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Egyptian Journal of Biological Pest Control
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Fungal and bacterial nematicides in integrated nematode management strategies

Egyptian Journal of Biological Pest Controlvolume 28, Article number: 74 (2018) | Download Citation

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Abstract

Plant-parasitic nematodes (PPNs) pose a serious threat to quantitative and qualitative production of many economic crops worldwide. An average worldwide crop loss of 12.6% (equaled $215.77 billion) annually has been estimated due to these nematodes for only the top 20 life-sustaining crops. Due to the growing dissatisfaction with hazards of chemical nematicides, interest in microbial control of PPNs is increasing and biological nematicides are becoming an important component of environmentally friendly management systems. Fungal and bacterial nematicides rank high among other biocontrol agents. In order to maximize their benefits, such bio-nematicides can be included in integrated nematode management (INM) programs, and ways that make them complimentary or superior to chemical nematode management methods were highlighted. This is especially important where bio-nematicides can act synergistically or additively with other agricultural inputs in integrated pest management programs. Consolidated use of bio-nematicides and other pesticides should be practiced on a wider basis. This is especially important, since there are many bio-nematicides which are or are likely to become widely available soon. Identification of research priorities for harnessing fungal and bacterial nematicides in sustainable agriculture as well as understanding of their ecology, biology, mode of action, and interaction with other agricultural inputs is still needed. Therefore, accessible fungal and bacterial nematicides with their comprehensive references and relevant information, i.e., the active ingredient, product name, type of formulation, producer, targeted nematode species and crop, and country of origin, are summarized herein.

Background

Plant-parasitic nematodes (PPNs) are considered hidden enemy of the farmers as the nematodes are subterranean in habitats and growers are unaware of losses caused by them. Much of the damage caused by nematodes goes unreported or is often confused with other causes such as fungal attack, water stress, or other physiological disorders, and by the time the disease is diagnosed, the loss to crops has already been incurred by these tiny organisms. A great loss to crops has been reported in quantitative, qualitative, and monetary terms. Abd-Elgawad and Askary (2015) reported an average worldwide crop loss of 12.6% (equaled $215.77 billion), due to these nematodes for only the top 20 life-sustaining crops based on the 2010–2013 production figures and prices. Moreover, 14.45% ($142.47 billion) was an average annual yield loss in the subsequent group of food or export crops. These figures are astonishing, and the authentic figure, when more crops throughout the world are considered, probably exceeds such estimations. At the same time, numerous relevant and challenging issues have been demonstrating the desperate need of human beings to provide more and better food for an over-populated world. Abd-Elgawad (2014) stressed the importance of such issues due to deregistration and banning of effective nematicides available because of environmental and health hazards, renewable manifestation of resistance-breaking nematode pathotypes on many important crops, climate change, increased adoption of intensive agriculture, and potential occurrence of quarantine nematodes. Therefore, nematode management and research should be continuously refined and oriented to offer better control of PPNs in an environmentally and economically beneficial manner.

Importance of biological control of pests is growing, and this is obviously reflected by considerable venture capital in research by multinational firms and also by their acquisitions of small biotechnology corporations with microbial product portfolios (Wilson and Jackson 2013). Bio-products containing antagonists of fungi and bacteria rank high among other bio-nematicides (Askary 2015a, b; Eissa and Abd-Elgawad 2015). As such nematicides represent living systems, a number of difficulties exist to develop commercial bio-nematicidal products. Problems with their culture and formulation, variable gap between laboratory and field performance, potential negative effects on non-target or beneficial organisms, and expectations of broad-spectrum activity and quick efficacy based on practice with synthetic chemical nematicides have been addressed in details by some workers (Glare et al. 2012; Askary and Martinelli 2015). Rapid progress has been made during the past two decades in different aspects of bio-nematicidal production and use. This was especially important for the development of in vitro mass culture concerning Pasteuria spp. and innovative, easy-to-use formulations of numerous products. Yet, there is still a desperate need to poise these bio-nematicides as more effective and reliable products against PPNs. This trend is currently materialized in a variety of approaches, including studies on their applications, improved shelf-life, mass-culture, and interaction with other biotic and abiotic factors as well as integration of biocontrol with other management techniques.

The objective of this review article is to highlight the current knowledge of the biological control potential of fungal and bacterial agents in attempt to include them in effective integrated nematode management (INM) programs. Also, research priorities and perceived factors for harnessing fungal and bacterial nematicides in sustainable agriculture were identified.

Fungal and bacterial interaction with other inputs

The most studied and promising groups among the nematode-antagonistic organisms are the nematophagous fungi and bacteria (Askary and Martinelli 2015). The two groups include many species. These bio-nematicides are frequently applied to sites and ecosystems that routinely receive other inputs including chemical pesticides, surfactants (e.g. wetting agents), fertilizers, mineral nutrition, and soil amendments which may interact with bio-active ingredients targeting PPNs. Fungal and bacterial biocontrol agents used with other components in INM are listed in Table 1. Basically, such biocontrol agents (BCA) are living systems sensitive to biotic and abiotic factors that result from inputs, especially in the soil rhizosphere. Thus, BCA should be compatible with them to maximize their benefits. In this respect, we propose that bio-nematicides should not be used as direct competitors with chemical nematicides for several reasons. Bio-nematicides fall behind chemical nematicides in traits prized by growers: price, performance, handling, distribution, and ease of both storage and use. Hence, our suggestion is especially important where bio-nematicides can act synergistically or additively with such inputs in INM programs. Positive results have been demonstrated (Table 1). For example, shoot dry weight of tomato had better (P ≤ 0.05) increase, when Pseudomonas fluorescens GRP3 was combined with organic manure for the management of Meloidogyne incognita than using either P. fluorescens or organic manure alone (Siddiqui et al. 2001b). New tactics for synergistically or even additively incorporating BCA with favorable inputs should be tried further and broadly disseminated for real and better penetration of markets and developed BCA. A similar plan was recently put forward for insecticides too (Stevens and Lewis 2017).

Table 1 Fungal and bacterial biocontrol agents used with other components in integrated nematode management
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We should also highlight and get use of approaches where bio-nematicides can be included in INM programs in ways that make them complimentary or superior to chemical pest management methods. In this respect, endospores formed by bacterial genera Bacillus, Clostridium, and Pasteuria are tolerant to exposures for most agrochemicals. Such endospore-forming bacteria are both the most heat-resistant form of life and highly resistant to desiccation and chemical destruction; these endospores have a prolonged shelf life (more than a year) and can also be applied to seeds several days before planting. They can be used along with inorganic and organic fertilizers, microelements, and several fungicides, herbicides, and pesticides; they can often be tank-mixed. Abd-Elgawad and Vagelas (2015) focused on widening this approach since a tank mix of one or more inputs with a bio-nematicide can save time and money. Also, bio-nematicides can also be used in rotation with such chemicals as pesticides to delay pest resistance by breaking pressure from a single mode of action. Clearly, consolidated use of bio-nematicides and other pesticides should be practiced on a wider basis. In this vein, only few companies are actively fostering the concerted use of bio-nematicides and chemical pesticide, e.g., the product VOTiVO™ and PONCHO®/VOTiVO™ mix, which is based on Bacillus firmus against PPNs, combined with a synthetic insecticide, Poncho1, as a seed treatment (Anonymous 2018).

Mode of action of fungal and bacterial nematicides

Fungi group may be divided into nematode-trapping, endoparasitic, egg- and female-parasitic, and toxin-producing fungi (Askary 1996; Jansson et al. 1997). For example, for the nematode-trapping fungus, entangled nematode with adhesive network of Monacrosporium megalosporum hypha is illustrated (Fig. 1). Catenaria anguillulae, an endoparasitic fungus, is a member of the Chytridiomycota, the only major group of true (chitin-walled) fungi that produce motile spores, termed zoospores (Deacon 2018). This fungus is often found as a facultative (non-specialized) parasite of nematodes and other small organisms. Phase-contrast microscopy was used to show the single and double chain of mature and immature fungal sporangium on parasitized nematodes (Fig. 2). It can be grown easily on culture media and different parts, under germination, of the fungus grown on agar surface (Fig. 3). Based on their modes of action, the nematophagous bacteria can also be broadly grouped into parasitic bacteria and non-parasitic rhizobacteria. Eissa and Abd-Elgawad (2015) adopted the following categories of nematophagous bacteria: obligate parasitic bacteria, opportunistic parasitic bacteria, rhizobacteria, cry protein-forming bacteria, endophytic bacteria, and symbiotic bacteria.

Fig. 1
figure1

Monacrosporium megalosporum. a A portion of hypha showing entangled nematode with adhesive net, the lower portion showing arched or circular hyphal meshes. b A portion of hypha with adhesive network

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Fig. 2
figure2

Catenaria anguillulae. a Chain of mature and immature sporangium. b Double chain of mature and immature sporangium on nematode cadaver

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Fig. 3
figure3

Catenaria anguillulae. A. A conidium on agar surface under germination. B. A portion of hypha with adhesive network. C. Detached conidium

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Several nematicides have been banned due to their health and environmental hazards; therefore, the merits and demerits of potential biological control agents with different modes of action against PPNs should be continuously researched for more details about their virulence mechanisms. The modes of action for common fungal and bacterial nematicides are summarized in Table 2. Predatory and egg-parasitic fungi, as well as the parasitic bacteria Pasteuria spp., were the most studied due to their PPN control potential, ease of laboratory production, and adaptation capability under different agricultural systems. Such bioagents, with different action mechanisms, can play a significant role in PPN management. They have a determined specificity against certain species or even stages of PPNs (Askary and Martinelli 2015). Hence, by considering and identifying such a specificity, PPN management can be targeted successfully. Clearly, sometimes, there is a significant difference in the effectiveness of a definite biocontrol agent against the same PPN species. Possible explanations for these differences include loss of virulence during the in vitro culture process or during formulation, or environmental factors occurring in the field (Crow et al. 2011). Also, current investigations of such mechanisms may lack in the exactitude of the applied parameter. Biochemical measures may be more accurate than others. Korayem et al. (1993) examined the effects of the plant extracts of Artemisia absinthium, Citrullus colocynthis, Punica granatum, Ricinus communis, and Thymus vulgaris on motility of Helicotylenchus dihystera and Meloidogyne incognita and the reversibility of the movement inhibition, the egg-hatching inhibition of M. incognita, and the inhibition of acetylcholinesterase (ACHEs) of H. dihystera. Surprisingly, AChE inhibition by extracts of P. granatum, T. vulgaris, and A. absinthium were more than that by oxamyl, which was reported as a strong inhibitor for AChE (Opperman and Chang 1990). Likewise, detail information is required regarding the modes of action of many bio-nematicides in terms of their effect on nematode acetylcholinesterase inhibition.

Table 2 Modes of action of fungal and bacterial biocontrol agents against phytonematodes (Askary and Martinelli 2015)
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Available products of fungal and bacterial biocontrol agents used against PPNs

In the past three decades, research workers have prepared different types of formulation of bionematicides that have been commercialized in the world market. Lists of some available fungal (Tables 3 and 4) and bacterial (Tables 5 and 6) nematicides, which indicate relevant information in terms of the active ingredient, product name, type of formulation, producer, targeted nematode species, crop, and country, are presented. There are also cottage industries, which use cheap labor to produce other unavailable microbial products mainly for domestic markets. These products of developing countries, especially in Asia, Africa, and Latin America, might be cost-effective and efficacious against PPNs. However, they have not usually undergone the strict and cost rules of registration schemes required in North America and Europe (Wilson and Jackson 2013). There are also some unpublished products sold on market, but their sell scale is either small, local, and/or has not been approved by the government, while other products are in the pipeline. Therefore, a globally standard procedure for approval by governments, especially for non-registered, available bio-nematicides, was suggested.

Table 3 List of commercial products of fungal biocontrol agents used in the nematode management (data are collected by the authors and based on Askary and Martinelli (2015))
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Table 4 Biocontrol agents of fungal species targeting nematodes on economic crops
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Table 5 List of commercial products of bacterial biocontrol agents used in the management of plant-parasitic nematodes
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Table 6 List of bacterial biocontrol agents against phytonematodes infesting agricultural crops
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Due to their ability to manage a wide range of PPN species, some BCA have been formulated in a commercial product to control different PPN species effectively via a single natural product rather than multiple chemical products (Askary and Martinelli 2015). Coating seeds with biopesticides is an inexpensive option that allows targeted delivery and potentially enhances rhizosphere colonization, but this delivery option requires improved efficacy of coating materials and technology or better formulation. Microbial seed treatment is used for disease control, PPN management, and also for insect control (Glare et al. 2012). Improved seed supply systems that reduce the storage period are required if this delivery mechanism is to become more familiar with BCA. Such multiple effects should be further investigated then materialized commercially.

Different formulations of the same pesticide may generally differ in their toxicity to target organisms. Owing to the continuous introduction of novel active ingredients, carriers, and formulations in different market segments and differences in susceptibility and reaction of bacterial species to nematicide formulations, comprehensive information about different aspects of relevant modules should be available to stakeholders and updated continuously. Current issues in experimentations of biological control agents and their applications against PPNs to maximize their benefits have been recently reviewed (Abd-Elgawad, 2016).

Future prospects

It should be clear that the use of bio-nematicides is not limited to beneficial BCA, but they should involve the use of their genes and/or products, such as metabolites, that reduce the negative effects of PPNs and promote positive responses by the growing plant. Furthermore, many products of fungi or bacteria used as soil conditioners, plant growth promoters, or plant strengtheners are not considered as bio-nematicides even though such outputs may increase plants’ ability to tolerate nematode attack (Wilson and Jackson 2013).

It goes without saying that the most successful product should be accepted by growers/end users. In order to achieve satisfaction of such users, more research, especially on the biology, ecology, interaction with other agricultural inputs, and mode of action of these fungal and bacterial biocontrol agents are needed when used as nematicides. Admittedly, such research priorities may call for further development of specialized techniques and realization of growers by merits and demerits of biocontrol agents. The end users should be adequately taught to optimize and adapt to suit their needs for sustainable and environmentally friendly PPN management tactics. Such information is essential for a realistic appraisal of the impact of molecular techniques to enhance their biocontrol potential and monitor their survival and efficacy aiming at developing advanced strategies for PPN control.

Conclusions

We have evaluated the different strategies of using fungi and bacteria in integrated management of plant-parasitic nematodes. This is a hot issue of present and future research. However, due to the wide versatility of this area, we consolidated uses of bio-nematicides and other pesticides which should be practiced on a wider basis; bio-nematicides can act synergistically or additively with other agricultural inputs in integrated pest management programs. Our presentation as a professional review article and meta-analysis study indicated research priorities for utilizing fungal and bacterial nematicides in sustainable agriculture.

References

  1. Aalten PM, Vitour D, Blanvillian D, Gowen SR, Sutra L (1998) Effect of rhizosphere fluorescent Pseudomonas strains on plant parasitic nematodes Radopholus similis and Meloidogyne spp. Letters Appl Microbiol 27:357–361

  2. Abd-Elgawad MMM (2014) Plant-parasitic nematode threats to global food security. J Nematol 46:130

  3. Abd-Elgawad MMM (2016) Comments on the use of biocontrol agents against plant-parasitic nematodes. Int J PharmTech Res 9:352–359

  4. Abd-Elgawad MMM, Askary TH (2015) Impact of phytonematodes on agriculture economy. In: Askary TH, Martinelli PRP (eds) Biocontrol Agents of Phytonematodes. CAB International, Wallingford, pp 3–49

  5. Abd-Elgawad MMM, Vagelas IK (2015) Nematophagous bacteria: field application and commercialization. In: Askary TH, Martinelli PRP (eds) Biocontrol Agents of Phytonematodes. CAB International, Wallingford, pp 276–309

  6. Abo-Elyousr KA, Khan Z, El-Morsi Award M, Abdel-Moneim MF (2010) Evaluation of plant extracts and Pseudomonas spp. for control of root-knot nematode, Meloidogyne incognita on tomato. Nematropica 40:89–99

  7. Adiko A, Gowen SR (1994) Comparison of two inoculation methods of root-knot nematodes for the assessment of biocontrol potential of Pasteuria penetrans. Afro-Asian J Nematol 4:32–34

  8. Ahmed R (1990) Studies on the efficacy of Pasteuria penetrans for the biological control of Meloidogyne species, Ph.D. dissertation. University of Reading, Reading

  9. Ahmed R, Abbas MK, Khan MA, Inam ul Haq M, Javed N, Sahi ST (1994) Evaluation of different methods of application of Pasteuria penetrans for the biocontrol of root-knot of tomato (Meloidogyne incognita). Pakistan J Nematol 12:155–160

  10. Akhtar A, Hisamuddin R, Abbasi S (2012) Interaction between Meloidogyne incognita, Pseudomonas fluorescens and Bacillus subtilis and its effect on plant growth of black gram (Vigna mungo L.). Int J Pl Path 3:66–73

  11. Al-Hazmi AS, Javeed MT (2016) Effects of different inoculum densities of Trichoderma harzianum and Trichoderma viride against Meloidogyne javanica on tomato. Saudi J Biol Sci 23:288–292

  12. Amin AW (2000) Efficacy of Arthrobotrys oligospora, Hirsutella rhossiliensis, Paecilomyces lilacinus and Pasteuria penetrans as potential biocontrol agents against Meloidogyne incognita on tomato. Pakistan J Nematol 18:29–33

  13. Anita B, Samiyappan R (2012) Induction of systemic resistance in rice by Pseudomonas fluorescens against rice root-knot nematode Meloidogyne graminicola. J Biopesticides 5:53–59

  14. Anita E, Rajendran G (2002) Nursery application of Pseudomonas fluorescens for the control of Meloidogyne incognita on tomato and brinjal. Nematol Medit 30:209–210

  15. Anonymous (1995) Annual Report 1994–95. Indian Institute of Spices Research (IISR). Calicut, India, p 89

  16. Anonymous (2018) Poncho/VOTiVO. Available at: https://agriculture.basf.com/us/en/Crop-Protection/Poncho-VOTiVO.html (Accessed 30 June 2018)

  17. Anver S (2003) Effect of different organic amendments with Paecilomyces lilacinus for the management of soil nematodes. Archiv Phytopath Pl Prot 36:103–109

  18. Anver S, Alam MM (1997) Control of Meloidogyne incognita and Rotylenchulus reniformis singly and concomitantly on pigeonpea with Paecilomyces lilacinus. Indian J Nematol 27:209–213

  19. Anver S, Alam MM (1999) Control of Meloidogyne incognita and Rotylenchulus reniformis singly and concomitantly on chickpea and pigeonpea. Archiv Phytopath Pl Prot 32:161–172

  20. Ashoub AH, Amara MT (2010) Biocontrol activity of some bacterial genera against root-knot nematode Meliodogyne incognita. J American Sci 6:321–328

  21. Ashraf MS, Khan TA (2008) Biomanagement of reniform nematode, Rotylenchulus reniformis by fruit wastes and Paecilomyces lilacinus on chickpea. World J Agric Sci 4:492–494

  22. Ashraf MS, Khan TA (2010) Integrated approach for the management of Meloidogyne javanica on eggplant using oil cakes and biocontrol agents. Archiv Phytopath Pl Prot 43:609–614

  23. Askary TH (1996) Studies on some nematophagous fungi in agriculture soil of Pusa Farm, Samastipur, Bihar. M.Sc. (Ag.) Thesis, Department of Nematology, Rajendra Agricultural University, Pusa, Bihar, India

  24. Askary TH (2008) Studies on root-knot nematode infesting pigeonpea and its integrated management. PhD Thesis, Department of Plant Protection, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh, India

  25. Askary TH (2012) Management of root-knot nematode Meloidogyne javanica in pigeonpea through seed treatment. Indian J Ecol 39:151–152

  26. Askary TH (2015a) Nematophagous fungi as biocontrol agents of phytonematodes. In: Askary TH, Martinelli PRP (eds) Biocontrol Agents of Phytonematodes. CAB International, Wallingford, pp 81–125

  27. Askary TH (2015b) Limitations, research needs and future prospects in the biological control of phytonematodes. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CAB International, Wallingford, pp 446–454

  28. Askary TH, Martinelli PRP (2015) Biocontrol agents of phytonematodes. CAB International, Wallingford, p 470

  29. Baheti BL, Dodwadiya M, Bhati SS (2017) Eco-friendly management of maize cyst nematode, Heterodera zeae on sweet corn (Zea mays L. saccharata). J Entomol Zool Stud 5:989–993

  30. Baidoo R, Mengistu T, McSorley R, Stamps RH, Brito J, Crow WT (2017) Management of root-knot nematode (Meloidogyne incognita) on Pittosporum tobira under greenhouse, field, and on-farm conditions in Florida. J Nematol 49:133–139

  31. Bhardwaj P, Trivedi PC (1996) Biological control of Heterodera avenae on wheat using different inoculum levels of Verticillium chlamydosporium. Ann Pl Prot Sci 4:111–114

  32. Bhat MY, Hisamuddin R, Bhat NA (2009) Histological interactions of Paecilomyces lilacinus and Meloidogyne incognita on bitter gourd. J American Sci 5:8–12

  33. Bhat MY, Wani AH (2012) Bio-activity of fungal culture filtrates against root-knot nematode egg hatch and juvenile motility and their effects on growth of mung bean (Vigna radiata L. Wilczek) infected with the root-knot nematode, Meloidogyne incognita. Archiv Phytopath Pl Prot 45:1059–1069

  34. Bhatt J, Chaurasia RK, Sengupta SK (2002a) Management of Meloidogyne incognita by Paecilomyces lilacinus and influence of different inoculums levels of Rotylenchulus reniformis on betelvine. Indian Phytopath 55:348–350

  35. Bhatt J, Sengupta SK, Chaurasia RK (2002b) Management of Meloidogyne incognita by Trichoderma viride in betelvine. Indian Phytopath 55:97–98

  36. Bhattacharya D, Swarup G (1988) Pasteuria penetrans, a pathogen of the genus Heterodera, its effect on nematode biology and control. Indian J Nematol 18:61–70

  37. Bokhari FM (2009) Efficacy of some Trichoderma species in the control of Rotylenchulus reniformis and Meloidogyne javanica. Archiv Phytopath Pl Prot 42:361–369

  38. Brahma U, Borah A (2016) Management of Meloidogyne incognita on pea with bioagents and organic amendment. Indian J Nematol 46:58–61

  39. Brown SM, Kepner JL, Smart GC Jr (1985) Increased crop yields following application of Bacillus penetrans to field plots infested with Meloidogyne incognita. Soil Biol Biochem 17:483–486

  40. Brown SM, Nordmeyer D (1985) Synergistic reduction in root galling by Meloidogyne javanica with Pasteuria penetrans and nematicide. Revue de Nemat 8:285–286

  41. Brown SM, Smart GC Jr (1985) Root penetration by Meloidogyne incognita juveniles infected with Bacillus penetrans. J Nematol 17:123–126

  42. Cabanillas E, Barker KR (1989) Impact of Paecilomyces lilacinus inoculums level of Meloidogyne incognita on tomato. J Nematol 21:115–120

  43. Cabanillas E, Barker KR, Nelson LA (1989) Survival of Paecilomyces lilacinus in selected carries and related effects on Meloidogyne incognita on tomato. J Nematol 21:121–130

  44. Candanedo-Lay E, Lara J, Jatala P, Gonzales F (1982) Preliminary evaluation of Paecilomyces lilacinus as a biological control of root-knot nematode Meloidogyne incognita in industrial tomatoes. Nematropica 12:154

  45. Chand R, Gill JS (2002) Evaluation of various application methods of Pasteuria penetrans against Meloidogyne incognita in tomato. Indian J Nematol 32:23–25

  46. Chatali L, Singh S, Goswami BK (2003) Effect of cakes with Trichoderma viride for the management of disease complex caused by Rhizoctonia bataticola and Meloidogyne incognita on okra. Ann Pl Prot Sci 11:178–180

  47. Chaudhary KK, Kaul RK (2013) Efficacy of Pasteuria penetrans and various oil seed cakes in management of Meloidogyne incognita in chili pepper (Capsicum annuum L.). J Agric Sci Tech 15:617–626

  48. Chen ZX, Dickson DW, McSorley R, Mitchell DJ, Hewlett TE (1996) Suppression of Meloidogyne arenaria race 1 by soil application of endospores of Pasteuria penetrans. J Nematol 28:159–168

  49. Chen ZX, Dickson DW, Mitchell DJ, McSorley R, Hewlett TE (1997) Suppression mechanism of Meloidogyne arenaria race 1 by Pasteuria penetrans. J Nematol 29:1–8

  50. Cho MR, Na SY, Yiem MS (2000) Biological control of Meloidogyne arenaria by Pasteuria penetrans. J Asia-Pacific Entom 3:71–76

  51. Ciancio A (1995) Density dependent parasitism of Xiphinema diversicaudatum by Pasteuria penetrans in a naturally infested field. Phytopathology 85:144–149

  52. Ciancio A, Bourijate M (1995) Relationship between Pasteuria penetrans infection levels and density of Meloidogyne javanica. Nemat Medit 23:43–49

  53. Crow WT, Luc JE, Giblin-Davis RM (2011) Evaluation of Econem™, a formulated Pasteuria sp. bionematicide, for management of Belonolaimus longicuadatus on golf course turf. J Nematol 43:10–109

  54. Dababat AA, Sikora RA (2007) Use of Trichoderma harzianum and Trichoderma viride for the biological control of Meloidogyne incognita on tomato. J Agric Sci 3:297–309

  55. Dababat AA, Sikora RA, Hauschild R (2006) Use of Trichoderma harzianum and Trichoderma viride for biological control of Meloidogyne incognita on tomato. Comm Agric Appl Biol Sci 71:953–961

  56. Daudi AT, Channer AG, Ahmed R, Gowen SR (1990) Pasteuria penetrans as a biocontrol agent of Meloidogyne javanica in the field in Malawi and in microplots in Pakistan. Proc Brighton Crop Prot Conf. Brighton, UK. 1:253–257

  57. Daudi AT, Gowen SR (1992) The potential for managing root-knot nematodes by use of pasteuria penetrans and oxamyl. Nematol Medit 20:241–244

  58. Davide RG, Zorilla RA (1986) Evaluation of a fungus Paecilomyces lilacinus for the biological control of Meloidogyne incognita on okra compared with a nematicide Isazofos. Int Nematol Network Newslet 3:32–33

  59. De Channer AG (1989) The potential of Pasteuria penetrans for the biological control of Meloidogyne species, Ph.D. dissertation. University of Reading, Reading

  60. De Leij FAAM, Davies KG, Kerry BR (1992) The use of Verticillium chlamydosporium and Pasteuria penetrans alone and in combination to control Meloidogyne incognita on tomato plants. Fund Appl Nematol 15:235–242

  61. De Leij FAAM, Kerry BR, Dennehy JA (1993) Verticillium chlamydosporium as a biocontrol agents for Meloidogyne incognita and M. hapla in pot and microplot tests. Nematologica 39:115–126

  62. Deacon J (2018) The microbial world. Available at: http://archive.bio.ed.ac.uk/jdeacon/microbes/catenar.htm (Accessed 30 June 2018)

  63. Deka R, Sinha AK, Neog PP (2002) Effect of Paecilomyces lilacinus and botanicals against Tylenchulus semipenetrans on Citrus jambhiri. Indian J Nematol 32:230–231

  64. Deori R, Borah A (2016) Efficacy of Glomus fasciculatum, Trichoderma harzianum for the management of Meloidogyne incognita and Rhizoctonia solani disease complex in green gram. Indian J Nematol 46:61–64

  65. Devapriyanga R, Jonathan EI, Sankarimeena K, Kavitha PG (2012) Bioefficacy of Pseudomonas and Bacillus isolates against root-knot nematode, Meloidogyne incognita in black pepper cv. Panniyur 1. Indian J Nematol 42:57–65

  66. Devi LS, Dutta U (2002) Effect of Pseudomonas fluorescens on root-knot nematodes, (Meloidogyne incognita) on okra plant. Indian J Nematol 32:215–216

  67. Devi LS, Hassan MG (2002) Effect of organic manure singly and in combination with Trichoderma viride against root-knot nematode (Meloidogyne incognita) of soybean (Glycin max L. Mrill). Indian J Nematol 32:190–192

  68. Devi LS, Sharma R (2002) Effect of Trichoderma spp. against root-knot nematodes, Meloidogyne incognita on tomato. Indian J Nematol 32:227–228

  69. Devi TS, Mahanta B, Borah A (2016) Comparative efficacy of Glomus fasciculatum, Trichoderma harzianum, carbofuran and carbendazim in management of Meloidogyne incognita and Rhizoctonia solani disease complex on brinjal. Indian J Nematol 46:161–164

  70. Devrajan K, Rajendran G (2002) Effect of fungal egg parasite Paecilomyces lilacinus (Thom.) Samson on Meloidogyne incognita in banana. Indian J Nematol 32:88–90

  71. Dhawan SC, Singh S (2009) Compatibility of Pochonia chlamydosporia with nematicide and neem cake against root-knot nematode, Meloidogyne incognita infesting okra. Indian J Nematol 39:85–89

  72. Dhawan SC, Singh S (2010) Management of root-knot nematode, Meloidogyne incognita using Pochonia chlamydosporia on okra. Indian J Nematol 40:171–178

  73. Dhawan SC, Singh S, Kamra A (2008) Bio-management of root-knot nematode, Meloidogyne incognita by Pochonia chlamydosporia and Pseudomonas fluorescens on brinjal in farmer’s field. Indian J Nematol 38:110–111

  74. Dhawan SS, Narayana R, Babu NP (2004) Biomanagement of root-knot nematode, Meloidogyne incognita in okra by Paecilomyces lilacinus. Ann Pl Prot Sci 12:356–359

  75. Dube B, Smart GC Jr (1987) Biological control of Meloidogyne incognita by Paecilomyces and Pasteuria penetrans. J Nematol 19:222–227

  76. Duponnois R, Netscher C, Mateille T (1997) Effect of rhizosphere microflora on Pasteuria penetrans parasitizing Meloidogyne graminicola. Nemat Medit 25:99–103

  77. Dwivedi K, Upadhyay KD, Verma RA, Ahmad F (2008) Role of bioagents in management of Pratylenchus thornei infecting chickpea. Indian J Nematol 38:138–140

  78. Eapen SJ, Ramana KV, Sarma YR, Edison S, Sasikumar B, Babu KN (1996) Evaluation of Pseudomonas fluorescens isolates for control of Meloidogyne incognita in black pepper (Piper nigrum L.). Proc Biotech spices, medic aromat pl, Calicut, India, 24–25 Apr, pp.129–133

  79. Eapen SJ, Venugopal MN (1995) Field evaluation of Trichoderma spp. and Paecilomuces lilacinus for control of root knot nematodes and fungal diseases of cardamom nurseries. Indian J Nematol 25:15–16

  80. Ebrahim A, Seddighe F, Hassan RE (2008) Potential for biocontrol of Heterodera schachtii by Pochonia chlamydosporia var. chlamydosporia on sugarbeet. Biocont Sci Tech 18:157–167

  81. Eissa MFM, Abd-Elgawad MMM (2015) Nematophagous bacteria as biocontrol agents of phytonematodes. In: Askary TH, Martinelli PRP (eds) Biocontrol Agents of Phytonematodes. CAB International, Wallingford, pp 217–243

  82. Eltayeb FME (2017) Biological control of root knot disease of tomato caused by Meloidogyne javanica using Pseudomonas fluorescens bacteria. Int J Cur Microbiol Appl Sci 6:1176–1182

  83. Esfahani MN, Pour BA (2006) The effects of Paecilomyces lilacinus on the pathogenesis of Meloidogyne javanica and tomato plant growth parameters. Iran Agric. Res 24:67–75

  84. Feyisa B, Lencho A, Selvaraj T, Getaneh G (2015) Evaluation of some botanicals and Trichoderma harzianum for the management of tomato root-knot Nematode (Meloidogyne incognita (Kofoid and White) Chitwood. Adv Crop Sci Tech 4:201. doi:https://doi.org/10.4172/2329-8863.1000201

  85. Feyisa B, Lencho A, Selvaraj T, Getaneh G (2016) Evaluation of some botanicals and Trichoderma harzianum against root-knot nematode Meloidogyne incognita (Kofoid and White) Chitwood in tomato. J Entomol Nematol 8:11–18

  86. Ganaie MA, Khan TA (2010) Biological potential of Paecilomyces lilacinus on pathogenesis of Meloidogyne javanica infecting tomato plant. European J Appl Sci 2:80–84

  87. Glare TR, Caradus J, Gelernter W, Jackson T, Keyhani N, KÖhl J, Marrone P, Morin L, Stewart A (2012) Have biopesticides come of age? Trends in Biotech 30:250–258

  88. Gogoi BB, Gill JS (2001) Compatibility of Pasteuria penertrans with carbofuran and organic amendments, its effect on Heterodera cajani. Ann Pl Prot Sci 9:254–257

  89. Gogoi D, Mahanta B (2013) Comparative efficacy of Glomus fasciculatum, Trichoderma harzianum, carbofuran and carbendazim in management of Meloidogyne incognita and Rhizoctonia solani disease complex on French bean. Ann Pl Prot Sci 21:172–175

  90. Gopinatha KV, Gowda DN, Nagesh M (2002) Management of root-knot nematode Meloidogyne incognita on tomato using bioagent Verticillium chlamydosporium, neem cake, marigold and carbofuran. Indian J Nematol 32:179–181

  91. Goswami BK, Mittal A (2004) Management of root-knot nematode infecting tomato by Trichoderma viride and Paecilomyces lilacinus. Indian Phytopath 57:235–236

  92. Goswami BK, Pandey RK, Rathour KS, Bhattacharya C, Singh L (2006) Integrated application of some compatible biocontrol agents along with mustard oil seed cake and furadan on Meloidogyne incognita infecting tomato plants. J Zhejiang Univ Sci 7:873–875

  93. Goswami BK, Singh S (2002) Effect of Aspergillus niger and cladosporium oxysporum on root-knot nematode (Meloidogyne incognita) multiplication on eggplant. Indian J Nematol 32:94–96

  94. Hallmann J, Quadt-Hallmann A, Rodrı́guez-Kábana R, Kloepper JW (1998) Interactions between Meloidogyne incognita and endophytic bacteria in cotton and cucumber. Soil Biol Biochem 30:925–937

  95. Hanna AI, Riad FW, Tawfik AE (1999) Efficacy of antagonistic rhizobacteria on the control of root-knot nematode, Meloidogyne incognita in tomato plants. Egyptian J. Agric Res 77:1467–1476

  96. Hasan N (2004) Evaluation of native strain of Paecilomyces lilacinus against Meloidogyne incognita in cowpea followed by Lucerne. Ann Pl Prot Sci 3:145–148

  97. Haseeb A, Kumar V, Abuzar S, Sharma A (2007) Integrated management of Meloidogyne incognita-Sclerotinia sclerotiorum disease complex of Mentha arvensis cv. Gomti by using Trichoderma species, neem seed powder, carbofuran and topsin-M. 7th National Symposium on plant Protection Options Implementation and Feasibility, 20–22 Dec. pp. 102

  98. Hewlett TE, Dickson DW, Mitchell DJ, Kannwischer-Mitchell ME (1988) Evaluation of Paecilomyces lilacinus as a biocontrol agent of Meloidogyne javanica on tobacco. J Nematol 20:578–584

  99. Hussain S, Zareen A, Zaki MJ, Abid M (2001) Response of ten chickpea (Cicer arietinum L.) cultivars against Meloidogyne javanica (Treub) Chitwood and disease control by fungal filtrates. Pakistan J Biol Sci 4:429–432

  100. Jamshidnejad V, Sahebani N, Etebarian H (2013) Potential biocontrol activity of Arthrobotrys oligospora and Trichoderma harzianum BI against Meloidogyne javanica on tomato in the greenhouse and laboratory studies. Archiv Phytopath Pl Prot 46:1632–1640

  101. Jansson H-B, Tunlid A, Nordbring-Hertz B (1997) Biological control: nematodes. In: Fungal biotechnology.Anke T (ed.). Chapman and Hall, Weinheim, pp 38–50

  102. Jatala P, Kaltenbach R, Bocangel M (1979) Biological control of Meloidogyne incognita acrita and Globodera pallida on potatoes. J Nematol 11:303

  103. Jatala P, Kaltenbach R, Bocangel M, Devaux AJ, Campos R (1980) Field application of Paecilomyces lilacinus for controlling Meloidogyne incognita on potatoes. J Nematol 12:226–227

  104. Javed N, El-Hassan S, Gowen SR, Pemproke B, Inam-ul-Haq M (2008) The potential of combining Pasteuria penetrans and neem (Azadirachta indica) formulations as a management system for root knot nematodes on tomato. European J Pl Path 120:53–60

  105. Jayakumar J, Ramakrishnan S, Rajendran G (2002) Effect of culture filtrate of Pseudomonas fluorescens strain PFl on cotton reniform nematode, Rotylenchulus reniformis. Indian J Nematol 32:228–230

  106. Jayakumar J, Ramakrishnan S, Rajendran G (2004) Biological control of cotton reniform nematode, Rotylenchulus reniformis with Pseudomonas fluorescens. Indian J Nematol 34:230–231

  107. Jayaraj MA, Mani A (1988) Biocontrol of Meloidogyne javanica with the bacterial spore parasite Pasteuria penetrans. Int Nematol Network Newslet 5:3–4

  108. Jegathambigai V, Wilson-Wijeratnam RS, Wijesundera RLC (2011) Effect of Trichoderma viride Strain NRRL 6418 and Trichoderma harzianum (Hypocrea lixii TWC1) on Livistona rotundifoliaroot-knot nematodeMeloidogyne incognita. J Entomol 8:229–239

  109. Jonathan EI, Barker KR, Abdel-Alim FF, Vrain TC, Dickson DW (2000) Biological control of Meloidogyne incognita on tomato and banana with rhizobacteria actinomycetes, and Pasteuria penetrans. Nematropica 30:231–240

  110. Jonathan EI, Cannayane I, Samiyappan R (2004) Field application of biocontrol agents for the management of spiral nematode, Helicotylenchus multicinctus in banana. Nematol Medit 32:169–173

  111. Jonathan EI, Padmanabhan D, Ayyamperumal A (1995) Biological control of root-knot nematode on betelvine, Piper betel by Paecilomyces lilacinus. Nematol Medit 23:191–193

  112. Jonathan EI, Rajendran G (2000) Biocontrol potential of the fungus Paecilomyces lilacinus against root-knot nematode Meloidogyne incognita in banana. J Biol Cont 14:67–69

  113. Jonathan EI, Sandeep A, Cannayane I, Umamaheswari R (2006) Bioefficacy of Pseudomonas fluorescens on Meloidogyne incognita in banana. Nematol Medit 34:19–25

  114. Jothi G, Sivakumar M, Rajendran G (2003) Management of root-knot nematode by Pseudomonas fluorescens in tomato. Indian J Nematol 33:87–88

  115. Kalaiarasan P, Lakhsmanan PL, Samiyappan R (2010) Induction of oxidative enzyme, peroxidise in groundnut (Arachis hypogaea) by application of Pseudomonas fluorescens as a defence against the root-knot nematode, Meloidogyne arenaria. Indian J Nematol 40:55–59

  116. Kasumimoto T, Ikeda R, Kawada H (1993) Dose response of Meloidogyne incognita infected cherry tomatoes to application of Pasteuria penetrans. Japanese J Nematol 23:10–18

  117. Kavitha J, Jonathan EI, Umamaheswari R (2007) Field application of Pseudomonas fluorescens, Bacillus subtilis and Trichoderma viride for the control of Meloidogyne incognita (Kofoid and White) Chitwood on sugarbeet. J Biol Cont 21:211–215

  118. Khalil MS, Allam AFG, Barakat AST (2012b) Nematicidal activity of some biopesticide agents and microorganisms against root-knot nematode on tomato plants under greenhouse conditions. J Pl Prot Res 52:47–52

  119. Khalil MS, Kenawy A, Gohrab MA, Mohammed EE (2012a) Impact of microbial agents on Meloidogyne incognita management and morphogenesis of tomato. J Biopesticides 5:28–35

  120. Khan A, Williams KL, Nevalainen HKM (2006) Control of plant-parasitic nematodes by Paecilomyce lilacinus and Monacrosporium lysipagum in pot trials. Biocontrol 51:643–658

  121. Khan MR, Goswami BK (2000) Effect of different doses of Paecilomyces lilacinus isolate 6 on Meloidogyne incognita infecting tomato. Indian J Nematol 30:5–7

  122. Khan MW, Esfahani MN (1990) Efficacy of Paecilomyces lilacinus for controlling Meloidogyne javanica on tomato in green house in India. Pakistan J Nematol 8:95–96

  123. Khan TA, Azam MF, Hussain SI (1984) Effect of fungal filtrates of A. niger and Rhizoctonia solani on penetration and development of root-knot nematodes and plant growth of tomato var. Marglobe. Indian J Nematol 14:106–109

  124. Khattak S, Khattak B (2011) Management of root-knot nematode with Trichoderma harzianum and spent mushroom compost. Proceedings 46th Croatian and 6th International Symposium on Agriculture held on 14th–18th February, 2011 at Opatija, Croatia. pp. 157–160

  125. Kokalis-Burelle N (2015) Pasteuria penetrans for control of Meloidogyne incognita on tomato and cucumber, and M. arenaria on snapdragon. J Nematol 47:207–213

  126. Korayem AM, Hasabo SA, Ameen HH (1993) Effects and mode of action of some plant extracts on certain plant parasitic nematodes. Anz Schädling 66:32–36

  127. Krishnaveni M, Subramanian S (2004) Evaluation of biocontrol agents for the management of Meloidogyne incognita on cucumber (Cucumis sativus L). Cur Nematol 15:33–37

  128. Kumar A, Walia RK, Kapoor A (2005b) Field evaluation of Pasteuria penetrans as nursery bed application against Meloidogyne javanica infecting brinjal. Int J Nematol 15:183–186

  129. Kumar D, Bhatt J, Sharma RL (2017) Efficacy of different bio control agents against Meloidogyne incognita and Fusarium oxysporum on black gram (Vigna mungo L). Int J Cur Microbiol Appl Sci 6:2287–2291

  130. Kumar P, Chand R (2015) Bioefficacy of trichoderma harzianum against root-knot nematode Meloidogyne incognita on brinjal. Ann Pl Prot Sci 23:361–364

  131. Kumar PS, Jonathan EI, Samiyappan R (2008) Field application of biocontrol agent, Pseudomonas fluorescens for the management of burrowing nematode, Radopholus similis in banana. Indian J Nematol 38:57–61

  132. Kumar S, Khanna AS (2006) Role of Trichoderma harzianum and neem cake separately and in combination against root-knot nematode on tomato. Indian J Nematol 36:264–266

  133. Kumar S, Prabhu S (2008) Biological control of Heterodera cajani in pigeonpea by Trichoderma harzianum and Pochonia chlamydosporia. Indian J Nematol 38:65–67

  134. Kumar T, Kang SC, Maheshwari DK (2005a) Nematicidal activity of some fluorescent Pseudomonads on cyst forming nematode, Heterodera cajani and growth of Sesamum indicum var. RT1. Agric Chem Biotech 48:161–166

  135. Kumar V, Jain RK (2010a) Management of root-knot nematode, Meloidogyne incognita using Pochonia chlamydosporium on okra. Indian J Nematol 40:171–178

  136. Kumar V, Jain RK (2010b) Management of root-knot nematode, Meloidogyne incognita, by Trichoderma viride, T. harzianum and bacterial antagonist, Pseudomonas fluorescens as seed treatment on okra. Indian J Nematol 40:226–228

  137. Kumar V, Singh RV, Singh HS (2011) Management of Meloidogyne incognita race 1 and Rotylenchulus reniformis by seed treatment with biological agents, organic cakes and pesticides on cowpea. Ann Pl Prot Sci 19:164–167

  138. Li S, Duan YX, Zhu XF, Chen LJ, Wang YY (2011) The effects of adding secondary metabolites of Aspergillus niger on disease resistance to root-knot nematode of tomato. China Vegetables 1:44–49

  139. Mahanta B, Borbora AC, Konwar B (2016) Effect of Paecilomyces lilacinus on Tylenchulus semipenetrans population in Khasi Mandarin. Indian J Nematol 46:55–81

  140. Maheswari TU, Mani A (1989) Combined efficacy of Pasteuria penetrans and Paecilomyces lilacinus on the biocontrol of Meloidogyne javanica on tomato. Int Nematol Network Newslet 5:10–11

  141. Mani MP, Rajeswari S, Siva Kumar CV (1998) Management of the potato cyst nematodes, Globodera spp. through plant rhizosphere bacterium Pseudomonas fluorescens Migula. J Biol Cont 12:131–134

  142. Mankau R, Prasad N (1972) Possibilities and problems in the use of a sporozoan endoparasite for biological control of plant parasitic nematodes. Nematropica 2:7–8

  143. Manzoor SM, Sinha AK, Bora BC (2002) Management of citrus nematode, Tylenchulus semipenetrans on Khasi Mandarin, by Paecilomyces lilacinus. Indian J Nematol 32:153–155

  144. Mehtab A, Javed N, Khan SA, Gondal AS (2013) Combined effect of Pasteuria penetrans and neem extract on the development of root-knot nematode in medicinal plants. Pakistan J Nematol 31:55–59

  145. Mendoza A, Sikora RA, Kiewnick S (2004) Efficacy of Paecilomyces lilacinus (strain 251) for the control of Radopholus similis in banana. Comm Agric Appl Biol Sci 69:365–372

  146. Meyer SF, Roberts DP, Chitwood DJ, Carta LK, Lumsden RD, Mao W (2001) Application of Burkholderia cepacia and Trichoderma virens, alone and in combinations, against Meloidogyne incognita on bell pepper. Nematropica 31:75–86

  147. Mokbel AA, Obad IM, Ibrahim IKA (2009) The role of antagonistic metabolites in controlling root-knot nematode, Meloidogyne arenaria on tomato. Alexandria J Agric Res 54:199–205

  148. Muthulakshmi M, Devrajan K (2015) Management of Meloidogyne incognita by Pseudomonas fluorescens and Trichoderma viride in mulberry. Int J Pl Prot 8:1–6

  149. Muthulakshmi M, Devrajan K, Jonathan EI (2010) Biocontrol of root-knot nematode, Meloidogyne incognita (Kofoid and White) Chitwood in mulberry (Morus alba L.). J Biopesticides 3:479–482

  150. Muthulakshmi M, Kumar S, Subramanian S, Anita B (2012) Compatibility of Pochonia chlamydosporia with other biocontrol agents and carbofuran. J Biopesticides 5:243–245

  151. Nagesh M, Hussaini SS, Singh SP, Biswas SR (2003) Management of root-knot nematode, Meloidogyne incognita (Kofoid and White) Chitwood in chrysanthemum using Paecilomyces lilacinus (Thom) Samson in combination with neem cake. J Biol Cont 17:125–131

  152. Nagesh M, Jankiram T (2004) Root-knot nematode problem in polyhouse roses and its management using dazomat, neem cake and Pochonia chlamydosporia (Verticillium chlamydosporium). J Ornament Hort, New Series 7:147–152

  153. Nagesh M, Parvatha Reddy P, Rama N (2001) Influence of oil cakes in combination with inorganic fertilizers on growth and sporulation of Paecilomyces lilacinus and its antagonism on Meloidogyne incognita infecting tomato. Nematol Medit 29:23–27

  154. Nama CP, Sharma HK (2017) Bio-management of root-knot nematode, Meloidogyne incognita on cowpea (Vigna unguiculata L.). J Entomo Zool Stud 5:50–52

  155. Narasimhamurthy HB, Ravindra H, Sehgal M (2017a) Management of rice root-knot nematode, Meloidogyne graminicola. Int J Pure Appl Biosci 5:268–276

  156. Narasimhamurthy HB, Ravindra H, Sehgal M, Ekabote SD, Ganapathi (2017b) Management of rice root-knot nematode, Meloidogyne graminicola. J Entomology and Zoology Studies 5:1433–1439

  157. Naserinasab F, Sahebani N, Etebarian HR (2011) Biological control of Meloidogyne javanica by Trichoderma harzianum BI and salicylic acid on tomato. African J Food Sci 5:276–280

  158. Nisha MS, Sheela MS (2016) Effect of fungal egg parasite, Paecilomyces lilacinus (Thom.) Samson on Meloidogyne incognita in brinjal. Indian J Nematol 46:157–159

  159. Oclarit EL, Cumagun CJR (2009) Evaluation of efficacy of Paecilomyces lilacinus as biological control agent of Meloidogyne incognita attacking tomato. J Pl Prot Res 49:337–340

  160. Oduor-owino P (2003) Integrated management of root-knot nematodes using agrochemicals, organic matter and the antagonistic fungus, Paecilomyces lilacinus in natural field soil. Nematol Medit 31:121–123

  161. Oostendorp M, Dickson DW, Mitchell DJ (1991) Population development of Pasteuria penetrans on Meloidogyne arenaria. J Nematol 23:58–64

  162. Opperman CH, Chang S (1990) Plant-parasitic nematodes acetylcholinesterase inhibition by carbamate and organophosphate nematicides. J Nematol 22:481–488

  163. Page SLJ, Bridge J (1985) Observations on Pasteuria penetrans as a parasite of Meloidogyne acronea. Nematologica 31:238–240

  164. Pandey G, Pandey RK, Pant H (2003) Efficacy of different levels of Trichoderma viride against rootknot nematode in chickpea (Cicer arietinum L.). Ann Pl Protect Sci 11: 101-103

  165. Parihar K, Rehman B, Ganai MA, Asif M, Siddiqui MA (2015) Role of oil cakes and Pochonia chlamydosporia for the management of Meloidogyne javanica attacking Solanum melongena L. J Pl Path and Microbiol (Special Issue) SI:1–5. https://doi.org/10.4172/2157-7471.SI-004

  166. Parvatha Reddy P, Khan RM (1988) Evaluation of Paecilomyces lilacinus for the biological control of Rotylenchulus reniformis infecting tomato, compared with cabofuran. Nematol Medit 16:113–115

  167. Parvatha Reddy P, Nagesh M, Devappa V (1997) Effect of integration of Pasteuria penetrans, Paecilomyces lilacinus and neem cake for the management of root-knot nematodes infecting tomato. Pest Manag Hortl Ecosyst 3:100–104

  168. Parvatha Reddy P, Rao MS, Nagesh M (1996) Management of the citrus nematode, Tylenchulus semipenetrans, by integration of Trichoderma harzianum with oil cakes. Nematologia Mediterranea 24:265–267

  169. Pathak B, Khan MR (2010) Comparative field efficacy of chemical, botanical and biological agents against foliar nematode, Aphelenchoides besseyi infecting tuberose. Indian J Nematol 40:83–87

  170. Pathak KN, Kumar B (2003) Effect of culture filtrates of Gliocladium virens and Trichoderma harzianum on the penetration of rice roots by Meloidogyne graminicola. Indian J Nematol 33:149–151

  171. Pathak KN, Ranjan R, Kumar M, Kumar B (2005) Biomanagement of Meloidogyne graminicola by Trichoderma harzianum and T. virens in rice. Ann Pl Prot Sci 13:438–440

  172. Perveen S, Ehteshamul-Haque S, Ghaffar A (1998) Efficacy of Pseudomonas aeruginosa and Paecilomyces lilacinus in the control of root rot-root knot disease complex on some vegetables. Nematol Medit 26:209–212

  173. Prakob W, Nguen-Hom J, Jaimasit P, Silapapongpri S, Thanunchai J, Chaisuk P (2009) Biological control of lettuce root knot disease by use of Pseudomonas aeruginosa, Bacillus subtilis and Paecilomyces lilacinus. J Agric Tech 5:179–191

  174. Prasad D, Anes KM (2008) Effect of metabolites of Trichoderma harzianum and T. viride on plant growth and Meloidogyne incognita on okra. Ann Pl Prot Sci 16:461–465

  175. Priya MS (2015) Biomanagement of rice root knot nematode, Meloidogyne graminicola Golden and Brichfield in aerobic rice. Int J Manag Soc Sci 3:591–598

  176. Ramakrishnan S, Nagesh M (2011) Evaluation of beneficial fungi in combination with organics against root-knot nematode, Meloidogyne incognita, in FCV tobacco nurseries. J Biol Cont 25:311–315

  177. Ramakrishnan S, Rao CP (2013) Evaluation of Paecilomyces lilacinus for the management of root-knot nematode, Meloidogyne incognita in flue cured Virginia (FCV) tobacco nursery. Indian J Nematol 43:65–69

  178. Ramakrishnan S, Sivakumar CV, Poornima K (1998) Management of rice root nematode, Hirschmanniella gracilis (de Man) Luc and Goodey with Pseudomonas fluorescens Migula. J Biol Cont 12:135–141

  179. Rangaswamy SD, Parvatha Reddy P, Nagesh M (2000) Evaluation of biocontrol agents (P. penetrans and T. viride) and botanicals for the management of root-knot nematode, M. incognita infecting tomato. Pest Manag Hort Ecosyst 6:135–138

  180. Rao MS (2007) Papaya seedlings colonized by the bio-agents Trichoderma harzianum and Pseudomonas fluorescens to control root-knot nematodes. Nematol Medit 35:199–203

  181. Rao MS, Dhananjay N, Shylaja M (2003) Management of Meloidogyne incognita on eggplant using a formulation of Pochonia chlamydosporia, Zare et al., (Verticillium chlamydosporium). Pest Manag Hort Ecosyst 9:71–76

  182. Rao MS, Dhananjay N, Shylaja M (2004) Biointensive management of root-knot nematode on bell pepper using Pochonia chlamydosporia and Pseudomonas fluorescens. Nematol Medit 32:159–163

  183. Rao MS, Parvatha Reddy P, Nagesh M (1997a) Management of root-knot nematode, Meloidogyne incognita on tomato by integration of Trichoderma harzianum with neem cake. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 104:423–425

  184. Rao MS, Parvatha Reddy P, Nagesh M (1997b) Integration of Paecilomyces lilacinus with neem leaf suspension for the management of root-knot nematodes on eggplant. Nematol Medit 25:249–252

  185. Rao MS, Parvatha Reddy P, Nagesh M (1998) Evaluation of plant based formulations of Trichoderma harzianum for the management of Meloidogyne incognita on eggplant. Nematol Medit 26:59–62

  186. Raveendra HR, Krishna Murthy R, Mahesh Kumar R (2011) Management of root knot nematode Meloidogyne incognita by using oil cake, bio-agent, trap crop, chemicals and their combination. Int J Sci Nat 2:519–523

  187. Ravichandra NG, Reddy BMR (2008) Efficacy of Pasteuria penetrans in the management of Meloidogyne incognita infecting tomato. Indian J Nematol 38:172–175

  188. Roman J, Rodriguez-Marcano A (1985) Effect of the fungus Paecilomyces lilacinus on the larval population and root-knot formation of Meloidogyne incognita in tomato. J Agric University Puerto Rico 69:159–166

  189. Saikia MK, Roy AK (1994) Efficacy of Paecilomyces lilacinus on the reduction of attack of Meloidogyne incognita on okra. Indian J Nematol 24:163–167

  190. Sandeep A (2004) Bioefficacy of Pseudomonas fluorescens (Native Isolates) on Meloidogyne incognita (Kofoid and White, 1919) Chitwood, 1949 in Banana (Musa spp.). M.Sc. (Ag.) Thesis, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India

  191. Sankaranarayanan C, Hussaini SS, Kumar PS, Rangeshwaran R (2000) Biological control of Meloidogyne incognita (Kofoid and White 1919) Chitwood, 1949 on tomato by Verticillium chlamydosporium Goddard culture on different substrates. J Biol Cont 14:39–43

  192. Santhi A, Sivakumar CV (1995) Biocontrol potential of Pseudomonas fluorescens (Migula) against root-knot nematode, Meloidogyne incognita (Kofoid and White, 1919) Chitwood, 1949 on tomato. J Biol Cont 9:113–115

  193. Santhi A, Sundarababu R, Sivakumar CV, Sundarababu R (1999) Field evaluation of rhizobacterium, Pseudomonas fluorescens for the management of the citrus nematode, Tylenchulus semipenetrans. Procnational symposium on rational approaches in nematode management for sustainable agriculture. Anand, India, 23–25 November, pp. 38–42.

  194. Santin RCM (2008) Potential usage of the fungi Trichoderma spp. and Paecilomyces lilacinus in the control of Meloidogyne incognita and Phaseolus vulgaris. Ph.D. thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.

  195. Seenivasn N, Lakshmanan PL (2002) Biocontrol potential of native isolates of Pseudomonas fluorescens against rice root nematode, Hirschmanniella gracilis. J Ecobiol 15(2):69–72.

  196. Seenivasan N (2007). Integrated management of root-knot nematode Meloidogyne incognita in medicinal Coleus. 7th Nat Sym plant Prot Options Implement Feasibility 20–22 Dec, pp. 100.

  197. Seenivasan N, David PMM, Vivekanandan P, Samiyappan R (2012) Biological control of rice root-knot nematode, Meloidogyne graminicola through mixture of Pseudomonas fluorescens strains. Biocont Sci Tech 22:611–632

  198. Seenivasan N, Poornima K (2010) Bio-management of root-knot nematode, Meloidogyne incognita (Kofoid and White) Chitwood in Jasmine (Jasminum sambac L.). Pest Manag Hort Ecosyst 16:34–40

  199. Sekhar NS, Gill JS (1991) Efficacy of Pasteuria penetrans alone and in combination with carbofuran in controlling Meloidogyne incognita. Indian J Nematol 21:61–65

  200. Senthilkumar P, Jonathan EI, Samiyappan R (2008) Bioefficacy of Pseudomonas fluorescens on burrowing nematode, Radopholus similis in banana. Indian J Nematol 38:46–52

  201. Shamalie BVT, Fonseka RM, Rajapaksha RGAS (2011) Effect of Trichoderma viride and carbofuran (Curator®) on management of root-knot nematodes and growth parameters of gotukola (Centella asiatica L.). Trop Agric Res 23:61–69

  202. Shanthi A, Rajeswari S, Sivakumar CV, Mehta UK (1998) Soil application of Pseudomonas fluorescens (Migula) for the control of root knot nematode (Meloidogyne incognita) on grapevine (Vitis vinifera Linn.). Nematology: challenges and opportunities in 21st Century. Procthe Third International Symposium of Afro-Asian Society of Nematologists (TISAASN). Sugarcane Breeding Institute (ICAR), Coimbatore, India, 16–19, Apr, 1998. pp. 203–206.

  203. Sharf R, Shiekh H, Syed A, Akhtar A, Robab MI (2014a) Interaction between Meloidogyne incognita and Pochonia chlamydosporia and their effects on the growth of Phaseolus vulgaris. Archiv Phytopath Pl Prot 47:622–630

  204. Sharf R, Abbasi A, Akhtar A (2014b) Combined effect of biofertilizers and fertilizer in the management of Meloidogyne incognita and also on the growth of red kidney bean (Phaseolus vulgaris). Int J Plant Pathology 5:1–11

  205. Sharma HK, Kamra A, Pankaj Lal J, Kumar J (2008) Effect of seed treatment with Pseudomonas fluorescens alone and in combination with soil application of carbofuran and neem seed powder against Meloidogyne incognita in okra. Pesticide Res J 20:79–82

  206. Sharma HK, Prasad D, Sharma P (2005) Compatibility of fungal bioagents as seed dressers with carbofuran in okra against Meloidogyne incognita. National Symposium on Recent Advances and Research Priorities in Indian Nematology, pp. 9–11.

  207. Sharma RD (1992) Biocontrol efficacy of Pasteuria penetrans against Meloidogyne javanica. Ciencia Biologica Ecologica e Systematica 12:43–47

  208. Sharon E, Bar EM, Chet I, Herrera EA, Kleifeld O, Spiegel Y (2001) Biological control of the root-knot nematode M. javanica by T. harzianum. Phytopathology 91:687–693

  209. Siddiqui IA, Ehteshamul-Haque S (2000) Effect of Verticillium chlamydosporium and Pseudomonas aeruginosa in the control of Meloidogyne javanica on tomato. Nematol Medit 28:193–196

  210. Siddiqui IA, Shaukat SS (2003) Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: importance of bacterial secondary metabolite 2,4-diacetylphloroglucinol. Soil Biol Biochem 35:1615–1623

  211. Siddiqui IA, Zareen A, Zaki MJ, Shaukat SS (2001a) Use of Trichoderma species in the control of Meloidogyne javanica, root knot nematode in okra and mungbean. Pakistan J Biol Sci 4:846–848

  212. Siddiqui ZA, Iqbal A, Mahmood I (2001b) Effects of Pseudomonas fluorescens and fertilizers on the reproduction of Meloidogyne incognita and growth of tomato. Appl Soil Ecol 16:179–185

  213. Siddiqui ZA, Mahmood I (1995) Some observations on the management of the wilt disease complex of pigeonpea by treatment with a vesicular arbuscular fungus and biocontrol agents for nematodes. Bioresource Tech 54:227–230

  214. Siddiqui ZA, Mahmood I (1996) Biological control of Heterodera cajani and Fusarium udum on pigeonpea by Glomus mosseae, Trichoderma harzianum, and Verticillium chlamydosporium. Israel J Pl Sci 44:49–56

  215. Siddiqui ZA, Mahmood I, Hayat S (1998) Biocontrol of Heterodera cajani and Fusarium udum on pigeonpea using Glomus mosseae, Paecilomyces lilacinus and Pseudomonas fluorescens. Thai J Agric Sci 31:310–321

  216. Siddiqui ZA, Qureshi A, Akhtar MS (2009) Biocontrol of root-knot nematode Meloidogyne incognita by Pseudomonas and Bacillus isolates on Pisum sativum. Archiv Phytopath Pl Prot 42:1154–1164

  217. Silva JO, Santana MV, Freire LL, Ferreira BS, Rocha MR (2017) Biocontrol agents in the management of Meloidogyne incognita in tomato. Available at: https://doi.org/10.1590/0103-8478cr20161053 (Accessed 9 Dec 2017).

  218. Simon LS, Pandey A (2010) Antagonistic efficacy of Paecilomyces lilacinus and Verticillium chlamydosporium against Meloidogyne incognita infecting okra. Indian J Nematol 40:113

  219. Singh B, Dhawan SC (1994) Effect of Pasteuria penetrans on the penetration and multiplication of Heterodera cajani in Vigna unguiculata roots. Nematol Medit 22:159–161

  220. Singh B, Dhawan SC (1996) Suppression of Heterodera cajani by Pasteuria penetrans during three successive plantings of cowpea. Indian J Nematol 26:216–221

  221. Singh B, Dhawan SC (1999) Comparison of different methods of application of Pasteuria penetrans for the control of Heterodera cajani in cowpea. Indian J Nematol 29:118–120

  222. Singh LM, Mahanta B (2013) Effect of carbosulfan, Glomus fasciculatum, Trichoderma harzianum and vermicompost alone and combination in management of Meloidogyne incognita on green gram. Ann Pl Prot Sci 21:154–156

  223. Singh M, Singh J, Gill JS (2008) Impact of Pasteuria penetrans on root-knot nematode (Meloidogyne incognita) infecting tomato (Lycopersicon esculentum). Indian J Agric Sci 78:1092–1094

  224. Singh P, Siddiqui ZA (2010) Biocontrol of root-knot nematode Meloidogyne incognita by the isolates of Pseudomonas on tomato. Archiv Phytopath Pl Prot 43:1423–1434

  225. Singh S (2013) Integrated approach for the management of the root-knot nematode, Meloidogyne incognita, on eggplant under field conditions. Nematology 15:747–757

  226. Singh SM, Azam MF, Khan AM, Saxena SK (1991) Effect of Aspergillus niger and Rhizoctonia solani on development of Meloidogyne incognita on tomato. Cur Nematol 2:163–166

  227. Sivakumar CV, Bhaskaramanian MD, Balasaraswathy S (1993) Control of root-knot nematode, Meloidogyne araneria in brinjal nursery with fungus, Paecilomyces lilacinus and systemic nematicide carbofuran. J Biol Cont 7:49–50

  228. Somasekhar N, Gill JS (1991) Efficacy of Pasteuria penetrans alone and in combination with carbofuran controlling Meloidogyne incognita. Indian J Nematol 21:61–65

  229. Sosamma VN, Geetha SM, Koshy PK (1994) Effect of the fungus, Paecilomyces lilacinus on the burrowing nematode Radopholus similis infesting betel vine. Indian J Nematol 24:50–53

  230. Spaull VW (1984) Observations on Bacillus penetrans infecting Meloidogyne in sugarcane fields in South Africa. Revue de Nematol 7:277–282

  231. Stevens G, Lewis E (2017) Status of entomopathogenic nematodes in integrated pest management strategies in the USA. In: Abd-Elgawad MMM, Askary TH, Coupland J (eds) Biocontrol agents: entomopathogenic and slug parasitic nematodes. CAB International, Wallingford, pp 289–311

  232. Stirling GR (1984) Biological control of Meloidogyne javanica with Bacillus penetrans. Phytopathology 74:55–60

  233. Sudha S, Sundararaju P, Iyer R (2000) Effect of Paecilomyces lilacinus for the control of burrowing nematode, Radopholus similis on arecanut seedlings. Indian J Nematol 30:101–103

  234. Thakur NSA, Devi G (2007) Management of Meloidogyne incognita attacking okra by nematophagous fungi, Arthrobotrys oligospora and Paecilomyces lilacinus. Agric Sci Digest 27:50–52

  235. Thakur S, Walia RK (2016) Potential of bacterial parasite, Pasteuria penetrans application as nursery soil treatment and seed treatment in controlling Meloidogyne graminicola infecting rice. Indian J Nematol 46:16–19

  236. Trifonova Z, Tsvetkov I, Bogatzevska N, Batchvarova R (2014) Efficiency of Pseudomonas spp. for biocontrol of the potato cyst nematode Globodera rostochiensis (Woll.). Bulgarian J Agric Sci 20:666–669

  237. Tzortzakakis EA (2007) The effect of the fungus Pochonia chlamydosporia on the root-knot nematode Meloidogyne incognita in pots. Russian J Nematol 15:89–94

  238. Umamaheswari R, Sivakumar M, Subramanian S, Samiyappan R (2004) Induction of systemic resistance by Trichoderma viride treatment in green gram (Vigna radiata) against root-knot nematode Meloidogyne incognita. Cur Nematol 15:1–7

  239. Umamaheswari T, Mani A, Rao PK (1987) Combined efficacy of the bacterial spore parasite, Pasteuria penetrans and nematicides in the control of Meloidogyne javanica on tomato. J Biol Cont l:53–57

  240. Umamaheswari T, Mani A, Rao PK (1988) Efficacy of the bacterial spore parasite, Pasteuria penetrans and oil Cakes in the control of Meloidogyne javanica on tomato. J Biol Cont 2:34–36

  241. Van Damme V, Hoedekie A, Viaene N (2005) Long-term efficacy of Pochonia chlamydosporia for the management of Meloidogyne javanica in glasshouse crops. Nematology 7:727–736

  242. Vargas R, Acosta N, Moullor A, Betancourt C (1992) Control of Meloidogyne spp. with Pasteuria penetrans (Thorne) Sayre and Starr. J Agric University Puerto Rico 76:63–70

  243. Verdejo-Lucas S (1992) Seasonal population fluctuations of Meloidogyne spp. and the Pasteuria penetrans group in Kiwi orchards. Pl Disease 76:1275–1279

  244. Verdejo-Lucas S, Sorribas FJ, Ornat C, Galeano M (2003) Evaluating Pochonia chlamydosporia in a double-cropping system of lettuce and tomato in plastic houses infested with Meloidogyne javanica. Pl Path 52:521–528

  245. Verma KK (2009) Management of Meloidogyne javanica by bacterial antagonist, Pseudomonas fluorescens as seedling root dip in tomato. Indian J Nematol 39:207–210

  246. Vetrivelkalai P, Sivakumar M, Jonathan EI (2010) Bio-control potential of endophytic bacteria on Meloidogyne incognita and its effect on plant growth in bhendi. J Biopesticides 3:52–457

  247. Viaene NM, Abawi GS (2000) Hirsutella rhossiliensis and Verticillium chlamydosporium as biocontrol agents of the root-knot nematode Meloidogyne hapla on lettuce. J Nematol 32:85–100

  248. Viggiano JR, Freitas LG, Lopes EA (2015) Pochonia chlamydosporia var. chlamydosporia (Goddard) Zare & W. Gams for the management of lettuce infected with Meloidogyne javanica (Treub, 1885). Chilean J Agric Res 75:255–258

  249. Vikram, Walia RK (2014) Efficacy of bacterial parasite, Pasteuria penetrans application as nursery soil treatment against root-knot nematode, Meloidogyne javanica infecting tomato in different seasons. Indian J Nematol 44:44–49

  250. Vikram, Walia RK (2015) Efficacy of bacterial parasite, Pasteuria penetrans application as seed treatment against root-knot nematode, Meloidogyne javanica. Indian J Nematol 45:1–6

  251. Wahla V, Maheshwari DK, Bajpai VK (2012) Nematicidal fluorescent pseudomonads for the in vitro and in vivo suppression of root knot (Meloidogyne incognita) of Capsicum annuum L. Pest Manag Sci 68:1148–1155

  252. Walia RK (1994) Assessment of nursery treatment with Pasteuria penetrans for the control of Meloidogyne javanica on tomato in green-house. J Biol Cont 8:68–70

  253. Walia RK, Dalal MR (1994) Efficacy of bacterial parasite, Pasteuria penetrans application as nursery soil treatment in controlling root-knot nematode, Meloidogyne javanica on tomato. Pest Manag Econ Zool 2:19–21

  254. Walia RK, Nandal SN, Bhatti DS (1999) Nematicidal efficacy of plant leaves and Paecilomyces lilacinus alone or in combination in controlling Meloidogyne incognita on okra and tomato. Nematol Medit 27:3–8

  255. Walker GE, Wachtel MF (1989) The influence of soil solarisation and non-fumigant nematicides on infection of Meloidogyne javanica by Pasteuria penetrans. Nematologica 34:477–483

  256. Walters SA, Barker KR (1994) Efficacy of Paecilomyces lilacinus in suppressing Rotylenchulus reniformis on tomato. J Nematol 26:600–605

  257. Wang K, Riggs RD, Crippen D (2005) Isolation, selection, and efficacy of Pochonia chlamydosporia for control of Rotylenchulus reniformis on cotton. Phytopathology 95:890–893

  258. Weibelzahl-Fulton E, Dickson DW, Whitty EB (1996) Suppression of Meloidogyne incognita and Meloidogyne javanica by Pasteuria penetrans in field soil. J Nematol 28:43–49

  259. Wilson MJ, Jackson TA (2013) Progress in the commercialisation of bionematicides. BioCont 58:715–722

  260. Windham GL, Windham MT, Williams WP (1989) Effects of Trichoderma spp. on maize growth and Meloidogyne arenaria reproduction. Pl Disease 73:493–495

  261. Zaki MJ, Maqbool MA (1990) Effect of Pasteuria penetrans and Paecilomyces lilacinus on the control of root-knot nematodes of brinjal and mung. Pakistan J Phytopath 2:37–42

  262. Zareen A, Zaki MJ, Ghaffar A (1999) Effect of culture filtrate of fungi in the control of Meloidogyne javanica root-knot nematodes on okra and broad bean. Pakistan J Biol Sci 2:1441–1444

  263. Zareen A, Zaki MJ, Khan NJ (2001) Effect of fungal filtrates of Aspergillus species on development of root-knot nematodes and growth of tomato (Lycopersicon esculentum Mill). Pakistan J Biol Sci 4:995–999

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Acknowledgements

This study was supported in part by the US-Egypt Project cycle 17 (no. 172) and NRC in-house project entitled “Pesticide alternatives against soilborne pathogens attacking legume cultivation in Egypt”.

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  1. Plant Pathology Department, National Research Centre, El-Behoos St., Dokki, Giza, 12622, Egypt

    • Mahfouz M. M. Abd-Elgawad

  2. Division of Entomology, Sher-e-Kashmir University of Agricultural Sciences and Technology, Shalimar, Srinagar, Jammu and Kashmir, India

    • Tarique Hassan Askary

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Keywords

  • Nematodes
  • Biocontrol
  • Bio-nematicides
  • Integrated pest management
  • Synergism