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  • Review article
  • Open Access

Fungal and bacterial nematicides in integrated nematode management strategies

  • 1Email author and
  • 2
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:

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

Neem cake

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

Castor cake

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

Karanj leaves

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

Mustard cake

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
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
Fig. 2

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

Fig. 3
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

Globodera pallida

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

R. reniformis

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

R. reniformis

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 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

Meloidogyne arenaria

Snapdragon

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

Grape

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

M. javanica

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

Meloidogyne spp.

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

Rotylenchulus reniformis

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.

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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

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 27:357–361View ArticleGoogle Scholar
  2. Abd-Elgawad MMM (2014) Plant-parasitic nematode threats to global food security. J Nematol 46:130Google Scholar
  3. Abd-Elgawad MMM (2016) Comments on the use of biocontrol agents against plant-parasitic nematodes. Int J PharmTech Res 9:352–359Google Scholar
  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 3–49View ArticleGoogle Scholar
  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 276–309View ArticleGoogle Scholar
  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 40:89–99Google Scholar
  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 4:32–34Google Scholar
  8. Ahmed R (1990) Studies on the efficacy of Pasteuria penetrans for the biological control of Meloidogyne species, Ph.D. dissertation. University of Reading, ReadingGoogle Scholar
  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 12:155–160Google Scholar
  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 3:66–73View ArticleGoogle Scholar
  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 23:288–292PubMedView ArticlePubMed CentralGoogle Scholar
  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 18:29–33Google Scholar
  13. Anita B, Samiyappan R (2012) Induction of systemic resistance in rice by Pseudomonas fluorescens against rice root-knot nematode Meloidogyne graminicola. J Biopesticides 5:53–59Google Scholar
  14. Anita E, Rajendran G (2002) Nursery application of Pseudomonas fluorescens for the control of Meloidogyne incognita on tomato and brinjal. Nematol Medit 30:209–210Google Scholar
  15. Anonymous (1995) Annual Report 1994–95. Indian Institute of Spices Research (IISR). Calicut, India, p 89Google Scholar
  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 36:103–109View ArticleGoogle Scholar
  18. Anver S, Alam MM (1997) Control of Meloidogyne incognita and Rotylenchulus reniformis singly and concomitantly on pigeonpea with Paecilomyces lilacinus. Indian J Nematol 27:209–213Google Scholar
  19. Anver S, Alam MM (1999) Control of Meloidogyne incognita and Rotylenchulus reniformis singly and concomitantly on chickpea and pigeonpea. Archiv Phytopath Pl Prot 32:161–172View ArticleGoogle Scholar
  20. Ashoub AH, Amara MT (2010) Biocontrol activity of some bacterial genera against root-knot nematode Meliodogyne incognita. J American Sci 6:321–328Google Scholar
  21. Ashraf MS, Khan TA (2008) Biomanagement of reniform nematode, Rotylenchulus reniformis by fruit wastes and Paecilomyces lilacinus on chickpea. World J Agric Sci 4:492–494Google Scholar
  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 43:609–614View ArticleGoogle Scholar
  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, IndiaGoogle Scholar
  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, IndiaGoogle Scholar
  25. Askary TH (2012) Management of root-knot nematode Meloidogyne javanica in pigeonpea through seed treatment. Indian J Ecol 39:151–152Google Scholar
  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 81–125View ArticleGoogle Scholar
  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 446–454View ArticleGoogle Scholar
  28. Askary TH, Martinelli PRP (2015) Biocontrol agents of phytonematodes. CAB International, Wallingford, p 470View ArticleGoogle Scholar
  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 5:989–993Google Scholar
  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 49:133–139PubMedPubMed CentralView ArticleGoogle Scholar
  31. Bhardwaj P, Trivedi PC (1996) Biological control of Heterodera avenae on wheat using different inoculum levels of Verticillium chlamydosporium. Ann Pl Prot Sci 4:111–114Google Scholar
  32. Bhat MY, Hisamuddin R, Bhat NA (2009) Histological interactions of Paecilomyces lilacinus and Meloidogyne incognita on bitter gourd. J American Sci 5:8–12Google Scholar
  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 45:1059–1069View ArticleGoogle Scholar
  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 55:348–350Google Scholar
  35. Bhatt J, Sengupta SK, Chaurasia RK (2002b) Management of Meloidogyne incognita by Trichoderma viride in betelvine. Indian Phytopath 55:97–98Google Scholar
  36. Bhattacharya D, Swarup G (1988) Pasteuria penetrans, a pathogen of the genus Heterodera, its effect on nematode biology and control. Indian J Nematol 18:61–70Google Scholar
  37. Bokhari FM (2009) Efficacy of some Trichoderma species in the control of Rotylenchulus reniformis and Meloidogyne javanica. Archiv Phytopath Pl Prot 42:361–369View ArticleGoogle Scholar
  38. Brahma U, Borah A (2016) Management of Meloidogyne incognita on pea with bioagents and organic amendment. Indian J Nematol 46:58–61Google Scholar
  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 17:483–486View ArticleGoogle Scholar
  40. Brown SM, Nordmeyer D (1985) Synergistic reduction in root galling by Meloidogyne javanica with Pasteuria penetrans and nematicide. Revue de Nemat 8:285–286Google Scholar
  41. Brown SM, Smart GC Jr (1985) Root penetration by Meloidogyne incognita juveniles infected with Bacillus penetrans. J Nematol 17:123–126PubMedPubMed CentralGoogle Scholar
  42. Cabanillas E, Barker KR (1989) Impact of Paecilomyces lilacinus inoculums level of Meloidogyne incognita on tomato. J Nematol 21:115–120PubMedPubMed CentralGoogle Scholar
  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 21:121–130PubMedPubMed CentralGoogle Scholar
  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 12:154Google Scholar
  45. Chand R, Gill JS (2002) Evaluation of various application methods of Pasteuria penetrans against Meloidogyne incognita in tomato. Indian J Nematol 32:23–25Google Scholar
  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 11:178–180Google Scholar
  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 15:617–626Google Scholar
  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 28:159–168PubMedPubMed CentralGoogle Scholar
  49. Chen ZX, Dickson DW, Mitchell DJ, McSorley R, Hewlett TE (1997) Suppression mechanism of Meloidogyne arenaria race 1 by Pasteuria penetrans. J Nematol 29:1–8PubMedPubMed CentralGoogle Scholar
  50. Cho MR, Na SY, Yiem MS (2000) Biological control of Meloidogyne arenaria by Pasteuria penetrans. J Asia-Pacific Entom 3:71–76View ArticleGoogle Scholar
  51. Ciancio A (1995) Density dependent parasitism of Xiphinema diversicaudatum by Pasteuria penetrans in a naturally infested field. Phytopathology 85:144–149View ArticleGoogle Scholar
  52. Ciancio A, Bourijate M (1995) Relationship between Pasteuria penetrans infection levels and density of Meloidogyne javanica. Nemat Medit 23:43–49Google Scholar
  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 43:10–109Google Scholar
  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 3:297–309Google Scholar
  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 71:953–961Google Scholar
  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. 1:253–257Google Scholar
  57. Daudi AT, Gowen SR (1992) The potential for managing root-knot nematodes by use of pasteuria penetrans and oxamyl. Nematol Medit 20:241–244Google Scholar
  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 3:32–33Google Scholar
  59. De Channer AG (1989) The potential of Pasteuria penetrans for the biological control of Meloidogyne species, Ph.D. dissertation. University of Reading, ReadingGoogle Scholar
  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 15:235–242Google Scholar
  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 39:115–126View ArticleGoogle Scholar
  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 32:230–231Google Scholar
  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 46:61–64Google Scholar
  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 42:57–65Google Scholar
  66. Devi LS, Dutta U (2002) Effect of Pseudomonas fluorescens on root-knot nematodes, (Meloidogyne incognita) on okra plant. Indian J Nematol 32:215–216Google Scholar
  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 32:190–192Google Scholar
  68. Devi LS, Sharma R (2002) Effect of Trichoderma spp. against root-knot nematodes, Meloidogyne incognita on tomato. Indian J Nematol 32:227–228Google Scholar
  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 46:161–164Google Scholar
  70. Devrajan K, Rajendran G (2002) Effect of fungal egg parasite Paecilomyces lilacinus (Thom.) Samson on Meloidogyne incognita in banana. Indian J Nematol 32:88–90Google Scholar
  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 39:85–89Google Scholar
  72. Dhawan SC, Singh S (2010) Management of root-knot nematode, Meloidogyne incognita using Pochonia chlamydosporia on okra. Indian J Nematol 40:171–178Google Scholar
  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 38:110–111Google Scholar
  74. Dhawan SS, Narayana R, Babu NP (2004) Biomanagement of root-knot nematode, Meloidogyne incognita in okra by Paecilomyces lilacinus. Ann Pl Prot Sci 12:356–359Google Scholar
  75. Dube B, Smart GC Jr (1987) Biological control of Meloidogyne incognita by Paecilomyces and Pasteuria penetrans. J Nematol 19:222–227PubMedPubMed CentralGoogle Scholar
  76. Duponnois R, Netscher C, Mateille T (1997) Effect of rhizosphere microflora on Pasteuria penetrans parasitizing Meloidogyne graminicola. Nemat Medit 25:99–103Google Scholar
  77. Dwivedi K, Upadhyay KD, Verma RA, Ahmad F (2008) Role of bioagents in management of Pratylenchus thornei infecting chickpea. Indian J Nematol 38:138–140Google Scholar
  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.129–133Google Scholar
  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 25:15–16Google Scholar
  80. Ebrahim A, Seddighe F, Hassan RE (2008) Potential for biocontrol of Heterodera schachtii by Pochonia chlamydosporia var. chlamydosporia on sugarbeet. Biocont Sci Tech 18:157–167View ArticleGoogle Scholar
  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 217–243View ArticleGoogle Scholar
  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 6:1176–1182View ArticleGoogle Scholar
  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 24:67–75Google Scholar
  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 8:11–18View ArticleGoogle Scholar
  86. Ganaie MA, Khan TA (2010) Biological potential of Paecilomyces lilacinus on pathogenesis of Meloidogyne javanica infecting tomato plant. European J Appl Sci 2:80–84Google Scholar
  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 30:250–258View ArticleGoogle Scholar
  88. Gogoi BB, Gill JS (2001) Compatibility of Pasteuria penertrans with carbofuran and organic amendments, its effect on Heterodera cajani. Ann Pl Prot Sci 9:254–257Google Scholar
  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 21:172–175Google Scholar
  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 32:179–181Google Scholar
  91. Goswami BK, Mittal A (2004) Management of root-knot nematode infecting tomato by Trichoderma viride and Paecilomyces lilacinus. Indian Phytopath 57:235–236Google Scholar
  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 7:873–875View ArticleGoogle Scholar
  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 32:94–96Google Scholar
  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 30:925–937View ArticleGoogle Scholar
  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 77:1467–1476Google Scholar
  96. Hasan N (2004) Evaluation of native strain of Paecilomyces lilacinus against Meloidogyne incognita in cowpea followed by Lucerne. Ann Pl Prot Sci 3:145–148Google Scholar
  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. 102Google Scholar
  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 20:578–584PubMedPubMed CentralGoogle Scholar
  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 4:429–432View ArticleGoogle Scholar
  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 46:1632–1640View ArticleGoogle Scholar
  101. Jansson H-B, Tunlid A, Nordbring-Hertz B (1997) Biological control: nematodes. In: Fungal biotechnology.Anke T (ed.). Chapman and Hall, Weinheim, pp 38–50Google Scholar
  102. Jatala P, Kaltenbach R, Bocangel M (1979) Biological control of Meloidogyne incognita acrita and Globodera pallida on potatoes. J Nematol 11:303Google Scholar
  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 12:226–227Google Scholar
  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 120:53–60View ArticleGoogle Scholar
  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 32:228–230Google Scholar
  106. Jayakumar J, Ramakrishnan S, Rajendran G (2004) Biological control of cotton reniform nematode, Rotylenchulus reniformis with Pseudomonas fluorescens. Indian J Nematol 34:230–231Google Scholar
  107. Jayaraj MA, Mani A (1988) Biocontrol of Meloidogyne javanica with the bacterial spore parasite Pasteuria penetrans. Int Nematol Network Newslet 5:3–4Google Scholar
  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 8:229–239View ArticleGoogle Scholar
  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 30:231–240Google Scholar
  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 32:169–173Google Scholar
  111. Jonathan EI, Padmanabhan D, Ayyamperumal A (1995) Biological control of root-knot nematode on betelvine, Piper betel by Paecilomyces lilacinus. Nematol Medit 23:191–193Google Scholar
  112. Jonathan EI, Rajendran G (2000) Biocontrol potential of the fungus Paecilomyces lilacinus against root-knot nematode Meloidogyne incognita in banana. J Biol Cont 14:67–69Google Scholar
  113. Jonathan EI, Sandeep A, Cannayane I, Umamaheswari R (2006) Bioefficacy of Pseudomonas fluorescens on Meloidogyne incognita in banana. Nematol Medit 34:19–25Google Scholar
  114. Jothi G, Sivakumar M, Rajendran G (2003) Management of root-knot nematode by Pseudomonas fluorescens in tomato. Indian J Nematol 33:87–88Google Scholar
  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 40:55–59Google Scholar
  116. Kasumimoto T, Ikeda R, Kawada H (1993) Dose response of Meloidogyne incognita infected cherry tomatoes to application of Pasteuria penetrans. Japanese J Nematol 23:10–18View ArticleGoogle Scholar
  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 21:211–215Google Scholar
  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 52:47–52Google Scholar
  119. Khalil MS, Kenawy A, Gohrab MA, Mohammed EE (2012a) Impact of microbial agents on Meloidogyne incognita management and morphogenesis of tomato. J Biopesticides 5:28–35Google Scholar
  120. Khan A, Williams KL, Nevalainen HKM (2006) Control of plant-parasitic nematodes by Paecilomyce lilacinus and Monacrosporium lysipagum in pot trials. Biocontrol 51:643–658View ArticleGoogle Scholar
  121. Khan MR, Goswami BK (2000) Effect of different doses of Paecilomyces lilacinus isolate 6 on Meloidogyne incognita infecting tomato. Indian J Nematol 30:5–7Google Scholar
  122. Khan MW, Esfahani MN (1990) Efficacy of Paecilomyces lilacinus for controlling Meloidogyne javanica on tomato in green house in India. Pakistan J Nematol 8:95–96Google Scholar
  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 14:106–109Google Scholar
  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. 157–160Google Scholar
  125. Kokalis-Burelle N (2015) Pasteuria penetrans for control of Meloidogyne incognita on tomato and cucumber, and M. arenaria on snapdragon. J Nematol 47:207–213PubMedPubMed CentralGoogle Scholar
  126. Korayem AM, Hasabo SA, Ameen HH (1993) Effects and mode of action of some plant extracts on certain plant parasitic nematodes. Anz Schädling 66:32–36Google Scholar
  127. Krishnaveni M, Subramanian S (2004) Evaluation of biocontrol agents for the management of Meloidogyne incognita on cucumber (Cucumis sativus L). Cur Nematol 15:33–37Google Scholar
  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 15:183–186Google Scholar
  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 6:2287–2291View ArticleGoogle Scholar
  130. Kumar P, Chand R (2015) Bioefficacy of trichoderma harzianum against root-knot nematode Meloidogyne incognita on brinjal. Ann Pl Prot Sci 23:361–364Google Scholar
  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 38:57–61Google Scholar
  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 36:264–266Google Scholar
  133. Kumar S, Prabhu S (2008) Biological control of Heterodera cajani in pigeonpea by Trichoderma harzianum and Pochonia chlamydosporia. Indian J Nematol 38:65–67Google Scholar
  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 48:161–166Google Scholar
  135. Kumar V, Jain RK (2010a) Management of root-knot nematode, Meloidogyne incognita using Pochonia chlamydosporium on okra. Indian J Nematol 40:171–178Google Scholar
  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 40:226–228Google Scholar
  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 19:164–167Google Scholar
  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 1:44–49Google Scholar
  139. Mahanta B, Borbora AC, Konwar B (2016) Effect of Paecilomyces lilacinus on Tylenchulus semipenetrans population in Khasi Mandarin. Indian J Nematol 46:55–81Google Scholar
  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 5:10–11Google Scholar
  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 12:131–134Google Scholar
  142. Mankau R, Prasad N (1972) Possibilities and problems in the use of a sporozoan endoparasite for biological control of plant parasitic nematodes. Nematropica 2:7–8Google Scholar
  143. Manzoor SM, Sinha AK, Bora BC (2002) Management of citrus nematode, Tylenchulus semipenetrans on Khasi Mandarin, by Paecilomyces lilacinus. Indian J Nematol 32:153–155Google Scholar
  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 31:55–59Google Scholar
  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 69:365–372Google Scholar
  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 31:75–86Google Scholar
  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 54:199–205Google Scholar
  148. Muthulakshmi M, Devrajan K (2015) Management of Meloidogyne incognita by Pseudomonas fluorescens and Trichoderma viride in mulberry. Int J Pl Prot 8:1–6Google Scholar
  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 3:479–482Google Scholar
  150. Muthulakshmi M, Kumar S, Subramanian S, Anita B (2012) Compatibility of Pochonia chlamydosporia with other biocontrol agents and carbofuran. J Biopesticides 5:243–245Google Scholar
  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 17:125–131Google Scholar
  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 7:147–152Google Scholar
  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 29:23–27Google Scholar
  154. Nama CP, Sharma HK (2017) Bio-management of root-knot nematode, Meloidogyne incognita on cowpea (Vigna unguiculata L.). J Entomo Zool Stud 5:50–52Google Scholar
  155. Narasimhamurthy HB, Ravindra H, Sehgal M (2017a) Management of rice root-knot nematode, Meloidogyne graminicola. Int J Pure Appl Biosci 5:268–276View ArticleGoogle Scholar
  156. Narasimhamurthy HB, Ravindra H, Sehgal M, Ekabote SD, Ganapathi (2017b) Management of rice root-knot nematode, Meloidogyne graminicola. J Entomology and Zoology Studies 5:1433–1439Google Scholar
  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 5:276–280Google Scholar
  158. Nisha MS, Sheela MS (2016) Effect of fungal egg parasite, Paecilomyces lilacinus (Thom.) Samson on Meloidogyne incognita in brinjal. Indian J Nematol 46:157–159Google Scholar
  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 49:337–340View ArticleGoogle Scholar
  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 31:121–123Google Scholar
  161. Oostendorp M, Dickson DW, Mitchell DJ (1991) Population development of Pasteuria penetrans on Meloidogyne arenaria. J Nematol 23:58–64PubMedPubMed CentralGoogle Scholar
  162. Opperman CH, Chang S (1990) Plant-parasitic nematodes acetylcholinesterase inhibition by carbamate and organophosphate nematicides. J Nematol 22:481–488PubMedPubMed CentralGoogle Scholar
  163. Page SLJ, Bridge J (1985) Observations on Pasteuria penetrans as a parasite of Meloidogyne acronea. Nematologica 31:238–240View ArticleGoogle Scholar
  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: 101-103Google Scholar
  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 16:113–115Google Scholar
  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 3:100–104Google Scholar
  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 24:265–267Google Scholar
  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 40:83–87Google Scholar
  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 33:149–151Google Scholar
  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 13:438–440Google Scholar
  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 26:209–212Google Scholar
  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 5:179–191Google Scholar
  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 16:461–465Google Scholar
  175. Priya MS (2015) Biomanagement of rice root knot nematode, Meloidogyne graminicola Golden and Brichfield in aerobic rice. Int J Manag Soc Sci 3:591–598Google Scholar
  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 25:311–315Google Scholar
  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 43:65–69Google Scholar
  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 12:135–141Google Scholar
  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 6:135–138Google Scholar
  180. Rao MS (2007) Papaya seedlings colonized by the bio-agents Trichoderma harzianum and Pseudomonas fluorescens to control root-knot nematodes. Nematol Medit 35:199–203Google Scholar
  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 9:71–76Google Scholar
  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 32:159–163Google Scholar
  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 104:423–425Google Scholar
  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 25:249–252Google Scholar
  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 26:59–62Google Scholar
  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 2:519–523Google Scholar
  187. Ravichandra NG, Reddy BMR (2008) Efficacy of Pasteuria penetrans in the management of Meloidogyne incognita infecting tomato. Indian J Nematol 38:172–175Google Scholar
  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 69:159–166Google Scholar
  189. Saikia MK, Roy AK (1994) Efficacy of Paecilomyces lilacinus on the reduction of attack of Meloidogyne incognita on okra. Indian J Nematol 24:163–167Google Scholar
  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, IndiaGoogle Scholar
  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 14:39–43Google Scholar
  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 9:113–115Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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 22:611–632View ArticleGoogle Scholar
  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 16:34–40Google Scholar
  199. Sekhar NS, Gill JS (1991) Efficacy of Pasteuria penetrans alone and in combination with carbofuran in controlling Meloidogyne incognita. Indian J Nematol 21:61–65Google Scholar
  200. Senthilkumar P, Jonathan EI, Samiyappan R (2008) Bioefficacy of Pseudomonas fluorescens on burrowing nematode, Radopholus similis in banana. Indian J Nematol 38:46–52Google Scholar
  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 23:61–69View ArticleGoogle Scholar
  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.Google Scholar
  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 47:622–630View ArticleGoogle Scholar
  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 5:1–11View ArticleGoogle Scholar
  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 20:79–82Google Scholar
  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.Google Scholar
  207. Sharma RD (1992) Biocontrol efficacy of Pasteuria penetrans against Meloidogyne javanica. Ciencia Biologica Ecologica e Systematica 12:43–47Google Scholar
  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 91:687–693PubMedView ArticlePubMed CentralGoogle Scholar
  209. Siddiqui IA, Ehteshamul-Haque S (2000) Effect of Verticillium chlamydosporium and Pseudomonas aeruginosa in the control of Meloidogyne javanica on tomato. Nematol Medit 28:193–196Google Scholar
  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 35:1615–1623View ArticleGoogle Scholar
  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 4:846–848View ArticleGoogle Scholar
  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 16:179–185View ArticleGoogle Scholar
  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 54:227–230View ArticleGoogle Scholar
  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 44:49–56View ArticleGoogle Scholar
  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 31:310–321Google Scholar
  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 42:1154–1164View ArticleGoogle Scholar
  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 40:113Google Scholar
  219. Singh B, Dhawan SC (1994) Effect of Pasteuria penetrans on the penetration and multiplication of Heterodera cajani in Vigna unguiculata roots. Nematol Medit 22:159–161Google Scholar
  220. Singh B, Dhawan SC (1996) Suppression of Heterodera cajani by Pasteuria penetrans during three successive plantings of cowpea. Indian J Nematol 26:216–221Google Scholar
  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 29:118–120Google Scholar
  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 21:154–156Google Scholar
  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 78:1092–1094Google Scholar
  224. Singh P, Siddiqui ZA (2010) Biocontrol of root-knot nematode Meloidogyne incognita by the isolates of Pseudomonas on tomato. Archiv Phytopath Pl Prot 43:1423–1434View ArticleGoogle Scholar
  225. Singh S (2013) Integrated approach for the management of the root-knot nematode, Meloidogyne incognita, on eggplant under field conditions. Nematology 15:747–757Google Scholar
  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 2:163–166Google Scholar
  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 7:49–50Google Scholar
  228. Somasekhar N, Gill JS (1991) Efficacy of Pasteuria penetrans alone and in combination with carbofuran controlling Meloidogyne incognita. Indian J Nematol 21:61–65Google Scholar
  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 24:50–53Google Scholar
  230. Spaull VW (1984) Observations on Bacillus penetrans infecting Meloidogyne in sugarcane fields in South Africa. Revue de Nematol 7:277–282Google Scholar
  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 289–311View ArticleGoogle Scholar
  232. Stirling GR (1984) Biological control of Meloidogyne javanica with Bacillus penetrans. Phytopathology 74:55–60View ArticleGoogle Scholar
  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 30:101–103Google Scholar
  234. Thakur NSA, Devi G (2007) Management of Meloidogyne incognita attacking okra by nematophagous fungi, Arthrobotrys oligospora and Paecilomyces lilacinus. Agric Sci Digest 27:50–52Google Scholar
  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 46:16–19Google Scholar
  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 20:666–669Google Scholar
  237. Tzortzakakis EA (2007) The effect of the fungus Pochonia chlamydosporia on the root-knot nematode Meloidogyne incognita in pots. Russian J Nematol 15:89–94Google Scholar
  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 15:1–7Google Scholar
  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:53–57Google Scholar
  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 2:34–36Google Scholar
  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 7:727–736View ArticleGoogle Scholar
  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 76:63–70Google Scholar
  243. Verdejo-Lucas S (1992) Seasonal population fluctuations of Meloidogyne spp. and the Pasteuria penetrans group in Kiwi orchards. Pl Disease 76:1275–1279View ArticleGoogle Scholar
  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 52:521–528View ArticleGoogle Scholar
  245. Verma KK (2009) Management of Meloidogyne javanica by bacterial antagonist, Pseudomonas fluorescens as seedling root dip in tomato. Indian J Nematol 39:207–210Google Scholar
  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 3:52–457Google Scholar
  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 32:85–100Google Scholar
  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 75:255–258View ArticleGoogle Scholar
  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 44:44–49Google Scholar
  250. Vikram, Walia RK (2015) Efficacy of bacterial parasite, Pasteuria penetrans application as seed treatment against root-knot nematode, Meloidogyne javanica. Indian J Nematol 45:1–6Google Scholar
  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 68:1148–1155PubMedView ArticlePubMed CentralGoogle Scholar
  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 8:68–70Google Scholar
  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 2:19–21Google Scholar
  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 27:3–8Google Scholar
  255. Walker GE, Wachtel MF (1989) The influence of soil solarisation and non-fumigant nematicides on infection of Meloidogyne javanica by Pasteuria penetrans. Nematologica 34:477–483View ArticleGoogle Scholar
  256. Walters SA, Barker KR (1994) Efficacy of Paecilomyces lilacinus in suppressing Rotylenchulus reniformis on tomato. J Nematol 26:600–605PubMedPubMed CentralGoogle Scholar
  257. Wang K, Riggs RD, Crippen D (2005) Isolation, selection, and efficacy of Pochonia chlamydosporia for control of Rotylenchulus reniformis on cotton. Phytopathology 95:890–893PubMedView ArticlePubMed CentralGoogle Scholar
  258. Weibelzahl-Fulton E, Dickson DW, Whitty EB (1996) Suppression of Meloidogyne incognita and Meloidogyne javanica by Pasteuria penetrans in field soil. J Nematol 28:43–49PubMedPubMed CentralGoogle Scholar
  259. Wilson MJ, Jackson TA (2013) Progress in the commercialisation of bionematicides. BioCont 58:715–722View ArticleGoogle Scholar
  260. Windham GL, Windham MT, Williams WP (1989) Effects of Trichoderma spp. on maize growth and Meloidogyne arenaria reproduction. Pl Disease 73:493–495View ArticleGoogle Scholar
  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 2:37–42Google Scholar
  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 2:1441–1444View ArticleGoogle Scholar
  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 4:995–999View ArticleGoogle Scholar

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