Fungal and bacterial nematicides in integrated nematode management strategies

Mahfouz M. M. Abd-Elgawad; Tarique Hassan Askary

doi:10.1186/s41938-018-0080-x

Review article
Open Access

Fungal and bacterial nematicides in integrated nematode management strategies

Mahfouz M. M. Abd-Elgawad¹Email author and
Tarique Hassan Askary²

Egyptian Journal of Biological Pest Control201828:74

https://doi.org/10.1186/s41938-018-0080-x

Received: 9 February 2018
Accepted: 7 September 2018
Published: 24 September 2018

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.

Keywords

Nematodes
Biocontrol
Bio-nematicides
Integrated pest management
Synergism

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

Fungus/bacterium	Integrated with	Nematode managed	Crop	Result	Reference
Pasteuria penetrans	Carbofuran	Meloidogyne javanica	Tomato	Combined application of P. penetrans and carbofuran reduced root galling by 50%.	Brown and Nordmeyer 1985
P. penetrans	Neem cake	Meloidogyne incognita	Tomato	P. penetrans in combination with neem cake was found most effective in parasitizing the nematode juveniles and adults as compared to individual treatment.	Rangaswamy et al. 2000
P. penetrans	Neem cake	M. incognita	Psoralea corylifolia	Nematode infection was least when P. penetrans and neem extract were applied in combination. Minimum number of juveniles per root system was observed.	Mehtab et al. 2013
P. penetrans	Neem cake	M. javanica	Tomato	Combined application of P. penetrans and neem (Azadirachta indica) cake reduced nematode population by 75%.	Umamaheswari et al. 1988
P. penetrans	Castor cake	M. incognita	Chilli	Combination of castor and P. penetrans showed greater reduction in galling index (84.75%) and soil population (85.74%) of M. incognita as compared to control (M. incognita alone).	Chaudhary and Kaul 2013
P. penetrans	Nematicides	M. javanica	Tomato	Combined effect of P. penetrans with nematicides (carbofuran, aldicarb, miral, scbufos, and phorate) reduced the root galling.	Umamaheswari et al. 1987
P. penetrans	Carbofuran	M. incognita	Tomato	Combined application of P. penetrans and carbofuran reduced gall formation on tomato roots by 63.02%.	Somasekhar and Gill 1991
P. penetrans	Carbofuran	Heterodera cajani	Pigeonpea	The penetration to host root was minimum when P. penetrans was applied with carbofuran. Number of healthy cysts, eggs/cyst, and total nematode population were significantly reduced in this treatment.	Gogoi and Gill 2001
P. penetrans	Neem cake	M. incognita	Tomato	Increase in plant growth parameters and parasitism of M. incognita female was found when P. penetrans was applied in combination with neem cake.	Parvatha Reddy 1997
P. penetrans	Neem cake	M. javanica	Tomato	Combined application of P. penetrans and neem cake reduced root galling by 32% as compared to nematode alone treatment. The spore-encumbered juveniles were more susceptible to the effects of the neem.	Javed et al. 2008
Pseudomonas fluorescens	Organic manure	M. incognita	Tomato	P. fluorescens GRP3 with organic manure was the best combination for the management of M. incognita on tomato.	Siddiqui et al. 2001b
P. fluorescens	Carbofuran	Meloidogyne graminicola	Rice	Combined application of P. fluorescens and carbofuran 3G increased plant height, root length, and grain yield and decreased nematode population by 79.34%.	Narasimhamurthy et al. 2017a
P. fluorescens	Neem cake (soil application)	M. incognita	Coleus forskohlii	Coleus cutting dipped in 0.1% P. fluorescens at planting + soil application of neem cake @ 400 Kg/ha + growing marigold (Tagetes erecta) as intercrop, uprooted and incorporated with soil at the time of earthing up (60–70 days after planting) reduced the root-knot nematode population by 72%.	Seenivasan 2007
P. fluorescens	Neem seed powder + carbofuran	M. incognita	Okra	Nematode penetration and galling was reduced by 54 and 70%, respectively, on integrated application of P. fluorescens, carbofuran, and neem seed powder as compared to control (nematode alone).	Sharma et al. 2008
Trichoderma harzianum	Neem cake	M. incognita	Tomato	A significant increase in plant growth and decrease in root galling and final population of M. incognita were observed in tomato seedlings transplanted in neem cake-amended soil incorporated with T. harzianum.	Rao et al. 1997a
T. harzianum	Neem cake	Tylenchulus semipenetrans	Acid lime	T. harzianum in combination with neem (Azadirachta indica), karanj (Pongamia pinnata), and castor (Ricinus communis) oil cakes was effective in increasing the growth of acid lime (Citrus aurantifolia) seedlings and reducing the population of T. semipenetrans both in soil and roots in pots.	Parvatha Reddy et al. 1996
	Karanj cake
	Castor cake
T. harzianum	Carbofuran	M. incognita	French bean	T. harzianum in combination with carbofuran resulted in decreased root galling, egg masses, and nematode population in soil by 65.15% as compared to untreated control.	Gogoi and Mahanta 2013
T. harzianum	Carbofuran	M. incognita	Brinjal	Combined application of T. harzianum and carbofuran resulted in decreased root galling, egg masses, and nematode population in soil.	Devi et al. 2016
T. harzianum	Carbofuran	M. incognita	Mentha arvensis	T. harzianum + carbofuran resulted in lowest root galling.	Haseeb et al. 2007
T. harzianum	Carbofuran	M. incognita	Pea	T. harzianum + carbofuran proved more effective than T. harzianum + neem cake in reducing the root galls, egg masses, and nematode population in soil.	Brahma and Borah 2016
T. harzianum	Neem cake	M. incognita	Pea		Brahma and Borah 2016
T. harzianum	Neem cake	M. incognita	Chick pea	Combined application of T. harzianum and neem cake reduced galling on chickpea roots.	Pant and Pandey 2002
T. harzianum	Lantana camara	M. incognita	Tomato	T. harzianum + Lantana camara resulted in a significant difference in the reduction of root-knot nematode population, nematode reduction rate, number of galls, and egg masses per plant.	Feyisa et al. 2015
T. harzianum	Neem cake + P. fluorescens	M. incognita	Brinjal	T. harzianum in combination with neem cake + P. fluorescens significantly reduced the incidence of root-knot disease of eggplant. Root galls were reduced by 81%, and yield of eggplant was enhanced by up to 70% as compared to check (nematode alone).	Singh 2013
T. viride	Carbofuran	M. graminicola	Rice	Combined application of T. viride and carbofuran increased plant height, root length, and grain yield and decreased nematode population by 69.17%.	Narasimhamurthy et al. 2017a
T. viride	P. lilacinus + carbofuran + mustard cake	M. incognita	Tomato	Integrated application of T. viride along with P. lilacinus, carbofuran, and mustard cake showed least nematode reproduction factor (0.0) as compared to untreated infested soil (1.783).	Goswami et al. 2006
T. viride	Compost	Meloidogyne spp.	Gotukola (Centella asiatica)	Treatments of T. viride + compost had significant reduction in root gall formation in Gotukola besides significant impact on plant growth that attributed to increased number of roots, leaf length, stalk length, and root length and highest fresh weight of leaves of first harvest.	Shamalie et al. 2011
T. viride	Neem cake	M. incognita	Tomato	T. viride in combination with either neem or castor cake was found most effective in parasitizing the egg masses of the nematode as compared to individual treatment.	Rangaswamy et al. 2000
T. viride	Castor cake	M. incognita	Tomato		Rangaswamy et al. 2000
T. viride	Neem cake	M. incognita	Tobacco	Integrated application of T. viride along with neem cake significantly reduced the number of galls and egg masses on tobacco root.	Raveendra et al. 2011
T. viride	P. chlamydosporia + urea	M. incognita	Red kidney bean	T. viride + P. chlamydosporia + urea reduced galls and egg masses per root system.	Sharf et al. 2014a, b
Paecilomyces lilacinus	Neem cake + NPK (nitrogen, phosphorus, potassium)	M. incognita	Tomato	The antagonistic potential of P. lilacinus against M. incognita infesting tomato seedlings under nursery conditions was enhanced (53.6%) when applied in combination with neem cake and NPK.	Nagesh et al. 2001
P. lilacinus	Neem cake	Heterodera zeae	Sweet corn	Combined application of P. lilacinus with neem cake and karanj leaves resulted in decline of cyst population in soil by 63.04% and 52.17%, respectively.	Baheti et al. 2017
P. lilacinus	Karanj leaves	Heterodera zeae	Sweet corn		Baheti et al. 2017
P. lilacinus	Neem seed powder + dimethoate	M. incognita	Pigeonpea	Seed treatment with P. lilacinus + neem seed powder + dimethoate improved the pigeonpea yield up to 30% and suppressed the galling and nematode population up to 77%.	Askary 2008
P. lilacinus	Neem leaf suspension	M. incognita	Brinjal	P. lilacinus + neem leaf suspension @ 5% and 10% resulted in nematode egg parasitization by 59 and 64%, respectively, and decrease in final nematode population by 64.10 and 71.47%, respectively.	Rao et al. 1997b
P. lilacinus	Aldicarb	M. javanica	Tomato	The smallest galling index, number of galls, and nematode population were in soils treated with P. lilacinus in combination with aldicarb followed by P. lilacinus + chicken manure, P. lilacinus + R. communis, P. lilacinus + T. minuta, and P. lilacinus + D. stramonium.	Oduor-Owino 2003
	Tagetes minuta
	Datura stramonium
	Ricinus communis
	Chicken manure
P. lilacinus	Groundnut cake	M. javanica	Brinjal	The highest improvement in plant growth and best protection against M. javanica was obtained by the integration of P. lilacinus with groundnut cake followed by neem cake, linseed cake, castor cake, and mahua cake.	Ashraf and Khan 2010
	Neem cake
	Linseed cake
	Castor cake
	Mahua cake
P. lilacinus	Neem cake	Soil nematodes	Pigeonpea	Damage caused by the nematodes was significantly reduced when P. lilacinus was added along with oil-cakes. Most effective combination of P. lilacinus was with neem cake.	Anver 2003
	Mustard cake
	Castor cake
P. lilacinus	Neem cake	M. incognita	Tomato	Increase in plant growth parameters and nematode egg parasitism was found when P. lilacinus was applied in combination with neem cake.	Parvatha Reddy et al. 1997
Pochonia chlamydosporia	P. fluorescens + T. viride + carbofuran	Globodera spp.	Potato	Combined application of P. chlamydosporia along with P. fluorescens, T. viride, and carbofuran resulted in significantly higher plant growth and lower cyst nematode (Globodera spp.) population in soil and root. There was 70.57% increase in tuber weight and 71.93% decrease in the cyst population. A significant reduction in the population of eggs and juveniles was also noted.	Muthulakshmi et al. 2012
P. chlamydosporia	Carbofuran	M. incognita	Tomato	P. chlamydosporia + carbofuran resulted in maximum plant growth and minimum galls and egg masses.	Gopinatha et al. 2002
P. chlamydosporia	Neem cake + dazomat	M. incognita	Rose	Soil application of P. chlamydosporia + neem cake + dazomat resulted in maximum percent healthy root and flower yield and reduced the root galls.	Nagesh and Jankiram 2004
P. chlamydosporia	Carbofuran + neem cake	M. incognita	Okra	Integrated application of P. chlamydosporia along with carbofuran and neem cake suppressed root-knot disease severity in terms of galling, egg production, and nematode population by 89%, 90%, and 81%, respectively.	Dhawan and Singh 2009
P. chlamydosporia	Neem cake	M. incognita	Brinjal	A significant reduction in nematode multiplication was observed when soil was treated with P. chlamydosporia + neem cake and P. chlamydosporia + mustard cake.	Parihar et al. 2015
P. chlamydosporia	Mustard cake	M. incognita	Brinjal		Parihar et al. 2015
P. chlamydosporia	Neem cake	H. zeae	Sweet corn	Combined application of P. chlamydosporia with neem cake resulted in decline of cyst population in soil by 54.35%.	Baheti et al. 2017

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
*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

Fig. 2
*Catenaria anguillulae*. a Chain of mature and immature sporangium. b Double chain of mature and immature sporangium on nematode cadaver

Fig. 3
*Catenaria anguillulae*. A. A conidium on agar surface under germination. B. A portion of hypha with adhesive network. C. Detached conidium

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)

	Mode of action
Fungus
Aspergillus niger	It is an egg parasite and induces systemic resistance against plant-parasitic nematodes. The fungus coming in contact with a cyst or an egg mass begins to grow rapidly. It colonizes the eggs where larval formation has not been completed, thus providing early protection to the growing plants against nematodes.
Paecilomyces lilacinus	It is mainly egg parasite. The fungus produces antibiotics viz., leucinostatin and lilacin and enzymes such as protease and chitinase. Protease has nematicidal activity, causes degradation of the eggshell, and inhibits hatching. Chitinase breaks down the eggshell making the route for the fungus to pass through. The decomposition of chitin releases ammonia, which is toxic to second-stage juveniles of root-knot nematode (RKN). Its hypha enters the vulva and anus of RKN females. The fungus penetrates the egg and develops profusely inside and over the eggs, completely inhibiting juvenile development. The infected eggs swell and buckle. As penetration continues, the vitelline layer of the egg splits into three bands and a large number of vacuoles; lipid layer disappears at this stage. The developing juvenile inside the egg is destroyed by the rapidly growing hyphae. Many conidiophores are produced and the hypha moves to the adjacent eggs.
Trichoderma harzianum	Secretes many lytic enzymes like chitinase, glucanases, and proteases which help parasitism of Meloidogyne and Globodera eggs. The chitin layer is dissolved through enzymatic activity. The hyphae of T. harzianum penetrate the eggs and juvenile cuticle, proliferate within the organism, and produce toxic metabolites.
T. viride	Produce antibiotics like trichodermin, dermadin, trichoviridin, and sesquiterpene heptalic acid which are involved in the suppression of nematodes.
Pochonia chlamydosporia	Parasitizes the eggs and adult females of plant-parasitic nematodes. The root-knot and cyst nematodes are the primary hosts of this fungus, but it is also known to parasitize citrus, burrowing, and reniform nematodes. The fungus enters the nematode cysts either through natural openings or it may directly penetrate the wall of the cyst. It forms a branched mycelia network when in close contact with the smooth eggshell. The fungus produces an appressorium that adheres to the eggshell by mucigens and from which an infection peg develops and penetrates the eggshell. Penetration also occurs from lateral branches of the mycelium. This results in disintegration of the eggshell’s vitelline layer and also partial dissolution of the chitin and lipid layers, possibly due to the activity of exoenzymes. Egg hatching is inhibited due to toxins secreted by the fungus.
Bacteria
Pasteuria penetrans	Bacterial spores are attached to the nematode’s body and germinate forming a germ tube that penetrates the body cuticle. Vegetative mycelial colonies eventually fill the body with a large number of endospores.
Pseudomonas fluorescens	Produce antibiotics viz., phenazines, tropolone, pyrrolnitrin, pyocyanin, and 2,4-diacetylphloroglucinol which have suppressive effect on plant-parasitic nematodes.
Bacillus firmus	Enzymatic action, degradation of root exudates, root-protection, and the production of a phytohormone.
B. thuringiensis	Nematicidal toxins found in families of B. thuringiensis proteins.
B. subtilis	The genes are encoding surfactin and iturin synthesis as antibiotics.

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))

Fungus	Product	Formulation	Company/institution	Country
Aspergillus niger	Kalisena	Soluble (liquid) concentrate	Cadila Pharmaceutical Limited	India
A. niger	Kalisena	Suspension concentrate for direct application	Cadila Pharmaceutical Limited	India
A. niger	Beej Bandhu	Wettable powder	–	India
A. niger	Pusa Mrida	Wettable powder	–	India
A. niger	Kalasipahi	Capsule	–	India
Pochonia chlamydosporia	KlamiC®	Granulate	Rothamsted Research and Centro Nacional de Sanidad Agropecuaria	UK, Cuba
P. chlamydosporia	PcMR-1 strain	Liquid	Clamitec, Myco solutions, Lda	Portugal
P. chlamydosporia	Xianchongbike	Liquid	Laboratory for Conservation and Utilization of Bio-resources, Yunnan University	China
P. chlamydosporia	IPP-21	–	–	Italy
Purpureocillium lilacinus	BIOACT®WG	Water-dispersible granulate	Bayer Crop Science	USA
P. lilacinus	BIOACT®WP	Water-dispersible powder	Bayer Crop Science	USA
P. lilacinus	PL Gold	Wettable powder	BASF Worldwide, Becker Underwood	South Africa
P. lilacinus	Stanes Bio Nematon	Liquid or powder	Imported from T. Stanes and Company Limited, India, by Gaara company, Egypt	India and Egypt
P. lilacinus	PL 251	Water-dispersible granulate	Biological Control Products	South Africa
P. lilacinus	BIOCON	Wettable powder	Asiatic Technologies Incorporation	Philippines
P. lilacinus	Shakti Paecil	Wettable powder	Shakti Biotech	India
P. lilacinus	PAECILO®	Wettable powder	Agri Life	India
P. lilacinus	Paecilon	Liquid	Enpro Bio Sciences Private Limited	India
P. lilacinus	Nematofree	Wettable powder	International Panaacea Limited	India
P. lilacinus	Gmax bioguard	Talc based carrier	Greenmax Agro Tech	India
P. lilacinus	Yorker	Wettable powder	Agriland Biotech	India
P. lilacinus	Miexianning	Talc based carrier	Agricultural Institute, Yunan Academy of Tobacco Science	China
P. lilacinus	Pl Plus® (P. lilacinus strain 251)	Wettable powder	Biological Control Products	South Africa
P. lilacinus	Melocon®WG	Water-dispersible granulate	Prophyta GmbH Certis	Germany, USA
Trichoderma harzianum	Romulus	Wettable powder	DagutatBiolab	South Africa
T. harzianum	ECOSOM®	Wettable powder	Agri Life	India
T. harzianum	Trichobiol	Wettable powder	Control Biologico Integrado; Mora Jaramillo Arturo Orlando—Biocontrol	Columbia
T. harzianum	Commander Fungicide	Wettable powder	H.T.C Impex Private Limited	India
T. viride	Trifesol	Wettable powder	Biocultivos Agricultura Sostenible	Columbia

Table 4

Biocontrol agents of fungal species targeting nematodes on economic crops

Fungus	Nematode managed	Crop	Reference
Aspergillus niger	Meloidogyne incognita	Mung bean	Bhat and Wani 2012
A. niger	Meloidogyne spp.	Tomato	Li et al., 2011
A. niger	Meloidogyne javanica	Tomato	Zareen et al. 2001
A. niger	M. javanica	Pigeonpea	Askary 2012
A. niger	Meloidogyne arenaria	Tomato	Mokbel et al. 2009
A. niger	M. incognita	Okra	Sharma et al. 2005
A. niger	Meloidogyne spp.	Tomato	Singh et al. 1991
A. niger	Meloidogyne spp.	Tomato	Khan et al. 1984
A. niger	M. incognita	Brinjal	Goswami and Singh 2002
A. niger	M. javanica	Chickpea	Hussain et al. 2001
Paecilomyces lilacinus	Meloidogyne graminicola	Rice	Narasimhamurthy et al. 2017a, b
P. lilacinus	M. incognita	Black gram	Kumar et al. 2017
P. lilacinus	M. incognita	Chrysanthemum	Nagesh et al. 2003
P. lilacinus	M. incognita	Banana	Devrajan and Rajendran 2002
P. lilacinus	M. incognita	Okra	Saikia and Roy 1994
P. lilacinus	M. incognita	Okra	Davide and Zorilla 1986
P. lilacinus	M. incognita	Okra	Simon and Pandey 2010
P. lilacinus	M. incognita	Tobacco	Ramakrishnan and Nagesh 2011
P. lilacinus	M. javanica	Tomato	Ganaie and Khan 2010
P. lilacinus	M. javanica	Tomato	Maheswari and Mani 1989
P. lilacinus	M. incognita	Pittosporum tobira (mock orange)	Baidoo et al. 2017
P. lilacinus	Rotylenchulus reniformis	Tomato	Walters and Barker 1994
P. lilacinus	R. reniformis	Chickpea	Ashraf and Khan 2008
P. lilacinus	M. incognita	Cardamom	Eapen and Venugopal 1995
P. lilacinus	Heterodera cajani	Pigeonpea	Siddiqui and Mahmood 1995
P. lilacinus	Radopholus similis	Banana	Mendoza et al. 2004
P. lilacinus	M. javanica	Tomato	Khan et al. 2006
	Rotylenchulus similis	Banana
	Heterodera avenae	Barley
P. lilacinus	M. incognita	Tomato	Oclarit and Cumagun 2009
P. lilacinus	M. incognita	Tomato	Khan and Goswami 2000
P. lilacinus	R. similis	Betelvine	Sosamma et al. 1994
P. lilacinus	R. similis	Arecanut	Sudha et al. 2000
P. lilacinus	M. incognita	Tomato	Candanedo-Lay et al. 1982
P. lilacinus	M. incognita	Tomato	Roman and Rodriguez-Marcano 1985
P. lilacinus	Meloidogyne spp.	Lettuce	Prakob et al. 2009
P. lilacinus	M. incognita	Tobacco	Ramakrishnan and Rao 2013
P. lilacinus	M. javanica	Tomato	Khan and Esfahani 1990
P. lilacinus	M. javanica	Pumpkin, Guar, Chili, Watermelon	Perveen et al. 1998
P. lilacinus	Tylenchulus semipenetrans	Citrus Jambhiri	Deka et al. 2002
P. lilacinus	M. incognita	Tomato	Goswami and Mittal 2004
P. lilacinus	M. incognita	Bitter gourd	Bhat et al. 2009
P. lilacinus	M. incognita	Brinjal	Nisha and Sheela 2016
P. lilacinus	M. incognita	Okra, Tomato	Walia et al. 1999
P. lilacinus	T. semipenetrans	Citrus (KhasiMandarin)	Mahanta et al. 2016
P. lilacinus	T. semipenetrans	Citrus (KhasiMandarin)	Manzoor et al. 2002
P. lilacinus	M. incognita	Tomato	Cabanillas and Barker 1989
P. lilacinus	M. incognita	Tomato	Khalil et al. 2012a
P. lilacinus	M. incognita	Tomato	Khalil et al. 2012b
P. lilacinus	M. incognita	Tomato	Amin 2000
P. lilacinus	M. incognita	Tomato	Cabanillas et al. 1989
P. lilacinus	M. incognita	Okra	Thakur and Devi 2007
P. lilacinus	H. cajani	Pigeonpea	Siddiqui et al. 1998
P. lilacinus	M. javanica	Tobacco	Hewlett et al. 1988
P. lilacinus	M. javanica	Tomato	Esfahani and Pour 2006
P. lilacinus	M. incognita acrita	Potato	Jatala et al. 1979
P. lilacinus	Globodera pallida	Potato	Jatala et al. 1979
P. lilacinus	M. incognita	Potato	Jatala et al., 1980
P. lilacinus	M. javanica	Pigeonpea	Askary 2012
P. lilacinus	M. incognita	Banana	Jonathan and Rajendran 2000
P. lilacinus	M. incognita	Betelvine	Jonathan et al. 1995
P. lilacinus	M. incognita	Cowpea	Hasan 2004
P. lilacinus	M. incognita	Okra	Dhawan et al. 2004
P. lilacinus	M. incognita	Betelvine	Bhatt et al. 2002a
P. lilacinus	R. reniformis	Tomato	Parvatha Reddy and Khan 1988
P. lilacinus	R. reniformis	Chickpea	Anver and Alam 1999
P. lilacinus	R. reniformis	Pigeonpea	Anver and Alam, 1997
P. lilacinus	M. javanica	Broad bean, Okra	Zareen et al. 1999
P. lilacinus	M. arenaria	Brinjal	Sivakumar et al. 1993
P. lilacinus	M. incognita	French bean	Santin 2008
Pochonia chlamydosporia	M. incognita	Tomato	Silva et al. 2017
P. chlamydosporia	M. javanica	Lettuce	Viggiano et al. 2015
P. chlamydosporia	M. javanica	Tomato and Pepper	Tzortzakakis 2007
P. chlamydosporia	M. incognita	Tomato	De Leij et al. 1992
P. chlamydosporia	M. javanica	Broad bean, Okra	Zareen et al. 1999
P. chlamydosporia	Heterodera schachtii	Sugar beet	Ebrahim et al. 2008
P. chlamydosporia	M. incognita	Brinjal	Parihar et al. 2015
P. chlamydosporia	M. incognita	Bell pepper	Rao et al. 2004
P. chlamydosporia	M. incognita	Tomato	Sankaranarayanan et al. 2000
P. chlamydosporia	H. cajani	Pigeonpea	Siddiqui and Mahmood 1995
P. chlamydosporia	Heterodera avenae	Wheat	Bhardwaj and Trivedi 1996
P. chlamydosporia	Meloidogyne hapla	Tomato	De Leij et al. 1993
P. chlamydosporia	M. javanica	Lettuce and Tomato	Verdejo-Lucas et al. 2003
P. chlamydosporia	M. incognita	Okra	Kumar and Jain 2010a
P. chlamydosporia	M. incognita	Okra	Dhawan and Singh 2010
P. chlamydosporia	M. javanica	Tomato	Siddiqui and Ehteshamul-Haque 2000
P. chlamydosporia	M. incognita	Pigeonpea	Askary, 2008
P. chlamydosporia	M. incognita	Common bean	Sharf et al. 2014a
P. chlamydosporia	M. incognita	Brinjal	Rao et al., 2003
P. chlamydosporia	M. incognita	Brinjal	Dhawan et al. 2008
P. chlamydosporia	R. reniformis	Cotton	Wang et al. 2005
P. chlamydosporia	M. hapla	Lettuce	Viaene and Abawi 2000
P. chlamydosporia	M. incognita	Lettuce and Tomato	Van Damme et al. 2005
P. chlamydosporia	H. cajani	Pigeonpea	Kumar and Prabhu 2008
Trichoderma harzianum	M. javanica	Tomato	Feyisa et al. 2016
T. harzianum	H. cajani	Pigeonpea	Kumar and Prabhu 2008
T. harzianum	M. javanica	Tomato	Naserinasab et al. 2011
T. harzianum	Meloidogyne spp.	Cardamom	Anonymous 1995
T. harzianum	M. incognita	Chickpea	Hemlata et al. 2002
T. harzianum	M. incognita	Chickpea	Pant and Pandey 2002
T. harzianum	M. incognita	Pea	Brahma and Borah 2016
T. harzianum	M. arenaria	Maize	Windham et al. 1989
T. harzianum	M. incognita	Brinjal	Devi et al. 2016
T. harzianum	M. incognita	Cardamom	Eapen and Venugopal 1995
T. harzianum	H. cajani	Pigeonpea	Siddiqui and Mahmood 1996
T. harzianum	M. incognita	French bean	Gogoi and Mahanta 2013
T. harzianum	M. incognita	Brinjal	Kumar and Chand 2015
T. harzianum	M. incognita	Green gram	Deori and Borah 2016
T. harzianum	M. incognita	Pigeonpea	Askary 2008
T. harzianum	M. incognita	Tomato	Kumar and Khanna 2006
T. harzianum	M. javanica	Tomato	Sharon et al. 2001
T. harzianum	M. incognita	Brinjal	Rao et al. 1998
T. harzianum	M. graminicola	Paddy	Pathak and Kumar 2003
T. harzianum	M. incognita	Green gram	Singh and Mahanta 2013
T. harzianum	M. javanica	Tomato	Jamshidnejad et al. 2013
T. harzianum	Meloidogyne spp.	Tomato	Khattak and Khattak 2011
T. harzianum, T. viride	M. incognita	Okra	Kumar and Jain 2010b
T. harzianum, T. viride	M. incognita	Okra	Prasad and Anes 2008
T. harzianum, T. viride	M. javanica	Tomato	Al-Hazmi and Javeed 2016
T. harzianum, T. viride	M. incognita	Tomato	Dababat et al. 2006
T. harzianum, T. viride	M. incognita	Tomato	Devi and Sharma 2002
T. harzianum, T. virens	M. graminicola	Rice	Pathak et al. 2005
T. harzianum, T. viride	M. incognita	Tomato	Dababat and Sikora 2007
T. harzianum, T. viride	M. javanica	Mung bean, Okra	Siddiqui et al. 2001a
T. harzianum, T. viride	Meloidogyne spp.	Roundleaf fountain Palm	Jegathambigai et al. 2011
T. harzianum, T. viride	M. javanica	Brinjal	Bokhari 2009
T. harzianum, T. viride	R. reniformis	Brinjal	Bokhari 2009
T. viride	M. incognita	Mulberry	Muthulakshmi et al. 2010
T. viride	M. incognita	Tomato	Goswami and Mittal 2004
T. viride	M. incognita	Soybean	Devi and Hassan 2002
T. viride	M. incognita	Chickpea	Pandey et al. 2003
T. viride	Helicotylenchus multicinctus	Banana	Jonathan et al. 2004
T. viride	M. incognita	Okra	Chatali et al. 2003
T. viride	Pratylenchus thornei	Chickpea	Dwivedi et al. 2008
T. viride	M. incognita	Cucumber	Krishnaveni and Subramanian 2004
T. viride	M. incognita	Tomato	Rangaswamy et al. 2000
T. viride	M. incognita	Mulberry	Muthulakshmi and Devrajan 2015
T. viride	M. incognita	Betelvine	Bhatt et al. 2002b
T. viride	M. graminicola	Rice	Priya 2015
T. viride	M. incognita	Green gram	Umamaheswari et al. 2004
T. viride	M. incognita	Sugar beet	Kavitha et al. 2007
T. viride	M. incognita	Cowpea	Kumar et al. 2011
T. viride	R. reniformis	Cowpea	Kumar et al. 2011
T. virens	M. incognita	Bell pepper	Meyer et al. 2001
Trichoderma spp.	M. incognita	Common bean	Santin 2008

Table 5

List of commercial products of bacterial biocontrol agents used in the management of plant-parasitic nematodes

Bacterium	Product name	Company/institution	Country
Pasteuria penetrans	Econem	Nematech	Japan
Pasteuria penetrans	Econem	Pasteuria Bioscience	USA
P. nishizawae	Clariva PN	Syngenta	Brazil
P. usage (or P. penetrans)	Econem	Bayer CropScience	Multi-national
Pseudomonas fluorescens	SHEATHGUARD (or Sudozone)	Agriland Biotech	India
Bacillus cereus (CM-1c strain) and Bacillus subtilis (CM-5 strain)	BioStart™ Defensor	Bio-Cat Microbials	USA
Bacillus thuringiensis	Avid 0.15EC (or abamectin)	Syngenta	Multinational
Bacillus subtilis	Stanes Sting	Imported from T. Stanes and Company Limited, India, by Gaara company, Egypt	India and Egypt
B. licheniformis B. subtilis	Quartzo	FMC Química do Brasil Ltda.	Brazil
B. licheniformis B. subtilis	Nemix C	FMC Química do Brasil Ltda.	Brazil
B. licheniformis strain FMCH001(DSM32154) B. subtilis strain FMCH002 (DSM32155)	Presense	FMC Química do Brasil Ltda.	Brazil
B. firmus	1. Bionem-WP 2. BioSafe-WP 3. Chancellor	Agro Green	Israel
B. firmus strain GB-126	VOTiVO®WP	Bayer Crop Science	Germany
B. methylotrophicus	Onix	Laboratorio de Bio Controle Farroupilha S.A.	Brazil
B. subtilis	Pathway Consortia®	Pathway Holdings	USA
B. chitinosporus, B. laterosporus, B. licheniformis (mixture)	BioStart® BioStart™	Bio-Cat Rincon-Vitova	USA
B. amyloliquefaciens	Nemacontrol	Simbiose Indústria e Comércio de Fertilizantes e Insumos	Brazil
Bacillus sp., Pseudomonas sp., Rhizobacterium sp., Rhizobium sp.	Micronema	Agricultural Research Centre	Egypt
B. cereus	Xian Mie	XinYi Zhong Kai Agro- Chemical industry CO., Ltd.	China
Bacillus spp.	Nemix	Chr. Hansen	Brazil
Burkholderia cepacia	Deny Blue circle	Stine Microbial Products	USA
Serratia marcescens produces volatile metabolites toxic to and other PPNs	Nemaless	Agricultural Research Centre	Egypt

Table 6

List of bacterial biocontrol agents against phytonematodes infesting agricultural crops

Bacterium	Nematode managed	Crop	Reference
Pasteuria penetrans	Meloidogyne incognita	Tomato, cucumber	Kokalis-Burelle 2015
Pasteuria penetrans	Meloidogyne arenaria	Snapdragon	Kokalis-Burelle 2015
P. penetrans	M. arenaria	Tomato, oriental melon	Cho et al. 2000
P. penetrans	Meloidogyne spp.	Brinjal, mung bean	Zaki and Maqbool 1990
P. penetrans	Heterodera cajani	Cowpea	Singh and Dhawan 1994, 1996, 1999
P. penetrans	Meloidogyne spp.	Sugarcane	Spaull 1984
P. penetrans	M. incognita	Tobacco, soybean, hairy vetch	Brown et al. 1985
P. penetrans	M. incognita	Tomato	Vargas et al. 1992
P. penetrans	M. incognita	Kiwi	Verdejo-Lucas 1992
	M. arenaria
	Meloidogyne hapla
P. penetrans	Xiphinema diversicaudatum	Peach	Ciancio 1995
P. penetrans	M. arenaria	Peanut	Chen et al. 1996, Chen et al. 1997
P. penetrans	M. javanica	Chickpea	Sharma 1992
P. penetrans	M. javanica	Tomato	Maheswari and Mani 1989
P. penetrans	M. incognita	Tomato	Mankau and Prasad 1972
	M. javanica
	Pratylenchus scribneri
P. penetrans	M. javanica	Tomato	Stirling 1984
P. penetrans	M. javanica	Grape	Stirling 1984
P. penetrans	M. arenaria	Peanut, rye, and vetch	Oostendorp et al. 1991
P. penetrans	M. acronea	Tomato	Page and Bridge 1985
P. penetrans	M. incognita	Banana, tomato	Jonathan et al. 2000
P. penetrans	M. incognita	Tomato	Chand and Gill 2002
P. penetrans	M. javanica	Tomato	Daudi et al. 1990
P. penetrans	M. javanica	Tomato	Daudi and Gowen 1992
P. penetrans	M. incognita	Tomato	De Channer 1989
P. penetrans	M. incognita	Tobacco, soybean, tomato, hairy vetch, pepper	Dube and Smart 1987
P. penetrans	M. graminicola	Tomato	Duponnois et al. 1997
P. penetrans	M. incognita	Tomato	Weibelzahl-Fulton et al. 1996
P. penetrans	M. javanica	Tomato	Weibelzahl-Fulton et al. 1996
P. penetrans	M. incognita	Tomato	Adiko and Gowen, 1994
P. penetrans	M. incognita	Brinjal, tomato, wheat	Ahmed 1990
P. penetrans	M. graminicola	Rice	Thakur and Walia 2016
P. penetrans	M. incognita	Tomato	Ahmed et al. 1994
P. penetrans	H. avenae	Wheat	Bhattacharya and Swarup 1988
P. penetrans	M. javanica	Tomato	Walia 1994
P. penetrans	M. incognita	Tomato	De Leij et al. 1992
P. penetrans	Pratylenchus penetrans	Tomato	Somasekhar and Gill 1991
P. penetrans	M. incognita	Tomato	Amin 2000
P. penetrans	M. incognita	Tomato	Rangaswamy et al. 2000
P. penetrans	M. incognita	Tomato	Sekhar and Gill 1991
P. penetrans	M. incognita	Tomato	Ravichandra and Reddy 2008
P. penetrans	M. javanica	Tomato	Ciancio and Bourijate 1995
P. penetrans	M. javanica	Grape	Walker and Watchtel 1989
P. penetrans	M. javanica	Tomato	Jayaraj and Mani 1988
P. penetrans	M. incognita	Tomato	Brown and Smart 1985
P. penetrans	M. incognita	Tomato	Singh et al. 2008
P. penetrans	M. incognita	Cherry tomato	Kasumimoto et al. 1993
P. penetrans	M. javanica	Tomato	Walia and Dalal 1994
P. penetrans	M. javanica	Brinjal	Kumar et al. 2005a, b
P. penetrans	M. javanica	Okra, chickpea	Vikram and Walia 2015
P. penetrans	M. javanica	Tomato	Vikram and Walia 2014
Pseudomonas fluorescens	M. graminicola	Rice	Narasimhamurthy et al. 2017a
P. fluorescens	M. graminicola	Rice	Narasimhamurthy et al. 2017b
P. fluorescens	M. incognita	Field pea	Siddiqui et al. 2009
P. fluorescens	M. graminicola	Rice	Seenivasan et al. 2012
P. fluorescens	M. incognita	Tomato	Santhi and Sivakumar 1995
P. fluorescens	H. cajani	Pigeonpea	Siddiqui et al. 1998
P. fluorescens	M. incognita	Okra	Devi and Dutta 2002
P. fluorescens	M. incognita	Bell pepper	Rao et al. 2004
P. fluorescens	M. incognita	Tomato, brinjal	Anita and Rajendran 2002
P. fluorescens	M. incognita	Cowpea	Nama and Sharma 2017
P. fluorescens	M. incognita	Chilli	Wahla et al. 2012
P. fluorescens	M. incognita	Tomato	Siddiqui et al. 2001b
P. fluorescens	Radopholus similis	Banana	Aalten et al. 1998
P. fluorescens	Meloidogyne spp.	Banana	Aalten et al. 1998
P. fluorescens	M. javanica	Tomato	Eltayeb 2017
P. fluorescens	M. incognita	Tomato	Singh and Siddiqui 2010
Pseudomonas sp.	M. incognita	Black pepper	Devapriyanga et al. 2012
P. fluorescens	M. incognita	Mulberry	Muthulakshmi et al. 2010
P. fluorescens	M. incognita	Papaya	Rao 2007
Pseudomonas sp.	Globodera rostochiensis	Potato	Trifonova et al. 2014
P. fluorescens	M. incognita	Maize	Ashoub and Amara 2010
P. fluorescens	Hirschmanniella gracilis	Rice	Seenivasn and Lakshmanan 2002
P. fluorescens	M. incognita	Okra	Kumar and Jain 2010b
P. fluorescens	M. arenaria	Groundnut	Kalaiarasan et al. 2010
P. fluorescens	M. incognita	Banana	Sandeep 2004
P. fluorescens	M. javanica	Tomato	Verma 2009
P. fluorescens	Aphelenchoides besseyi	Tuberose	Pathak and Khan 2010
P. fluorescens	M. incognita	Cowpea	Kumar et al. 2011
P. fluorescens	Rotylenchulus reniformis	Cowpea	Kumar et al. 2011
P. fluorescens	M. incognita	Banana	Jonathan et al. 2006
P. fluorescens	R. similis	Banana	Kumar et al. 2008
P. fluorescens	R. similis	Banana	Senthilkumar et al. 2008
P. fluorescens	Helicotylenchus multicinctus	Banana	Jonathan et al. 2004
P. fluorescens	M. javanica	Tomato	Siddiqui and Shaukat 2003
P. fluorescens	R. reniformis	Cotton	Jayakumar et al. 2004
P. fluorescens	R. reniformis	Cotton	Jayakumar et al. 2002
P. fluorescens	M. incognita	Cotton, cucumber	Hallmann et al. 1998
P. fluorescens	M. incognita	Tomato	Hanna et al. 1999
P. fluorescens	Hirschmanniella gracilis	Rice	Ramakrishnan et al. 1998
P. fluorescens	Tylenchulus semipenetrans	Citrus	Santhi et al. 1999
P. fluorescens	M. incognita	Black pepper	Eapen et al. 1996
P. fluorescens	M. incognita	Grapevine	Shanthi et al. 1998
P. fluorescens	M. incognita	Tomato	Khalil et al. 2012b
P. fluorescens	M. incognita	Cucumber	Krishnaveni and Subramanian 2004
P. fluorescens	M. incognita	Sugar beet	Kavitha et al. 2007
P. fluorescens	M. incognita	Okra	Sharma et al. 2008
P. fluorescens	Pratylenchus thornei	Chickpea	Dwivedi et al. 2008
P. fluorescens	M. incognita	Black gram	Akhtar et al. 2012
P. fluorescens	Globodera spp.	Potato	Mani et al. 1998
P. fluorescens	H. cajani	Sesamum indicum	Kumar et al. 2005a, b
P. fluorescens	M. incognita	Tomato	Jothi et al. 2003
P. fluorescens	M. graminicola	Rice	Anita and Samiyappan 2012
P. fluorescens	M. graminicola	Rice	Priya 2015
P. fluorescens	M. incognita	Jasmine	Seenivasan and Poornima 2010
P. fluorescens	M. incognita	Mulberry	Muthulakshmi and Devrajan 2015
P. fluorescens	M. incognita	Tomato	Abo-Elyousr et al. 2010
Pseudomonas sp.	M. incognita	Okra	Vetrivelkalai et al. 2010

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.

Declarations

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”.

Availability of data and materials

The data sets supporting the conclusions of this article are included within the article.

Authors’ contributions

Both authors read and approved the final manuscript. They contributed according to the order of authors.

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Authors’ Affiliations

(1)

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

(2)

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

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