This article was downloaded by: [North Carolina State University] On: 09 March 2015, At: 15:29 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Canadian Journal of Plant Pathology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tcjp20 Effect of Inoculation Sequence on the Interaction between Glomus Intraradices and Fusarium Oxysporum f. sp. RadicisLycopersici in Tomatoes M. Caron a b c , J.A. Fortin a b c & C. Richard a b c a Experimental Farm, Agriculture Canada , P.O. Box 1070, L 'Assumption, Quebec, JOK 1G0 b Centre de Recherches en Biologie Foreslière , Université Laval , Quebec, G1K 7P4 c Research Station, Agriculture Canada , 2560, Boul. Hochelaga, SainteFoy, Quebec, G1V 2J3 Published online: 29 Dec 2009. To cite this article: M. Caron , J.A. Fortin & C. Richard (1986) Effect of Inoculation Sequence on the Interaction between Glomus Intraradices and Fusarium Oxysporum f. sp. Radicis-Lycopersici in Tomatoes, Canadian Journal of Plant Pathology, 8:1, 12-16, DOI: 10.1080/07060668609501835 To link to this article: http://dx.doi.org/10.1080/07060668609501835 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions CANADIAN JOURNAL OF PLANT PATHOLOGY 8: 12-16, 1986 Effect of inoculation sequence on the interaction between Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes M. Caron, J.A. Fortin, and C. Richard Experimental Farm, Agriculture Canada, P.O. Box 1070. L 'Assumption, Quebec JOK I GO (Contribution No. J-1005, Saint-Jean Research Station); Centre de recherches en biologie foreslière, Université Laval, Quebec (Quebec) Gl K 7 P4; and Research Station, Agriculture Canada, 2560, boul. Hochelaga, Sainle-Foy, Quebec, GIV2J3 (Contribution No. 285, Sainte-Foy Research Station). Present address of M. Caron: Centre de recherches, Les Tourbières Premier Ltée, Chemin Témiscouata, C. P. 482, Rivière-du-Loup (Quebec) G5R3Z1. Downloaded by [North Carolina State University] at 15:29 09 March 2015 Accepted for publication 1986 02 03 To determine if the decrease caused by Glomus intraradices, a vesicular-arbuscular mycorrhizal (VAM) fungus, in root rot of tomatoes and in the population of Fusarium oxysporum f.sp. radicis-lycopersici varies with the sequence of inoculation of the two fungi, tomato plants were inoculated with Glomus 4 weeks before, simultaneously with, and 4 weeks after the inoculation with Fusarium. Reductions in root rot and in the population of F. oxysporum were observed in all treatments and were not influenced by the sequence of inoculation with the two microorganisms. Root colonization by G. intraradices was significantly increased when F. oxysporum was inoculated simultaneously with or 4 weeks before the VAM fungus. Plant dry mass was not increased by the presence of G. intraradices alone, but compensation for dry mass loss due to F. oxysporum occurred when the VAM fungus was inoculated after the Fusarium. Caron, M., J.A. Fortin, and C. Richard. 1986. Effect of inoculation sequence on the interaction between Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes. Can. J. Plant Pathol. 8; 12-16, Afin d'établir si la diminution de la pourriture des racines de tomate et de la population de Fusarium oxysporum f.sp. radicislycopersici associée a la presence du Glomus intraradices, champignon mycorhizien a vésicules et arbuscules, varie en fonction de l'ordre d'inoculation des deux champignons, des plants de tomate ont été inoculés avec le Glomus 4 semaines avant l'inoculation avec le Fusarium, en même temps, et 4 semaines après. Une diminution du niveau de pourriture des racines et de la population fusarienne a été observée pour tous les traitements, mais n'a pas été influencée par la sequence d'inoculation des deux micro-organismes. La colonisation des racines par le G. intraradices a été augmentée de fagon significative lorsque le F. oxysporum a été inoculé simultanément ou 4 semaines avant le champignon mycorhizien. La masse sèche des plantes n'a pas été augmentée en presence du G. intraradices inoculé seul bien qu'il y ait eu compensation pour la perte en masse sèche due au Fusarium en presence du G. intraradices lorsqu'inoculé après le Fusarium. Interaction studies in which a host plant is inoculated with a vesicular-arbuscular mycorrhizal (VAM) fungus prior to its inoculation with a fungal root pathogen have indicated various effects by the VAM fungi on the development of the pathogen and on the severity of diseases induced in the host plants (Baath & Hayman 1983, Davis et al. 1978, Kaye et al. 1984). A few studies have been conducted in which a VAM fungus and a fungal root pathogen were inoculated simultaneously but none where the pathogen was inoculated prior to the VAM fungus. When inoculated simultaneously, a decrease (Krishna & Bagyaraj 1983, Zambolim & Schenck 1983), an increase (Davis et al. 1979, Ross 1972), or no effect (Schönbeck & Dehne 1977) of the VAM fungi on the development of the pathogen or the severity of disease induced in the host plants was observed. In previous studies (Caron et al. 1985, 1986a, 1986b), we have demonstrated that the presence of the VAM fungus Glomus intraradices Schenck & Smith can decrease both root rot of tomatoes {Lycopersicon esculentum Mill.) and the development of the pathogen Fusarium oxysporum Schlecht. f.sp. radicis-lycopersici Jarvis & Shoemaker. The objective of this work was to determine if such effects are influenced by the sequence of inoculation of the two fungi. Materials and methods Seeds of tomato (cv. Vendor) were surfacesterilized for 1.5 min in 3% sodium hypochlorite, blotted dry on sterilized filter papers and germinated for 5 days at 26°C on potato dextrose agar (PDA, Difco) in petri dishes. Germinated seeds without contaminants were then planted in sand, grown in a greenhouse, watered as needed with demineralized distilled water (DDW), and, 2 weeks after planting, fertilized with a Long Ashton solution (Hewitt 1966) modified by adding 300 mg of KC1 per L (Plenchette et al. 1982). Three-week-old seedlings were carefully removed from the seedbeds and the root system gently washed free of sand with DDW. The seedlings were transplanted to 18-cm-diameter pots containing pasteurized calcined montmorillonite clay (Turface, IMC Imcore, Mundelein, Illinois 60060) (Caron et al. 1985). The initial available P content of Turface as determined by extraction in 0.1 NHCl +0.3 7VNH4F and analysed by the 12 Downloaded by [North Carolina State University] at 15:29 09 March 2015 CARON ET AL.:TOMATO/FUSARIUM/GLOMUS vanadomolybdophosphoric yellow color method in nitric acid system (Jackson 1958) was 115 /ug'g'; the initial pH was 6.1. One hour prior to transplanting the seedlings, the substrate in each pot was watered with 500 mL of DDW followed by 100 mL of modified Long Ashton solution. The pathogen F. oxysporum f.sp. radicislycopersici (MC-27) was grown on PDA. Macroconidia were harvested in sterilized-distilled water from 26-day-old cultures incubated at 26° C under fluorescent lights (40 /xE-s'-nr2) and the conidial suspension was sieved (45 /xm). The concentration of the inoculum was approximat i v e ^ 5.4 x 104 macroconidia/mL for both inoculation periods. At the time of transplanting, a set of seedlings was inoculated with G. intraradices (G+) only, by placing 1 g (fresh mass) of mycorrhizal leek roots {Allium porrum L. cv. Alaska) 5 cm below the soil surface. To introduce into the nonmycorrhizal treatment (G ) the microflora usually associated with pot culture inoculum, 1 mL of a spore-free washing, obtained by wet sieving mycorrhizal roots through a 45 /xm mesh sieve, was added to the control pots together with 1 g of autoclaved mycorrhizal leek roots. A second set of seedlings was inoculated with F. oxysporum f.sp. radicislycopersici (F+) by spreading 1 mL of the conidial suspension onto the roots using a calibrated pipette. Uninoculated control (F~) plants received 1 mL of sterilized distilled water. A third set of seedlings was transplanted and kept for subsequent inoculation. Four weeks after transplanting, all plants were carefully uprooted. Tomato plants previously inoculated only with G intraradices, and their corresponding controls, were then inoculated with Fusarium following the procedure previously described, viz., G + F , G+F+, G F+, G F . Similarly, tomato plants previously inoculated only with the Fusarium, and their corresponding controls, were inoculated with G. intraradices a previously described, viz., G+F , G+F+, G~F+, G~F~. Tomato plants which had not been inoculated with either of the two microorganisms at the time of transplanting were inoculated simultaneously (G+F+) with both microorganisms, and appropriate controls (G~F , G+F , G F+) were added. Regardless of the time of inoculation with Glomus and Fusarium, the interaction between the two fungi in the tomato plants was for a 5-week period for each set of seedlings. Each treatment was replicated eight times. All plants were harvested at week 12, 5 weeks after the second inoculation. For each plant, the percentage of root necrosis was visually assessed on the basis of the proportion 13 of the root system showing surface necrosis at harvest. Root pieces of each plant, with and without necrosis, were plated on sucrose nutrient agar (Nirenberg 1981) to detect the presence of F. oxysporum f.sp. radicis-lycopersici. Survival of F. oxysporum f.sp. radicislycopersici was evaluated in each pot by placing 2 g of substrate free of plant material in 100 mL of water agar (0.12%) in a 125-mL flask and shaking for 1 h; subsequently, the substrate was allowed to settle for 10 min, after which 1 mL of the supernatant was diluted in 9 mL of water agar (0.12%). From each flask and each subsequent dilution, 1 mL of the suspension was spread on each of four petri dishes containing Komada's selective medium for F. oxysporum Schlecht. (Komada 1975). The petri dishes were incubated in the dark for 10 days at 24°C, after which period F. oxysporum colonies were counted, and the number of propagules per gram of dry mass of substrate was determined. Root samples from each plant were cleared and stained according to Phillips and Hayman (1970) using acid fuchsin instead of cotton blue (Berch & Kendrick 1982). A root endomycorrhizal colonization (REC) index (Plenchette et al. 1982) for each plant was established from an examination of three sites 3 mm apart on each of 40 1-cm-long root segments randomly sampled. The dry mass of the tomato plants was determined after drying at 65°C for 24 h. The experimental design was a randomized complete block design (8 blocks). The variances of the percent of root necrosis, the number of F. oxysporum propagules, the REC index, and the dry mass were analysed following a 3 * 2 * 2 factorial. Results The sequence of plant inoculation with F. oxysporum f.sp. radicis-lycopersici and G. intraradices significantly influenced (P= 0.05) the effect of Fusarium on colonization of the root by G. intraradices (Table 1). An analysis of variance of the REC index for each sequence of inoculation indicated that the presence of Fusarium inoculated 4 weeks after G. intraradices had no effect (P=0.05) on root colonization by the VAM fungus, while the presence of Fusarium inoculated simultaneously or 4 weeks before the inoculation with G. intraradices resulted in significant increases (P=0.0l) in the REC index of 6.2% (8.1-14.3%), and 17.1% (8.3-25.4%), respectively. The presence of G. intraradices resulted in significant reductions (P=0.0\) in root necrosis caused by Fusarium independently of the sequence of inoculation of the two fungi, as indicated by the 14 CANADIAN JOURNAL OF PLANT PATHOLOGY, VOLUME 8, 1986 Downloaded by [North Carolina State University] at 15:29 09 March 2015 Table 1. Analysis of variance of the root endomycorrhizal colonization (REC) index, the percent of root necrosis, the number of F, oxysporum propagules and the dry mass of tomato plants inoculated with G. intraradices 4 weeks before, simultaneously with, or 4 weeks after inoculation with F. oxysporum f.sp. radicis-lycopersici Sum of squares Mean square Source of variation d.f. REC index Blocks(B) Sequence of inocu lation (I) Glomus (G) Fusarium (F) IxG 1xF G» F \ *G*F Error Total 7 2 1 1 2 2 1 2 77 95 210.96 132.90 4030.04 570.38 172.77 157.69 459.37 227.31 2038.54 7999.96 30.14 66.45 4030.04 570.38 86.39 78.84 459.37 113.66 26.47 Root necrosis Blocks (B) Sequence of inoci lation (I) Glomus (G) Fusarium (F) 1 xG 1 xF G» F l«G»F Error Total 7 2 1 1 2 2 1 2 77 95 314.46 5390.39 8855.04 65000.04 1650.39 5390.39 8855.05 1650.39 8307.79 105413.96 44.92 2695.20 8855.04 65000.04 825.19 2695.19 8855.05 825.19 107.89 Number of F. oxysporum propagules Blocks(B) Sequence of inoci lation (I) Glomus (G) Fusarium (F) Ix G Ix F G» F 1 x Gx F Error Total 7 2 1 1 2 2 1 2 77 95 Dry mass of tomato plants Blocks(B) Sequence of inoci lation (I) Glomus (G) Fusarium (F) 1 x G 1 xF Gx F lx Gx F Error Total 7 2 1 1 2 2 1 2 77 95 1161938.7 6205245.8 36298532.0 137465896.0 339631.2 7729573.4 34422135.7 898571.5 69889703.1 294411227.4 84.22 195.73 26.78 51.19 11.32 7.04 0.01 7.21 166.84 580.33 165991.2 3102622.9 36298532.0 137465896.0 169815.6 3864786.7 34422135.7 449285.8 907658.5 12.03 97.87 26.78 51.19 5.66 18.52 0.01 3.60 2.17 F. ratio 1.14 n.s. 2.51 n.s. 152.22** 21.54** 3.26* 2.98 n.s. 17.35 ** 4.29* 0.42 24.98 82.07 602.45 7.65 24.98 82.07 7.65 n.s. ** ** ** ** ** ** ** 0.2 n.s. 3.4* 40.0 ** 151.5** 0.2 n.s. 4.3 * 37.9 ** 0.5 n.s. 5.55** 45.17** 12.36** 23.62 ** 2.61 n.s. 8.55 ** 0.002 n.s. 1.66 n.s. d.f. Degrees of freedom. n.s. Not significant. 5% level of significance. 1% level of significance. analysis of variance of the percent of root necrosis for each sequence of inoculation. However the differences of the percent of root necrosis between the presence and the absence of G. intraradices indicated a greater reduction (58.8%) when G. intraradices was inoculated 4 weeks after the inoculation with Fusarium, than when it was inoculated simultaneously (38.3%) or 4 weeks before (18.1%) the inoculation with Fusarium. Similarly plant inoculation with G. intraradices 4 weeks before, simultaneously with, or 4 weeks after inoculation with Fusarium resulted in significant reductions (P - 0.01) in the number of propagules of Fusarium of 2749, 2021, and 2513, respectively; these variations in the population of Fusarium in the presence and absence of G. intraradices were independent of the sequence of inoculation of the two fungi (Table 1). Plant mortality (25% of the Downloaded by [North Carolina State University] at 15:29 09 March 2015 CARON ET AL.: TOMATO/FUSARIUM/GLOMUS plants) occurred only in plants inoculated with Fusarium but not followed by inoculation with G intraradices. There were significant differences (P-0.0\) between blocks (Table 1) for the dry mass of tomato plants; these differences were not related to the treatments but to the position of the blocks in the greenhouse. There was a significant interaction (Z5 = 0.01) between the time of inoculation with Fusarium and its effect on the dry mass of plants (Table 1). The differences between the means of the dry mass of plants in the presence (F+) and the absence (F ) of Fusarium were obtained by using the following equation: (G+ mean - G~ mean) for F+ - (G+ mean - G mean) for F~. This calculation indicated no effect on plant dry mass either in the presence or in the absence of Fusarium when Glomus was inoculated 4 weeks before Fusarium. When Glomus and Fusarium were inoculated simultaneously, the difference between the means for F+ and F" (-1.3) showed that Glomus had a greater effect on plant dry mass in the absence of Fusarium. Similarly the difference between the means for F+ and F~ indicates that Glomus had an effect (+1.3) on plant dry mass in the presence of Fusarium only when the later was inoculated 4 weeks before the inoculation with Glomus. Discussion The observation that the presence of G. intraradices resulted in a decrease in root necrosis and in the population of F. oxysporum f.sp. radicislycopersici when inoculated prior, simultaneously or after the pathogen clearly indicates that this effect of G. intraradices on root rot and on the population of F. oxysporum f.sp. radicislycopersici is independent of the sequence of inoculation with the two microorganisms. The absence of an effect of F. oxysporum f.sp. radicis-lycopersici on root colonization by G. intraradices when the former was added after the VAM funguss, generally confirms our previous results (Caron et al. 1985, 1986a), although in one instance (Caron et al. 1986b) an increase was obtained. Kaye et al. (1984) have reported a greater colonization of roots of poinsettia by Glomus fasciculatum (Thaxter sensu Gerd.) Gerd. & Trappe Dn the presence of Pythium ultimum Trow. inoculated after the VAM fungus than in the absence of Pythium. On the other hand, Baath and Hayman (1983) have observed a lower root colonization of tomatoes by Glomus caledonium (Nicol. & Gerd.) Trappe & Gerd. inoculated prior to Verticillium albo-atrum Reinke & Berthold than in the absence of the pathogen. When inoculated simultaneously no effect of Fusarium on root 15 colonization by G. intraradices has been observed in our study. Krishna and Bagyaraj (1983) have observed a reduction in root colonization of peanut by Glomus fasciculatum in he presence of Sclerotium rolfsii Curzi inoculated simultaneously with the VAM fungus compared to absence of the pathogen. A reduction in root colonization of soybean by Glomus mosseae (Nicol. & Gerd.) Gerd & Trappe was also reported by Zambolim and Schenck (1983) when Macrophomina phaseolina (Tassi) Goid., Rhizoctonia solani Kuhn, or Fusarium solani (Mart.) App. & Wr. emend. Snyd. & Hans, were inoculated simultaneously with the VAM fungus, compared to the amount of root-colonization by Glomus obtained in their absence. This supports the belief that the effect of a root fungal pathogen on root colonization by a VAM fungus may be consistent within a system but could vary in different VAM fungus/root pathogen/host plant systems under study. The inoculation of G. intraradices after F. oxysporum f.sp. radicis-lycopersici resulted in a substantial increase in root endomycorrhizal colonization. This phenomenon cannot be explained at present but it clearly demonstrates that G. intraradices can colonize roots extensively despite its introduction 4 weeks after the Fusarium. This is the first report of an increase in root colonization by a VAM fungus when inoculated after a pathogen. The absence of an effect on plant dry mass when G. intraradices is inoculated prior to the Fusarium inoculation is not surprising since the interaction between the two fungi was monitored for only 5 weeks. In a previous study under the same experimental conditions (Caron et al. 1986a), G. intraradices had no effect on plant dry mass over a 12-week period. On the other hand, Fusarium significantly reduced plant dry mass only after a 10week period of interaction with Glomus. The observation that the presence of G. intraradices did not generally result in dry mass increase was also expected (Caron et al. 1985, 1986a, Fairweather & Parbery 1982). The inoculation with Fusarium 4 weeks before the inoculation with Glomus resulted in more root necrosis and plant mortality, and consequently more plant dry-mass loss, which in turn enhanced the effect of Glomus on Fusarium. While the effects of G. intraradices on root rot of tomatoes and on populations of F. oxysporum f.sp. radicis-lycopersici appear to be independent of the sequence of inoculation with the two microorganisms, the effect of the Fusarium on root colonization by G. intraradices is affected by the sequence of inoculation. Similar results were obtained by Kellam and Schenck (1980) in an 16 CANADIAN JOURNAL OF PLANT PATHOLOGY, VOLUME 8, 1986 Downloaded by [North Carolina State University] at 15:29 09 March 2015 interaction study on soybean (Glycine max (L.) Merr.) between Glomus macrocarpus (Nicol. & Gerd.) Gerd. & Trappe and the root-knot nematode Meloidogyne incognita (Kofoid & White) Chitwood. This study demonstrates that we need to investigate not only the mechanism by which VAM fungi can reduce disease incidence and pathogen development but also the means by which a fungal pathogen can enhance root colonization by a VAM fungus. The authors thank M. Bernier-Cardou for assistance in statistical analyses, D. LeQuéré for her technical assistance, and M. Chartrand for typing the manuscript. Baath, E., and D.S. Hayman. 1983. Plant growth responses to vesicular-arbuscular mycorrhiza. XIV. Interactions with Verticillium wilt on tomato plants. New Phytol. 95: 419-426, Berch, S.M., and B. Kendrick. 1982. Vesicular-arbuscular mycorrhizae of Southern Ontario and fern-allies. Mycologia 74: 769-776. Caron, M., J.A. Fortin, and C. Richard. 1985. 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