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A New Method for Isolating and Selecting Agents with High Antagonistic Ability Against Plant Parasitic Nematodes
Tung-Tsuan Tsay1,3, Peichen Chen1 and Wen-Shi Wu2
Department of Plant Pathology, National Chung Hsing University, Taichung 402, Taiwan. Department of Plant Pathology and Microbiology, National Taiwan University, Taipei 106, Taiwan. 3 Corresponding author; E-mail: firstname.lastname@example.org; TEL: +886-4-22873791; FAX: +886-422876712 Accepted for publication: Jamuary, 18, 2006
Tsay, T. T., Chen P. C., and Wu, W. S. 2006. A new method for isolating and selecting agents with high antagonistic ability against plant parasitic nematodes. Plant Pathol. Bull. 15: 9-16. The conventional baiting, sprinkled plate method, modified baiting bags and a novel baiting tape method were compared for their efficacies of recovering different antagonists including fungi, bacteria, nematodes and mites. The baiting bag method had the highest isolation rates of nematodetrapping fungi and nematode parasitic bacterium Pasteuria penetrans, and was the only method capable of recovering predatory nematodes and mites. The novel baiting tape method had the lowest isolation rates of all the antagonists except actinomycetes. However, Arthrobotrys sp., Dactylaria sp. and Dactylella sp. baited by the baiting tape method had the best nematode-trapping activity and Streptomyces saraceticus, the highest chitinolytic activity in the in vitro assays. Isolates of the three nematode trapping fungi and S. saraceticus with the best antagonistic activities in vitro, along with Pasteuria penetrans and a predatory nematode Mononchus sp. were tested in the greenhouse experiments. All of these antagonists, except Mononchus sp., greatly reduced the number of J2 rootknot nematodes in soil and the egg masses on roots. P. penetrans and S. saraceticus had better controlling ability than the three nematode trapping fungi. The new baiting method has the ability to baite and select antagonists with high biocontrol efficacy. Key words: Antagonists, Arthrobotrys sp., baiting methods, biological control, Dactylaria sp., Dactylella sp., Mononchus sp., Pasteuria penetrans , plant parasitic nematodes, Streptomyces saraceticus
Antagonistic isolates from the same taxon differed markedly in general appearance, reflecting genetic differences which are invariably manifest as differences in their antagonistic abilities. This suggested that selection of the most virulent isolate from the material available must be one of the first steps in any biological control program (22).
Most early biological control researches were empirical and mainly concerning nematode-trapping fungi. Seventy six percents of researches on the natural enemies of plant parasitic nematodes were related to fungi, 5 % to bacteria and only 2 % to predatory mites. Few studies considered the fate of the organisms after it entered the soil, or the choice of target pests (10). Many antagonists isolated were,
. Culturable microorganisms on these plates were isolated again using a spread-plate technique to obtain pure cultures. dactyloides . A. and a new species Dactylella formosana. of which 23 species belong to the genera Arthrobotrys. were identified (5). oligospora . and then observed under a dissecting microscope (Olympus SZ60) to identify nematodes that were infected by fungi or other microorganisms. not effective when introduced to the field (13. Arthrobotrys cladodes . The plates were incubated at room temperature (approximately 23 ) in the dark for one week. Each infected nematode was transferred to a fresh 0. juveniles. Lin and Tsay (13) conducted a survey in 2003 and found Monacrosporium eudermata. M. In this paper.. ellipsosporum had the higher occurrence rates. Sampling methods were slightly different according to crop planted in the surveying field. and the plates were kept under the same condition for another five days. they tend to favor aggressive predacious fungi. none of the methods were able to isolate all antagonistic organisms from natural environments. including Dactylaria haptospora. (2) creating a baiting environment similar to natural habitats to ensure the antagonists would function when applied in fields. This is different from the survey done in Ireland that Dactylella bemicodes . because the factors required for optimal growth and predatory activities were different for every individual species (15). Up to date. Dactylaria. Pasteuria spp. mammillata and M.5 g of the soil sample was added into 1% corn meal agar plate containing 1. 22). Modified baiting bag method: A 20 g mixture of perlit: corn: coarsely chopped .7% PDA plate. hostspecific endoparasitic species (20). sprinkled plate method is the most common method employed to isolate potential nematode antagonists. A total of 120 zigzag spots was chosen in the vegetable crop fields and 60 spots in the fruit tree orchards (Table 1) to collect soil for the conventional baited. including Arthrobotrys cladodes . The questions of how to effectively isolate and select virulent antagonists are critical in developing biological control agents. Dacylella cionopaga-were found (24). and four of them. haptotyla.800 samples were coleected for analysis. a novel method following the three principles: (1) providing minimum artificial nutrients to select strong competitors.Dactylaria candidas . adults and cysts (18). Soil from parasitic nematode-infested fields was collected and air-dried till the water content was less than 10%. All experiments have been performed three times dating from 1995 to 1998 and approximately 3. three more species. sprinkled plate method and to place the baiting units for the baiting bag and baiting tape methods (see text below for preparation of the baiting units). A 0. A conventional method for direct observation and isolation was done by slide-adhered agar discs (1 cm diameter. D.7% PDA slants for future experiments. 0. actinomycetes. Monacrosporium and Nematoctonus. and three baiting methods were used independently in these six fields (Table 1) to compare their baiting efficacies for antagonists in different taxon. or predatory nematodes. After identification. and (3) observing the collected sample directly to understand the mechanism of the antagonist-was described in this manuscript. heavily sporulating and probably were over represented compared with slow-growing. which were fast-growing. In 1975.10 15 1 2006 isolation efficacies targeting at different antagonists and the antagonistic abilities of the baited antagonists by different methods were studied. sprinkled plate method: The method was modified from the previous procedure (3). Dactylella ellipsospora and Dactylaria sp. conoides . were first reported in Taiwan (26). Six fields were selected each for a unique target antagonist. the pure cultures of putative antagonists were maintained on 0.3 cm thickness) that were buried in soilcontaining Petri dishes for a period of time to attract antagonists (7) .500 Aphelenchoides besseyi. Conventional baited. This indicated that nematode trapping fungi were ubiquitous but the distribution pattern would be slightly different from place to place. therefore. The data collected from the three independent experiments were pulled together and the efficacy of each method was calculated by the proportion of samples containing the target antagonist. ellipsospoum had the comparable high occurrence rates among 11 species recovered. the MATERIALS AND METHODS Isolation of organisms antagonistic to plant parasitic nematodes A nationwide survey was launched to locate fields that had either nematode trapping fungi. The first report on plant parasitic nematode trapping fungi in Taiwan was published in 1964 (6) and six nematode trapping fungi. In light of this consideration. Monacrosporium coelobrocha. D. A. Nematoctonus robustus. A thorough sample collection from all geographic area in Taiwan was conducted in 1993 and a total of 27 species of nematode trapping fungi were identified. Over 200 species from 6 different classes of fungi were reported to parasitize on nematode eggs. Although such method have proved invaluable. A. Baited.
were selected as biological control agents (Table 1). Chitinolytic actinomycetes: Collodial chitin medium (14) was used to evaluate the chitinolytic ability of actinomycetes.5 g content from the center was taken and the putative antagonistic microorganisms were isolated using the conventional baited. the baits were retrieved and placed individually in a clean plastic bag. Streptomyces saraceticus that has the highest chitinolytic activity among the baited chitinolytic actinomycetes was selected as a biocontrol agent in the greenhouse experiments.8 cm width x 10 cm length. that produce adhesive net. Taiwan) using a clean paintbrush. The infected root systems were air-dried. The plates were incubated at room temperature for 48 hours and the nematode trapping rates were determined. respectively. the mixture was replaced with 20 g crab and shrimp shell pieces. Five discs with younger hyphae were punched out using a 0.7% PDA for a week and their conidia were washed out and adjusted to a concentration of 1x104 spores / ml for inoculation.. Pasteuria penetrans actinomycetes Mononchus sp. Four Pillar company. The fungi were cultured on 0. insects or predatory nematodes that prey on nematodes were located mainly on the periphery of the bag. the baiting tapes were observed directly. with the non-sticky side facing up. and each agar disc was transferred to the middle of a fresh 1% corn meal agar plate. Dactylaria spp. Chitinolytic activity was calculated by the width of the clear zone. under an upright microscope to look for deformed nematodes that were potentially infected by antagonists. The deformed nematodes were picked for the isolation of antagonists using the spread-plate technique. and Dactylaria sp. Greenhouse experiments for the biological control efficacy of six isolated antagonists Preparation of antagonists for inoculation: Three nematode-trapping fungi.. The baiting bags were opened under a dissecting microscope for inspection. Therefore. Mites. Field locality Tai Nan county Chang Hua county Chang Hua county Ping Tung county Hsing Chu county Nan Tow county Crop associated Sponge guard Eggplant Snow pea Banana Citrus Banana 11 Soil type Sandy clay loam Sandy clay Loamy sand Sandy loam Sandy loam Sandy loam peanut = 2:1:1 (w/w) was wrapped in a 50-mesh nylon cloth (Finnpeat®. Pasteuria penetrans that was found to parasitize Meloidogyne incognita on banana roots (Table 1) was collected. the original disc was removed and a 0. ground into powder. The number of endospores in the suspension were counted using the Hausser hemocytometer and adjusted to 80 endospores / ml for inoculation. 0.2 ml suspension of 200 Aphelenchoides besseyi was added in the middle. and re-suspended in distilled water to the final concentration of 20% (w/v). The novel baiting tape method: The baiting tape was made by brushing a 0. Each isolated actinomycetes strain was cultured on the Collodial chitin medium and incubated at 28 for five days. The corn meal and peanut powder mixture were substituted by crab and shrimp shell powders to bait for chitinolytic actinomycetes in the field at Hsing Chu County. sprinkled plate method. Dactylella sp. Netherlands) as a baiting bag. The baits in annual crop fields were retrieved two weeks later.New method for isolating microorganisms antagonistic to phytonematodes Table 1. and in perennial plant fields one month later. Data were obtained from five replicates and the experiment was repeated three times. Kekkila. Streptomyces saraceticus was In vitro e v a l u a t i o n o f t h e a n t a g o n i s t i c a c t i v i t i e s of baited antagonists Nematode trapping fungi: Isolated nematode trapping fungi were cultured on . The baiting bags were buried into soil at the depth of 5-20 cm near the nematode-infested rhizoshpere. One week later..4 g mixture of corn meal and peanut powder (volume ratio = 1:1) evenly onto the sticky side of a clear tape (4. The baiting tape was stapled with a cloth labeled with date. and crop species on it and buried vertically at the depth of 5-20 cm near infested rhizosphere with the baiting mixture facing roots. After removing soil particles from the non-sticky side. For baiting chitinolytic actinomycetes. When the new colony reached 4 cm in diameter. Information of six fields used for isolating specific antagonists Antagonism Arthrobotrys spp.7% PDA for a week. Dactylella spp. Arthrobotrys sp. and adhesive knob. 0.8 cm-diameter cork borer. location. constricting ring.
The data were analyzed by Duncan's Multiple Range test (P = 0. All treatments had five replicates and the experiment was conducted twice. sprinkle plate method and 85. Known-You Co. free-living nematodes ( Rhabditis sp. Two hundreds Mononchus sp.5% (Table 2).A. while the baiting tape method had only 17. actinomycetes had the highest isolation rates regardless of the isolating methods. Inoculations and plant bioassays: In the first part of the bioassay. saraceticus at the described ratio.3%-24. were put into a 250 ml flask containing 50 g moist coarsely chopped peanuts and incubated at room temperature for two weeks. For instance. A treatment without any antagonists was also included as the control treatment. Plants were fertilized with 10 ml Hyponex® soluble fertilizer (N: P: K= 20: 20: 20. The sterile soil has a pH value of 5. Kaohsiung. or 500 Mononchus sp. U. 12 cm in height) that contained 1 L soil in each pot for the following experiments. The experiments were conducted in a greenhouse to 36 .6% isolation rates of the three nematode trapping fungi. It was identified by the perineal patterns and juvenile morphomatric data (9). Meloidogyne incognita as the pathogen inoculums was collected from banana rhizosphere in Kaohsiung County.8% of organic matter. 931. the potting soil used in greenhouse tests was obtained from a grape orchard (Chang Hua county. and the rest existed in a minute amount. Taiwan) was chosen as the experimental host because of its high susceptibility to Meloidogyne incognita and apparent gall formation (25). RESULTS Comparison of different baiting methods In a preliminary survey. 15 lb) for one hour to eliminate biological factors. Horsham. All three methods had high isolation rates (89. and Dactylaria spp. for inoculation. using the baiting bag method Arthrobotrys spp. The baiting tape coated with corn and peanut powder had only 3.05% Tween 20. The spores were counted using hemacytometer (Hausser Scientific.8% samples from Chang Hua County.. 100 ml of Arthrobotrys spp.) were provided as the food source. by sucrose gradient centrifugation and floatationsieving technique (2. PA. nematodes and 2..).9 and contains 0. the soil samples were obtained a month post inoculation for M.12 15 1 2006 plastic pot. Dactylella spp. penetrans . The isolation rate for each antagonist shown in Table 2 was the percentage of the samples pooled from the three experiments conducted in the same field. The fresh weight (in grams) of the water spinach aerial parts was recorded as the plant yield. the modified baiting bag method had 74..5% isolation rate for Pasteuria penetrans. The second-staged juveniles (J2) hatched from a single egg mass were used to inoculate water spinach roots. Dactylaria spp. To culture the predatory Mononchus sp. Taiwan) and autoclaved (121 . peanut powder. M. Taiwan. was first grown in a mixture containing equal volumes of perlit. grown in liquid collodial chitin medium with shaking (85 rpm) at room temperature for three days. were added into the pots.2%) for chitinolytic actinomycetes (Table 2). S.05% bleach (NaOCl) for 30 minutes and rinsed with water. The disease severity was evaluated by the number of M. the concentration was adjusted to 1 x 107 spores / ml by adding desterilized water with 0. Experimental design: To provide a testing environment similar to the field conditions. Among the three baiting methods. Meloidogyne incognita was inoculated at the concentration of one J2 per gram soil when the water spinach was transplanted to the . Rhabditis sp. we found that the presence of antagonistic microorganisms was regional specific. incognita.000 Rhabditis sp.S. P. 4). incognita egg masses on the root system and the number of J2 per 200 g randomly sampled pot soil. were found in 74.. After one month.5%-95.6% samples collected from Tai Nan County. whereas the baiting bag method was the only method that isolated predatory nematodes and mites.05). The bacterial filaments were removed by passing the culture through double cheese cloth and the spores were collected in a clean beaker. Sterile seeds were sown in moist peat moss till five-leaf stage and transplanted to plastic pots (14 cm in diameter. was then collected by modified Baermann's funnel technique and separated from Rhabditis sp. and the egg masses collected from a single plant were used for the inoculation. Seeds were sterilized by immersing in 1.05% of Tween 20 was added to help the spores suspending in the solution. and were 20 days after the co-inoculation in the second part of the bioassay. weredetected in 85. incognita and the six antagonists were inoculated together at the time of transplanting. a with the temperature ranging from 18 photoperiod of 12 hours and relative humidity of 78%95%. In the first part of the bioassay. and soybean powder to get large quantity.5% for the baiting bag methods. Among the antagonists. 1 g / L) every week. Mononchus sp. which was very low compared to the 82% for the baited.8%-85. For the second part of the bioassay. Water spinach ( Ipomea reptans cv.. 0. Only one antagonist species was dominant and had the highest recovery rate at each site.
the fresh top weights of water spinach treated with P. penetrans and S. The strains of chitinolytic actinomycetes isolated by the baiting tape method were capable of utilizing chitin and produced clear zones with an average radius of 0. The Arthrobotrys spp. heavier than these treated with other antagonists.6 a 0. 37 of Dactylaria spp. 34 commonly found isolates of Arthrobotrys spp. When antagonists were applied after the establishment of root knot nematodes.6 b 38.0 b 38. which reduced egg masses number from 207. Means in the same row followed by the same letter were not significantly different (P = 0. respectively. Comparison of antagonistic activity of three nematode trapping fungi and a chytinolytic actinomycete isolated by sprinkle plate. 42 of Dactylella spp. one isolate from each antagonist taxon that showed the highest antagonistic activity was selected for the greenhouse experiments. isolates baited by the baiting tape method had the average nematode-trapping rates of 62. penetrans and S.New method for isolating microorganisms antagonistic to phytonematodes 13 Antagonistic ability of organisms baited by different methods The three baiting methods resulted in thousands of putative antagonists identified based on morphological characteristics..5 g and 99. Based on the in vitro antagonistic activity assays.9% and 47.0 a 89.3 a 82..6 a 81.1 and 83. Among the five microorganisms.2 g respectively. and Dactylella spp.05) according to Duncan's multiple range test. all but Mononchus spp. was chosen because it was found in all three baiting methods and showed the highest chitinolytic activity. which was significantly larger than the radius produced by the strains of the baiting bag method (Table 3).5 b 95.6 ab Antagonistic activity Baiting bag 42.05) according to Duncan's multiple range test. a chitinolytic actinomycete.6 Baiting tape 24.8 a 2 3 Activity of predatory fungi was estimated by the percentage of nematodes trapped out of 200 nematodes. when the antagonists and M. Similarly.9 a 47.05) (Table 4).3%. .2 b 0. NA: data not anailable.8 cm on the collodial chitin media. Mites 1 2 Sprinkle plate 86. 1 Dactylella sp.2 a2 74. The results indicated that the baiting tape method was able to bait for microorganisms that had high antagonistic abilities. Pasteuria penetrans actinomycetes Mononchus sp. 1 Dactylaria sp. Means in the same row followed by the same letter are not significantly different (P = 0.5 a NA3 NA Isolation rate (%)1 Baiting bag 85. saraceticus were 98.4 b 0.3 c 20.3 a 58.7 b 34. respectively (Table 3).3. baiting bag and baiting tape methods Antagonistic organisms Arthrobotrys sp. Dactylaria spp..5 and 122. The efficacy of the six antagonists as biological control agents under greenhouse conditions Streptomyces saraceticus. incognita were inoculated at the same time.6. For the growth of the host plants.5 b3 42. which were the highest among the three methods. saraceticus had the best antagonistic abilities.5 b Baiting tape 62. Activity of Streptomyces saraceticus was determined by the radius of the clear zone (cm) on collodial medium. and J2 nematodes in 200 g soil from 425 to 136.1 b 3. data were means of 5 replicates. 1 Streptomyces saraceticus2 1 Sprinkle plate 4. significantly decreased the number of J2 root knot nematodes in soil and egg masses on roots (P = 0.6%. incognita population and Table 2. respectively. all antagonists except Mononchus spp.3 a 93.8 a 85. 58.1 a 74. Dactylella spp.5 b 17. baiting bag and baiting tape methods on recovering specific organisms antagonistic to nematodes Antagonistic organism Arthrobotrys spp.8 24. even though the isolation rates were low (Table 2). significantly reduced the M. Isolation rates of sprinkled plate.8 to 90.2 a NA NA 3 Percentage of valid baiting units containing the target antagonist baited from the field soil. Data were means of 50 replicates. To compare the antagonistic ability of the same taxon baited by different methods.8 b 69. and 30 of chitinolytic actinomycetes isolates were studied.5 a 92. Dactylaria spp. Table 3. P.
0 a 40. microorganisms that were able to colonize the substance in the baiting bag or on the baiting tape would increased the top weight of the water spinach (P = 0. and direct observation for picking the active microorganisms.0 b 98. or animal feeding activities. Effect of antagonistic organisms to nematodes as a protecting agent on the growth of water spinach and the population of Meloidogyne incognita Antagonism Arthrobotrys sp.0 c 35.6 b 203.8 b 30.0 a 88.3 b 63.4 b 62. 15). Presumably.2 a 90.0 c # of egg mass 65.2 c 89. Dactylaria sp. The conventional method baited antagonists by taking the field soil away and then providing artificial nutrient to microorganisms under controlled environments.5 a 99. This would favor the fast-growing and heavily sporulating microorganisms (20). flooding.2 a 48. Pasteuria penetrans Streptomyces saraceticus Mononchus sp. Dactylella sp. Dactylaria sp. Pasteuria penetrans Streptomyces saraceticus Mononchus sp. Check 1 Plant top weight (g) 60. which may lead to mis-presentation of data.0 c 47. Due to the climate changes. Another environmental factor that might jeopardize the baiting efficiency in this study was the dynamic interactions among soil microorganisms. the recovery rates of the Table 4. incognita either before or after they invaded the host.5 c # of egg mass 199. Results of this study show that the novel baiting tape method with these principles did elevate the opportunity for isolating antagonists that have better qualities as biological control agents.4 b 60. This might explain the high antagonistic ability of those baited with this method. One of the questions this study tried to answer was whether the antagonists baited by different methods would have different antagonistic abilities (21).0 b 136.05) according to Duncan's multiple range test. Baiting bags containing rich substance were buried near the rhizosphere. These five antagonists tested were able to reduce the population of M.9 bc 30. Our results showed that antagonists belonging to the same taxon baited by the novel baiting tape method had significantly higher antagonistic efficacies compared to those baited by other two methods (Table 3). only microorganisms that had fast colonizing and utilizing ability would be able to compete for the substrate. Check 1 Plant top weight (g) 27.5 b 37. Prolonging the baiting time by increasing the amount of baiting substance would also help to select antagonists with better competition ability.0 c 19. .4 b 333.0 b1 28.0 a Means in the same column followed by the same letter were not significantly different (P = 0.5 b 328.7 b1 63.1 b 37. Some baiting units were lost due to heavy rains.8 a # of J2/200g soil 364. the three nematode trapping fungi. such design would allow primary colonizers to compete and interact.1 b 83. The baiting tape method provided very limited nutrient.2 c 40. Effect of six antagonistic organisms to nematodes as biological control agents on the growth of water spinach and the population of Meloidogyne incognita Antagonism Arthrobotrys sp. Nutrients in the agar plate might not be sufficient to revive dormant spores which had good antagonistic ability. These problems were overcome by starting with many baiting units at the beginning of the experiments. and S.14 15 1 2006 baiting units were not 100%. Therefore.05) (Table 5). penetrans.2 a 174. DISCUSSION Three principles proposed for designing a novel baiting method are minimum artificial nutrient provided. saraceticus that showed high in vitro antagonistic activities were proved to be effective biological control agents in the greenhouse experiments.5 bc 21. Fungistatic factors that prevent fungal spores from germination are prevailing in the soil (11. P.5 a # of J2/200g soil 28.4 b 27.5 c 122.0 a 180. baiting environment similar to natural habitats. Table 5.05) according to Duncan's multiple range test.5 a Means in the same column followed by the same letter were not significantly different (P = 0.5 a 20.6 a 425.5 a 36.5 a 207. Those microorganisms isolated would have a better chance to survive and perform the desired antagonistic ability.6 c 22. Dactylella sp.3 c 443.
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