Plant and Soil

, Volume 338, Issue 1–2, pp 399–409 | Cite as

Alterations in peroxidase activity and phenylpropanoid metabolism induced by Nacobbus aberrans Thorne and Allen, 1944 in chilli (Capsicum annuum L.) CM334 resistant to Phytophthora capsici Leo.

  • Noé López-Martínez
  • Ma. Teresa Colinas-León
  • Cecilia B. Peña-Valdivia
  • Yolanda Salinas-Moreno
  • Patricia Fuentes-Montiel
  • Magdalena Biesaga
  • Emma Zavaleta-Mejía
Regular Article

Abstract

Chilli CM334 (Capsicum annuum L.) is resistant to Phytophthora capsici Leonian (Pc), but Nacobbus aberrans Thorne and Allen, 1944 (Na) broke down its resistance in plants previously infected by the nematode. Peroxidase (POD) and L-phenylalanine ammonia-lyase (PAL) activity, total soluble phenols (TSP) and chlorogenic acid concentration in CM334 plants inoculated with either or both pathogens (Na-Pc) were compared; also, the toxic effect of some phenolic acids on Na was tested in vitro. The highest POD activity (5.3 μM tetraguaiacol mg−1 protein min−1) was registered in plants inoculated only with Pc, while those inoculated only with Na showed the lowest (3.3 μM) (P ≤ 0.05). PAL activity was 39.9 nM trans-cinnamic acid μg−1 protein min−1 in plants inoculated only with Pc, and it was lower (19.3 nM) and similar in non-inoculated plants or those with Na and with Na-Pc (P ≤ 0.05). Usually, plants inoculated with Pc alone had higher contents of TSP (P ≤ 0.05) (1.9 mg tannic acid g−1 dry matter) and plants inoculated with Na or Na-Pc had lower levels (0.8 and 0.9 mg) than those non-inoculated (1.3 mg). CM334 plants inoculated with Na showed a significant reduction (10–37% and 12–17%, in roots and leaves) in the concentration of chlorogenic acid as compared to the non-inoculated. Vanillic, trans-cinnamic, p-coumaric and syringic acids had greater nematicidal effects (P ≤ 0.05) than chlorogenic acid in vitro. Apparently Na modified the defence responses in CM334 plants as POD and PAL activities and TSP and chlorogenic acid concentrations were reduced.

Keywords

Chlorogenic acid PAL Peroxidase Plant defences Resistance breaking Root-knot nematodes 

Notes

Acknowledgements

We would like to thank Dr. S. Fernández-Pavia for supplying the isolate 6143 of P. capsici; Dr. O. Gómez-Rodríguez for helping to establish the plant assays; and Dr Miguel Ángel Martínez-Tellez (CIAD-México), Technician Cecilio Bautista (UACh-México) and Dr Juan Pablo Fernández-Trujillo (UPCT-Spain) for their advice on enzymatic analysis. We also appreciate the critical review of this paper by Dr Ken Evans and Cristina Cárdenas-Rudderow. We thank CONACYT for the scholarship provided to the first author and the financial support of the Research Project 46331-Z.

References

  1. Alcantara TP, Bosland PW (1994) An inexpensive disease screening technique for foliar blight of chile pepper seedlings. HortScience 29:1182–1183Google Scholar
  2. Anterola AM, Lewis NG (2002) Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry 61:221–294CrossRefPubMedGoogle Scholar
  3. Baldridge GN, O’Neill N, Samac D (1998) Alfalfa (Medicago sativa L.) resistance to the root-lesion nematode, Pratylenchus penetrans: defence-response gene mRNA and isoflavonoid phytoalexin levels in roots. Plant Mol Bio 38:999–1010CrossRefGoogle Scholar
  4. Benveniste P (2004) Biosynthesis and accumulation of sterols. Annu Rev Plant Biol 55:429–457CrossRefPubMedGoogle Scholar
  5. Boudet AM (2000) Lignins and lignification: selected issues. Plant Physiol Biochem 38:81–96CrossRefGoogle Scholar
  6. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  7. Cahill DM, McComb JA (1992) A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi. Physiol Mol Plant Pathol 40:315–332CrossRefGoogle Scholar
  8. Candela ME, Alcázar MD, Espin A, Egea C, Almela L (1995) Soluble phenolic acids in Capsicum annuum stems infected with Phytophthora capsici. Plant Pathol 44:116–123CrossRefGoogle Scholar
  9. Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775CrossRefGoogle Scholar
  10. Chitwood DJ, Lusby WR (1991) Metabolism of plant sterols by nematodes. Lipids 26:619–627CrossRefPubMedGoogle Scholar
  11. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L (2002) The phenylpropanoid pathway and plant defence: a genomics perspective. Mol Plant Pathol 3:371–390CrossRefPubMedGoogle Scholar
  12. Edens RM, Anand SC, Bolla RI (1995) Enzymes of the phenylpropanoid pathway in soybean infected with Meloidogyne incognita or Heterodera glycines. J Nematol 27:292–303PubMedGoogle Scholar
  13. Egea C, Sid AA, Candela ME (2001) Elicitation of peroxidase activity and lignin biosynthesis in pepper suspension cells by Phytophthora capsici. J Plant Physiol 158:151–158CrossRefGoogle Scholar
  14. Elliot ChG (1983) Physiology of sexual reproduction in Phytophthora. In: Erwin DC, Bartniki-Garcia S, Tsao PH (eds) Phytophthora. Its biology, taxonomy, ecology and pathology. The American Phytopathological Society, St. Paul, Minnesota, pp 71–80Google Scholar
  15. Fernández-Pavia S (1997) Host-Pathogen interactions in the root rot resistant Phytophthora capsici/Capsicum annuum resistant CM-334 pathosystem. Ph.D. Dissertation, University of New Mexico StateGoogle Scholar
  16. Gayoso C, Pomar F, Merino F, Bernal MA (2004) Oxidative metabolism and phenolic compounds in Capsicum annuum L. var. annuum infected by Phytophthora capsici Leon. Sci Hort 102:1–13CrossRefGoogle Scholar
  17. Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Ann Rev Phytopathol 40:1991–219Google Scholar
  18. Goddijn OJM, Lindsey K, Van der Lee FM, Klap LC, Sijmons PC (1993) Differential gene expression in nematode-induced feeding structures of transgenic plants harboring promoter-gus A fusion constructs. Plant J 4:863–873CrossRefPubMedGoogle Scholar
  19. Godínez-Vidal D, Rocha-Sosa M, Sepulveda García EB, Lara-Reyna J, Rojas-Martínez R, Zavaleta-Mejía E (2008) Phenylalanine ammonia lyase activity in chilli cm-334 infected by Phytophthora capsici and Nacobbus aberrans. Eur J Plant Pathol 120:299–303CrossRefGoogle Scholar
  20. Gómez-Vásquez R, Day R, Buschmann H, Randles S, Beeching JR, Cooper RM (2004) Phenylpropanoids, phenylalanine ammonia lyase and peroxidases in elicitor-challenged cassava (Manihot esculenta) suspension cells and leaves. Ann Bot 94:87–97CrossRefPubMedGoogle Scholar
  21. Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol. Plant Mol Bio 40:347–369CrossRefGoogle Scholar
  22. Hernández AAM, Zavaleta-Mejía E, Carrillo G (1992) Efecto de Nacobbus aberrans (Thorne y Allen, 1944) en la infección de Phytophthora capsici Leo. en chile. Rev Mex Fitopatol 10:166–174Google Scholar
  23. Hills T, Brockie PJ, Maricq AV (2004) Dopamine and glutamate control area-restricted search behaviour in Caenorhabditis elegant. J Neurosci 24:1217–1225CrossRefPubMedGoogle Scholar
  24. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468CrossRefPubMedGoogle Scholar
  25. Huang CL, Rhode RA (1973) Phenol accumulation related to resistance in tomato to infection by root-knot and lesion nematodes. J Nematol 5:253–258Google Scholar
  26. Mahajan R, Prabhsharan S, Krishan LB (1985) Nematicidal activity of some phenolic compounds against Meloidogyne incognita. Rev Nematol 8:161–164Google Scholar
  27. Mahajan R, Kaur DJ, Bajaj KL (1992) Nematicidal activity of phenolic compounds against Meloidogyne incognita. Nematol Medit 20:217–219Google Scholar
  28. Maheshwari TU, Sharma SB, Reddy DDR, Hawara MP (1995) Co-infection of wilt resistant chickpeas by Fusarium oxysporum f. sp. ciceri and Meloidogyne javanica. J Nematol 27:649–653PubMedGoogle Scholar
  29. Manzanilla-López RH, Costilla MA, Doucet M, Franco J, Inserra RN, Lehman PS, Del Prado-Vera IC, Souza RM, Evans K (2002) The genus Nacobbus Thorne and Allen, 1994 (Nematoda: Pratylenchidae): Systematics, biology and management. Nematropica 32:149–227Google Scholar
  30. Martinez-Tellez MA, Lafuente MT (1997) Effect of high temperature conditioning on ethylene, phenylalanine ammonia-lyase, peroxidase and polyphenol oxidase in flavedo of chilled “Fortune” mandarin fruit. J Plant Physiol 150:674–678Google Scholar
  31. Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T (2006) Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root-knot nematode interactions. New Phytol 170:501–512CrossRefPubMedGoogle Scholar
  32. Mozzetti CL, Ferraris G, Tamietti A (1995) Variation in enzyme activities in leaves and cell suspensions as markers of incompatibility in different Phytophthora-pepper interactions. Physiol Mol Plant Pathol 46:95–107CrossRefGoogle Scholar
  33. Pegard A, Brizzard A, Fazari O, Soucaze P, Djian-Caporalino C (2005) Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum. Phytopathology 95:158–165CrossRefPubMedGoogle Scholar
  34. SAS Institute, 1999–2000. SAS user’s guide: Statistics. Version 8.1. SAS Institute Inc. Carry, NC. USA. 1290Google Scholar
  35. Sasser JN, Lucas GB, Powers HR (1955) The relationship of root-knot nematodes to black shank resistance in tobacco. Phytopathology 45:459–461Google Scholar
  36. Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA (2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. Phytochemistry 64:153–161CrossRefPubMedGoogle Scholar
  37. Trujillo-Viramontes F, Zavaleta-Mejía E, Rojas-Martínez RI, Lara J (2005) Tiempo de inoculación y nivel de inóculo, factores determinantes para el rompimiento de resistencia a Phytophthora capsici inducido por Nacobbus aberrans en chile (Capsicum annuum). Nematropica 35:37–44Google Scholar
  38. Vargas EMT, Zavaleta-Mejía E, Hernández AAM (1996) Rompimiento de resistencia a Phytophthora capsici Leo en chile (Capsicum annuum L) serrano CM-334 por Nacobbus aberrans Thorne y Allen. Nematropica 26:159–166Google Scholar
  39. Vercauteren I, Van Der Schueren E, Van Montagu M, Gheysen G (2001) Arabidopsis thaliana genes expressed in the early compatible interaction with root-knot nematodes. Mol Plant-Microbe Interact 14:288–99CrossRefPubMedGoogle Scholar
  40. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell, LondonGoogle Scholar
  41. Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745CrossRefPubMedGoogle Scholar
  42. Wuyts N, Lognay G, Swennen R, De Waele D (2006a) Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 57:2825–2835CrossRefPubMedGoogle Scholar
  43. Wuyts N, Swennen R, De Waele D (2006b) Effects of plants phenylpropanoid products and selected terpenoids and alkalids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incógnita. Nematology 8(1):89–101CrossRefGoogle Scholar
  44. Xu EL, Chun YL, Pieqin H (2005) Study on the inhibitory effects on chlorogenic acid originated from the leavez of Actium lappa L. on pathogenic fungi. Plant Prot 31(3):35–38Google Scholar
  45. Zacheo G, Orlando C, Bleve-Zacheo T (1993) Characterization of anionic peroxidases in tomato isolines infected by Meloidogyne incognita. J Nematol 25:249–256PubMedGoogle Scholar
  46. Zavaleta-Mejía E (2002) Rompimiento de resistencia a hongos fitopatógenos por nematodos fitoparásitos, una hipótesis. Rev Mex Fitopatol 20:118–122Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Noé López-Martínez
    • 1
  • Ma. Teresa Colinas-León
    • 2
  • Cecilia B. Peña-Valdivia
    • 3
  • Yolanda Salinas-Moreno
    • 4
  • Patricia Fuentes-Montiel
    • 1
  • Magdalena Biesaga
    • 5
  • Emma Zavaleta-Mejía
    • 1
  1. 1.Fitopatología, Colegio de PostgraduadosMontecilloMéxico
  2. 2.Departamento de FitotecniaUniversidad Autónoma ChapingoChapingoMéxico
  3. 3.Botánica, Colegio de PostgraduadosMontecilloMéxico
  4. 4.Campo Experimental Valle de México CIRCE INIFAPTexcocoMéxico
  5. 5.Department of ChemistryUniversity of WarsawWarsawPoland

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