way, H.M.; Kazan, K.; Goulter, K.C.; Birch, R.G.; Manners, J.M. Expression of the Shpx2 peroxidase gene of Stylosanthes humilis in transgenic tobacco leads to enhanced resistance to Phytophthora parasitica pv. nicotianae and Cercospora nicotianae. Mol. Plant Pathol. 2000, 1, 223-232.
25. Liu, G.; Sheng, X.; Greenshields, D.L.; Ogieglo, A.; Kaminskyj, S.; Selvaraj, G.; Wei, Y. Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Mol. Plant-Microbe Interact. 2005, 18, 730-741.
26. Kim, Y.H.; Kim, C.Y.; Song, W.K.; Park, D.S.; Kwon, S.Y.; Lee, H.S.; Bang, J.B.; Kwak, S.S. Overexpression of sweetpotato swpa4 peroxidase results in increased hydrogen peroxide production and enhances stress tolerance in tobacco. Planta 2008, 227, 867-881.
27. Choi, H.; Hwang, B. The pepper extracellular peroxidase CaPO2 is required for salt, drought and oxidative stress tolerance as well as resistance to fungal pathogens. Planta 2012, 235, 1369-1382.
28. 2 production, and peroxidase activity during the hypersensitive response to Xanthomonas campestris pv. vesicatoria in Capsicum annuum. Mol. Plant-Microbe Interact. 2003, 16, 196-205.
29. Chmielowska, J.; Veloso, J.; Gutierrez, J.; Silvar, C.; Diaz, J. Cross-protection of pepper plants stressed by copper against a vascular pathogen is accompanied by the induction of a defence response. Plant Sci. 2010, 178, 176-182.
30. Blokhina, O.; Virolainen, E.; Fagerstedt, K.V. Antioxidants, oxidative damage and oxygen deprivation stress: A review. Ann. Bot-London 2003, 91, 179-194.
31. Baltruschat, H.; Fodor, J.; Harrach, B.D.; Niemczyk, E.; Barna, B.; Gullner, G.; Janeczko, A.; Kogel, K.H.; Schäfer, P.; Schwarczinger, I.; et al. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 2008, 180, 501-510.
32. Murata, N.; Ishizaki, N.O.; Higashi, S.; Hayashi, H.; Tasaka, Y.; Nishida, I. Genetically engineered alteration in the chilling sensitivity of plants. Nature 1992, 356, 710-713.
33. Sreenivasulu, N.; Grimm, B.; Wobus, U.; Weschke, W. Differential response of antioxidant compounds to salinity stress in salt tolerant and salt sensitive seedlings of foxtail millet (Setaria italica). Physiol Plantarum 2000, 109, 435-442.
34. Menezes-Benavente, L.; Teixeira, F.K.; Kamei, C.L.A.; Pinheiro, M.M. Salt stress induces altered expression of genes encoding antioxidant enzymes in seedlings of a Brazilian indica rice (Oryza sativa L.). Plant Sci. 2004, 166, 323-331.
35. Koussevitzky, S.; Suzuki, N.; Huntington, S.; Armijo, L.; Sha, W.; Cortes, D.; Shulaev, V.; Mittler, R. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 2008, 283, 34197-34203.
36. Donahue, J.L.; Okpodu, C.M.; Cramer, C.L.; Grabau, E.A.; Alscher, R.G. Responses of antioxidants to paraquat in pea leaves. Plant Physiol. 1997, 113, 249-257.
37. Cazale, A.C.; Rouet-Mayer, M.A.; Barbier-Brygoo, H.; Mathieu, Y.; Lauriere, C. Oxidative burst and hypoosmotic stress in tobacco cell suspension. Plant Physiol. 1998, 116, 659-669.
38. An, S.H.; Sohn, K.H.; Choi, H.W.; Hwang, I.S.; Lee, S.C.; Hwang, B.K. Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 2008, 228, 61-78.
39. Lee, S.C.; Hwang, B.K. Functional roles of the pepper antimi-crobial protein gene, CaAMP1, in abscisic acid signaling and salt and drought tolerance in Arabidopsis. Planta 2009, 229, 383-391.
40. Choi, D.S.; Hwang, B.K. Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 2011, 23, 823-842.
41. Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005, 43, 205-227.
42. Mur, L.A.J.; Kenton, P.; Atzorn, R.; Miersch, O.; Wasternack, C. The outcomes of concentrationspecific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 2006, 140, 249-262.
43. Liu, Y.; Schiff, M.; Dinesh-Kumar, S.P. Virus-induced gene silencing in tomato. Plant J. 2002, 31, 777-786.
44. Chung, E.; Seong, E.; Kim, Y.C.; Chung, E.J.; Oh, S.K.; Lee, S.; Park, J.M.; Joung, Y.H.; Choi, D. A method of high frequency virus-induced gene silencing in chili pepper (Capsicum annuum L. cv. Bukang). Mol. Cells 2004, 17, 377-380.
45. An, S.H.; Choi, H.W.; Hwang, I.S.; Hong, J.K.; Hwang, B.K. A novel pepper membrane-located receptor-like protein gene CaMRP1 is required for disease susceptibility, methyl jasmonate insensitivity and salt tolerance. Plant Mol. Biol. 2008, 67, 519-533.
46. Hwang, I.S.; Hwang, B.K. The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol. 2010, 152, 948-967.
47. Kim, H.J.; Nahm, S.H.; Lee, H.R.; Yoon, G.B.; Kim, K.T.; Kang, B.C.; Choi, D.; Kweon, O.Y.; Cho, M.C.; Kwon, J.K. BAC-derived markers converted from RFLP linked to Phytophthora capsici resistance in pepper (Capsicum annuum L.). Theor. Appl. Genet. 2008, 118, 15-27.
48. Bioinformatics Tool. Available online: http:/blast.ncbi.nlm.nih.gov/ (accessed on 15 December 2012).
49. Bioinformatics Tool. Available online: http://www.ncbi.nlm.nih.gov/stucture/cdd.shtml (accessed on 15 December 2012).
50. Wan, H.J.; Yuan, W.; Ruan, M.; Ye, Q.; Wang, R.; Li, Z.; Zhou, G.; Yao, Z.; Zhao, J.; Liu, S.; Yang, Y. Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L.). Biochem. Biophy. Res. Co. 2011, 416, 24-30.
51. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T) Method. Methods 2001, 25, 402-408.
52. Liu, Y.; Schiff, M.; Marathe, R.; Dinesh-Kumar, S.P. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 2002, 30, 415-429.
53. Cunningham, F.X.; Gantt, E. Genes and enzymes of cartotenoid biosynthesis in plants. Plant Mol. Biol. 1998, 49, 557-583.
54. Beffa, R.; Martin, H.V.; Pilet, P.E. In vitro oxidation of indoleacetic acid by soluble auxin-oxidasesand peroxidases from maize roots. Plant Physiol. 1990, 94, 485-491.