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Received: 16 August 2008 Revised: 28 January 2009 Accepted: 30 January 2009 Published online in Wiley Interscience: 8 May 2009
(www.interscience.wiley.com) DOI 10.1002/ps.1777
Biocontrol of Meloidogyne incognita on tomato using antagonistic fungi, plant-growth-promoting rhizobacteria and cattle manure
Zaki A Siddiquia,b ∗ and Kazuyoshi Futaib
BACKGROUND: Biocontrol achieved by a single biocontrol agent is generally inconsistent under ﬁeld conditions. The aim of the present study was to increase the competitiveness and efﬁcacy of biocontrol agents by using them together with cattle manure. RESULTS: The effects of antagonistic fungi [Aspergillus niger v. Teigh., Paecilomyces lilacinus (Thom) Samson and Penicillium chrysogenum Thom] and plant-growth-promoting rhizobacteria (PGPR) [Azotobacter chroococcum Beijer., Bacillus subtilis (Ehrenberg) Cohn and Pseudomonas putida (Trev.) Mig.] were assessed with cattle manure on the growth of tomato and on the reproduction of Meloidogyne incognita (Kof. & White) Chitwood. Application of antagonistic fungi and PGPR alone and in combination with cattle manure resulted in a signiﬁcant increase in the growth of nematode-inoculated plants. The highest increase (79%) in the growth of nematode-inoculated plants was observed when P. putida was used with cattle manure, followed by use of P. lilacinus plus cattle manure. Paecilomyces lilacinus resulted in a high reduction in galling and nematode multiplication, followed by P. putida, B. subtilis, A. niger, A. chroococcum and P. chrysogenum. The combined use of P. lilacinus with cattle manure resulted in a maximum reduction in galling and nematode multiplication. CONCLUSION: Application of P. lilacinus or P. putida with cattle manure was useful to achieve greater biocontrol of M. incognita on tomato. c 2009 Society of Chemical Industry Keywords: antagonistic fungi; biocontrol; cattle manure; nematode; PGPR; Solanum lycopersicum
Tomato, Solanum lycopersicum L., is an important vegetable crop, and its cultivation is worldwide. Yield loss due to root-knot nematodes (Meloidogyne spp.) on tomato range from 40 to 46% in India.1,2 Plants infected with Meloidogyne spp. show typical symptoms of root galling. Some infected plants exhibit deﬁciency symptoms, particularly nitrogen.3 This disease has become a major constraint to the successful cultivation of tomato in India.4 Rhizosphere microorganisms provide an initial barrier against pathogen attack on the root.5 The rhizosphere organisms, antagonistic fungi, have a great potential against plant pathogens.6 The fungus Paecilomyces lilacinus (Thom) Samson is primarily a saprophyte, infecting the eggs and females of root-knot nematodes and destroying the embryo within 5 days,7 and it is a successful biocontrol agent under various conditions.8 The commercial product MeloCon WG (Prophyta GmbH, Germany) of P. lilacinus strain 251 is successfully used for the control of nematodes.9 Aspergillus and Penicillium are common genera occurring in most agricultural ﬁelds of India. Aspergillus species are known to produce a variety of secondary metabolites and have shown biocontrol potential against plant-parasitic nematodes.10 Similarly, Penicillium spp. are also useful as antagonists of nematodes.11 On the other hand, plant-growth-promoting rhizobacteria (PGPR) may
impart beneﬁcial effects on plants. PGPR enhance plant emergence, colonise roots and stimulate overall plant growth, and also improve seed germination, root development, nutrient uptake, water utilisation and plant health.12 The management of the crop rhizosphere with PGPR towards enhanced biocontrol of plant pathogens has shown considerable promise.12,13 Organic manure may suppress plant-parasitic nematodes and improve crop tolerance.14 Nematode-infected plants generally show foliar symptoms of nutrient deﬁciency,3,15 and application of manures may inﬂuence nematode development and reproduction.4,16,17 Composted cattle manure is commonly available and used by the farmers in India. Although this manure has been found to be less effective than other manures in reducing galling and nematode multiplication in chickpea,18 it still provides a good source of nutrients for rhizosphere microorganisms.
Correspondence to: Zaki A Siddiqui, Department of Botany, Aligarh Muslim University, Aligarh 202002, India. E-mail: zaki email@example.com
a Department of Botany, Aligarh Muslim University, Aligarh 202002, India b Graduate School of Agriculture, Kyoto University, Kyoto, Sakyo-ku 606-8502, Japan
Pest Manag Sci 2009; 65: 943–948
c 2009 Society of Chemical Industry
and post-effects with other treatments. while a signiﬁcant difference between rows (between no manure and cattle manure) is shown by ∗ . The aim of the present study was to increase the efﬁcacy of PGPR and antagonistic fungi for the biocontrol of nematodes by using them in combination with cattle manure. The inoculum suspensions were poured or placed around the roots.19 This may sometimes account for inconsistent performance because a single agent is not active in all soil environments or against all pathogens that attack the host plant.6 a∗ 77.1 g mycelia mL−1 ). Teigh.2 ef∗ 73. a single biocontrol agent is used to control a single pathogen. Aligarh. chroococcum. India. the inoculum was further multiplied on a few other eggplants. Treatments were 2000 freshly hatched J2 of M. subtilis and P. Seeds were sown in seedling trays and transplanted. Mumbai. Bacillus subtilis (Ehrenberg) cohn and Pseudomonas putida (Trev.9 b 73.. lilacinus P.1 bc∗ 59. Aligarh.5 d 56. which had been lined with cross-layered tissue paper.2 c 55. These fungi were found to have antagonistic potential against the tested nematode. and the soil was replaced.2 Nematode inoculum Meloidogyne incognita was collected from tomato ﬁeld soil and multiplied on eggplant (Solanum melongena L.2 a 71.1% sodium hypochlorite for 2 min and then washed 3 times with distilled water.18 The rhizosphere harbours a variety of microorganisms including bacteria. K Futai Table 1. P. Aspergillus niger v.2 cd∗ 78. Two days after transplanting.1 Preparation of soil Sandy loam soil (pH 7. incognita in a preliminary test in ice cream cups. Water was poured into each bag to wet the soil before transferring them to an autoclave for sterilisation at 137.7 def∗ 68.4 Manure preparation A quantity of 10 g of composted cattle manure was added. On the other hand. but here it was added at the time when nematodes.4 a 71. seedlings were inoculated with the treatments. subtilis P. & White) Chitwood. These isolates were designated as A.) using a single egg mass. cattle manure (10 g).www.6c d 58. was added to jute bags.4 a 72. and 10 L water was added after mixing. 65: 943–948 944 www. uninoculated plants served as a control. Two thousand hatched second-stage juveniles (J2 ) in 10 mL water were applied to each plant as described below. India) incubated at 37 ± 2 ◦ C for 72 h. A. chrysogenum. India).4 bc∗ 79. chroococcum Control A. P. PGPR (A.5 × 107 cells mL−1 ) was used as inoculum per plant. ZA Siddiqui. An equal volume of sterile water was added to control treatments. chrysogenum B.4 g∗ 70. subtilis P. Pest Manag Sci 2009.5 × 107 bacterial cells mL−1 ). A quantity of 10 mL of the suspension (1.interscience.5 ab∗ 75.2) collected from the ﬁeld of the Department of Botany. chroococcum No manure 65. chrysogenum CAI (CAI = Chherat Aligarh. putida A.9 cd Cattle manure 68. 2. India. 2. For inoculation of M.5 Experimental set-up Seeds of tomato variety K-25 were surface sterilised in 0. The effects of these fungi were tested on the hatching and penetration of M. putida) were obtained from the Microbial Type Culture Collection and Gene Bank. putida A. one seedling per pot.3 f∗ With nematode a 2 MATERIALS AND METHODS Data followed by different letters within one column are signiﬁcantly different at P = 0. niger. A quantity of 100 g of mycelium from each was macerated in 1000 mL distilled water. The manure was mixed at 10 day intervals. Cattle manure is generally added to the soil before planting the crop.4 ab∗ 80.9 de∗ 69. Institute of Microbial Technology. India.3 cd 58.5 e 56. 1 g antagonistic fungus (10 mL at 0. were isolated from the rhizosphere of tomatoes grown at a ﬁeld near Chherat. niger P.3 Biocontrol agent preparation Three fungi.) Mig.soci. this contained about 30 mg N.7 a 73. antagonistic fungi and cattle manure. fungi and arbuscular mycorrhizal (AM) fungi. 4. niger P. These antagonistic fungi were separately cultured on Richard’s liquid medium for 15 days. Aligarh Muslim University.com/journal/ps c 2009 Society of Chemical Industry . incognita. niger CAI.org In most studies. PGPR and antagonistic fungi were inoculated in order to avoid pre. and were therefore selected for the present study. incognita (10 mL nematode suspension with 200 juveniles mL−1 ). lilacinus CAI and P. Three antagonistic fungi (Paecilomyces lilacinus (Thom) Samson. 2.20 Mycelia mats of each were collected separately on blotting paper to absorb excess of water and nutrients. AMU Aligarh.5 a 42. and prior to use had been allowed to decompose in a 50 L plastic drum for 1 year. and Penicillium chrysogenum Thom) and the same number of PGPR species [Azotobacter chroococcum Beijer. Egg masses from the roots of these plants were hand picked using sterilised forceps and placed in 9 cm diameter sieves of 1 mm pore size. PGPR (10 mL at 1.7 f∗ 77.05. 2. The sieves were placed in petri dishes with distilled water for hatching and incubated at 27 ◦ C.4 mg K. and 10 mL of this suspension containing 1 g fungus was used as inoculum per plant.9 kPa for 20 min. Department of Botany.6 a 71.] were tested alone and together with cattle manure for their effect on the growth of tomato and on the reproduction of the root-knot nematode Meloidogyne incognita (Kof. 2 weeks after germination. After 3 months. B.7 c 54. Chandigarh. Pure cultures of these fungi were stored in the Mycology Laboratory.wiley. Sterilised soil was allowed to cool to room temperature before ﬁlling 15 cm diameter clay pots with 1 kg of sterilised soil. Cattle dung was collected from local farmers. combining biocontrol agents with organic manures might improve biocontrol efﬁcacy because manures generally facilitate multiplication and establishment of biocontrol agents in the rhizosphere.4 mg P and 8. A quantity of 10 g of composted cattle manure was added to the treatments (see Table 1).2 f∗ 72. PGPR. PGPR were grown on nutrient broth (HiMedia Laboratories. lilacinus P.5 f∗ 72. Seedlings were placed in a greenhouse and watered as needed. the soil around the root was carefully removed without damaging the roots. Effects of biocontrol agents and cattle manure on the length (cm) of tomato plants inoculated with Meloidogyne incognita and uninoculated plantsa Treatment Without nematode Control A. chrysogenum B. as shown in Table 1. 2. India. lilacinus and P.
Similarly.20 f Cattle manure 20.21 For estimating the numbers of eggs.86 i∗ 19.93 d 20. followed by B. Graphs for galling and nematode population were prepared using SigmaPlot and error bars showing standard error. chroococcum No manure 17.4% increase in shoot dry weight. chrysogenum. These four treatments were tested alone and together with cattle manure (4 × 2 = 8 treatments). putida (37. subtilis. subtilis P.7%) and A.3%) and P. and the experiment was repeated once. lilacinus resulted in a 37. Use of P. On the other hand. and 0. lilacinus. percentage root colonisation and nematode population.96 e 14. chroococcum. Antagonistic fungi were re-isolated from nematode eggs and females to determine percentage infection in the remaining population. Integration of P. Data obtained were analysed statistically by analysis of variance Pest Manag Sci 2009.2%). putida. in ﬁve replicates. These 14 treatments were tested both in the presence and in the absence of M.6 Plant parameters and nematode quantiﬁcation The plants were harvested 90 days after inoculation.com/journal/ps . shoot dry mass.1%).9%).42 f 15. subtilis (33.02 g∗ 18.92 g∗ 20. incognita (14 × 2 = 28 treatments). niger (33. chroococcum.4%). Moreover. putida with cattle manure resulted in the highest increase (23. (3) B. lilacinus P. (4) P.75 c 19. chrysogenum (28.9%) of nematodeinoculated plants among combined treatments (Table 2).1% mercuric chloride for 2 min.soci. The roots of one treatment were cut into small pieces. putida. Cary. chrysogenum with cattle manure was the least effective in increasing growth (62.Biocontrol of M. 2.85 c 20. application of P. Subsamples (1 g) of roots from the different treatments. and plants were grown as described in Section 2. juveniles and females inside the roots.1% sodium hypochlorite and washed with sterilised water. subtilis. A. subtilis P.9%).05) was then used to distinguish differences between treatments. All these analyses were performed by computer software Stat View 5. Application of A. Colonies of rhizobacteria falling within 30–300 colony-forming units (CFU) on a petri dish were selected and multiplied by a reciprocal dilution factor to obtain the bacterial colony number22 and represented as CFU g−1 root. lilacinus P.7% increase in shoot dry weight over the uninoculated control. A 250 g subsample of well-mixed soil from each treatment was processed by Cobb’s sieving and decanting method. (6) B. chrysogenum (10. The plates were placed on a Quebec colony counter for counting the bacterial colonies. Effects of biocontrol agents and cattle manure on the shoot dry weight (g) of tomato plants inoculated with Meloidogyne incognita and uninoculated plantsa Treatment Without nematode Control A. lilacinus (11. compared with the control. chroococcum Control A. (5) A. Data of both experiments were almost similar.0 (SAS Institute. niger P. were taken from the homogeneous mixtures and crushed separately in sterile normal saline solution (NSS). and counts were made on the suspensions thus obtained.32 cd∗ 21. Each of the 28 treatments was replicated 5 times (28 × 5 = 140 pots).42 j∗ 19. The number of nematodes in roots was calculated by multiplying the number of nematodes in 1 g of root by the total root mass. The nematode eggs and females were collected from roots obtained by macerating the latter in a Waring blender as described above.44 h∗ 20. B. followed by P. roots of different treatments were cut separately into small pieces.1% increase in shoot dry weight. niger.8 Statistical analysis The biocontrol agents were tested in a 2 × 2 factorial design. Data were recorded on plant length. lilacinus plus cattle manure (72. (P = 0. 2.3%). were collected from well-mixed homogeneous mixtures and macerated separately in a Waring blender. incognita The experiment was set up in a completely randomised block design with seven experimental variables: (1) control.05). and this paper presents pooled data of both experiments. Application of antagonistic fungi and PGPR alone or in combination with cattle manure to plants with and without nematodes resulted in a signiﬁcant increase in the growth of tomato over the uninoculated and nematodeinoculated controls (Tables 1 and 2).78 c 11. Subsamples (1 g).93 e 15. These seven treatments were tested alone and together with cattle manure (7 × 2 = 14 treatments).93 ab∗ 20. with ﬁve replicates. eggs and females were surface sterilised with 0. except for the interactions of all three factors on plant length. number of galls. fungus growth was identiﬁed and counted. washed 3 times in distilled water and placed on potato dextrose agar medium.88 e 15.93 bc 19. Use of cattle manure on plants without nematodes resulted in a 14. NC).wiley. niger to plants without nematodes resulted in a 13. putida A. putida A. putida to plants without nematodes resulted in a 13. 945 c 2009 Society of Chemical Industry www. Tomato roots inoculated with PGPR were collected 1 month after sowing.org Table 2.12 hi∗ With nematode a Data followed by different letters within one column are signiﬁcantly different at P = 0. Tukey’s test (P = 0.interscience.7 Biocontrol agent quantiﬁcation A separate experiment to determine root colonisation by PGRP was conducted. The combined use of P. (2) A.58 g 15.56 f∗ 21.96 e∗ 21.24 d∗ 16. A.45 f 15. These eight treatments were tested both in the presence and in the absence of M.9%) in shoot dry weight of plants without nematodes (Table 2). niger P. chroococcum (10. chroococcum (31. (7) P. biocontrol agents and cattle manure individually and their interactions were signiﬁcant at P = 0. 65: 943–948 www. chrysogenum B. 2.28 ab 19. (2) A.1 mL serially diluted extracts were plated on nutrient agar plates and incubated at 37 ◦ C for 24 h.2%) and P. For re-isolation. incognita (8 × 2 = 16 treatments). followed by Baermann’s funnel extraction to determine the nematode population.8% increase in shoot dry weight of nematode-inoculated plants.76 ef∗ 19. subtilis (10.05. After 1 week of incubation at 25 ◦ C. 3 RESULTS Effects of nematodes. (4) P. addition of cattle manure resulted in a 42% increase in the growth of nematodeinoculated plants.05 both on plant length and shoot dry weight. use of P. (3) P.2%).65 bc∗ 22.3%) in shoot dry weight of nematode-inoculated plants.22 a∗ 21. while a signiﬁcant difference between rows (between no manure and cattle manure) is shown by ∗ .5. The experiment was set up in a completely randomised blocked design with four experimental variables: (1) control. followed by P. chrysogenum B. Roots were surface sterilised in 0. putida with cattle manure resulted in the highest increase (79. compared with the control (Table 2). Each of the 16 treatments was replicated 5 times (16 × 5 = 80 pots). followed by P.34 a 19.
lilacinus P. incognita eggs and females by P.5 × 105 d 1. chrysogenum was applied with cattle manure (Fig.9 × 105 e 2.5.1 × 105 a∗ 4 DISCUSSION With nematode Data followed by different letters within one column are signiﬁcantly different at P = 0. growth-promoting hormones. Re-isolation of fungal biocontrol agents from females and eggs of Meloidogyne incognita obtained from plants inoculated with cattle manure and uninoculated plantsa Re-isolation of antagonistic fungi Treatment No manure Control A. niger. nicotinic acid.46.3 × 105 cd 2.com/journal/ps c 2009 Society of Chemical Industry . IAA and siderophores. Aspergillus and Penicillium inhibit egg hatch.05. Colonisation of roots by PGPR was increased in the presence of cattle manure but reduced in the presence of nematodes.42. producing biologically active substances. chrysogenum Control A. Colonisation of tomato roots by rhizobacteria in the presence and absence of cattle manure in nematode inoculated and uninoculated plantsa Treatment Without nematode Control B. biotin.44 Similarly.11 Results revealed that P. maximum reduction (73%) in galling and nematode multiplication was observed when P. The effects of biocontrol agents and cattle manure individually and their interactions on root galling and nematode multiplication were signiﬁcant at P = 0. Paecilomyces lilacinus parasitised eggs of M. A.12. a Table 4. the enzymatic disintegration of vitelline and chitin layers might have increased the permeability of eggshell and enhanced the mycelial penetration.05.45 and has an ability to produce antipathogenic substances. pantothenic acid. Application of P. Similar parasitism by P. putida performed better than the other two species of PGPR because of its ability to produce greater HCN. while females were parasitised at the anus. lilacinus resulted in reduced nematode multiplication. indicating their inability to parasitise the nematodes. chroococcum forms considerable quantities of biologically active substances such as vitamins of the B group. while interaction of nematodes and cattle manure was non-signiﬁcant. chrysogenum. while a signiﬁcant difference between rows (between no manure and cattle manure) is shown by ∗ . lilacinus was used with cattle manure. this bacterium improved plant growth by inhibiting non-parasitic root pathogens.38 Generally. The effect of cattle manure on the re-isolation of antagonistic fungi from females and eggs of nematodes was non-signiﬁcant. subtilis increased the yields of several crops.37 In a previous study. and minimum reduction when P. chrysogenum females – 3c 42 b 4c – 5c 47 a 6c eggs – 1b 75 a 2b – 2b 79 a 4b Cattle manure a Data followed by different letters within one column are signiﬁcantly different at P = 0. chroococcum (Table 3). P. Inoculation of antagonistic fungi and PGPR alone and together with cattle manure resulted in a signiﬁcant reduction in galling and nematode multiplication (Fig. siderophores and HCN. putida resulted in greater root colonisation than the other two PGPR tested. including HCN and siderophores. They can also solubilise phosphorus. which suggests the involvement of mechanisms other than parasitism. putida A. resulting in improved growth of nematode-inoculated plants. lilacinus resulted in high reduction in galling and nematode multiplication. a non-cellular extract of B.wiley. The parasitism on M.niger may be attributed to its ability to produce a variety of secondary metabolites. subtilis. leading to total disintegration of the egg contents.1 × 105 d∗ 2. Only parasitism of nematode females by P.40.43 Additionally.5 × 105 b∗ – 2. chroococcum No manure – 2. lilacinus was increased in the presence of cattle manure (Table 4). chroococcum and P. various secondary metabolites secreted by Pseudomonas spp. niger P. subtilis P. Nutrient broth itself does have some nutrients.35 Moreover. and are known to produce a variety of secondary metabolites. niger P. followed by B. P. have inhibitory effects against different phytopathogens. chroococcum Control B. 65: 943–948 946 www. Improvement in growth may be attributed to the inhibitory effect of B.30 – 32 Pseudomonads may also improve plant growth by suppressing parasitic and non-parasitic root pathogens33 through the production of biologically active substances34 or the conversion of unavailable minerals and organic compounds into forms available to plants.41 Previous studies indicated that treatments with B. A.interscience. In combined treatments. 1).47 PGPR were cultured in nutrient broth.4 × 105 e∗ 2. some may be left in the broth unconsumed. putida A. subtilis and A.8 × 105 c∗ 3. and hence their exogenous effect. 1). subtilis P. putida resulted in a greater colonisation of roots.05. K Futai Table 3. Pest Manag Sci 2009. lilacinus P. The effects of nematodes and cattle manure individually on colonisation of roots by PGPR were signiﬁcant at P = 0.05.26 – 28 They play a critical role in naturally occurring soil that is suppressive to Fusarium wilt29 and produce a wide variety of antibiotics. heteroauxin and gibberellins. Moreover.7.23 Aspergillus species commonly occur in soils in warmer climates and in compost and decaying plant material.6 × 105 a Cattle manure – 2.25 The biocontrol potential of A. lilanicus has been reported earlier. and thereby an increase in the growth of nematode-infected plants.39 Bacillus subtilis also reduced nematode galling and multiplication. or by transforming unavailable mineral and organic compounds into forms available to plants. and the inoculum added contained bacteria plus broth.36 The plant growth promotion ability of Pseudomonas is a function of good colonisation of roots and production of growth hormones.www.35.6 × 105 bc∗ 3.11 as neither species was isolated from eggs or females of nematodes. Paecilomyces lilacinus was isolated from a larger number of nematode females and improved plant growth to a greater extent than other antagonistic fungi used. B. Moreover.32. and. A.1 × 105 bc 2. Pseudomonads can indirectly protect plants by inducing systemic resistance against various pests and diseases. putida. although most of these are utilised by growing bacteria.0 × 105 b – 2. subtilis against plant pathogens.soci. subtilis was also reported to have a high degree of larvicidal properties against root-knot and cyst nematodes..org ZA Siddiqui. incognita more frequently and destroyed the embryo.24 Some Aspergillus species have also been reported for their biocontrol potential against root-knot nematodes. followed by P.
Annu Rev Phytopathol 24:453–489 (1986). 6 Papavizas GC. Springer.48 Edaphic microorganisms stimulated by these amendments contribute to the suppressive activity of the amended soils through all four principal mechanisms of biological control: (a) competition. putida Pest Manag Sci 2009. in Tropical Nematology.Biocontrol of M. When added to ﬁeld soil. C = control. pp. Dordrecht. Bioresource Technol 58:229–239 (1996). Moreover.com/Publications/VEG5. Vegetable Report 5. putida or P.org 160 140 120 g f i h d ef fg d a e d g c c b a b i e de e g Nematode number No. 113–138 (1968).pdf [12 January 2008]. Number of galls per root system 947 c 2009 Society of Chemical Industry www. Gainesville. of galls / root system 12000 10000 8000 6000 4000 2000 0 C g j i 100 80 60 40 20 0 An Pl Pc Bs Pp Ac C An Pl Pc Bs Pp Ac No manure Treatments Cattle manure Figure 1.soci. The present experiments were performed in pots and with sterilised soil. Hawaii Agriculture Research Center (2004).14 Increase in plant growth and reduction in nematode population by the use of cattle manure may be attributed to the above-mentioned factors. Biological control of plant parasitic nematodes by fungi. incognita on tomato. Pl = Paecilomyces lilacinus. the authors feel that the use of cattle manure with P. 2 Reddy DDR. ecology and potential for biocontrol. Iqbal A and Mahmood I.wiley. ed. 9 Schenck S. respectively. by Smart GC and Perry VG. Annu Rev Phytopathol 23:23–54 (1985). 10 Siddiqui IA. 11 Eapen SJ. Biological control of soil borne plant pathogens in the rhizosphere with bacteria. 5 Weller DM. 4 Siddiqui ZA. Letters Appl Microbiol 39:74–83 (2004). environmental conditions will also inﬂuence the survival and efﬁcacy of these biocontrol agents under ﬁeld conditions. AnnuRevPhytopathol 26:379–407 (1988). 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