Journal of Life Sciences and Technologies Vol. 1, No.

1, March 2013

Impact of Some Antagonistic Organisms in Controlling Meloidogyne Arenaria Infecting Tomato Plants
Asmaa A. Mokbel
Alexandria University, Faculty of Agriculture/ Plant Pathology Department, Alexandria, Egypt E.mail: dr. mokbel_71@yahoo.com

Abstract—Effect of three isolates of Bacillus subtilis, two isolates of B. thuringiensis subsp. aegypti, three species of Trichoderma and the nematicide Furadan®10G, were evaluated on Meloidogyne arenaria infected tomato plants. Treatments with Furadan®10G, washed pellet of B. thuringiensis, sporulated bacterial cells of B. subtilis isolates and mixed Trichoderma filtrates caused (63.9–96.8%) inhibition on M. arenaria egg-hatching and J2 activity in the laboratory experiment and showed 66.2-98.4% reduction in nematode reproduction in the pot experiment. In the field experiment, the greatest reductions (70.0-99.8%) in the number of nematode root galls, egg-masses/plant and number of J2/250 cc soil and greatest increase (40.2-62.2%) in the dry weight of shoot and root systems were recorded with the treatments of Furadan®10G, mixed filtrates of the tested Trichoderma species and washed pellet of B. thuringiensis isolate 7N compared to check treatment. Index Terms—Bacillus spp, Root-knot nematodes, meloidogyne arenaria, tomato, trichoderma spp.

[24]. Hence, the present study designed to showed the efficacy of three B. subtilis isolates and two B. thuringiensis isolates, three species of Trichoderma (T. hamatum, T. harzianum and T. viride) compared with the chemical nematicide, Furadan®10G, on egg-hatching and 2nd stage juvenile (J2) activity of M. arenaria under laboratory as well as its infection on tomato plants under greenhouse and filed conditions. II MATERILAS AND METHODS A. Bacillus & Trichoderma Cultures Three isolates of B. subtilis & T. hamatum (Bon.) Bain., T. harzianum Rifai and T. viride Per. Ex Gray, used in this study, were obtained from the cultures collection of the Department of Plant Pathology, Faculty of Agriculture, Alexandria University, Alexandria, Egypt. The two isolates of B. thuringiensis subsp. aegypti (7N and Soto) were obtained from the Agricultural Genetic Engineering Research Institute (AGERI), Agricultural Research Centre, Giza, Egypt. B. Root-knot Nematode, M. arenaria Inoculum Preparation Cultures of M. arenaria (Neal) Chitwood were established from single egg-masses of adult females previously identified by the morphological characteristics of the female perineal patterns [4] [11] and reared on tomato plants (Lycopersicon esculentum Mill) cv. Super Strain B in a greenhouse. The root-knot nematode eggs were extracted from infected tomato roots using sodium hypochlorite (NaOCl) solution as described by [21]. M. arenaria eggs and the hatched 2nd stage juveniles (J2) were placed in sterile distilled water and used in all tests. C. Doses of Bacillus Isolates, Trichoderma and Furadan®10G One dose of sporulated bacterial cells for each of B. subtilis isolates (5× 105 cfu/ml distilled water), five ml/pot or plant was used, and (10 ml of each of bacterial cell free-filtrates of B. subtilis isolate/pot or plant) was used for pot and field experiments. Treatments were applied at the same time of nematode inoculation and 21
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I

INTRODUCTION

Root-knot nematodes Meloidogyne spp. are one of the major pathogens of tomato world wide and limit fruit production, estimated yield losses ranging from 28-68% [18]. Root-knot nematode infestations on tomato (Lycopersicon esculentum Mill) are common in Egypt and cause severe crop damage especially in light soils [15]. These nematodes can be managed effectively by chemical treatments but many of the nematicides are expensive, pose human and environmental risk or have been withdrawn from use [15]. Management of root-knot nematodes with biological control agents has been receiving growing consideration [14]. A wide range of bacteria and fungi create the possibility for control plantparasitic nematodes [24]. Numerous Bacillus species and strains especially B. subtilis and B. thuringiensis can suppress root-knot nematodes [1], [9], [10]. Also, Trichoderma spp. can produce a variety of fungal metabolites, termed mycotoxins, which affect adult nematode activity and inhibit egg-hatching and juvenile development and enhance plant growth [2], [8], [12],

Manuscript received October 15, 2012; revised December 5 2012.

Egypt. thuringiensis isolate were used. arenaria were included as check treatments. 70 Pots were treated with 5 ml/pot of the sporulated bacterial cells suspension (5× 105 cfu/ml distilled water) and 10 ml of bacterial cell free-filtrates/pot of each B. Observation of the on the effects of different treatments on egg-hatching and J2 activity was taken 24 hours after adding nematode eggs or J2 in Trichoderma filtrates. and 21 days later. Each treatment was replicated five times. All treatments were replicated five times and were laid out in a completely randomized block design for two months duration. Philadelphia-PA 19103 (USA) was used at the rate of (0. subtilis. 2. thuringiensis isolates and Furadan®10G on egg-hatching and J2 activity of M. Pot experiment Effects of B. For check treatments. isolate 7N of B. sterilized NB medium and sterilized T3 medium. Treatments were applied in 24-well tissue culture plates. Field plot experiments were 3m × 5. 5× 105 cfu/ml distilled water of sporulated bacterial cell for each B.25 g nematicide/100 ml distilled water) for egghatching and J2 activity experiments and (2. Super Strain B. Super Strain B were transplanted in 120 plastic pots. G. Data were collected 60 days after final treatments. Treatments were done in 24-well tissue culture plates. Pots were arranged in randomized complete block maintained at 27± 2° C and irrigated daily. March 2013 days later [19] [20]. D. FMC Chemical.Journal of Life Sciences and Technologies Vol. Dry weight of shoot and root systems.25 g/100 ml distilled water) of Furadan®10G were tested to study their effect on egg-hatching and J2 activity. arenaria on tomato under greenhouse conditions Four-wk-old tomato seedlings cv. Statistical Analysis: Data obtained were statistically analyzed according to SAS software program [25]. NB and T3 mediums plus M.3dihydro-2. Laboratory Experiments: Effects of Trichoderma filtrates and Furadan®10G on egg-hatching and J2 activity of M. thuringiensis isolates and Furadan®10G on M. Fifteen pots. arenaria eggs or J2 were placed in sterile distilled water. M. washed pellet (4 mg/ml distilled water) and supernatant for each B. B. The soil was sandy loam with 2. arenaria eggs or J2 were incubated in sterile distilled water and sterilized CDL medium.5% organic matters. 1. Treatments were maintained at 25± 2° C in an incubator. B. Numbers of nematode root galls and eggmasses/plant were determined. A total of 200 M. Effects of B. viride filtrates (10ml/plant) either alone or as a mixture filtrates of Trichoderma speies and Furadan®10G at the rate of 2. each well received 3 ml of each treatment. For check treatments. M. subtilis isolate. were transplanted at 50-cm distance three days later.5 g/plant were applied. Field Experiment: Effects of two isolates of B. Comparison among means was made via the least . arenaria under laboratory conditions Sporulated bacterial cells (5× 105 cfu/ml distilled water) or bacterial cell free-filtrates for each B.5g nematicide/pot or plant) for pot and field experiments.2-dimethylbenzofuran-7-yl Methylcarbamate. The granular nematicide carbofuran. T. thuringiensis isolate and (0. sterilized NB medium and liquid T3 medium were served as check treatments. No. Treatments were maintained at 25± 2° C in an incubator. were used alone or as a mixed filtrate of the three Trichoderma species on egg-hatching and J2 activity. received sterile distilled water. arenaria eggs or 95 fresh hatched J2/well were added in 50 µ l of water. 30 cm diam. one week before nematode inoculation. The experiments were terminated 35 days after nematode inoculation. One dose of washed pellet of B. arenaria (600 eggs or J2/pot). 5 pots each. each well received 3 ml of each treatment. washed pellet (4mg/plant) for B. aegypti (4mg/pot or plant) and (10 ml of supernatant/pot or plant) were used for pot and field experiments. (5 plants per row). arenaria at the same time with the following treatments. subtilis. Twelve plants and 10 soil samples from the rhizosphere of tomato plants up to a depth of 20 cm (250 cc soil/sample) from each plot were taken for analysis. number of nematode root galls and egg-masses/plant and number of J2/250cc soil were determined.5 g nematicide/pot. Data of the numbers of nematode root galls. egg-masses and juveniles were transformed to x 1 before statistical analysis. subtilis isolate. subtilis isolate (isolates 2&3) at 5 ml of the suspension/plant. for each isolate and applied at the same time with M.. Alexandria University. Each plant received 2000 eggs&J2 of M. F. Treatments were applied at the same time of M. Trichoderma filtrates and Furadan®10G on M.0 m for each treatment (4 rows of 3 meter long and 85-cm wide with 50-cm gap between rows). A total of 270 M. Separate rows of tomato plants treated with sterilized CDL. arenaria eggs/well or 125 fresh hatched J2 was added in 50 µ l of water. Each treatment was replicated eight times. Rows of tomato plants received only sterilized distilled water without nematode served as control treatment. FPRL Agrochemical Products Group. thuringiensis isolate 7N. Furadan® 10G. arenaria on tomato under field conditions Field experiment was conducted at the farm of Faculty of Agriculture. v:v) and inoculated with M. Each treatment was replicated eight times. cv. arenaria The collected culture filtrates of each of the three tested Trichoderma spp. All rows were irrigated to full water holding capacity and three weeks old tomato seedlings. E. one seedling/pot. The nematode J2 were considered to be inactive when they did not move. Four mg washed pellet/pot and 10ml supernatant/pot of each tested B. arenaria inoculation and 7 days later. subtilis. harzianum or T. Alexandria. thuringiensis subsp. arenaria inoculation and 21 days later. thuringiensis. Furadan®10G was used at the rate of 2. Pots were filled with sandy clay soil (2:1. 1.

2 55.3 66. Data are averages of 5 replicates.2 cd Cell free-filtrates 97.8 48. Check treatment* CDL + MA T.1 82.9 67.8 bc 88.7 26. Data are averages of 8 replicates. SUBTILIS.1b 21. Red.2 bc 289.1 a 122.9-73.2 97.8 51.9 57. 1.0 5.6 79.4a 40. % 0.6 29.7 50.y % 0.3 68. hamatum +MA T.9 38.1 19.5 67. thuringiensis isolates.3 c 166. harzianum and T.0 b ® 6.1cd 66.3 ef 238.5 f Supernatant 236. Also. Check treatment * NB medium +MA T3 medium +MA Bacillus subtilis + MA Isolate 1 Sporulated cells 275. No.5 a 499. as in Table I.8%) in egghatching and J2 activity.2 d 249.1 c 89.7 0.0 c B.4 bc Isolate 2 Sporulated cells 120.6-96.1cd 70.0 1. of active J2 in check treatment Number of hatched and active juveniles was transformed to angular transformation before statistical analysis. T.5c Inh. subtilis isolate 1.3 99. thuringiensis isolates + MA 7N Washed pellet 92. arenaria under Laboratory Conditions: Data presented in Table II indicated that Furadan®10G caused the greatest reduction (94.9 52.2 de Cell free-filtrates 265.2% and 98.5 b 29.1 1.4 bc Isolate 3 Sporulated cells 53.1e Cell free-filtrates 255. EFFECTS OF B. of hatched J2 in each treatment/No.5 81.Hx= Relative hatching % = No. water) of Soto isolate caused 63.6 96. The greatest reduction in egghatching and J2 activity (96.4 79.6% inhibition in egg-hatching and J2 activity of M.9 30.0 a 123. whereas treatments with T. Nematode = 200 MA eggs/treatment for hatched experiment & = 125 fresh J2/treatment for activity experiment.9 46.4 3.7 63.1 98.3 e 0. Values of each column. harzianum+ MA T.5–89. *=Dist. NB medium = Nutrient Broth medium.5c 3.5 96.5 a Red. THURINGIENSIS ISOLATES ® AND FURADAN 10G ON EGG-HATCHING AND J2 ACTIVITY OF M. arenaria on Tomato Plants under Greenhouse Conditions: Data presented in Table III indicated that treatments with Furadan®-10G (2.0 b Cell free-filtrates 251. SUBTILIS.5 82.4% in number of nematode root galls and egg masses/plant.8 56.7 51.4 c Cell free-filtrates 107.4 d 7N Washed Pellet Supernatant 110.2 a 503.8 44. bacterial cell free-filtrates and supernatant of all Bacillus spp. TABLE II.8 a 264.2 e 241. Effects of B.0 a NB medium+MA 196. water) of sporulated bacterial cells of B.9 a 53. C.5 81.2 44.1 10.0 bc 89.0 1.0 99. M.0 96.2 50.0 b 100.6%) inhibition in egghatching and J2 activity.0 c Soto Washed pellet 174.5 f 229.5 a T3 medium+MA 198.0 d * = Dist. subtilis isolate (2&3) and (4mg of washed pellet/ml Dist.H x % Inhy % Treatment Treated J2 after 24 h Active J2 Inh z % Check treatment* 200.5 d Supernatant 257.4% reduction in egg-hatching and J2 activity.3 48. Effects of B. Inhibition y % = 100 – Relative hatch%.0 bc 8.6 74.7 65. subtilis isolates (2&3) and (4mg 71 .7 69. thuringiensis Isolates and Furadan®10G on egg-hatching and J2 activity of M.Journal of Life Sciences and Technologies Vol. followed by the same letter (s).5 1.8%) reductions in egg-hatching and J2 activity. viride filtrates showed 47. Treatments with sporulated bacterial cells and washed pellet showed the highest reduction than bacterial cell free-filtrates and supernatant treatments on nematode root galls and egg masses /plant for all B. cfu = No.6 bc Isolate 2 Sporulated cells 61. R.6 94.6 Treated J2 after 24 h Active J2 95. B. while treatments with (5× 105 cfu/ ml Dist. ARENARIA (MA) UNDER LABORATORY CONDITIONS Treated Eggs afte 24 h Hatched Eggs R. THURINGIENSIS ISOLATES ® AND FURADAN 10G ON M.2 bc ® Furadan 10G + MA 14. III RESULTS A.0a 268. subtilis.6 55. thuringiensis with (76. of active J2 in treatment 100.8 68.5 43.5 b Isolate 3 Sporulated cells 105. subtilis and B.9 Inh. % =Reduction%. EFFECTS OF TRICHODERMA FILTRATES AND FURADAN®10G ON EGG-HATCHING AND J2 ACTIVITY OF M. % 0.4 51. hamatum. Values of each column.5 a 510.7-57.8%) was achieved with Furadan®10G. Treatments with (5× 105 cfu/ml) of sporulated bacterial cells of B.9 b 65.5 32.05 of LSD test. ARENARIA (MA) ON TOMATO UNDER GREENHOUSE CONDITIONS Treatment Galls/ plant 516.3 e Furadan 10G+MA 100. Water + MA CDL= Czapek's Dox Liquid medium.3 30.6 48. arenaria compared with the check treatment (Table I). are not significantly different at P = 0.4 g B.4 35.1–96.0 67.1cd 76.0a 89.1 47.7-81.8 125. arenaria = 600 eggs and J2/pot. Treatments with (5× 105 cfu/pot) of sporulated bacterial cells of B.05 of LSD test.1 a Bacillus subtilis +MA Isolate 1 Sporulated cells 95.4 e R.z % 0. arenaria egg-hatching and J2 activity were presented in Table I.7 33.0 3. respectively.4 46.7 57. EFFECTS OF B. Nematode = 270 M.4 c Cell free-filtrates 102. thuringiensis isolates + MA 36.0 1.1b 80.4 51.Hx % 100. subtilis. arenaria eggs /treatment for hatching experiment & = 95 fresh J2/treatment for J2 activity experiment. Inhibitionz %= No.0a 123. followed by treatments with isolate 7N (4mg washed pellet /ml) of B.4 66.5 c Soto Washed Pellet Supernatant 112. B. of active J2 in check -No. TABLE I. followed by the same letter (s) are not significantly different at P = 0.8 showed considerable significant reductions ranged from 35. March 2013 significant difference (LSD) at the 5% level of probability.4 b 43. Effects of Trichoderma Filtrates on Egg-hatching and J2 Activity of M.5 53.4% in egg-hatching and J2 activity.3 73. thuringiensis Isolates and Furadan®10G on M.0 0.2 c 80.6 Legend.7 48.5g/pot) caused the greatest reduction 97.2 1. No. treatments with Trichoderma mixture filtrates caused (79. respectively.6-74.0 1.8 bc 94.2 80.7 53.0 98. water + MA CDL= Czapek's Dox Liquid medium.7 47.2 EM/ plant 509.1d 66.1 43. EM= Egg-masses NB medium = Nutrient Broth medium. viride + MA Mixture filtrates+MA Furadan®10G+MA TABLE III. B.4 b 45. B.8 b 6. of hatched J2 in check treatment100.5 18.3 46.3 45.4 a 509.8 76.3 52. ARENARIA (MA) UNDER LABORATORY CONDITIONS Treated Eggs After 24 h Treatment Hatched eggs 270. Inh.5 c 28.4 b 40. arenaria under Laboratory Conditions: The effects of Trichoderma filtrates and Furadan®10G on M. 1. of Sporulated bacterial cells units/ml.3 76.7 46.5 bc B. y %= Inhibition %.1 54.2 d 10.2 g Red .2 0.

egg-masses/plant and numbers of J2/250 cc soil were achieved with Furadan®10G (2.1 a B. thuringiensis isolate 7N and filtrates of T.2 42.4%) in the dry weight of shoot and root systems.8 54.0 0.2 60. egg-masses/plant and number of J2/250 cc soil compared to check treatments.1 c 14.9 73.5 bc Mixture filtrates 278. viride 534.0 a 915.05 of LSD test.3 2.8-59.4 99. subtilis. thuringiensis isolate 7N + MA Washed pellet 307.2c 581.7 a 22. ARENARIA (MA) ON TOMATO UNDER FIELD CONDITIONS Treatment Galls/ plant Red.6 c 14. treatments with washed pellet (4mg/pot) of B.0 70.0 a 3052. TRICHODERMA FILTRATES AND FURADAN®10G ON M. EM= Egg-masses.1 c 19.4 a 1880.7 47.5 a CDL medium+MA 1893. THURINGIENSIS.5 a 3011. subtilis + MA Isolate2 Sporulated cells Isolate3 Sporulated cells 7N + MA Washed pellet Trichoderma Filtrates +MA T. TRICHODERMA SPP.8 1. water + MA CDL= Czapek's Dox Liquid medium.6 69. subtilis isolates 2 & 3. Values of each column.9 c 25.9 a 37.Journal of Life Sciences and Technologies Vol. Meanwhile. Nematode = 1950 eggs and larvae /plant. % 0.0 1.6 67. SUBTILIS AND B. Microorganisms which grown in soil rhizosphere are ideal for use as biocontrol agents since rhizosphere of many plants provides front line defense for roots against attack by soil-borne pathogens [3]. March 2013 washed pellet/pot) of B.5 d Furadan®10G+MA 9. THURINGIENSIS ISOLATES. ISOLATE 7N OF B.9 85.2-67.6 81.8 c 15.9 a Inc.8 a 1875. No. harzianum 512. thuringiensis isolate TABLE IV.8 Check treatment* 1901. 1. thuringiensis isolate Soto showed significant reductions ranged from (66. % 0.5 e *=Dist.7 b 23.0 0.5g/plant) caused the greatest increase (60. Also. Data presented in Table V showed that treatment with the nematicide Furadan®10G (2.8 a Inc.7 86.2b 265. IV DISCUSSION Over the past twenty years a numerous studies have been undertaken to investigate the effects of using microorganisms (as biocontrol agents) and bioproducts in comparison with the nematicides against nematode pests TABLE V.3%. FILTRATES AND FURADAN®10G ON DRY WEIGHTS OF TOMATO INFECTED WITH M. D.4 c 4. treatments with the mixture filtrates of Trichoderma species.2 85.9 87.0 a 35.9 b 20.5 57.6%) in the number of nematode root galls.7 83. Trichoderma Filtrates and Furadan®10 G on M.8 51. SUBTILIS.4 3. harzianum and T.2 d Trichoderma filtrates+MA T. Red.8%) in the number of nematode root galls.0 0.4 b 24. Shoot DW* (g) 14.0 c 12.3 59. treatment with sporulated bacterial cells (5× 105 cfu/plant) of each B.6 e Red.2%) reductions in the number of nematode root galls.0 53.2 70.2 0.0 g Red.6 68.5g/plant).2 a 1879. % 0.1 a 554.0 f 7.7 99. bacterial cell free-filtrates and supernatant of all tested isolates caused considerable reductions (43.0 a T3 medium+ MA 1895.2 72.2-42.4%) nematode root galls and egg masses /plant.5 50. treatments with (5× 105 cfu/pot) of sporulated bacterial cells of B. % 0. followed by the same letter are not significantly different at P = 0.4 Root DW* (g) 11. subtilis isolate 1.2 e 500. Thuringiensis.0 1.1 70. as in Table IV.0 a 3004.2 b Isolate 3 576. followed by treatments with sporulated bacterial cells (5× 105 cfu/plant) of B.0 42.4 0. arenaria on Tomato Under Field Conditions Data presented in Table IV showed that the greatest reductions (99. Effects of Two Isolates of B.3b 379.8 b 25.6 a NB Medium + MA 1890. NB medium = Nutrient Broth medium. Isolate 7N of B.1de 251. viride each alone showed (68.5 0.8 b 26.3 61. subtilis isolates (2 & 3) and treatment with filtrates of T.5 1. 7N showed significant reductions ranged from (81.9 c 12. Data are averages of 5 replicates.2 53.4 a 34.7 0. EFFECTS OF B. 1.2d 960.5 EM/ plant 1884.6-73.5% increase in the dry weight of shoot and root systems compared to check treatment.0 d 513. viride alone showed great increases ranged from 47. Also. which caused 39.5 b 888.1 69.2 72 . eggmasses/plant and number of J2/250 cc soil.7 40.1 b B.4 c 12.2-55%) of nematode root galls and egg masses/plant compared to check treatments.2 c T.2 b 989.2-61. ARENARIA (MA) UNDER FIELD CONDITIONS Treatment Check treatment* CDL Medium+ MA NB Medium+ MA T3 Medium+ MA B.1 70.187.6 J2/250 cc soil 3056. [23]. harzianum or T. harzianum T. Meanwhile. % 0.7-82.1 99.6%) in number of nematode root galls and egg masses /plant. thuringiensis isolate 7N showed great reductions ranged from (76.3 o.1 71.5 b 576. [5] [13].5-99.0 b 31. viride Mixture filtrates Furadan®10G + MA Legend.0 a 29. Treatment with mixture filtrates of all Trichoderma species and washed pellet (4mg/kg soil) of B. washed pellet (4mg/kg soil) of B.6 a 30. [13].0 4. subtilis isolates (Sporulated cells)+ MA Isolate 2 568.5 39. [15]. % =Reduction%. EFFECTS OF TWO ISOLATES OF B.8 73.

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Egypt.03 Edition-6th SAS Institute Inc. Arab Society for Plant Protection.Alexandria – Egypt. Faculty of Agriculture.Journal of Life Sciences and Technologies Vol. University of Alexandria.D. Research interests: plant pathology. is a member in Egyptian Society of Plant Pathology. Dr. Dr. Egyptian Society of Agricultural Nematology. Her Educational background: B.Faculty of Science– Biology Department. Asmaa Abd El-Hamid Mokbel. Egypt.” Nematropica.20/April/1971. pp. Assistant Lecturer. Egyptian Society for Experimental Biology. Release 6. 1996 and Ph. She published more than 15 paper in the filed of plant nematology. Faculty of Agriculture. 2002.Sc. March 2013 meloidogyne incognita on bell pepper. pp. No. 31. University of Alexandria.Jazan University– Kingdom of Saudi Arabia. 1028. 1992. Egypt . [25] SAS Institute. nematology & microbiology. M. The scientific degrees: Demonstrator. She works now as an Associate Professor of Botany. Alexandria. 2001. in Plant Pathology (Nematology). Author’s formal photo 74 . in Plant Pathology (Nematology). 75-86. was born in Alexandria. Asmaa. Assistant Professor and Associate Professor of Plant Pathology. SAS/STAT User's Guide. 1.Sc. 1. vol. in Plant Pathology. North Carolina.. 1997. Journal of Agricultural Research .