Abstract
Tomato plants pre-colonised by the arbuscular mycorrhizal fungusGlomus mosseae showed decreased root damage by the pathogenPhytophthora nicotianae var.parasitica. In analyses of the cellular bases of their bioprotective effect, a prerequisite for cytological investigations of tissue interactions betweenG. mosseae andP. nicotianae v.parasitica was to discriminate between the hyphae of the two fungi within root tissues. We report the use of antibodies as useful tools, in the absence of an appropriate stain for distinguishing hyphae ofP. nicotianae v.parasitica from those ofG. mosseae inside roots, and present observations on the colonisation patterns by the pathogenic fungus alone or during interactions in mycorrhizal roots. Infection intensity of the pathogen, estimated using an immunoenzyme labelling technique on whole root fragments, was lower in mycorrhizal roots. Immunogold labelling ofP. nicotianae v.parasitica on cross-sections of infected tomato roots showed that inter or intracellular hyphae developed mainly in the cortex, and their presence induced necrosis of host cells, the wall and contents of which showed a strong autofluorescence in reaction to the pathogen. In dual fungal infections of tomato root systems, hyphae of the symbiont and the pathogen were in most cases in different root regions, but they could also be observed in the same root tissues. The number ofP. nicotianae v.parasitica hyphae growing in the root cortex was greatly reduced in mycorrhizal root systems, and in mycorrhizal tissues infected by the pathogen, arbuscule-containing cells surrounded by intercellularP. nicotianae v.parasitica hyphae did not necrose and only a weak autofluorescence was associated with the host cells. Results are discussed in relation to possible processes involved in the phenomenon of bioprotection in arbuscular mycorrhizal plants.
Similar content being viewed by others
References
Baltruschat H and Schönbeck F 1975 The influence of endotrophic mycorrhiza on the infestation of tobacco byThielaviopsis basicola. Phytopathol. Z. 84, 172–188.
Benhamou N and Côté F 1992 Ultrastructure and cytochemistry of pectin and cellulose degradation in tobacco roots infected by Phytophthoraparasitica var.nicotianae. Cytol. Histol. 82, 468–478.
Benhamou N, Fortin J A, Hamel C, St-Arnaud M and Shatilla A 1994 Resistance responses of mycorrhizal Ri T-DNA-transformed carrot roots to infection byFusarium oxysporum f. sp.chrysanthemi. Phytopathol. 84, 958–968.
Caron M, Fortin J A and Richard C 1986a Effect ofGlomus intraradices on infection byFusarium oxysporum f. sp.radicislycopersici in tomatoes over 12-week period. Can. J. Bot. 64, 552–556.
Caron M, Fortin J A and Richard C 1986b Effect of phosphorus concentration andGlomus intraradices on fusarium crown and root rot of tomatoes. Phytopathol. 76, 942–946.
Caron M, Richard C and Fortin J A 1986c Effect of preinfestation of the soil by a vesicular-arbuscular mycorrhizal fungus,Glomus intraradices, on fusarium crown and root rot of tomatoes. Phytoprotection 67, 15–19.
Caron M 1989 Potential use of mycorrhizae in control of soil-borne diseases. Can. J. Plant Pathol. 11, 177–179.
Cordier C, Gianinazzi-Pearson and Gianinazzi S 1995 Immunodetection de champignons endomycorhiziens à arbuscules in planta. Acta Bot. Gallica 141, 465–468.
Davis R M, Menge J A and Erwin D C 1979 Influence ofGlomus fasciculatus and soil phosphorus onVerticillium wilt of cotton. Phytopathol. 9, 453–456.
Davis R M and Menge J A 1980 Influence ofGlomus fasciculatus and soil phosphorus onPhytophthora root rot of citrus. Phytopathol. 70, 447–452.
Davis R M and Menge J A 1981Phytophthora parasitica inoculation and intensity of vesicular-arbuscular mycorrhizae in citrus. New Phytol. 87, 705–715.
Dehne W H and Schönbeck F 1978 The influence of endotrophic mycorrhiza on plant diseases. 3. Chitinase-activity and ornithinecycle. Z. Planzenkr. Pflanzenschutz. 82, 666–678.
Dehne H W 1982 Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathol. 75, 1115–1119.
Feder N and O'Brien T P 1968 Plant microtechnique: some principles and new methods. Am. J. Bot. 55, 123–142.
Fernandez M R and Heath M C 1986 Cytological responses induced by five phytopathogenic fungi in a nonhost plantPhaseolus vulgaris. Can. J. Bot. 64, 648–657.
Gianinazzi S and Gianinazzi-Pearson V 1992 Cytology, histochemistry and immunocytochemistry as tools for studying structure and function in endomycorrhiza. Methods Microbiol. 24, 109–139.
Gianinazzi-Pearson V, Tahiri-Alaoui A, Antoniw J F, Gianinazzi S and Dumas-Gaudot E 1992 Weak expression of the pathogenesis related PR-b1 gene and localisation of related protein during symbiotic endomycorrhizal interactions in tobacco roots. Endocytobiosis Cell Res. 8, 177–185.
Gianinazzi-Pearson V, Dumas-Gaudot E, Gollotte A, Tahiri-Alaoui A and Gianinazzi S 1996 Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol. 133, 45–58.
Goode P M 1966 Infection of strawberry roots by zoospores ofPhytophthora fragariae. Trans. Br. Mycol. Soc. 39, 367–377.
Graham J H and Menge J A 1982 Influence of vesicular-arbuscular mycorrhizae and soil phosphorus on take-all disease of wheat. Phytopathology 72, 95–98.
Guillemin J P, Gianinazzi S, Gianinazzi-Pearson V and Marchal J 1994 Contribution of arbuscular mycorrhizas to biological protection of micropropagated pineapple (Ananas comosus (L.) Merr) againstP. cinnamomi rands. Agric. Sci. Finland. 3, 241–251.
Harrison M J and Dixon R A 1994 Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots ofMedicago truncatula and the mycorrhizal fungusGlomus versiforme. Plant J. 6, 9–20.
Hickman C J 1940 The red core root disease of the strawberry caused byPhytophthora fragariae. sp. J. Pomol. Hortic. Sci. 18, 89–118.
Hooker J E, Jaizme-Vega M and Atkinson D 1994 Biocontrol of plant pathogens using arbuscular mycorrhizal fungi.In Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems. Eds. S Gianinazzi and H Schüepp. pp 191–200. Birkhäuser Verlag, Basel, Switzerland.
Hwang S F, Chang K F and Chakravarty P 1992 Effects of vesiculararbuscular mycorrhizal fungi on the development of verticillium and fusarium wilts of alfafa. Plant Dis. 76, 239–243.
Jalali B L and Jalali I 1991 Mycorrhiza in plant disease control.In Handbook of Applied Mycology. Vol. I. Soil and Plants. Ed. D K Arora, B Rai, K G Mukherjee and D Knudsen. pp 131–154. Marcel Dekker Inc, New York, USA.
Klotz L J and De Wolfe T A 1965 Tetrazolium, an indicator of extent of infection inPhytophthora root rot of citrus. Plant Dis. Rep. 49, 423–424.
Lambais M R and Mehdy M C 1995 Differential expression of defense-related genes in arbuscular mycorrhiza. Can. J. Bot. 73 Suppl. 1, S533-S540.
Linderman R C 1994 Role of VAM fungi in biocontrol.In Mycorrhizae and Plant Health. Eds. Pfleger and Linderman. pp 1–27. The American Phytopathological Society Press, St Paul, USA.
Liu R J 1995 Effect of vesicular-arbuscular mycorrhizal fungi onVerticillium wilt of cotton. Mycorrhiza 5, 293–297.
Morandi D, Bailey J A and Gianinazzi-Pearson V 1984 Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol. Plant Pathol. 24, 357–364.
Phillips J M and Hayman D S 1970 Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc. 55, 158–161.
Schenck N C and Kellam M K 1978 The influence of vesicular-arbuscular mycorrhizae on disease development. Fl. Agric. Exp. Stn. Tech. Bull. 798, 1–16.
Stössel P, Lazarovitz G and Ward E W B 1980 Penetration and growth of compatible and incompatible races ofPhytophthora megasperma var.sojae in soybean hypocotyl tissues differing in age. Can. J. Bot. 58, 2594–2601.
Thiéry J P 1967 Mise en évidence des polysaccharides sur coupes semi-fines en microscopie électronique. J. Microsc. 6, 987–1018.
Tisserant B, Gianinazzi-Pearson V, Gianinazzi S and Gollotte A 1993 In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular endomycorrhizal infections. Mycol. Res. 97, 245–250.
Trouvelot A, Kough J L and Gianinazzi-Pearson V 1986 Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle.In Physiological and Genetical Aspects of Mycorrhizae. Eds. V Gianinazzi-Pearson and S Gianinazzi. pp 217–221. INRA, Paris, France.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cordier, C., Gianinazzi, S. & Gianinazzi-Pearson, V. Colonisation patterns of root tissues byPhytophthora nicotianae var.parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185, 223–232 (1996). https://doi.org/10.1007/BF02257527
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02257527