Plant-Parasitic Nematodes and Microbe Interactions: A Biological Control Perspective

Chapter 4
Plant-Parasitic Nematodes and Microbe

Interactions: A Biological Control
Perspective
Fouad Mokrini, Salah-Eddine Laasli, Said Ezrari, Zineb Belabess,

and Rachid Lahlali
Abstract Plant parasitic nematodes (PPN) cause significant damage to a broad

range of vegetables and crops, worldwide. Biological control agents (BCA) repre-
sent a promising approach to manage these dangerous organisms. A comprehensive
overview is presented on fundamental mechanisms governing the interactions
between beneficial BCA vs PPN, alongside exploring the diverse biological and
molecular relationships crucial to mitigate damage in agricultural crops. Different
nematicidal activities and their large-scale efficiency are also discussed. Finally, an
overview is provided about most significant factors affecting the success or failure
of BCA in a reliable strategy to control PPN.
Keywords Biocontrol · Interaction · Nematodes · Parasitism
F. Mokrini (*) · S.-E. Laasli

National Institute for Agricultural Research (INRA), Regional Center of Rabat,
Rabat, Morocco
S. Ezrari
Department of Plant Protection, Phytopathology Unit, Ecole Nationale d’Agriculture de
Meknès, Meknès, Morocco
Microbiology Unit, Laboratory of Bioresources, Biotechnology, Ethnopharmacology and
Health, Faculty of Medicine and Pharmacy Oujda, University Mohammed Premier,
Oujda, Morocco
Z. Belabess
National Institute for Agricultural Research (INRA), Regional Center of Meknès,
Meknès, Morocco
R. Lahlali
Department of Plant Protection, Phytopathology Unit, Ecole Nationale d’Agriculture de
Meknès, Meknès, Morocco
Plant Pathology Laboratory, AgroBioSciences, College of Sustainable Agriculture and
Environmental Sciences, Mohammed VI Polytechnic University, Ben Guerir, Morocco
e-mail: rlahlali@enameknes.ac.ma
© The Author(s), under exclusive license to Springer Nature 89

Switzerland AG 2024
K. K. Chaudhary et al. (eds.), Sustainable Management of Nematodes in
Agriculture, Vol.2: Role of Microbes-Assisted Strategies, Sustainability in Plant
and Crop Protection 19, https://doi.org/10.1007/978-3-031-52557-5_4
90 F. Mokrini et al.
4.1 Introduction
Global crop production faces a significant challenge from plant-parasitic nematodes

(PPN), causing substantial economic losses in the vegetable industry. The estimated
annual cost of crop damage caused by PPN ranges from 100 to 157 billion USD
worldwide (Tikoria et al., 2022). More than 4100 PPN species have been identified
and, due to the frequent identification of new species, a number of genera are recog-
nized as major pests for various important crops (Ning et al., 2022). PPN encompass
diverse species with distinct lifestyles that can significantly harm worldwide horti-
cultural crops. The severity of nematode damage is often influenced by edapho-
climatic and agronomic factors such as the type of soil and monoculture practices
(Simon et al., 2018).
In recent decades, the widespread utilization of synthetic nematicides has been
the primary approach to manage PPN. However, there are growing concerns about
some negative impacts of these chemicals on soil, water, and the environment.
Additionally, there is a troubling issue of unintentional harm caused to non-target
organisms, due to toxicity. There is hence an urgent need to explore alternative bio-
logical methods for controlling PPN (Zhang et al., 2017).
Scientists actively seek highly effective and eco-friendly tools and strategies to
manage PPN sustainably (Li et al., 2015). Consequently, environment-friendly
alternatives are investigated and developed, including exploring genetic resistance,
implementing crop rotation practices, utilizing fallow periods, applying organic
amendments, and delving into biological control. Among these alternatives, bio-
logical control is one of the most promising strategies for a sustainable management
of PPN (Barker & Koenning, 1998). This approach involves harnessing natural
mechanisms and predators to regulate nematode populations, without causing harm
to the ecosystem.
Biological control has emerged as an excellent alternative for reducing pest dam-
age by utilizing living organisms that have a potential to manage plant diseases and
pests, effectively (Stirling, 1991). Recently, various biological methods, including
the use of microbial antagonists such as nematophagous or endophytic fungi, acti-
nomycetes, bacteria, and entomopathogenic nematodes, have been used for the PPN
management (Mennan et al., 2006; Askary, 2015). These methods fall into different
categories, including the use of predators that feed on PPN, parasites that invade and
harm or kill many nematodes, and microbes that indirectly suppress the growth and
survival of pathogens and pests (Eilenberg et al., 2001). Biological control also uses
products derived from living organisms to mitigate PPN-induced damages or losses
(Barratt et al., 2018).
The utilization of microbial agents, such as native or introduced mycorrhizal
fungi, nematophagous and endophytic fungi, bacteria, entomopathogenic nema-
todes, and other natural predators, along with the application of organic fertilizers,
4 Plant-Parasitic Nematodes and Microbe Interactions: A Biological Control Perspective 91
presents a promising alternative for PPN management (Dhital, 2020). They act as
antagonists, generating specific substances that eliminate or interfere with develop-
ing PPN. Alternatively, they can act as parasites or pathogens, colonizing and
destroying nematodes. Resource competition may also affect their effectiveness
(Kerry, 2000; Abd-Elgawad, 2020). Consequently, these attributes, alone or in com-
bination, make them highly suitable BCA. Numerous genera of PPN are susceptible
to attack by diverse soil organisms.
This chapter focuses on PPN management through biological control. It provides
a comprehensive overview of critical mechanisms involved in the interactions
between nematophagous microorganisms and PPN (Fig. 4.1). The first section
examines the potential of nematophagous bacteria and fungi in establishing biologi-
cal and molecular relationships with nematodes, as a starting point for effective
management in agricultural fields. We also highlights major factors influencing the
success or failure of biological control as a sustainable solution for nematode man-
agement, particularly considering the challenges posed by yield and socio-economic
factors that complicate decision-making for crop protection. Finally we discuss
future perspectives on nematode BCA.
Fig. 4.1 Possible mechanisms of action of parasitic and endophytic bacteria, fungi, and plant
extracts acting vs plant-parasitic nematodes
4.2 Nematophagous Microorganisms Interactions:

An Overview
The soil environment provides a favourable habitat for various nematophagous

microorganisms, which play a vital role in agricultural systems due to their multi-
functionality. They engage in complex interactions influenced by both biotic and
abiotic factors. Among the biotic factors, competition with other microorganisms
and the ability of plants to recognize microbial patterns are significant determinants
of their activities. Similarly, abiotic factors, such as environmental conditions and
soil physicochemical properties, directly shape the nature of interactions between
these organisms, impacting their effects on plants and influencing the plant develop-
ment (Marschner & Timonen, 2005; Hoitink et al., 2006; Siddiqui & Akhtar, 2008;
Radjacommare et al., 2010).
Numerous studies have investigated the interactions of nematophagous species
also at the molecular level (Luo et al., 2006; Lopez-Llorca et al., 2008; Liu et al.,
2014; Li et al., 2015). Antagonists that show promising potential as BCA include
nematophagous fungi, arbuscular mycorrhizal fungi (AMF), nematophagous bacte-
ria, and entomopathogenic nematodes (EPNs).
4.2.1 Nematophagous Bacteria Mechanisms
Bacteria have a significant potential in managing a wide range of PPN (Li et al.,
2015). In the soil environment, numerous species interact with nematodes, directly
or indirectly influencing their functions such as behavior, feeding, and reproduction,
by releasing enzymes or toxins (Usman & Siddiqui, 2013). Various bacteria
(Table 4.1) show antagonistic properties, including endophytes and rhizobacteria,
that control PPN (Dong & Zhang, 2006). They are classified into different genera,
such as: Actinomyces, Agrobacterium, Alcaligenes, Arthrobacter, Aureobacterium,
Azotobacter, Bacillus, Beijerinckia, Brevibacillus, Burkholderia, Chromobacterium,
Clavromobacterium, Clostridium, Comamonas, Corynebacterium, Curtobacterium,
Desulfovibrio, Enterobacter, Flavobacterium, Gluconobacter, Hydrogenophaga,
Klebsiella, Methylobacterium, Pasteuria, Pseudomonas, Rhizobiacterium,
Sphingobacterium. Among these, members of genera Bacillus, Pseudomonas, and
Pasteuria are the dominant nematophagous bacteria found in soil, known for their
ability to attack and kill nematodes through parasitism, toxin production, antibiosis,
enzyme activity, as well as competition for nutrients, promotion of induced sys-
temic resistance (ISR) in plants, and facilitation of plant growth (Tian et al., 2007;
Li et al., 2015). However, Pasteuria penetrans is the sole obligate nematode parasite
among these bacteria (Siddiqui & Mahmood, 1999; Tian et al., 2007; Terefe et al.,
2009; Li et al., 2015).
4
Table 4.1 Activity of bacteria species and isolates on plant-parasitic nematodes

Bacteria Nematode Plant Mode of action References
Pasteuria penetrans Meloidogyne Sugarcane Reduced populations Bhuiyan et al. (2018)
javanica
Escherichia coli, Serratia marcescens Bursaphelenchus Pine Significant nematicidal activity Liu et al. (2019)
xylophilus
Streptomyces sp. CBG9 M. incognita Coffea canephora Inhibition of egg hatching and causes Hoang et al. (2020)
mortality of second stage juveniles
(J2)
Bacillus subtilis IIHR BS-2 M. incognita Daucus carota Inhibition of egg hatching and J2 Rao et al. (2017)
mortality
Stenotrophomonas sp., Bacillus sp. B. xylophilus Pinus Significant nematicidal effect on two Ponpandian et al.
stages of the nematode life cycle (L3/ (2019)
L4 and adults)
Erwinia sp. A41C3, Rouxiella sp. Arv20#4.1 B. xylophilus Pinus pinaster Secretion of metabolites under iron Proença et al. (2019)
limitation and biocontrol
Rhizobacteria strains M. ethiopica and Grapevine Secretion of metabolites and Aballay et al. (2017)
X. index exoenzymes with a nematicidal
activity
Bacillus sp., Paenibacillus sp., Xanthomonas M. graminicola Rice Secretion of volatile compounds Bui et al. (2020)
sp.
B. cereus, B. subtilis, P. putida M. incognita Tomato Larvicidal and ovicidal activity Zhao et al. (2018)
Microbacterium, Sphingopyxis, Brevundimonas, M. hapla Tomato Attachment to the nematode affects Topalović et al. (2019)
Acinetobacter, Micrococcus J2 mortality, motility, and eggs
hatching
Rhizosphere Bacillus spp. M. incognita S. lycopersicum cv Reduction of J2 and galling Colagiero et al. (2018)
Tondino
Bacillus spp. Meloidogyne spp. Black pepper trees Chitinase and protease activities Nguyen et al. (2019)
Plant-Parasitic Nematodes and Microbe Interactions: A Biological Control Perspective
associated with inhibition of egg

hatching; natural compounds with
93
thermal stability killing J2

(continued)
Table 4.1 (continued)
94
Bacteria Nematode Plant Mode of action References

Pseudomonas fluorescens, B. subtilis M. graminicola Rice Direct antagonism by enzymes, Mhatre et al. (2019)
toxins, and other metabolic products;
indirect effect by repellents affecting
host recognition
Bacillus sp. Meloidogyne spp. Glycine max Reduction of gall and egg mass Chinheya et al. (2017)
numbers
Pseudomonas sp. Bacillus sp. Meloidogyne spp. Tomato Reduction of galls, lowering the egg Zhou et al. (2019)
masses
B. methylotrophicus R2-2, Lysobacter M. incognita Tomato Nematicidal activity Zhou et al. (2016)
antibioticus 13-6
B. firmus T11, B. aryabhattai A08, M. incognita Daucus carota Reduction of gall numbers and egg Viljoen et al. (2019)
Paenibacillus barcinonensis A10, Paenibacillus mass
alvei T30, B. cereus N10w
S. pactum, S. rochei Pratylenchus Tomato Activating plant systemic resistance Ma et al. (2017)
thornei and defensive mechanisms
Helicotylenchus
dihystera
Ditylenchus
destructor
Geocenamus
quadrifer
P. fluorescens CHA0 M. javanica S. lycopersicum cv. Bio-induction of plant defense Sahebani and
Calj N3 responses Gholamrezaee (2020)
Cucumis sativus cv.
Super N3
P. putida M. graminicola Oryza sativa cv. Inhibition of egg hatching and caused Haque et al. (2018)
PS-5 mortality to nematode juveniles
Lysobacter enzymogenes C3 H. schactii Brassica oleracea Nematode decrease in the Yuen et al. (2018)
H. glycines Beta vulgaris rhizosphere; suppression of nematode
F. Mokrini et al.
Soybean feeding and reproduction

The Gram-positive P. penetrans is a hyperparasite known for forming infective

and resting endospores. It is particularly effective against root-knot nematodes
(RKN) Meloidogyne spp. controlling these nematodes across various crops, includ-
ing tobacco, tomato, grapevines, and others (Bhuiyan et al., 2018). Pasteuria spp.,
particularly P. penetrans, showed a notable ability to diminish PPN-induced dam-
age, ensuring that the hosts remain beneath economically damaging levels, thus
boosting the yield of affected crops (Chaudhary & Kaul, 2012; Mukhtar et al.,
2013). Notably, Pasteuria spp. parasitize a broad range of PPN of economic impor-
tance (Viaene et al., 2013). On RKN, P. penetrans cycle starts with the activation of
the endospores attached to the cuticles of J2s. From there, these endospores germi-
nate producing a tube that breaks through the cuticle, infects the pseudocoelom, and
spreads across the nematode body (Davies et al., 2011). This initial step hinges on
several factors, primarily the elements of the cuticle surface coat. Among these,
fatty acid and retinol-binding (FAR) proteins are key players in endospore attach-
ment and significantly influence the development, reproduction, and infection of
RKN (Cheng et al., 2013). Interestingly, when the Mi-far-1 gene (which is respon-
sible for FAR protein synthesis) was knocked down, endospore attachment to the
juvenile cuticle increased, leading to changes in the nematode ability to locate hosts,
infect roots and reproduce (Phani et al., 2017).
Many Pasteuria species and isolates have been studied regarding their effective-
ness against PPN and their safe and eco-friendly usage as bio-nematicides has been
established (Giblin-Davis et al., 2003; Mukhtar et al., 2013; Stirling, 2014). Luc
et al. (2011) in-vitro evaluated the biocidal potential of Pasteuria usgae endospores
vs the sting nematode, Belonolaimus longicaudatus attacking turf grass, showing a
nearly 70% decrease of the nematode population. However, in vivo experiments
have shown different results using P. penetrans against Meloidogyne spp. (Davies
et al., 1994), due to a strict host specificity shown by this bacterium. On the other
hand, Chaudhary and Kaul (2010) reported an intense decrease in the final popula-
tion of M. incognita caused by the application of P. penetrans.
Understanding the distinction between rhizobacteria and endophytic bacteria is
of paramount importance. Rhizobacteria colonize roots and form associations with
the plants (Siddiqui & Mahmood, 1999; Dong & Zhang, 2006). On the other hand,
endophytic bacteria refer to any bacterium found within the internal tissues of
plants. This category encompasses (a) active or latent pathogens, (b) bacteria that
inhabit plant tissues without causing any harm, and (c) bacteria that live in plant
tissues in a mutually beneficial relationship (Hallmann et al., 1997; Lodewyckx
et al., 2002). Over 80 genera of endophytic bacteria are reported, with Gram-
negative genera Pseudomonas and Enterobacter as most predominant (Lodewyckx
et al., 2002).
Nematophagous bacteria can be classified based on the interactions with their
hosts, leading to the following distinctions: (i) parasites (e.g., P. penetrans), (ii)
opportunistic parasites (e.g., Brevibacillus laterosporus and specific Bacillus
strains), (iii) rhizobacteria, (iv) bacteria producing Cry proteins (e.g., Bacillus
thuringiensis and Lysinibacillus sphaericus), and (v) endophytic and symbiotic bac-
teria (e.g., Xenorhabdus and Photorhabdus spp.) (Tian et al., 2007). Among the
genera considered non-parasitic with both endophytic and epiphytic (rhizobacteria)

life-styles, Bacillus spp. stand out due to their repeated use as biocontrol agents
against various insect orders, including more recent applications against nematodes
(Li et al., 2015). Bacillus and Pseudomonas clades dominate the rhizosphere and
possess nematode-controlling abilities (Tian et al., 2007). The Gram-positive
Bacillus comprises spore-forming bacteria producing endospores, that inhabit the
soil as saprotrophs (Rodas Junco et al., 2009). Notably, some Bacillus spp. such as
B. thuringiensis are known for carrying plasmids containing genes that encode crys-
tals of insecticidal endotoxins known as Cry proteins (Li et al., 2015).
Bacillus thuringiensis, within this group, has been extensively documented and
exploited as a BCA since 1970, with at least 60,000 isolates recorded, worldwide
(Shand, 1989). Its popularity as a BCA can be attributed to its specificity and safety
towards beneficial insects, birds, fish, mammals, and plants (Tian et al., 2007).
Moreover, B. thuringiensis thrives in various environments, including soil, freshwa-
ter, and marine ecosystems, and tolerates harsh conditions such as desiccation and
heat due to endospores resistance (Tian et al., 2007). Over the past four decades,
mass production techniques have further facilitated the widespread use and com-
mercialization of B. thuringiensis as a potent BCA (Tian et al., 2007).
Some opportunistic parasitic bacteria may also parasitize PPN. Numerous stud-
ies have recorded that some PPN, such as Heterodera glycines and Bursaphelenchus
xylophilus, can be successfully controlled by isolates of Brevibacillus laterosporus
(Huang et al., 2005). Another special type of bacteria related to the root system
(Rhizobacteria) has long been considered for PPN control (Sikora, 1992). For
example, Serratia marcescens reduced M. incognita development and reproduction
in tomato plants (Solanum lycopersicum) (Abd-Elgawad & Kabeil, 2010). Similarly,
Bacillus spp., known by their aerobic endospore formation, showed an antagonistic
reaction to PPN, mainly Meloidogyne, Heterodera, and Rotylenchulus (Tian et al.,
2007). Studies carried out by Noel (1990), under green field conditions with soy-
bean (Glycine max), indicated the involvement of the entomocidal crystalline
δ-endotoxin called ‘thuringiensin’, produced by B. thuringiensis, in the mortality of
H. glycines. A mechanism of action different from that deployed by the same toxin
in insects has been suggested. In this regard, Mendoza et al. (2008) pointed out that
the size of bacteria, wider than the nematode esophageal lumen, prevents them from
passively entering the PPN body.
Leyns et al. (1995) discovered that the nematicidal impact of B. thuringiensis can
be linked to crystal proteins classified as Cry V and Cry VI. Furthermore, Marroquin
et al. (2000) demonstrated in-vitro that Cry5 toxins had lethal effects on the bacte-
riophagous nematode Caenorhabditis elegans. These effects were characterized by
ageing in internal morphology, reduced coloration, sluggish movements, and dimin-
ished reproductive capability. Surprisingly, the study did not observe any discern-
ible impact on the nervous or muscular systems. However, at higher toxin
concentrations, the nematodes exhibited symptoms similar to those of insects
affected by Cry1Ab in the intestine.
More recently, the presence of 6 families of Cry proteins with nematicidal effect
(Cry5, Cry6, Cry12, Cry13, Cry14, and Cry21) was noted in 22 out of 70 B.
thuringiensis isolates, the most common being the Cry6 family, with 22.8% of the
total (Salehi Jouzani et al., 2008). Subsequent studies on tomato plants using mix-
tures of protein crystals and endospores of these 22 isolates showed mortality rates
in M. incognita ranging from 0% to 100%. Most of isolates with the highest mortal-
ity rates were evaluated in vitro at two doses (1.0 × 108 and 2.0 × 108 CFU/mL),
showing, after 3–4 days, inhibition of egg hatching and mortality in emerged larvae.
All treatments showed a nematicidal impact on M. incognita and 81% mortality
rate. The higher dose induced a 100% mortality rate. Inhibition of egg hatching
showed a maximum of 46%. Although, a mechanism of action similar to that occur-
ring in insects has been reported in bacterivorous nematodes such as Panagrellus
redivivus (Salehi Jouzani et al., 2008) and C. elegans (Marroquin et al., 2000), a
contact effect of toxins cannot be overlooked in the context of biological control.
Luo et al. (2013) conducted a study demonstrating how the protein Cry6Aa2
adversely affected C. elegans by causing growth inhibition, reducing brood size,
and inducing abnormal motility. An intriguing finding was that when Cry6A was
combined with Cry5B, it resulted in a synergistic activity against the nematode.
This combination proved to be a promising and effective biocontrol strategy for
PPN (Yu et al., 2014). Other studies also highlighted the potential of B. thuringien-
sis strains in controlling PPN (Chen et al., 2000a; Li et al., 2007; Salehi Jouzani
et al. 2008; Sanahuja et al., 2011). However, various environmental conditions i.e.
UV radiations, temperature, and desiccation, significantly impact the B. thuringien-
sis survival, limiting its usage as BCA to large-scale applications in agricultural
fields, and narrowing its application to greenhouse cultivations (Raymond
et al., 2010).
Plant growth-promoting rhizobacteria (PGPR), in particular Bacillus and
Pseudomonas strains, may affect o the population numbers of M. incognita (Siddiqui
et al., 2009). In vitro and greenhouse trials centring around pea plants (Pisum sati-
vum), demonstrated the capacity of both bacteria to hinder nematode egg hatching,
improving plant growth, and decreasing the number of galls and nematodes within
the root system. Nevertheless, both bacterial strains exerted disease suppression
through various competitive mechanisms, including Fe (III) competition, inhibition
through volatile compounds, induction of resistance, vigorous rhizosphere coloni-
zation, and plant growth promotion (Siddiqui et al., 2009).
Serine protease (an extracellular enzyme) obtained from Bacillus isolates showed
nematicidal propertiesagainst Panagrellus redivivus (Qiuhong et al., 2006).
Furthermore, Tian et al. (2007) emphasized that B. subtilis is the most extensively
studied bacterium in terms of its potential for this specific purpose. Moreover, B. fir-
mus has demonstrated significant potential in laboratory and greenhouse environ-
ments against M. incognita and Ditylenchus dipsaci (Mendoza et al., 2008; Terefe
et al., 2009). Jonathan and Umamaheswari (2006) reported that applying an endo-
phytic isolate of B. firmus to banana plants in nursery conditions reduced the popu-
lation of PPN such as Radopholus similis, Pratylenchus coffeae, Helicotylenchus
multicinctus, and M. incognita. The isolate also increased the height and weight of
the aerial and root parts, with a higher number of leaves. Moreover, the bacterium
demonstrated efficacy in controlling other nematode species such as M. hapla,
Heterodera spp., Tylenchulus semipenetrans, and Xiphinema index (Terefe et al.,

2009). In-vitro experiments revealed that the crude filtrates of B. firmus induced
significant paralysis and mortality rates in M. incognita, D. dipsaci and R. similis
while reducing the M. incognita outbreak. Additionally, B. firmus cell suspensions
without extracellular substances led to a 41% reduction in the survival of R. similis
(Mendoza et al., 2008).
Rhizobacteria employ a variety of strategies vs PPN, by generating a diverse
array of metabolic products, enzymes, and toxins that effectively suppress nema-
tode reproduction, eggs hatching, gall formation, and the survival of juvenile stages
(Siddiqui & Mahmood, 1999). This study underscores a significant role of second-
ary metabolites and extracellular proteases in controlling PPN. Previous research
has identified the nematicidal properties of compounds produced by Bacillus spp.,
such as B. thuringiensis, or by Burkholderia ambifaria and P. cepacia. Various
enzymes i.e., proteases, chitinases, and collagenases, have also a lytic activity
affecting nematodes (Qiuhong et al., 2006; Wei et al., 2009). Moreover, several
other Bacillus spp., such as B. cereus, B. pumilus, and B. licheniformis, have been
reported for their nematicidal effects (Siddiqui & Mahmood, 1999).
Interestingly, some rhizobacteria indirectly antagonize nematodes by promoting
plant growth and reducing the damages inflicted by PPN infestations (Khan et al.,
2007). In some cases, a combination of strategies is employed for enhanced effi-
cacy. For example, researchers reported the effect of hydrogen cyanide released by
P. aeruginosa in conjunction with the nematicidal activity of proteases and chitin-
ases produced by B. licheniformis. This combination significantly amplified the
nematicidal effect compared to the impact of each component alone (Gallagher &
Manoil, 2001; Ahmed et al., 2007).
Several traits characterize the Bacillus potential for use in industry and biologi-
cal control against plant pests and diseases. They include, in particular, its ability to
produce chitinolytic and proteolytic enzymes. It is well known that both degrade
essential constituents of the exoskeleton of insects, the eggs cuticle, the juvenile and
adult stages of nematodes, and the cell walls of fungi. By prospecting and isolating
in different geographic regions, it has been possible to produce strains that retain
these properties, in particular for well known beneficial bacteria such as B. thuringi-
ensis (Carreras Solís et al., 2009). Salehi Jouzani et al. (2008) highlighted that look-
ing for native strains of bacteria with activity on PPN could have a global impact on
control. In this sense, the isolation from a PPN suppressive soils and the establish-
ment of a system to determine their in vitro potential could lead to the design of
effective BCA.
The use of different bacteria (B. thuringiensis, B. subtilis, and P. cepacia) in a
mixture with some fungi (Trichoderma spp., Clonostachys spp., and Lecanicillium
lecanii) was evaluated on the reproduction of R. similis (Vargas & Araya, 2007).
Results underlined that B. thuringiensis and the B. thuringiensis + B. subti-
lis + P. cepacia mixture exhibited biocontrol efficacy rates of 51% and 67%, com-
pared to the BCA-free control inoculated with nematodes only. Applying B. subtilis
and the three antagonistic bacteria in mixture resulted in more remarkable vegeta-
tive growth, exceeding the commercial control with a nematicide (oxamyl).
However, fungi provided lower control levels (35%) without significant differences.
In another study, Vargas and Araya (2007) evaluated the biocidal potential of an
individual or combined application of Trichoderma spp., B. subtilis, and Streptomyces
spp., suggesting that the combined application of these three BCA reduced the num-
ber of nematodes by 47%. In contrast, the individual application of B. subtilis,
Trichoderma spp., and Streptomyces spp. reduced the nematode density by 39%,
33%, and 30%, respectively, without any significant difference from the control
inoculated with nematodes.
In brief, the interactions between bacteria and nematodes exhibit diverse mecha-
nisms. These encompass various processes, such as direct parasitism and the impact
of secondary metabolites, enzymes, toxins, and antibiotics. Additionally, they
involve competing for essential nutrients such as iron, disrupting host recognition,
and influencing nematode behaviour during the root penetration phase. Moreover,
bacteria induce systemic resistance and facilitate plant growth. These findings are
consistently supported by results from many studies (Li et al., 2015; Liang et al.,
2019; Mendoza et al., 2008; Siddiqui & Mahmood, 1999; Terefe et al., 2009; Tian
et al., 2007). Furthermore, many of these mechanisms are also attributed to the
effect of PGPR that release phytohormones and enhance nutrient availability, com-
pete for space, and reduce ethylene production (Liang et al., 2019; Vetrivelkalai
et al., 2010).
4.2.2 Entomopathogenic Nematodes in PPN Management
Entomopathogenic nematodes (EPNs), belonging to genera Steinernema and

Heterorhabditis, are widely employed as BCA to combat insect pests on a global
scale (Ehlers, 2001; Kaya et al., 2006; Khan et al., 2009; Rumbos & Athanassiou,
2017; Sayedain et al., 2020). EPNs enter their hosts through natural openings such
as the anus, spiracles, or mouth (Campbell & Lewis, 2002; Griffin et al., 2005).
Once inside the host body, the infective juveniles (IJs) release Photorhabdus and
Xenorhabdus bacteria, stored in their intestines, inside the insect body cavity, caus-
ing the host death within a short span of 24–48 h (Grewal & Georgis, 1999; Kaya &
Gaugler, 1993). Utilizing native EPN populations or species proves to be advanta-
geous, as these nematodes are better adapted to local environmental conditions,
enhancing their survival after soil application. Additionally, these nematodes dem-
onstrate effective biocontrol against a wide array of economically significant PPN
(Lewis & Grewal, 2005). Their use as BCA is further endorsed due to their friendly
effect on both fauna and flora (Ehlers & Shapiro-Ilan, 2005), potential for large-
scale production in artificial media (Ehlers & Shapiro-Ilan, 2005), and ease of appli-
cation through simple spraying, irrigation, or injection equipment (Georgis, 1990).
Numerous studies extensively documented the suppressive effects of different
EPN species vs PPN such as Meloidogyne spp., R. reniformis, H. schachtii, and
Globodera rostochiensis (Pérez & Lewis, 2004; Raza et al., 2015; Kepenekci et al.,
2016; Khan et al., 2016; Caccia et al., 2018; Sayedain et al., 2020). Specifically, the
effectiveness of various EPNs against J2 and egg masses of Meloidogyne spp. has
been documented (Molina et al., 2007; Noweer & El-Wakeil, 2007; Khan et al.,
2009). For instance, Khan et al. (2009) conducted a study evaluating four EPN iso-
lates, namely S. glaseri, S. asiatica, H. indica, and H. bacteriophora, and observed
a significant J2 decrease in M. incognita populations parasitizing tomato plants.
Pérez and Lewis (2004) found that a single application of 25 IJs/cm2 of S. feltiae
reduced the number of M. hapla on peanuts. Similarly, Sayedain et al. (2020) dem-
onstrated PPN-suppressive effects for H. bacteriophora and S. carpocapsae.
The suppressive effects of EPNs on PPN can be attributed to various factors,
including competition between nematode groups for space in the plant root system
(Tsai & Yeh, 1995) or attraction to root exudates (Robinson, 1995). Furthermore,
the EPN-symbiotic bacteria complex can produce various allelochemicals that
influence PPN survival (Lewis et al., 2001; Samaliev et al., 2000). Increased popula-
tions of natural enemies may also contribute to the observed effects (Grewal &
Georgis, 1999).
4.2.3 Nematophagous Fungi and PPN Management
Nematophagous fungi (NFs) exhibit a remarkable capacity to attack PPN through-

out all phases of their development (Dong & Zhang, 2006). Numerous fungi have
undergone extensive investigation as biocontrol agents targeting nematodes that
threaten plants, particularly the root-knot nematodes (Table 4.2). The principal
groups encompass endophytic fungi, arbuscular mycorrhizal fungi (AMF),
nematode-trapping, and parasitic fungi (Kerry, 2000; Dong & Zhang, 2006).
4.2.3.1 Endophytic Fungi
Endophytic fungi have emerged as a promising and innovative solution for PPN
management, with a specific focus on RKN (Hallmann & Sikora, 1994; Kerry,
2000; Dong & Zhang, 2006). The usage of endophytic fungi as BCA is an ever-
expanding realm of research that has captured the attention of scientists, worldwide.
These fungi, which thrive as saprotrophs, establish a mutually beneficial relation-
ship with plant tissues, causing no harm to the plants and allowing them to remain
healthy and symptom-free. The successful colonization by endophytic fungi imparts
protection to the plants against various biotic and abiotic stresses, leading to their
designation as mutualistic endophytes (Carroll & Johnson, 1990; Latz et al., 2018).
Among 200 endophytic fungi isolated from tomato roots in various pot experi-
mentsrevealed a sub-set of 40 isolates with a control capability for M. incognita.
Notably, when four strains of F. oxysporum were applied, they successfully reduced
M. incognita-induced gall formation by 52–75%. Furthermore, the infiltration of
M. incognita in the tomato seedlings was significantly impeded by a F. oxysporum
cell-free filtrate (Hallmann & Sikora, 1994).
4
Table 4.2 Endophytic fungi and their biocontrol potential against nematodes
Endophytic fungi Nematode Plant Mode of action References
Piriformospora indica M. incognita Tomato Inhibition of egg hatching and causing mortality Varkey et al. (2018)
of secondary juveniles
Arthrobotrys, Motierella Meloidogyne Tomato Nematode-trapping fungi form adhesive hyphal Topalović et al. (2020)
Haptocillium, Pochonia spp. traps, and endoparasitic fungi utilize spores
Arthrobotrys spp., Acremonium Meloidogyne Tomato, zucchini Reduction of root galling and the number of eggs Peiris et al. (2020)
spp. spp. Lettuce, eggplant and egg masses in roots
Purpureocillium lilacinum, Meloidogyne Solanum. lycopersicum cv. Reduction of root galling Tazi et al. (2020)
Arthrobotrys oligospora spp. Calvi
Trichoderma harzianum Globodera S. sisymbriifolium Significant reduction of G. pallida populations Dandurand and
pallida S. tuberosum Knudsen (2016)
Aspergillus flavus, Penicillium M. incognita Cucumis sativa L. Strong nematicidal activity exhibited by fungal Naz et al. (2020)
chrysogenum, Pochonia cultural filtrates
chlamydosporia
Trichoderma citrinoviride M. incognita S. lycopersicum cv L-402 Metabolites of T. citrinoviride Snef1910 Fan et al. (2020)
Snef1910 susceptible to M. incognita significantly decreased the number of root galls,
J2s, and nematode egg masses and J2s population
density in soil and significantly promoted the
growth of tomato plants
Talaromyces assiutensis M. javanica Olea europaea L. Adhesive networks, constricting rings, hyphal Aït Hamza et al. (2017)
tips, adhesive conidia and mycotoxins
T. harzianum, T. viride M. incognita S. lycopersicum L. Significant reductions in the number of galls, egg Tariq (2018)
masses, eggs per egg mass and reproductive
factors of M. incognita
P. lilacinum, Metarhizium Nacobbus B. vulgaris var. conditiva, B. Use hyphae and adhesive conidia in host Sosa et al. (2018)
robertsii, Plectosphaerella aberrans vulgaris var. cicla infection processes
plurivora
(continued)
101
102
Endophytic fungi Nematode Plant Mode of action References

Orbiliomycetes Meloidogyne Maize Exhibition of nematicidal activities by the Degenkolb and
spp. production of several substances Vilcinskas (2016)
Heterodera and
Globodera spp.
T. asperellum, F. oxysporum M. incognita S. lycopersicum Reduction of root-knot nematode egg densities Bogner et al. (2016)
Exophiala sp., P. H. schachtii Beta vulgaris Infection of cysts and eggs colonization Haj Nuaima et al.
chlamydosporia, Pyrenochaeta (2021)
sp.
Arthrobotrys conoides Duddingtonia S. lycopersicum Trapping nematodes into the trapping devices and Pandit et al. (2017)
flagrans extracellular hydrolytic enzyme plays a decisive
role in the degradation of nematode’s exterior
cuticle
Mortierella globalpina Caenorhabditis S. lycopersicum cv. Rutgers Hyphal adhesion and cuticle penetration, DiLegge et al. (2019)
elegans subsequent digestion of host cellular contents,
M. chitwoodi reduced RKN symptomology in vivo via
significant reduction of galls
P. chlamydosporia Meloidogyne Potato and tomato Parasitism of eggs competition with other soil Sellitto et al. (2016)
spp. microorganisms
P. lilacinum (PLSAU 1, M. incognita Tomato (L. esculentum), Reduction of galls, egg parasitism, egg hatching Aminuzzaman et al.
PLSAU 2), P. chlamydosporia eggplant (S. melongena), inhibition, J2 mortality (2018)
(PCSAU 1) cucumber
P. Chlamydosporia PC-1, PC-6 M. incognita Tomato plant Inhibitory activity of culture filtrates on egg Uddin et al. (2019)
hatching and M. incognita J2, at different
concentrations
Snef1216 (Penicillium M. incognita Tomato and cucumber plants Egg hatching inhibition and mortality of Sikandar et al. (2020)
chrysogenum) second-stage juveniles
P. chlamydosporia var. M. enterolobii Tomato cv. Santa Clara, Eggs parasitism, lower J2 hatching and number Silva et al. (2017)
catenulata, and var. banana cv. Terra of eggs
chlamydosporia, P. lilacinum
F. Mokrini et al.
Endophytic fungi counter nematodes through a diverse array of strategies. They

use lytic secondary metabolites, which exhibit antibiosis, while simultaneously
engaging in competitive interactions with PPN (Schouten, 2016; Yang et al., 2013).
When faced with aggressors, plants demonstrate defence responses through ISR or
systemic acquired resistance (SAR). SAR heavily relies on salicylic acid (SA) and
prompts the production of pathogenesis-related proteins (PR) involved in defence.
In contrast, ISR is controlled by jasmonic acid (JA) and ethylene (ET) without sig-
nificantly affecting PR protein expression (Vlot et al., 2008; Pieterse et al., 2009).
BCA can induce both SAR and ISR in plants attacked by pests and/or pathogens.
However, to successfully establish themselves within the host root tissues, they
must partially suppress these defence mechanisms (Busby et al., 2016). An excel-
lent example of such beneficial microorganisms is the genus Epichloë, comprising
essential endophytic fungi commonly found in grasses and extensively studied for
their capability to protect plants by synthesizing various alkaloids (Caradus &
Johnson, 2020). These fungi have demonstrated their effectiveness in enhancing
plant immunity against insects and promoting defence mechanisms (Bastias et al.,
2017). Moreover, they are effective in perennial ryegrass against foliar fungal patho-
gens, particularly Bipolaris sorokiniana (Li et al., 2018).
A plethora of distinct and varied mechanisms are implicated in regulating nema-
tode populations through the actions of endophytic fungi. These fungi employ many
strategies against nematodes, including direct assaults, lethal attacks, immobiliza-
tion, and repellent tactics. Additionally, they can bewilder nematodes upon detect-
ing their host, impede the development of nursing cells, compete for essential
resources, and even synergistically combine multiple strategies (Mwaura et al.,
2010; Schouten, 2016). Several studies have focused on the effectiveness of F. oxy-
sporum in controlling the lesion nematode P. goodeyi, as it induces total paralysis
and eradicates nematodes in the root. Similarly, Acremonium implicatum colonizes
tomato root xylem, parasitize, and obliterates M. incognita eggs in soil (Yao et al.,
2015). Another recent investigation by Khan et al. (2019) showcased how nemati-
cidal secondary metabolites produced by Chaetomium globosum may affect
M. javanica, including 3-methoxyepicoccone, 4,5,6-trihydroxy-7-methylphthalide,
chaetoglobosin A, chaetoglobosin B, and flavipin. Moreover, volatile organic com-
pounds (VOCs) of Daldinia cf. concentric exhibited higher efficacy against
M. javanica, as reported by Liarzi et al. (2016). In contrast, the production of alter-
nariol 9-methyl ether by Alternaria spp. was effective against the pinewood nema-
tode B. xylophilus (Lou et al., 2016). However, a few reports have indicated that
Beauveria bassiana increased the reproduction of potato nematodes and caused
damage to potato tubers due to Ditylenchus destructor and D. dipsaci (Mwaura
et al., 2017).
4.2.3.2 Arbuscular Mycorrhizal Fungi (AMF)
AMF are commonly found in soil, where they are crucial to the ecosystem stability.
These remarkable fungi establish mutualistic symbioses with about 80% of terres-
trial plant species, including various crops (Smith & Read, 2008). As obligate bio-
trophic organisms, AMF foster the growth and development of plants by enhancing
their nutrition, resulting in significant uptakes of nutrients (Bethlenfalvay et al.,
1991). Furthermore, they act as protectors, shielding their host plants from both
abiotic and biotic stress factors, notably drought stress and infection caused by PPN
(Pinochet et al., 1996; Schouteden et al., 2015). The mycorrhizal associations are
conventionally classified into two main groups: ectomycorrhizas and vesicular-
arbuscular mycorrhiza (Frouz et al., 2019). Each group plays a unique role in the
intricate web of interactions within the soil ecosystem.
The utilization of AMF offers an ecologically sustainable approach to the bio-
logical management of PPN, (Table 4.3), affecting PPN through various mecha-
nisms and strategies (Schouteden et al., 2015). Endomycorrhizae, the predominant
type of mycorrhizal symbiosis, are commonly found in a broad range of cultivated
plants, including vegetables, fruits, flowers, forest trees, and plantations. The hyphae
of endomycorrhizal fungi colonize the root surface, establish an appressorium, and
subsequently penetrate the cortex. Within the cortical root cells, the hyphae grow
inter- and intracellularly, giving rise to two critical structures vital for survival: ves-
icles and arbuscules (Wani et al., 2017).
Numerous studies highlighted the function of AMF in controlling PPN attacks
and reducing their densities in the soil, mostly focusing on the impact on Meloidogyne
species (Hol & Cook, 2005; Liu et al., 2012; Marro et al., 2017; Campos, 2020; De
Sá & Campos, 2020). The colonization by AMF provides essential nutrients to host
plants and exerts a suppressive effect on root-knot nematodes. Previous findings
have demonstrated that roots heavily colonized by AMF before nematode infesta-
tion experienced lower rates of nematode attacks (Poveda et al., 2020; Zhang et al.,
2020). Moreover, AMF protect their host plants against nematode attacks.
Greenhouse studies have shown a decreased effect in the penetration of RKN in
infected plants when an AMF, such as Glomus mosseae, was present. These fungi
interact with the host plant and nematodes, competing for space in the roots or the
rhizosphere environment (Hussey & Roncadori, 1982; Stirling, 1991).
Plants harbouring a well-established symbiotic density exhibit remarkable
strength and heightened resistance to both biotic and abiotic stress factors. This
resilience allows them to fend off soil nematodes and endure adverse conditions
such as salinity, temperature fluctuations, and drought. An additional, fundamental
advantage is the bolstered phosphate assimilation (Wani et al., 2017).
For many years, scientists have diligently explored the advantageous effects of
endomycorrhizal fungi on plants parasitized by nematodes (Wani et al., 2017).
Basic hypothesis was that symbiotic mycorrhizae could alter or diminish root exu-
dates, affecting nematode eggs hatching or attraction to roots. Moreover, these fungi
effectively hinder the development and reproduction of nematodes within the root
tissues while parasitizing female nematodes and eggs (Zhang et al., 2020). The
4
Table 4.3 Effects of arbuscular mycorrhizal fungi (AMF) on most severe nematode pests
Endophytic AMF Nematode Plant Mode of action References
Gigaspora albida M. Guava (Psidium Enhanced growth of seedlings and increased amount of De Sá and Campos (2020)
Claroideoglomus enterolobii guajava) phloem, reduction of Meloidogyne numbers in roots
etunicatum
Acaulospora longula
Glomus mosseae M. incognita Solanum Reduction in M. incognita penetration in the tomato Vos et al. (2012a)
lycopersicum cultivar Marmande after it received mycorrhizal root
exudates, due to a negative effect on nematode motility
in the soil
Rhizophagus irregularis M. incognita S. lycopersicum Optimal plant growth, minimizing nematode parasitism; Sharma and Sharma (2017a)
strong phenolic activity and defensive enzymes
(polyphenyloxidase, superoxide dismutase, peroxidase);
decrease in malondialdehyde and hydrogen peroxide
levels
Glomus fasciculatum, G. Pratylenchus Sugarcane Enhanced shoot and root growth, declining the P. zeae Sankaranarayanan and Hari
mosseae zeae population (2020)
Rhizophagus irregularis M. incognita Tomato Boost plant growth while reducing nematode population; Sharma and Sharma (2017a)
improvements in physiological and biochemical
parameters
Rhizophagus intraradices, Nacobbus Tomato Decreased number of J2; reduced penetration of Marro et al. (2017)
Funneliformis mosseae aberrans nematodes
R. intraradices M. incognita Tomato Alterations in the expression of tomato genes associated Balestrini et al. (2019)
with nematodeparasitism
Acaulospora colombiana Meloidogyne Cassava esculenta Suppression or reduction of nematode reproduction Séry et al. (2016)
Ambispora appendicula spp.
Glomus mosseae M. incognita Solanum Reduction of nematode penetration, up-regulation of Vos et al. (2013b)
lycopersicum genes expressed in co-inoculated plants involving the
phenylpropanoid pathway and reactive oxygen species
(ROS)
105
(continued)
106
Endophytic AMF Nematode Plant Mode of action References

F. mosseae M. incognita S. lycopersicum Increased tomato growth, reduction of parasitism severity Flor-Peregrín et al. (2014)
and final nematode densities
Acaulospora longula, P. penetrans Apple Reduction of the nematode population in soil of Ceustermans et al. (2018)
Claroideoglomus AMF-inoculated seedlings
claroideum, Glomus
intraradices
Claroideoglomus H. glycines Soybean Reduction of the number of cysts Pawlowski and Hartman
claroideum, Diversispora (2020)
eburnea, Dentiscutata
heterogama, F. mosseae,
Rhizophagus intraradices
F. mosseae M. incognita Tomato Nematode suppression; increase of leaf chlorophyll Flor-Peregrín et al. (2016)
content and raise in the canopy temperature
Rhizophagus irregularis Radopholus Banana In vitro reduction of the total R. similis population and Koffi et al. (2013)
MUCL 41833 similis the surface of root necrosisin the AMF-colonized banana
plantlets
F. Mokrini et al.
successful establishment and efficacy of the mycorrhizal association rely on several

factors, including the host characteristics, the type of fungus involved, and soil
physiochemical properties such as texture, pH, and the presence of other microor-
ganisms (Carrenho et al., 2007; Wani et al., 2017; Mahmoudi et al., 2020).
Mycorrhizae arise from the meeting between a mycorrhizal fungus and the root.
This meeting allows the two partners to enter into a symbiosis, with mutual benefits
(Goltapeh et al., 2008; Bonfante & Genre, 2010). The fungus swaddles a network of
hyphae around the ends of the rootlets that develop as a thick mycelium tissue of
filaments. The length of hyphae allow the plants to draw nutrients over much longer
distances. The success and control of this mycorrhizal symbiosis is a complex phe-
nomenon involving several regulatory components functioning at different levels
(Schouteden et al., 2015). In recent years, molecular tools allowed for insightful
investigations into the role of defence phytohormones in shaping mycorrhizal inter-
actions. The phytohormones are active from the initial recognition events till the
establishment of symbiosis (Liao et al., 2018). Several studies showed that mycor-
rhizal fungi can induce plant defence responses, such as ISR, upon pathogen and
pest attacks (Pozo & Azcón-Aguilar, 2007; Hohmann & Messmer, 2017; Jacott
et al., 2017). Initially, the fungi trigger plant defense mechanisms akin to those acti-
vated by biotrophic pathogens, but they subsequently modify them to ensure a suc-
cessful colonization (Jung et al., 2012; Cameron et al., 2013).
SA plays a pivotal role in initiating plant responses against biotrophic pathogens.
AMF enhance this signalling pathway, eventually dialling it down to facilitate the
establishment of symbiotic interactions (Campo & San Segundo, 2020; Kaur &
Suseela, 2020). Once mycorrhization is successfully established, the activation of
induced resistance and priming, regulated by JA, mirrors the responses mediated by
the JA and ethylene (ET) pathways when countering necrotrophic pathogens
(Hohmann & Messmer, 2017). However, previous studies have uncovered a signifi-
cant overlap between SAR (ISR, indicating extensive communication and cross-talk
among these pathways (Mathys et al., 2012; Pieterse et al., 2014). As a result, it was
concluded that the AMF-mediated plant defence response against PPN is unlikely to
depend solely on the JA-dependent pathway (Schouteden et al., 2015).
Extensive research has been conducted on the AMF role in providing resistance
against PPN (Zhang et al., 2020). However, differentiating between the contribu-
tions of systemic resistance and direct effects on infection reduction implies recur-
rent challenges. It is essential to consider that plant defence responses play a
significant role in this process. Various mechanisms have been proposed to elucidate
how AMF can effectively control PPN. These mechanisms include enhancing plant
tolerance, engaging in nutrient and space competition, inducing ISR, and altering
interactions within the rhizosphere, (Schouteden et al., 2015). Notably, reports have
emphasized the systemic reduction of nematode infection in mycorrhizal roots
(Zhang et al., 2020).
Vos et al. (2012a) conducted a split-rot experiment using tomato plants and found
the potential of mycorrhizal fungi to induce systemic resistance. They partitioned
the root system into two compartments, introducing G. mosseae to one compart-
ment while leaving the other fungus-free. The outcomes revealed a noteworthy
reduction in the nematode infectivity in the compartment with G. mosseae com-

pared to the one lacking the fungus. Similar findings were observed in banana
plants, where Rhizophagus irregularis displayed systemic suppression of R. similis
and P. coffeae, utilizing the same split-rot configuration (Elsen et al., 2008).
Furthermore, a comparable mechanism of systemic suppression against the ecto-
parasitic nematode X. index was also reported (Hao et al., 2018). Previous studies
have also demonstrated a systemic impact of AMF against various other pathogens
(Khaosaad et al., 2007; Castellanos-Morales et al., 2011). However, no conclusive
evidence was provided regarding the systemic suppression of Pratylenchus pene-
trans by AMF, in dune grass species (De La Peña et al., 2006).
One notable aspect involves the activation of specific genes, such as those encod-
ing chitinases, pathogenesis-related (PR) proteins, and enzymes responsible for
detoxifying reactive oxygen species (ROS), such as glutathione S-transferase (SAT)
and superoxide dismutase (SOD). Additionally, AMF-triggered responses encom-
pass lignin biosynthesis and the shikimate pathway (Schouteden et al., 2015). The
shikimate pathway holds particular significance in AMF-mediated biocontrol
against various PPN. This pathway plays a pivotal role in producing precursors for
aromatic secondary metabolites (Hao et al., 2012; Vos et al., 2013a; Sharma &
Sharma, 2017b). Most of them are synthesized via the phenylpropanoid pathway,
except flavonol synthase being primed instead (Vos et al., 2013b). In vitro studies
showed detrimental effects of several phenylpropanoid pathway products, including
flavonols, on different nematode species (Wuyts et al., 2006). These findings have
helped unravel the intricate interactions between AMF, plants, and nematodes and
establish potential avenues for biocontrol strategies.
The interaction between PPN and AMF depends on various factors, including the
specific nematode and AMF species involved and the host plant (Hol & Cook,
2005). AMF application reduced the development of sedentary nematodes, such as
Meloidogyne spp. and Heterodera spp. Additionally, AMF exhibited greater effi-
cacy in curtailing the populations of specific PPN i.e., Nacobbus aberrans and
Pratylenchus penetrans in tomato plants (Vos et al., 2012b). Moreover, after mycor-
rhizal inoculation, Forge et al. (2001) noted a significant decrease in root lesions
induced by P. penetrans on apple tree roots. The presence of M. chitwoodi did not
affect the development of arbuscules and vesicles during the establishment of
mycorrhizal fungi, that effectively decreased the nematode numbers (Botello
et al. (1999).
Finally, the symbiotic association with mycorrhizal fungi also triggers physio-
logical changes in plants, which can impact the recognition and establishment of
microorganisms inhabiting the rhizosphere (Botello et al., 1999; Posta et al., 1994).
4.2.3.3 Nematode-Trapping and Nematophagous Fungi
Nematophagous fungi (NF) offer a promising approach to managing PPN, effec-

tively (Li et al., 2016). These fungi are widespread and evolved as natural antago-
nists of nematodes. They can remarkably adapt from a saprotrophic lifestyle to a
carnivorous behavior, enabling them to feed on nematodes even under challenging

conditions. This remarkable adaptability allows NF to develop intricate strategies
(Braga & De Araújo, 2014; Degenkolb & Vilcinskas, 2016). According to Singh
et al. (2006), organic matter and nematodes heavily influence the population and
diversity of these organisms in soil. NF can be classified into four primary groups
(Jiang et al., 2017). The first one is represented by the nematode-trapping fungi,
which possess specialized trapping structures distinct from their hyphae. The sec-
ond group is given by endoparasitic fungi that utilize their spores to infect nema-
todes. The third group comprises egg-parasitic species, which invade or colonize
nematode eggs. Lastly, the fourth group is composed by toxin-producing fungi that
immobilize nematodes before invading them.
Nematode-trapping fungi (NTF) includes specific clades of saprotrophic or pred-
ators that entrap moving stages of nematodes by forming specialized structures to
ambush their prey (Lopez-Llorca et al., 2008; Dong & Zhang, 2006; Yang et al.,
2020). NTF, including Arthrobotrys obligospora, A. dactyloides, Dactylella can-
dida, Monacrosporium cionopagum, etc., use sticky structures produced on mycelia
to disrupt nematode mobility. This group is ubiquitous, includes many species, and
is essential to the soil ecosystem. Most of these fungi belong to the order Orbiliales
(Ascomycota). Based on the morphological structure of traps, the NTF have been
classified into four genera: adhesive nets-forming (Arthrobotrys), non-constricting
rings forming (Dactylellina), constricting rings-forming (Drechslerella), and adhe-
sive branches and unstalked knobs-forming (Gamsylella) (Moosavi & Zare, 2012;
Jiang et al., 2017; Rong et al., 2020; Baweja & Rawat, 2020). NTF can survive as
saprotrophs in soil without a specific host (Jiang et al., 2017). Besides, they can
secrete nematicidal compounds such as linoleic acid and pleurotin (Moosavi &
Zare, 2012).
A distinctive group of NF is formed by endoparasitic species that exclusively
parasitize nematodes and exhibit a restricted range of host species. To initiate
nematode infection, these fungi employ specialized spores, namely adhesive
conidia or zoospores (Viaene et al., 2013). Once germinated, they penetrate nema-
todes cuticle. Another NF groups is formed by egg and cyst parasites. These fungi
utilize specific structures, such as appressoria or lateral mycelial branches, to
enzymatically degrade the nematode eggshells. They include species like P. chla-
mydosporia, Trichoderma and Fusarium spp. which infiltrate the root system,
specifically targeting eggs in masses or sedentary stages of RKN or cyst nema-
todes. Another NF group is known for producing toxins that immobilize nema-
todes, afterwards penetrating the host cuticles with their hyphae (Yang & Zhang,
2014; Li et al., 2015).
The intricate processes governing the recognition of nematodes by NF is par-
tially understood, awaiting more comprehensive elucidations. Prior investigations
have proposed that chemical communication is pivotal in identifying and control-
ling morphogenesis. Specifically, certain substances produced by nematodes, such
as ascarosides and nemin, known as nematode pheromones, can be detected and
harnessed by nematophagous fungi, instigating trap morphogenesis. This detection
enables NTF to switch from a saprotrophic to a predatory habit. Furthermore, the
fungi employ olfactory mimicry to allure their prey into traps, employing diverse
VOCs that stimulate nematodes olfactory neurons. These responses are orchestrated
by numerous G protein-coupled receptors (GPCRs) continually generated by endo-
parasitic fungi (Yang et al., 2020).
The adherence of NF to their host nematodes occurs through adhesive proteins
accumulated on the outer surfaces of adhesive traps or spores, including lectins and
specific extracellular polymers (Li et al., 2015; Wang et al., 2015). Following recog-
nition and adhesion, NF penetrate the host using extracellular hydrolytic enzymes
(serine proteases, collagenases, and chitinases) and mechanical pressure (Yang
et al., 2007). Subsequently, an infection vesicles are formed within the cuticle lay-
ers, which then infiltrate the host body. The hyphae then develop inside the infected
nematode, absorbing its internal contents (Braga & De Araújo, 2014; Li et al.,
2015). At this stage, the invading fungi start digest the whole nematode, utilized as
a valuable nutrient source (Jiang et al., 2017).
Numerous research endeavours have been dedicated to harnessing NF as highly
effective biocontrol agents. Duponnois et al. (1996) extensively studied various
strains of Arthrobotrys, revealing their remarkable ability to impede RKN growth
and development. Moreover, Bíró-Stingli and Tóth (2011) documented the effi-
cacy of A. oligospora in curbing the female population numbers of M. hapla on
green pepper. Significantly, this fungus exhibited comparable results vs other
PPN, including D. dipsaci (the stem nematode) and G. rostochiensis (the potato
cyst nematode).
Numerous studies have extensively investigated the interplay between nema-
todes and endo-parasitic fungi. For instance, Chen et al. (2000b) reported the patho-
genic nature of Hirsutella minnesotensis towards the soybean cyst nematode
H. glycines. Similarly, the same species induced a substantial decline of M. hapla in
tomato roots (Mennan et al., 2006). Del Sorbo et al. (2003) recorded the parasitic
ability of H. rhossiliensis against the cyst nematode H. daverti. This fungus had
proven effective against the criconematid nematode Mesocriconema xenoplax para-
sitizing peach (Jaffee & Zehr, 1982) and on the cyst nematode H. schachtii (Lackey
et al., 1992).
Utilizing P. chlamydosporia as a BCA represents a promising strategy for man-
aging RKN, specifically against M. incognita and M. javanica at lvarying densities
ranging from 5000 to 60,000 chlamydospores per g of soil (Kerry, 2000;
Tzortzakakis, 2007). Likewise, encouraging results were reported by applying
P. chlamydosporia vs M. javanica (Olivares-Bernabeu & López-Llorca, 2002). de
Leij et al. (1993) reported a remarkable 90% decrease in the population of M. hapla
on tomato plants grown in sandy loam soil treated with P. chlamydosporia. This
finding highlighted the effectiveness of this BCA in reducing nematode popula-
tions. Furthermore, Wang et al. (2005) successfully controlled R. reniformis by
introducing this fungus. The latter effectively parasitized the nematode eggs, lead-
ing to a significant suppression of the reniform nematode population. Pochonia
chlamydosporia is also an endophyte, inducing the expression of several defense
genes in colonized roots (Kerry, 2000; Pentimone et al., 2019).
4.3 Factors Affecting BCA Success/Failure
BCA may result effective and sustainable in managing PPN. They offer long-term
protection without residual issues, boasting an extensive range of antagonistic activ-
ities, covering various nematode species. Notably, BCA operate through multifari-
ous mechanisms, ensuring their efficacy while being non-toxic to plants and humans.
Moreover, they are eco-friendly and easily manufactured, making them a cost-
effective alternative to conventional agrochemicals. Their straightforward applica-
tion process in the field also contributes to their practicality (Verma et al., 2019).
Despite these benefits, the successful implementation of BCA products faces spe-
cific challenges, particularly concerning their performance under diverse field con-
ditions and the need for advancements in mass production and formulation
technologies. Another crucial aspect is the ability of BCA to effectively control a
broad spectrum of nematodes and diseases while reducing reliance on harmful
chemical pesticides (Abate et al., 2017).
Nonetheless, BCA hold great promise as a substitute for chemical nematicides in
managing PPN. To optimize their utilization, several measures can be undertaken.
First and foremost, enhancing sampling techniques will aid in better assessing their
efficiency and impact. Moreover, a deeper understanding of the ecology and interac-
tions of BCA with soil microbiota will provide valuable insights for their successful
integration into agricultural practices. Raising awareness about BCA techniques
among farmers will also encourage their widespread adoption and utilization (Abd-
Elgawad & Askary, 2020).
Sampling plays a significant role in the success of PPN control. It includes the
time, method, and process of precisely detecting and diagnosing PPN issues.
Furthermore, the density of the nematode population in a given sample must be
determined. The precision of sampling and its accuracy are a substantial pre-
consideration that requires intensive work, high cost, and consumption of time and
effort. Such issues may affect decisions in BCA strategies and their application in
large-scale farming systems (Briar et al., 2016; Abd-Elgawad & Askary, 2020).
BCA marketing is influenced by various factors, including intrinsic, environ-
mental, technological, societal, economic, and commercial aspects. These factors
can significantly impact effectiveness and overall success of biological agent-based
products (Moosavi & Zare, 2015). Intrinsic parameters encompass the behavior and
adaptive capacity of BCA during their application in the field. This includes their
ability to establish and disperse in new environments and their interactions with the
rhizosphere environment, involving soil biology and ecology. These parameters can
affect the efficacy and reproduction of BCA in soil, their capacity to produce nema-
totoxic substances and antibiotics, and the formation of resilient survival struc-
turesto enhance plant growth and stimulate host plant defence mechanisms (Brodeur,
2012; Abate et al., 2017; Abd-Elgawad, 2020; Abd-Elgawad & Askary, 2020). The
foundation for designing an effective BCA is the isolation of a particular strain from
i.e. a nematode-suppressive soil and the establishing of a system to assess its in vitro
potential. Ecological factors encompass both biotic elements (indigenous soil
organisms, susceptibility of host plants to PPN infestation, interactions among soil

biotic factors, rhizosphere characteristics, host-emitted molecules, and damaged
roots) and abiotic factors (edaphic factors such as soil characteristics, temperature,
humidity, pH, nutritional status, and concentration of heavy metals) (Zhou et al.,
2016; Labaude & Griffin, 2018; Abd-Elgawad, 2020).
Technological parameters involve scaling production, formulation, stabilization,
and delivery systems (Labaude & Griffin, 2018; Abd-Elgawad, 2020). However,
these parameters may pose certain risks, including high production costs, limited
availability of suitable and stable formulations, impractical dosage advice, specific
storage requirements, inadequate immobilizing materials, and inappropriate deliv-
ery systems and application methods (Moosavi & Zare, 2015; Le Mire et al., 2016;
Ibrahim et al., 2017). It is important to note that the economical production of BCA
on a large scale is a key criterion to develop commercial products. Societal param-
eters are reflected in public concerns regarding excessive chemical pesticides,
global food security, and the desire for eco-friendly biological alternatives (Li et al.,
2015; Abd-Elgawad, 2020). Regulatory parameters pertain to the rigorous and
costly registration processes to assess ecological impact, toxicity and protect intel-
lectual property rights (Velivelli et al., 2014; Abd-Elgawad, 2020).
4.4 Conclusions and Perspectives
In contemporary agriculture, many farmers rely on chemical methods to manage

PPN as a last-ditch effort to boost yields. However, the increasing environmental
concerns surrounding the use of chemical-based nematicides are gradually dimin-
ishing their effectiveness. Consequently, exploring safe and environmentally
friendly alternatives is advisable to develop effective strategies for biological con-
trol of PPN. Various nematophagous microbes, such as NF, AMF, nematophagous
bacteria, and EPNs, have demonstrated substantial reductions in PPN populations
while significantly contributing to soil and plant health. BCA employ diverse mech-
anisms to exhibit antagonistic activities against nematodes. They offer several
advantages, including safer crop protection, improved soil fertility, effective bios-
timulation, enhanced plant growth and yield potential, increased plant resistance
against nematodes, and a broad spectrum of pathogens and pests. Furthermore,
BCA are pivotal in mitigating abiotic stresses such as drought, salinity, and extreme
temperatures. Although significant progress has been made in comprehending the
mechanisms underlying interactions between BCA and nematodes, further research
is required. The combination of metagenomics, proteomics, metabolomics, and
transcriptomic analyses presents a valuable approach for comprehensively evaluat-
ing bacterial metabolites. This approach enables the screening of several biologi-
cally active molecules, facilitating the discovery of novel metabolites characterized
by high selectivity and potent nematicidal activities. Additionally, it aids in elucidat-
ing nematode infection processes, understanding cellular mechanisms and signal-
ling pathways that influence host immune responses, identifying biosynthetic genes
that determine the BCA mode of action. This valuable information will undoubtedly
serve as a beacon to illuminate the path toward crafting more efficacious strategies.
Subsequent investigations should prioritize the exploration of pragmatic methodol-
ogies for examining and implementing BCA against PPN. These techniques should
encompass mass culturing, formulation development, and storage application meth-
ods. By embarking on such endeavours, we can anticipate substantial advantages in
conducting extensive and enduring field assessments, in the times to come.
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Chapter 4

Plant-Parasitic Nematodes and Microbe

Fouad Mokrini, Salah-Eddine Laasli, Said Ezrari, Zineb Belabess,

Abstract Plant parasitic nematodes (PPN) cause significant damage to a broad

Keywords Biocontrol · Interaction · Nematodes · Parasitism

F. Mokrini (*) · S.-E. Laasli

© The Author(s), under exclusive license to Springer Nature 89

Global crop production faces a significant challenge from plant-parasitic nematodes

4.2 Nematophagous Microorganisms Interactions:

The soil environment provides a favourable habitat for various nematophagous

4.2.1 Nematophagous Bacteria Mechanisms

Table 4.1 Activity of bacteria species and isolates on plant-parasitic nematodes

associated with inhibition of egg

thermal stability killing J2

Bacteria Nematode Plant Mode of action References

Soybean feeding and reproduction

The Gram-positive P. penetrans is a hyperparasite known for forming infective

genera considered non-parasitic with both endophytic and epiphytic (rhizobacteria)

Heterodera spp., Tylenchulus semipenetrans, and Xiphinema index (Terefe et al.,

4.2.2 Entomopathogenic Nematodes in PPN Management

Entomopathogenic nematodes (EPNs), belonging to genera Steinernema and

4.2.3 Nematophagous Fungi and PPN Management

Nematophagous fungi (NFs) exhibit a remarkable capacity to attack PPN through-

Endophytic fungi Nematode Plant Mode of action References

Endophytic fungi counter nematodes through a diverse array of strategies. They

4.2.3.2 Arbuscular Mycorrhizal Fungi (AMF)

Endophytic AMF Nematode Plant Mode of action References

successful establishment and efficacy of the mycorrhizal association rely on several

reduction in the nematode infectivity in the compartment with G. mosseae com-

4.2.3.3 Nematode-Trapping and Nematophagous Fungi

Nematophagous fungi (NF) offer a promising approach to managing PPN, effec-

carnivorous behavior, enabling them to feed on nematodes even under challenging

4.3 Factors Affecting BCA Success/Failure

organisms, susceptibility of host plants to PPN infestation, interactions among soil

4.4 Conclusions and Perspectives

In contemporary agriculture, many farmers rely on chemical methods to manage

Pozo, M. J., & Azcón-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Current

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4.2 Nematophagous Microorganisms Interactions:

4.2.1 Nematophagous Bacteria Mechanisms

4.2.2 Entomopathogenic Nematodes in PPN Management

4.2.3 Nematophagous Fungi and PPN Management

4.2.3.2 Arbuscular Mycorrhizal Fungi (AMF)

4.2.3.3 Nematode-Trapping and Nematophagous Fungi

4.3 Factors Affecting BCA Success/Failure

4.4 Conclusions and Perspectives