Abstract
Previous studies have described that arbuscular mycorrhizal fungi (AMF) can reduce the deleterious effect of Verticillium dahliae Kleb. on pepper growth and yield. In mycorrhizal plants, the bioprotection against soil-borne pathogens can result from the preactivation of defence responses that include some structural modifications and the accumulation of Pathogenesis-Related (PR) proteins. Our first objective was to study if V. dahliae induced defence mechanisms in roots before infected pepper developed visible symptoms of disease. The second aim was to determine if AMF induced defence-related enzymatic activities in pepper roots before or after pathogen’s attack. Results showed that the colonization of pepper roots by Glomus deserticola (Trappe, Bloss and Menge) induced the appearance of new isoforms of acidic chitinases, superoxide dismutase (SOD) and, at early stages, peroxidases. In contrast, V. dahliae neither stimulated the phenylpropanoid pathway nor elicited hydrolytic activities in infected pepper roots. Only in mycorrhizal plants, the inoculation with V. dahliae slightly increased both phenylalanine ammonia-lyase (PAL) and peroxidase activities two weeks later. Mycorrhizal-specific induction of new isoforms of acidic chitinases and SOD together with enhanced peroxidase and PAL activities 2 weeks after pathogen inoculation could be involved in the biocontrol of Verticillium-induced wilt in pepper by AMF.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- AMF:
-
arbuscular mycorrhizal fungi
- DM:
-
dry matter
- PAGE:
-
polyacrylamide gel electrophoresis
- PAL:
-
phenylalanine ammonia-lyase
- SOD:
-
superoxide dismutase
References
S.S. Adams, D.I. Rouse and R.L. Bowden, Performance of alternative versions of POTWIL: a computer model that simulates the seasonal growth of Verticillium-infected potato (Abstract). Am. Potato J. 64 (1987) 429
C. Azcón-Aguilar, M.C. Jaizme-Vega and C. Calvet, The contribution of arbuscular mycorrhizal fungi for bioremediation. In: S. Gianinazzi, H. Schüepp, J.M. Barea and K. Haselwandter (eds.) Mycorrhizal Technology in Agriculture. From Genes to Bioproducts. Berlin, Germany: Birkhäuser Verlag (2002) pp. 187-197
C.O. Beauchamp and I. Fridovich, Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44 (1971) 276-287
P. Bonfante-Fasolo, Anatomy and morphology of VA mycorrhizae. In: C.L. Powell and D.J. Bagyaraj (eds.) VA Mycorrhiza. Florida, USA: CRC Press, Boca Raton (1984) pp. 35-46
M.M. Bradford, A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal. Biochem. 12 (1976) 961-973
Y. Cui, A.A. Bell, O. Joost and C. Magill, Expression of potential defense response genes in cotton. Physiol. Mol. Plant Pathol. 56 (2000) 25-31
B.J. Davis, Disc electrophoresis. II. Method and application to human serum proteins. Ann. NY Acad. Sci. 121 (1964) 404-427
H.W. Dehne and F. Schönbeck, The influence of endotrophic mycorrhiza on plant diseases, 3, Chitinase activity and Ornithine cycle. Z. Pflanzenkr. Pflanzenschutz 82 (1978) 666-678
H.W. Dehne and F. Schönbeck, Investigations on the influence of endotrophic mycorrhiza on plant diseases. II. Phenol metabolism and lignification. Phytopathol. Z. 95 (1979) 210-216
I.A. Dubery and V. Slater, Induced defence responses in cotton leaf disks by elicitors from Verticillium dahliae. Phytochemistry 44 (1997) 1429-1434
I.A. Dubery and F. Smit, Phenylalanine ammonia-lyase from cotton (Gossypium hirsutum) hypocotyls: properties of the enzyme induced by a Verticillium dahliae phytotoxin. Biochim. Biophys. Acta 1207 (1994) 24-30
D.C. Dunn, L.W. Duncan and J.T. Romeo, Changes in arginine, PAL activity, and nematode behaviour in salinity-stressed citrus. Phytochemistry 49 (1998) 413-417
L.L.M. Fries, R.S. Pacovsky and G.R. Safir, Expression of isoenzymes altered by both Glomus intraradices colonization and formononetin application in corn (Zea mays L.) roots. Soil Biol. Biochem. 28 (1996) 981-988
I. Garmendia, N. Goicoechea and J. Aguirreolea, Plant phenology influences the effect of mycorrhizal fungi on the development of Verticillium-induced wilt in pepper. Eur. J. Plant Pathol. 110 (2004a) 227-238
I. Garmendia, N. Goicoechea and J. Aguirreolea, Effectiveness of three Glomus species in protecting pepper (Capsicum annuum L.) against verticillium wilt. Biol. Control 31 (2004b) 296-305
S. Gianinazzi and V. Gianinazzi-Pearson, Cytology, histochemistry and immunocytochemistry as tools for studying structure and function in endomycorrhiza. In: J.P. Norris, D.J. Read and A.K. Varma (eds.) Techniques for the Study of Mycorrhizal: Methods in Microbiology. London: Academic Press (1992) pp. 109-139
N. Goicoechea, J. Aguirreolea, S. Cenoz and J.M. García-Mina, Verticillium dahliae modifies the concentrations of proline, soluble sugars, starch, soluble protein and abscisic acid in pepper plants. Eur. J. Plant Pathol. 106 (2000) 19-25
J. Grenier and A. Asselin, Detection of β-1,3-glucanase activity in gels containing alkali-soluble yeast glucan. Anal. Biochem. 212 (1993) 301-302
D. Guenoune, S. Galili, D.A. Phillips, H. Volpin, I. Chet, Y. Okon and Y. Kapulnik, The defense response elicited by the pathogen Rhizoctonia solani is suppressed by colonization of the AM-fungus. Glomus intraradices. Plant Sci. 160 (2001) 925-932
C. Guillon, M. St-Arnaud, C. Hamel and S.H. Jabaji-Hare, Differential and systemic alteration of defence-related gene transcript levels in mycorrhizal bean plants infected with. Rhizoctonia solani. Can. J. Bot. 80 (2002) 305-315
S.-H. Ha, J.-B. Kim, Y.-S. Hwang and S.-W. Lee, Molecular characterization of three 3-hydroxy-3-methylglutaryl-CoA reductase genes including pathogen-induced Hmg2 from pepper (Capsicum annuum). Biochim. Biophys. Acta-Gene Struct. Expression 1625 (2003) 253-260
D.S. Hayman, J.M. Barea and R. Azcón, Vesicular-arbuscular mycorrhiza in southern Spain: Its distribution in crops growing in soil of different fertility. Phytopathol. Mediterr. 15 (1976) 1-6
Hewitt, E.J., 1966. Sand and water culture methods used in the study of plant nutrition. In: Technical Communication No. 22, 2nd ed., rev. Commonwealth Agricultural Bureaux, London.
G.P. Hoyos, F.I. Laurer and N.A. Anderson, Early detection of Verticillium wilt resistance in potato breeding program. American Potato J. 70 (1993) 535-541
T. Kervinen, S. Peltonen, T.H. Teeri and R. Karjalainen, Differential expression of phenylalanine ammonia-lyase genes in barley induced by fungal infection or elicitors. New Phytol. 139 (1998) 293-300
M.R. Lambais, Regulation of plant defense-related genes in arbuscular mycorrhizae. In: G.K. Podila and D.D. Douds (eds.) Current Advances in Mycorrhizae Research. Minnesota, USA: APS Press (2000) pp. 45-59
M.R. Lambais, W.F. Ríos-Ruiz and R.M. Andrade, Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol. 160 (2003) 421-428
D. Michaud and A. Asselin, Application to plant proteins of gel electrophoretic methods. J. Chromatogr. A 698 (1995) 263-279
R. Mittler, Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7 (2002) 405-410
D. Morandi, Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant Soil 185 (1996) 241-251
K.G. Mukerji, Mycorrhiza in control of plant pathogens: molecular approaches. In: K.G. Mukerji, B.P. Chamola and R.K. Upadhyay (eds.) Biotechnological Approaches in Biocontrol of Plant Pathogens. New York: Kluwer Academic/Plenum Publishers (1999) pp. 135-155
J.M. Palma, M.A. Longa, L.A. del Río and J. Arines, Superoxide dismutase in vesicular arbuscular-mycorrhizal red clover plants. Physiol. Plantarum 87 (1993) 77-83
G.F. Pegg, Pathogenesis in vascular diseases of plants. In: P.G. Ayres (ed.) Effects of Disease on the Physiology of the Growing Plant. Cambridge: Cambridge University Press (1989) pp. 149-177
J.M. Phillips and D.S. Hayman, Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc . 55 (1970) 158-161
F. Pomar, M. Novo, M.A. Bernal, F. Merino and A. Ros Barceló, Changes in stem lignins (monomer composition and crosslinking) and peroxidase are related with the maintenance of leaf photosynthetic integrity during Verticillium wilt in Capsicum annuum. New Phytol. 163 (2004) 111-123
M.J. Pozo, E. Dumas-Gaudot, S. Slezack, C. Cordier, A. Asselin, S. Gianinazzi, V. Gianinazzi-Pearson, C. Azcón-Aguilar and J.M. Barea, Induction of new chitinase isoforms in tomato roots during interactions with Glomus mosseae and/or Phytophthora nicotianae var parasitica. Agronomie 16 (1996) 689-697
M.J. Pozo, C. Azcón-Aguilar, E. Dumas-Gaudot and J.M. Barea, Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophthora parasitica. J. Exp. Bot. 49 (1998) 1729-1739
M.J. Pozo, C. Azcón-Aguilar, E. Dumas-Gaudot and J.M. Barea, β-1,3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci. 141 (1999) 149-157
M.J. Pozo, S. Slezack-Deschaumes, E. Dumas-Gaudot, S. Gianinazzi and C. Azcón-Aguilar, Plant defense responses induced by arbuscular mycorrhizal fungi. In: S. Gianinazzi, H. Schüepp, J.M. Barea and K. Haselwandter (eds.) Mycorrhizal Technology in Agriculture. From Genes to Bioproducts. Berlin: Birkhäuser Verlag (2002) pp. 103-111
M.J. Pozo, C. Cordier, E. Dumas-Gaudot, S. Gianinazzi, J.M. Barea and C. Azcón-Aguilar, Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J. Exp. Bot. 53 (2002) 525-534
R.A. Reisfeld, V.J. Lewis and D.E. Williams, Disk electrophoresis of basic proteins and peptides on polyacrylamide gels. Nature 195 (1962) 281-283
J.M. Ruiz-Lozano, R. Azcón and J.M. Palma, Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol. 134 (1996) 327-333
W.C. Schnathorst, Life cycle and epidemiology of Verticillium. In: M.E. Mace, A.A. Bell and C.H. Beckman (eds.) Fungal Wilt Diseases of Seedlings. New York: Academic Press (1981) pp. 81-111
R. Singh, A. Adholeya and K.G. Mukerji, Mycorrhiza in control of soil borne pathogens. In: K.G. Mukerji, B.P. Chamola and J. Singh (eds.) Mycorrhizal Biology. New York: Kluwer Academic Publishers (2000) pp. 173-196
P. Spanu and P. Bonfante-Fasolo, Cell-wall-bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytol. 109 (1988) 119-124
L.C. Loon Van and E.A. Strien Van, The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type protein. Physiol. Mol. Plant Pathol. 55 (1999) 85-97
X.S. Ye, S.Q. Pan and J.A. Kúc, Activity, isoenzyme pattern, and cellular localization of peroxidase as related to systemic resistance of tobacco to blue mold (Peronospora tabacina) and to tobacco mosaic virus. Phytopathology 80 (1990) 1295-1299
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Garmendia, I., Aguirreolea, J. & Goicoechea, N. Defence-related Enzymes in Pepper Roots During Interactions with Arbuscular Mycorrhizal Fungi and/or Verticillium dahliae . Biocontrol 51, 293–310 (2006). https://doi.org/10.1007/s10526-005-4238-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-005-4238-6