Abstract
The present work examined the oxidative stress induced by different concentrations (0.02 and 0.2 mg l-1) of two sterol biosynthesis inhibitor fungicides (fenpropimorph and fenhexamid) in non-target chicory root colonised or not by Glomus intraradices in a monoxenic system. The fungicides were found to cause oxidative damage by increasing lipid peroxidation measured by malondialdehyde production in non-colonised roots. Detoxification of the H2O2 product was measured at 0.2 mg l-1 of fenpropimorph by an increase in peroxidase activities suggesting an antioxidant capacity in these roots. Moreover, this study pointed out the ability of arbuscular mycorrhiza to alleviate partially the oxidative stress in chicory roots, probably by lowering reactive oxygen species concentrations, resulting from increases in antioxidant defences. Our results suggest that the enhanced fungicide tolerance in the AM symbiosis could be related to less cell membrane damage.
Similar content being viewed by others
References
Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Bailly C, Benamar A, Corbineau F, Côme D (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plant 97:104–110
Beilby JP (1980) Fatty acid and sterol composition of ungerminated spores of the vesicular–arbuscular mycorrhizal fungus, Acaulospora laevis. Lipids 15:949–952
Ben Youssef N, Zarrouk M, Ben Miled DD, Cherif A, Ghorbal MH (2003) Effets du cadmium sur la composition en lipides foliaires de plantules de colza (Brassica napus L.). Riv Ital Sostanze Grasse 80:165–170
Bidar G, Garçon G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553
Bidar G, Verdin A, Garçon G, Pruvot C, Laruelle F, Grandmougin-Ferjani A, Douay F, Shirali P (2008) Changes in fatty acid composition and content of two plants (Lolium perenne and Trifolium repens) grown during 6 and 18 months in a metal (Pb, Cd, Zn) contaminated field. Water Air Soil Pollut 192:281–291
Bjørnlund L, Ekelund F, Christensen S, Jacobsen CS, Krogh PH, Johnsen K (2000) Interactions between saprotrophic fungi, bacteria and protozoa on decomposing wheat roots in soil influenced by the fungicide fenpropimorph (Corbel®): a field study. Soil Biol Biochem 7:967–975
Blanckaert A, Belingheri L, Vasseur J, Hilbert JL (2000) Changes in lipid composition during somatic embryogenesis in leaves of Cichorium. Plant Sci 157:165–172
Brundrett M, Melville L, Peterson L (1994) Clearing and staining mycorrhizal roots. In: Brundrett M, Melville L, Peterson L (eds) Practical methods in mycorrhiza research. Mycologue Publications, Waterloo, British Columbia, pp 42–46
Campagnac E, Fontaine J, Lounès-Hadj Sahraoui A, Laruelle F, Durand R, Grandmougin-Ferjani A (2008) Differential effects of fenpropimorph and fenhexamid, two sterol biosynthesis inhibitor fungicides, on arbuscular mycorrhizal development and sterol metabolism in carrot roots. Phytochemistry 69:2912–2919
Clijsters H, Van Assche F, Gora L (1991) In: Rozema J, Verkleij JAC (eds) Ecological responses to environmental stresses. Kluwer, The Netherlands, p 22
Costet-Corio M-F, Benveniste P (1988) Sterol metabolism in wheat treated by N-subsituted morpholines. Pestic Sci 22:343–357
Dat J, Vandenabeele S, Vranovà E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795
Debiane D, Garçon G, Verdin A, Fontaine J, Durand R, Grandmougin-Ferjani A, Shirali P, Lounès-Hadj Sahraoui A (2008) In vitro evaluation of the oxidative stress and genotoxic potentials of anthracene on mycorrhizal chicory roots. Environ Exp Bot 64:120–127
Debieu D, Gall C, Gredt M, Bach J, Malosse C, Leroux P (1992) Ergosterol biosynthesis and its inhibition by fenpropimorph in Fusarium species. Phytochemistry 31:1223–1233
Declerck S, Strullu DG, Plenchette C (1998) Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 9:579–585
Declerck S, D’Or D, Cranenbrouck S, Le Boulengé E (2001) Modelling the sporulation dynamics of arbuscular mycorrhizal fungi in monoxenic culture. Mycorrhiza 11:225–230
Declerck S, Strullu DG, Fortin JA (2005) In vitro cultures of mycorrhizas. Springer-Verlag, Heidelberg
Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog Lipid Res 43:200–227
Ekelund F (1999) The impact of the fungicide fenpropimorph (Corbel®) on bacterious and fungivorous protozoa in soil. J Appl Ecol 36:233–243
Escobar JA, Rubio MA, Lissi EA (1996) SOD and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radic Biol Med 20:285–290
Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malondialdehyde and related aldehydes. Free Radic Biol Med 11:81–128
Fortin J, Bécard G, Declerck S, Dalpé Y, St-Arnaud M, Coughlan AP, Piché Y (2002) Arbuscular mycorrhiza on root organ cultures. Can J Bot 80:1–20
Georgin P, Gouet M (2005) Statistiques avec excel. Presses Universitaires de Rennes, Paris
Gopi R, Jaleel CA, Sairam R, Lakshamanan GMA, Gomathinayagam M, Panneerselvam R (2007) Differential effects of hexaconazole and paclobutrazol on biomass, electrolyte leakage, lipid peroxidation and antioxidant potential of Daucus carota L. Colloids Surf B Biointerfaces 60:180–186
Graham JH, Hodge NC, Morton JB (1995) Fatty acid methyl ester profiles for characterization of glomalean fungi and their endomycorrhizae. Appl Environ Microbiol 61:58–64
Grandmougin A, Bouvier-Navé P, Ullmann P, Benveniste P, Hartmann MA (1989) Cyclopropyl sterol and phospholipid composition of membrane fractions from maize roots treated with fenpropimorph. Plant Physiol 90:591–597
Grandmougin-Ferjani A, Fontaine J, Durand R (2005) Carbon metabolism, lipid composition and metabolism in arbuscular mycorrhizal fungi. In: Declerck S, Strullu DG, Fortin JA (eds) In vitro culture of mycorrhizas. Springer, Berlin, pp 159–180
Halliwel B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Claredon Press, Oxford
He JX, Fujioka S, Li TC, Kang SG, Seto H, Takatsuto S, Yoshida S, Jang JC (2003) Sterols regulate development and gene expression in Arabidopsis. Plant Physiol 131:1258–1269
He Z, He C, Zhang Z, Zou Z, Wang H (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B Biointerfaces 59:128–133
Hewitt HG (1998) Fungicides in crop protection. CAB, Wallingford
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146
Hillis DG, Antunes P, Sibley PK, Kliromonos JN, Solomon KR (2008) Structural responses of Daucus carota root-organ cultures and the arbuscular mycorrhizal fungus, Glomus intraradices, to 12 pharmaceuticals. Chemosphere 73:344–352
Hodge A (2000) Microbial ecology of the arbuscular mycorrhiza. FEMS Microbiol Ecol 32:91–96
Jaleel CA, Gopi R, Lakshmanan GMA, Panneerselvam R (2006) Triadimephon induced changes in the antioxidant metabolism and ajmalicine production in Catharanthus roseus (L.) G. Don. Plant Sci 171:271–276
Khalil IA, Mercer EI (1991) Accumulation of 9β, 19-cyclopropysterols in cereals treated with fenpropimorph. J Agric Food Chem 39:404–407
Kishorekumar A, Jaleel CA, Manivannan P, Sankar B, Sridharan R, Murali PV, Panneerselvam R (2008) Comparative effects of different triazole compounds on antioxidant metabolism of Solenostemon rotundifolius. Colloids Surf B Biointerfaces 62:307–311
Manivannan P, Jaleel CA, Kishorekumar A, Sankar B, Somasundaram R, Sridharan R, Panneerselvam R (2007) Changes in antioxidant metabolism of Vigna unguiculata (L.) Walp. by propiconazole under water deficit stress. Colloids Surf B Biointerfaces 57:69–74
Marin M, Ybarra M, Fé A, Garcia-Férriz L (2002) Effect of arbuscular mycorrhizal fungi and pesticides on Cyanara cardunculus growth. Agric Food Sci Finl 11:245–251
McGonigle TP, Miller MH, Evans DG, Faichild GL, Swan JA (1990) A method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501
Mitchell HJ, Hall JL, Barber MS (1994) Elicitor-induced cinnamyl alcohol dehydrogenase activity in lignifying wheat (Triticum aestivum L.) leaves. Plant Physiol 104:551–556
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Morrison WR, Smith LM (1964) Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J Lipid Res 5:600–608
Mosleh YY, Paris-Palcios S, Couderchet M, Biagianti-Risbourg S, Vernet G (2005) Metallothionein induction, antioxidative responses, glycogen and growth changes in Tubifex Tubifex (oligocaete) exposed to the fungicide, fenhexamid. Environ Pollut 135:73–82
Nordby HE, Nemec S, Nagy S (1981) Fatty acids and sterols associated with citrus root mycorrhizae. J Agric Food Chem 29:396–401
Nourissat P, Travert M, Chevanne M, Tekpli X, Rebillard A, Le Moigne-Muller G, Rissel M, Cillard J, Dimanche-Boitrel M-T, Lagadic-Gossmann D, Sergent O (2008) Ethanol induces oxidative stress in primary rat hepatocytes through the early involvement of lipid raft clustering. Hepatology 47:59–70
Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310
Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal MH (1997) Cadmium- and copper-induced changes in tomato membrane lipids. Phytochemistry 45:1343–1350
Pacovsky RS, Fuller G (1988) Mineral and lipid composition of Glycine–Glomus–Bradyrhizobium symbioses. Physiol Plant 72:733–746
Parent C, Capelli N, Dat J (2008) Formes réactives de l’oxygène, stress et mort cellulaire chez les plantes. C R Biol 331:255–261
Rosslenbroich H-J (1999) Efficacy of fenhexamid (KBR 2738) against Botrytis cinerea and related fungal pathogens. Pflanzenschutz-Nachr 52:127–144
Sancholle M, Dalpé Y, Grandmougin-Ferjani A (2001) Lipids of mycorrhizae. In: Hock B (ed) Fungal associations. Springer, Berlin, Heidelberg, pp 63–93
Sanità Di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Schaller H, Maillot-Vernier P, Benveniste P, Belliard G (1991) Sterol composition of tobacco calli selected for resistance to fenpropimorph. Phytochemistry 30:2457–2554
Schrick K, Fujioka S, Takatsuto S, Stierhof Y-D, Stransky H, Yoshida S, Jürgens G (2004) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38:227–243
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Shirali P, Teissier E, Marez T, Hildebrand HF, Haguenoer JM (1994) Effect of alpha Ni3S2 on archidonic acid metabolites in cultured human lung cells (L132 cell line). Carcinogenesis 15:759–762
Siedow JN (1991) Plant lipoxygenase: structure and function. Annu Rev Plant Physiol Plant Mol Biol 42:145–188
Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New-York
Sinha S, Saxena R, Singh S (2005) Chromium induced lipid peroxidation in the plants of Pistia stratiotes L.: role of antioxidants and antioxidant enzymes. Chemosphere 58:595–604
Skórzyńska-Polit E, Krupa Z (2006) Lipid peroxidation in cadmium-treated Phaseolus coccineus plants. Arch Environ Contam Toxicol 50:482–487
Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Effect of lead on lipid peroxidation of the hepatic subcellular organelles of developing chick embryos. Biochem Int 27:803–809
Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172:22–34
Strullu DG, Romand C (1986) Méthode d’obtention d’endomycorhizes à vésicules et arbuscules en conditions axéniques. C R Acad Sci III 303:245–250
Taylor GJ (1988) The physiology of aluminum phytotoxicity. In: Sigel H (ed) Metal ions in biological systems: aluminum and its role in biology, vol 24. Marcel Dekker, New York, pp 123–163
Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001
Thirup L, Johnsen K, Torsvik V, Spliid NH, Jacobsen CS (2001) Effects of fenpropimorph on bacteria and fungi during decomposition of barley roots. Soil Biol Biochem 33:1517–1524
Thompson GAJR (1992) The regulation of membrane lipids. CRC, Boca Raton, FL
Thompson JE, Froese CD, Madey E, Smith MD, Hong Y (1998) Lipid metabolism during plant senescence. Prog Lipid Res 37:119–141
Van Breusegem F, Vranovà E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414
Verdin A, Lounès-Hadj Sahraoui A, Fontaine J, Grandmougin-Ferjani A, Durand R (2006) Effects of anthracene on development of an arbuscular mycorrhizal fungus and contribution of the symbiotic association to pollutant dissipation. Mycorrhiza 16:397–405
Wan MT, Rahe JE, Watts RG (1998) A new technique for determining the sublethal toxicity of pesticides to the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. Environ Toxicol Chem 17:1421–1428
Wu YX, von Tiedemann A (2001) Physiological effects of azoxystrobin and epiconazole on senescence and the oxidative status of wheat. Pestic Biochem Physiol 71:1–10
Wu YX, Zou YN, Xia RX (2006a) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots. Eur J Soil Biol 42:166–172
Wu YX, Xia RX, Zou YN (2006b) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110
Yamauchi Y, Furutera A, Seki K, Toyoda S (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Biochem 46:786–793
Zhang LZ, Zhu YG, Lin AJ, Chen BD, Smith SE, Smith FA (2006) Arbuscular mycorrhizal fungi can alleviate the adverse effects of chlorothalonil on Oryza sativa L. Chemosphere 64:1627–1632
Zhang LZ, Wei N, Wu QX, Ping ML (2007) Anti-oxidant response of Cucumis sativus L. to fungicide carbendazim. Pestic Biochem Physiol 89:54–59
Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509
Zocco D, Fontaine J, Lozanova E, Renard L, Bivort C, Durand R, Grandmougin-Ferjani A, Declerck S (2008) Influence of two sterol biosynthesis inhibitor fungicides (fenpropimorph and fenhexamid) on the development of an arbuscular mycorrhizal fungus. Mycol Res 112:592–601
Zohrehvand S (2005) On activated seed swelling technique. Polym Int 54:1191–1195
Acknowledgements
In this paper, the first position is shared by the two co-authors: A. Lounès-Hadj Sahraoui and E. Campagnac. This work was supported by a Marie-Curie Early stage Research Training Fellowship of the European Community’s Sixth framework Programme under contract number MEST-CT-2004-514213. The laboratory participates in the Institut de Recherches en Environnement Industriel (IRENI), which is financed by the Communauté Urbaine de Dunkerque, the Région Nord-Pas de Calais, the Ministère de l’enseignement supérieur et de la recherche, and European funds (FEDER). We thank Bayer and BASF, which kindly provided the SBI fungicides, and we are grateful to Natacha Bourdon for technical help.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Campagnac, E., Lounès-Hadj Sahraoui, A., Debiane, D. et al. Arbuscular mycorrhiza partially protect chicory roots against oxidative stress induced by two fungicides, fenpropimorph and fenhexamid. Mycorrhiza 20, 167–178 (2010). https://doi.org/10.1007/s00572-009-0267-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-009-0267-9