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The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control



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Chapter 7
The Impact of Plant-Parasitic Nematodes on
Agriculture and Methods of Control
Gregory C. Bernard, Marceline Egnin and
Conrad Bonsi
Additional information is available at the end of the chapter
Plant-parasitic nematodes are costly burdens of crop production. Ubiquitous in nature,
phytoparasitic nematodes are associated with nearly every important agricultural crop
and represent a signicant constraint on global food security. Root-knot nematodes
(Meloidogyne spp.) cyst nematodes (Heterodera and Globodera spp.) and lesion nematodes
(Pratylenchus spp.) rank at the top of list of the most economically and scientically
important species due to their intricate relationship with the host plants, wide host range,
and the level of damage ensued by infection. Limitations on the use of chemical pesti-
cides have brought increasing interest in studies on alternative methods of nematode
control. Among these strategies of nonchemical nematode management is the identi-
cation and implementation of host resistance. In addition, nematode genes involved in
parasitism represent key targets for the development of control through gene silencing
methods such as RNA interference. Recently, transcriptome proling analyses has been
used to distinguish nematode resistant and susceptible genotypes and identify the spe-
cic molecular components and pathways triggered during the plant immune response
to nematode invasion. This summary highlights the importance of plant-parasitic nema-
todes in agriculture and the molecular events involved in plant-nematode interactions.
Keywords: plant-parasitic nematodes, agriculture, crops, genetics, resistance,
1. Introduction
Over millions of years, the association of plants and nematodes has resulted in the evolution
of the plant-parasitic nematode. Widely distributed pathogens of vascular plants, enormous
losses in yields have been aributed to the presence of nematodes. The intricate relationship
© 2017 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons
Attribution License (, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
between the parasitic nematode and plant has culminated in an “evolutionary arms race”.
Phyto-parasitic nematodes have evolved strategies to suppress host immune responses for
the development of feeding sites. In turn, plants have developed specic molecules to rec-
ognize pathogens signaling the activation of immune responses. Declining use of chemical
pesticides has brought great aention to research in alternative methods of nematode control.
An eective strategy for nematode management involves the utilization and implementation
of nematode-resistant cultivars into crop breeding programs. Currently, genetic sequencing
analyses are widely utilized in the identication of molecular components of nematode para-
sitism and is also used to distinguish nematode-resistant and susceptible plant genotypes.
These detailed analyses have signicantly contributed to our overall understanding of the
dynamic and complex nature of plant-nematode interactions.
2. Nematode morphology
Nematodes are a fascinating, biologically diverse group of organisms. Their ability to adapt
to a wide variety of habitats including; marine, soil and aquatic, provides an evolutionary
advantage for species longevity. Phylum Nematoda is largely distinguished by three major
monophyletic groups including: Enoplia (marine), Dorylaimia (parasitic trichinellids and
mermithids and Chromadoria (nematodes of various environments). Nematodes belong to
the group Ecdysozoa, which comprises animals that can shed their cuticle. Over 30,000 spe-
cies of round worms are found in Nematoda [1] typically ranging in size from 0.2 mm to
over 6 m. Nematode body structure is relatively simple and characterized as limbless, cylin-
drical, and elongated. Essentially the body plan is a “tube within a tube”, the inner tube or
alimentary canal, consists of a digestive tract and gonad which are surrounded by an outer
tube; a body wall containing a series of dorsal and ventral longitudinal muscles aached to
the hypodermis. These muscles are activated by the dorsal and ventral nerves and their con-
tractions allow for locomotion in sinusoidal waves. In plant-parasitic nematodes, a primary
infection structure called a stylet is located at the anterior end of the nematode which is fol-
lowed by an esophageal region that connects the stylet to the intestines. A typical tylenchoid
esophagus consists of an anterior procorpus, a median bulb and the posterior basal bulb. The
median bulb functions in the transfer of enzymes involved in primary infection and facilitates
the movement of plant nutrients into the intestine. Inside of the exterior body wall lies the
pseudocoelom, a unlined, pressurized, uid-lled cavity formed directly from the blastula
surrounding the gut cavity. The pseudocoelom is lled with uid which provides turgor pres-
sure for the entire body containing the internal organs and aides in the transfer of nutrients,
oxygen and metabolic products. The excretory system is composed of four distinctive cells, an
excretory pore cell, a duct cell, one canal cell, and a fused pair of gland cells. Nematodes are
enclosed within an exoskeleton called a cuticle which is secreted by inner hypodermal cells,
and is primarily composed of collagens, insoluble proteins (cuticlins), glycoproteins and lip-
ids. The cuticle plays an important role in movement, environmental protection and growth
and development [2]. The typical male reproductive structures include a testis, a seminal
vesicle and a vas deferens leading to a cloaca, while the female reproductive system is tubular
containing one or two ovaries, seminal receptacles, an uterus, ovijector and a vulva.
Nematology - Concepts, Diagnosis and Control122
3. Evolution of plant-parasitic nematodes
Why do some nematodes become plant parasites? The dynamic association of nematode and
plant host has resulted in plant parasitism which has evolved three times culminating in
substantial benets for nematode survival and development [3, 4]. An existing evolutionary
hypothesis places the origins of these ancient microscopic roundworms around 400 million
years before the explosion of animal phyla (pre-“Cambrian explosion”) [5]. Evidence suggests
the initial presence of plant-parasitic nematodes to have occurred around 235 BC [6] while the
rst described plant parasitic nematodes were reported by Needham who observed symp-
toms of galling in wheat [7]. An agriculturally important species of plant-parasitic nematodes
called root-knot nematodes, were initially identied by Berkeley who observed the presence
of galls on cucumber roots [8].
The plant-nematode association has resulted in the development of specic feeding struc-
tures and secretory products that are involved in host infection and nutrient absorption. Plant
parasitic nematodes are specialized by the stylet and subventral and dorsal esophageal glands
which are considered the most signicant evolutionary adaptations for plant parasitism [4, 9].
Plant-parasitic nematodes utilize a hollow, needle-like, protrusible stylet to probe plant tis-
sue and release an assortment of proteinaceous secretions from the subventral and dorsal
glands which comprises the integrity of the host cell and allow for nematode entry. These
glandular secretions induce cellular remodications that are essential for development of a
metabolically active feeding cell [10]. Among the secretory molecules are a group of carbohy-
drate-active enzymes. Since cellulose is the primary component of plant cell walls, cellulases
(β-1,4-endoglucanases) are secreted to degrade the cell wall which allows nematode entry into
host tissue. Genomic analyses of root-knot nematodes have revealed the presence of a suite
of enzymes called CAZymes (cellulases, xylanases and other glycosyl hydrolase family mem-
bers (GHFs)) [11]. Beta-1,4-endoglucanase genes have been isolated from plant-parasitic cyst
nematodes with catalytic domains belonging to family 5 of the glycosyl hydrolases [12, 13].
Glycosyl hydrolase families G5 and G45 have been identied in plant-parasitic nematodes.
Plant-parasitic nematode GH5 cellulases show closes homologies with bacterial G5s, which
suggests an initial horizontal gene transfer of bacterial G5 cellulases into nematode genomes
during the evolution of the plant-parasitic order Rhabditida (suborder Tylenchina) [14, 15].
G45 cellulases have been found in plant-parasitic nematode Bursaphelenchus xylophilus of the
Aphelenchida order [16]. Phylogenetic analyses have shown similarities in gene structure
between G45 sequences found in these nematodes and ascomycetous fungi which supports
the hypothesis of a horizontal gene transfer event from fungi to nematodes [17].
Plant-parasitic nematodes dier in lifestyles. Some nematodes will invade the plant cells while
others simply obtain nutrition externally. Ectoparasitic nematodes remain outside the host
cells and feed on plant roots while endoparasitic nematodes establish residence within plant
tissue. An example of ectoparasitic nematode is Xiphinema (California dagger nematode)
which transmits the Grapevine fanleaf virus. The resulting viral infection causes tremendous
economic losses in grapes worldwide [18]. Endoparasitic nematodes are further divided into
migratory and sedentary groups. Migratory endoparasitic nematodes move within the root
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
and remove cytoplasm killing the host cell while sedentary nematodes become immobile after
the development of a feeding site within the host tissue [19]. Migratory endoparasitic nema-
todes of economic signicance include Pratylenchus spp. (lesion nematode), Radopholus spp.
(burrowing nematodes) and Hirschmanniella (rice root nematode).
4. The impact of plant-parasitic nematodes on crops
Plant-parasitic nematodes are a costly burden in agricultural crop production. Over 4100 spe-
cies of plant-parasitic nematodes have been identied [20]. Collectively, they cause an esti-
mated $80–$118 billion dollars per year in damage to crops [21, 22]. Encompassing 15% of
all identied nematode species, the most economically important species directly target plant
roots of major production crops and prevent water and nutrient uptake resulting in reduced
agronomic performance, overall quality and yields. Nematodes in the order Tylenchida are
pathogens of plants, invertebrates, and fungi and are considered the most important agricul-
tural pests [22].
Of all the important plant-parasitic nematodes, the most successful species are the seden-
tary groups which establish a permanent feeding site within the plant host and obtain nutri-
ents while completing their lifecycles. Sedentary nematodes have a natural advantage over
their migratory relatives due to a fascinating and complex method of host cell transforma-
tion resulting in the development a sustainable feeding structure. Interestingly, with over
4000 described plant-parasitic nematodes, only a small amount produce signicant economic
losses in crops. In a survey conducted on a variety of crops in the U.S, the major genera of phy-
toparasitic nematodes reported to cause crop losses were Heterodera, Hoplolaimus, Meloidogyne,
Pratylenchus, Rotylenchulus, and Xiphinema [23].
4.1. Wheat
Wheat (Triticum aestivum) is the most important cereal crop in the world. A staple food source
for 40% of the world's population, approximately 758 million tons are produced globally [24].
Wheat yields are signicantly decreased by the presence of cereal cyst nematodes (Heterodera
spp.) in the Heterodera avenae group (H. avenae, Heterodera lipjevi, and Heterodera latipons)
which also damage other important cereals including barley (Hordeum vulgare) and oat (Avena
sativa). An estimated 3.4 million in prots are lost each year in U.S. wheat cultivating states
Idaho, Oregon, and Washington [25]. In some wheat elds, the losses caused by H. avenae can
range from 30 to 100% [26, 27]. In addition to cereal cyst nematodes, further losses of wheat
are caused by root-lesion nematodes Pratylenchus neglectus and Pratylenchus thornei, and the
seed gall or ear-cockle nematode, Anguina tritici. An inverse relationship between H. avenae
and P. neglectus was shown on P. neglectus resistant and susceptible wheat cultivars infested
with H. avenae [28] where a reduction in P. neglectus population densities was observed on
both wheat genotypes. Anguina tritici is often a vector for Rathayibacter tritici, a Gram-positive
soil bacterium which associates with Clavibacter tritici causing seed gall [29].
Nematology - Concepts, Diagnosis and Control124
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
4.5. Sweetpotato
The sweetpotato [Ipomoea. batatas (L) LAM] has been regarded as a plant of great signicance
throughout human history. Its cultivation dates to the prehistoric era, and it has been grown
continuously as a staple food source. Global productions of sweetpotato is estimated at 105 mil-
lion metric tons [44]. Currently, the sixth most important food crop, sweetpotato produc-
tion has improved the economic status for communities throughout the world particularly in
developing nations where it ranks as the fth most important crop [44]. Approximately 10.2%
of sweetpotato yields are lost each year due to the presence of plant-parasitic nematodes [20].
Root-knot nematodes (RKNs) are signicant pests of sweetpotato causing symptoms of infec-
tion which include: stunted plant growth, yellowing of leaves, abnormal ower production,
and gall production on roots leading to decreased nutrient and water absorption and necrosis
and cracking on eshy storage roots. Due to the economic importance of the storage root,
root cracking is a primary concern for producers. Successful sweetpotato root-knot nematode
resistant breeding programs involve the determination of resistance genes. Nematode resis-
tance is governed by genotype [45] and is primarily quantitative [46]; therefore, the identica-
tion of genetic markers associated with root-knot nematode resistance requires broad scale
molecular studies.
4.6. Root-knot nematodes
In a recent survey, the top 10 most important genera of parasitic nematodes in molecular plant
pathology were ranked based on scientic and economic importance [47]. Ranked at the top
of the list are root-knot nematodes (Meloidogyne spp.). The root-knot nematode (Meloidogyne
spp.) comprises over 100 species, with Meloidogyne javanica, Meloidogyne arenaria, Meloidogyne
hapla, and Meloidogyne incognita representing the most devastating threat to agricultural crop
production [48]. The Meloidogyne spp. are globally distributed, have enormous host range and
develop dynamic disease complexes with fungal species and bacteria which may exacerbate
disease incidences in cultivated plants. The lifecycle of Meloidogyne spp. involves four develop-
mental stages including larval stage 1 (within the egg), larval stage 2 (migratory), larval stage
juvenile 3 (sedentary), larval stage 4 (sedentary) and adult stage (sedentary). Under favorable
environmental conditions, rst stage moulting to J1 larval stage within the egg occurs result-
ing in hatching, with or without the presence of a chemical stimulus. Infective second-stage
juveniles (J2s) are often aracted to root exudates and migrate to root tips where they inl-
trate behind the root cap at the elongation zone. Root knot nematodes aenuate plant cells
by stylet thrusting and secrete cell wall degrading enzymes to separate the middle lamella
during intercellular migration through root cortex cells as they target the undierentiated
procambium cells of the vascular cylinder. During later stages in primary infection, dorsal
gland activity increases to promote shuling of secretory granules to the stylet where pro-
teinaceous secretions are released in the development of the primary feeding site—the giant
cell [49]. The multi-nucleated giant cell is a result of nematode-induced endoreduplication
within the host cell in the absence of cytokinesis. Cellular ingrowths arise to sequester solutes
from the xylem [50] further enhancing nutrient availability. J2 larvae moult into larval stage
3 (J3) during the initial intake of plant nutrients from giant cells. Additional moulting occurs
Nematology - Concepts, Diagnosis and Control126
resulting into the J4 and nal adult stage. Further reproductive development in females results
in the characteristic “apple” shape associated with the Greek nomenclature Meloidogyne. The
lifecycle completes when eggs are released into the soil from the gelatinous egg matrix formed
on epidermal root tissue. Root-knot nematode infection is typically characterized by stunted
growth, wilting, root galling and abnormalities in root formation.
4.7. Cyst nematodes
Cyst forming nematodes, or cyst nematodes, (Heterodera and Globodera spp.) rank second to
root-knot nematode in agricultural and economic importance. The biology of cyst nematodes
is similar to that of root-knot nematodes where J2 larvae infect the host and develop to adult
stages within host tissue. In contrast, to root-knot nematode reproduction where eggs are
deposited into a gelatinous matrix on root systems, eggs produced by cyst nematodes are
preserved within the body of the female and are protected after her death until hatching under
favorable conditions. Cyst nematodes enter root tips and induce specialized feeding structures
in the infected plant roots called syncytia via esophageal gland secretions released by the sty-
let [51]. These secretions promote cell wall degradation and protoplast fusion of numerous
adjacent cells to form the syncytium [52]. In agriculture, the most signicant cyst nematode
species are the potato cyst nematodes Globodera rostochiensis and G. pallida, the soybean cyst
nematode (Heterodera glycines) and cereal cyst nematodes (CCNs) (including Heterodera avenae
and H. lipjevi. In the U.S., losses due to H. glycines is estimated at 1.286 billion [53]. Globodera
pallida originated in South America and is now widely distributed in 55 countries. Yield losses
of potato due to G. pallida range from 50 to 80% in heavily infested soils [54]. Although the beet
cyst nematode, Heterodera schachtii, is a primary pathogen of sugar beets, it can parasitize plant
species in 23 dierent plant families with losses of 30% in the families of Chenopodiaceae [55, 56].
4.8. Lesion nematodes
Ranked third among the most damaging nematodes in agriculture [57], approximately 70 spe-
cies of root-lesion nematodes (Pratylenchus spp.) are distributed worldwide with a host range
of nearly 400 plant species [57]. Among Pratylenchus spp., P. thornei is associated with yield
reductions in wheat by as much as 85% in Australia, 70% in Israel, 50% in Oregon and 37% in
Mexico [58]. Lesion nematodes are migratory, feeding mainly in the root cortex and may
enter vascular tissues obtaining nutrients. Infection typically results in lesion formation and
necrosis on roots with aboveground symptoms of chlorosis as well as reductions in leaf num-
ber and size [58, 59]. Host tissue injury resulting from infection may represent areas for sec-
ondary infection from other pathogens. Recently two new species of root-lesion nematodes
(Pratylenchus. kumamotoensis, Pratylenchus. pseudocoeae) were identied in Korea by morpho-
metric and molecular analyses of internal transcribed spacer (ITS) and ribosomal DNA [60].
4.9. Burrowing nematode
The burrowing nematode, Radopholus similis [(Cobb, 1893) Thorne, 1949] is a migratory plant
parasitic nematode, listed as a quarantine plant pest worldwide [61]. Over 250 plant species
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
serve as hosts for R. similis where it causes severe economic losses in yields. R. similis damages
banana, citrus, pepper, coee and other agronomic and horticultural crops and is considered
the most important phytopathogenic nematode in banana-growing areas [62]. Eective con-
trol of R. similis remains problematic worldwide, and eective approaches must be identi-
ed and implemented. Radopholus Calreticulin (CRT) is a Ca2+-binding protein that plays key
roles in parasitism and represents a candidate target for controlling R. similis. R. similis CRT
(Rs-CST) is expressed in the esophageal, reproductive and gastrointestinal regions as well as
the eggs. Using plant-mediated RNA interference, Rs-CRT expression was signicantly inhib-
ited in the nematodes, and enhanced resistance was demonstrated in transgenic tomato plants
[63]. In a bioassay-based study, phenylphenalenones extracted from Musa spp. showed anti-
nematode eects on R. similis which was demonstrated by nematode motility inhibition [64].
5. Nematode parasitism genes
Nematode parasitism is conferred by the actions of a variety of genes that are upregulated
during host infection. In an earlier review, a comprehensive discussion highlighted the struc-
ture, origin and functions of nematode parasitism genes and further supported the acquisi-
tion of parasitism genes through horizontal transfer from bacteria [49]. Since parasitism genes
are usually required for infection, they represent important targets for the development of
control measures. Parasitism genes often encode for eectors which are proteins or chemi-
cals that elicit an immune response and/or trigger changes in the host cell architecture [51].
Recently two eector genes (MhTTL2 and Mh265) were identied in the root-knot nematode
M. hapla and were shown to be upregulated during primary infection [65]. MhTTL2 encodes
for a secreted protein bearing a transthyretin-like protein domain and is expressed in the
amphids, with a potential role in the nervous system while Mh265 is expressed in subventral
glands. Nematode eectors including expansin, β-1,4-endoglucanase and polygalacturonase
are released during primary infection and feeding site development. In plants, expansin pro-
teins are secreted during growth processes to allow for cell enlargement [66]. Nematodes
are believed to cause dierential expressions of plant genes encoding cell wall modifying
proteins including expansins [67] quite possibly to mimic endogenous expansin production
during feeding site development. HaEXPB2, a predicted expansin-like protein found in cereal
cyst nematode Heterodera avenae was associated with cell death in tobacco plants [68]. During
primary infection of tobacco, HaEXPB2 gene expression was localized in subventral glands
of J2 nematodes and was later found in the cell wall. Silencing of HaEXPB2 by RNA interfer-
ence was associated with reduced nematode infectivity. Transcriptome sequencing analyses
of early stage H. avenae juveniles has revealed a variety of potential eectors including plant
cell wall-modifying proteins and homologues of secreted proteins involved in the detoxi-
cation of reactive oxygen species (ROS) including: peroxiredoxin, glutathione peroxidase,
glutathione-S-transferase [69]. ROS release is associated with onset of plant defense signal-
ing. New evidence suggests that root-knot nematodes may utilize plant peroxidase to reduce
ROS levels and parasitize plants bearing the Mi-1 root-knot nematode resistance gene [70].
In plants, pathogens may trigger a hypersensitive response which involves programmed
Nematology - Concepts, Diagnosis and Control128
cell death (a form of apoptosis) in the site of infection to prevent pathogen colonization.
Apoptosis regulator BAX (BCL-2 protein 4) is a member of the Bcl-2 family of proteins found
in plants and animals [71]. Two secretory eector candidate genes (No. 5, No. 100) identied
by transcriptome proling in Meloidogyne enterolobii suppressed BAX-induced programmed
cell death suggesting their roles as plant immune modulators for nematode infection [72].
The SPRY (SPla and the RYanodine Receptor) protein domain is most likely a scaold for
mediating protein-protein interactions [73]. SPRY eectors from Globedera spp. was shown to
suppress the plant defense responses [74].
6. Molecular basis of nematode resistance
The development of a resistance response may encompass a variety of physiological out-
comes including: minor or complete absence of galling, dierences in the degree of necrosis,
the inability of the nematode to establish a permanent feeding site, and a decrease in female
fecundity or egg output. To date, the majority of plant-parasitic nematode resistance genes
bear the characteristic NBS-LRR (Nucleotide binding site—Leucine Rich Repeat) domains.
These include the Mi-1 gene from Solanum peruvianum (formerly Lycopersicon peruvianum)
[75], Hs1pro-1 from sugar beet [76] and Gpa2 and Gro1-4 from potato [77, 78].
Resistance to Meloidogyne in commercial resistant tomato cultivars (Lycopersicon esculentum)
was originally identied in its wild relative L. peruvianum Mill. [79] followed by introgres-
sion of resistance into commercial breeding lines through backcrossing [80]. Several root-
knot resistance gene homologues have been identied in tomato. Mi-1.2 (referred to as
Mi-1) confers resistance to multiple species of root-knot nematodes, [75] the potato aphid,
Macrosiphum euphoribiae [81] and the whitey, Bemisia tabaci [82]. Rme1 is considered a poten-
tial component of the Mi-1-mediated signaling pathway as studies have indicated tomato
Rme1 mutants lack resistance to nematodes and whiteies [66]. Molecular changes in Rme1
protein conformation due to the presence of pathogens, may be recognized by Mi-1.1 which
signals the hypersensitive response in the “guard hypothesis” [83]. In carrots, inherited dom-
inance of two root-knot nematode resistance genes Mj1 [84] and Mj2 [85] conferred resistance
to M. javanica. The RMIa gene located in a subtelomeric position 300 kb physical distance
between AMPP117 and AMPP116 markers and is associated with M. incognita resistance in
peach (Prunus spp.) [86]. The Myrobalam plum (Prunus cerasifera) harbors dominant alleles
(Ma1, Ma2, and Ma3) of a single gene Ma, a TIR-NBS-LRR class resistance gene, which confers
broad spectrum resistance to multiple Meloidogyne spp. [87]. Using polymorphic sequencing
analyses and genetic linkage mapping (RFLP, SSR) the Ma loci was precisely identied in the
Myrobalan plum linkage group 7, while in a Japanese plum variety, a Rjap gene was localized
at the same position in co-segregation with SSR markers previously associated with root-
knot nematode resistance [88]. In sweetpotato, 275 candidate resistance gene analogs have
been identied by degenerate PCR and molecular mining [89]. Plant-parasitic nematodes
have been shown to manipulate host gene expression, therefore the identication of dieren-
tial expression paerns of transcript levels for defense-related genes is a critical component
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
in the determination of molecular factors of root-knot nematode resistance. Traditional iden-
tication of root-knot nematode resistance has involved the use of bulk segregant analysis
[90] to map out qualitative traits between pooled plant genomes. Bulk segregant analysis has
been used in tandem with random amplied polymorphic DNA assays to identify molecular
markers at specic loci associated with root knot resistance in sweetpotato where genotypes
are often isogenic [91]. Polymorphic events in resistance genes that confer eector recogni-
tion has been demonstrated in Arabidopsis resulting in a bifurcation that distinguishes resis-
tant and susceptible allele clades [92].
Genome-wide expression proling analyses using next-generation sequencing technologies
are often employed in the analysis of host-nematode interactions. The resultant data from
global transcriptome assays are used to target genetic traits associated with plant immune
responses in response to various pathogens and to distinguish plant genotypes for resistance
or susceptibility to certain diseases. Our general understanding of discreet molecular events
involved in compatible (susceptible) and incompatible (resistant) plant-nematode interac-
tions is limited in comparison to other signicant host-pathogen associations. Recently, RNA-
Sequencing has been frequently used in plant pathological studies to prole gene expression
paerns in host plants and pathogens [93, 94]. Dierential genetic expression proles of many
specic genes involved in plant immune responses has been shown in resistant and suscep-
tible plants challenged by root-knot nematodes [48, 95]. The identication of novel defense-
related transcripts and the elucidation of pathways involved in plant immune responses
to nematodes have been recorded for important economic crops including coon [96], rice
[97], and soybean [98]. Transcriptome proling of resistant and susceptible tobacco varieties
infected with root-knot nematodes has shown dierential expression paerns among genes
involved in cell wall modication, auxin production and oxidative stress [99].
6.1. Plant immune responses
Due to their immobile lifestyle, plants have developed sophisticated molecular strategies
to prevent pathogen invasion [100]. Plant defense has been characterized as a two- prong
approach. In incompatible (resistant) plant-pathogen interactions, the presence of microbial/
pathogen/-associated molecular paerns (M/PAMPs) including: toxins, glycoproteins, carbo-
hydrates, fay acids and proteins can trigger the upregulation of a network of host genes and
corresponding proteins involved in an innate response termed pathogen-triggered immu-
nity (PTI). Plant pathogens have evolved specialized eector molecules to suppress this rst
line of defense leading to eector-trigged susceptibility (ETS). In turn, plants have developed
resistance genes which recognize specic eectors triggering a more robust defense response
characterized as eector-triggered immunity (ETI). A hallmark of ETI is a hypersensitive cell
death response (HR) at the infection site which prevents pathogen colonization [101].
6.2. Reactive oxygen species and antioxidant production
During plant metabolic processes, the accumulation of reactive oxygen species (ROS) by-
products including superoxide anion (O2
), hydrogen peroxide (H2O2), singlet oxygen (1O2)
Nematology - Concepts, Diagnosis and Control130
and hydroxyl radicals (OH) is often continuous, as these highly reactive molecules are local-
ized to various cellular compartments. ROS are primarily generated by NADPH oxidases and
superoxide dismutases and production is associated with numerous abiotic and biotic stress
responses. Activation of ROS was shown to be critical during the defense response to root-
knot nematode invasion [102]. ROS accumulation is toxic to nematodes and can often lead to
induced oxidative destruction of infected cells during the hypersensitive response, to prohibit
pathogen colonization. Increased ROS production is often correlated with the activation of
antioxidant gene expression. These oxidative/reduction reactions must be tightly regulated to
eliminate inadvertent plant tissue damage. Antioxidant enzymes including peroxidases are
primarily responsible for the maintenance of a steady-state ROS level however, certain classes
of peroxidases act as producers of ROS depending on the cyclic (catalytic or the hydroxylic)
nature of the enzyme. ROS- producing Class III peroxidase genes were upregulated during
an incompatible reaction in H. avenae-resistant wheat cultivars [103]. Peroxidase reduces H2O2
levels via H2O2-dependent polymerization of hydroxycinnamyl alcohols which promotes
defense responses including lignin synthesis and cell-wall reinforcement by the cross-linkage
of cell wall proteins [104]. Higher induction of peroxidase groups was observed in resistant
plant species during H. avenae and M. incognita infection [105].
6.3. Pathogenesis-related proteins
Presently, 17 families of pathogenesis-related (PR) proteins have been identied based pri-
marily on their enzyme function, activity and amino acid sequence homologies [106]. The PR
family are characterized as plant allergens inclusive of an assortment of proteins such as: b-1,3
glucanases, chitinases, proteinase inhibitors, defensins, ribonucleases and thionins. PR gene
expression is often induced by ethylene, salicylic acid, jasmonic acid, xylanase, and systemin
signaling pathways. The molecular functions of PR proteins are often species specic with
great diversity in the mode of action and structure between protein groups. Most PRs pos-
sess antifungal, antiviral, antibacterial and insecticidal activity and are primarily involved in
plant developmental processes and environmental stress responses. PR proteins were initially
reported in tobacco leaves during a hypersensitive response to the tobacco mosaic virus (TMV)
[107, 108] and have been induced in response a wide variety of pathogens including nema-
todes. During nematode infections, PR transcripts may accumulate in high concentrations and
are associated with the long distance immune response termed systemic acquired resistance
(SAR) [109]. Increased expression of PR-1(P4) transcripts was observed at 3 days' post-infection
in the G. rostochiensis-infected resistant plants compared with the uninoculated controls [110].
6.4. Callose deposition
Cell wall modications often occur during plant-pathogen interactions which are demon-
strated by the deposition of cell wall appositions leading to the development of papillae.
Structural components associated with papillae formation are: callose, phenolics including lig-
nin, phenolic conjugates such as phenolic–polyamines, reactive oxygen species, peroxidases,
cell wall structural proteins (arabinogalactan proteins and hydroxyproline-rich glycopro-
teins) and cell wall polymers (pectin and xyloglucans). Callose (beta-1-3-glucan) deposition,
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
lignication and suberization are plant developmental processes further associated with the
restriction of systemic pathogen movement during PTI. Defense-associated cell wall strength-
ening through lignin and callose synthesis is signaled by cell wall degradation in a feedback
mechanism which occurs in response to pathogens [111]. In addition to promoting declines
in localized microbial populations, callose deposition also prevents the translocation of PTI-
suppressive eectors. Interestingly, the cuticular chitin derivatives of plant-parasitic nema-
todes may activate the innate immune response. Although the cuticle is generally believed
to be devoid of chitin, it is possible that chitin derivatives or chitin previously deposited in
the stylet are recognized by the host which activates callose deposition at the site of penetra-
tion. The overexpression of the ethylene response transcription factor RAP2.6 in Arabidopsis
enhanced plant basal resistance to H. schachtii [112]. Increased expression of jasmonic acid-
related genes and callose deposition were observed at nematode infection sites.
7. WRKY transcription factors
WRKY transcription factors are transcriptional regulators of many developmental processes
in plants and are associated with abiotic and biotic stress responses. The WRKY domain is
almost exclusive to plants characterized by a highly-conserved core WRKYGQK motif and a
zinc nger region. The critical role of WRKY transcription factors (WRKY TFs) in plant defense
responses has been well documented [113, 114]. Their ability to bind to pathogen responsive
cis acting W-box promoter elements in PR1 genes is indicative of their role in plant immunity
[113]. Arabidopsis WRKY72 was reported to have a signicant contribution to Mi-1-mediated
defense against RKNs, potato aphids [114] and oomycete pathogen Hyaloperonospora arabidop-
sidis the causal agent of downy mildew [115]. WRKY gene expression is altered during plant-
parasitic nematode interactions. The development of cyst nematode H. schachtii feeding site
(syncytia) involves the up-regulation of WRKY23 [116]. Conversely, endogenous WRKY33
gene expression levels were strongly downregulated in syncytia formed in Arabidopsis roots,
while plants overexpressing WRKY33 showed a 20–30% reduction in the presence of female
nematodes [117] a possible indication of its role in plant defense.
7.1. Calreticulin proteins
In animals, endoplasmic reticulum (ER) localized calreticulin proteins are integral compo-
nents in calcium homeostasis as well as protein folding and are involved in other signi-
cant cellular functions [118]. Ubiquitously expressed in plants, calreticulin performs similar
functions to its animal counterpart despite 50% dierences in amino acid sequence homol-
ogy. Plant calreticulin is described as a molecular calcium-binding chaperone that promotes
protein folding, calcium signaling and homeostasis, and oligomeric assembly in a calreticu-
lin/calnexin cycle. Calreticulin may interact with a majority of monoglucosylated glycopro-
teins synthesized in the ER, while certain isoforms have been associated with the expression
and quality control of the elongation factor Tu receptor-like protein kinase (EFR) [119] an
important event in M/PAMP-triggered immune responses. The signicance of calreticulin
Nematology - Concepts, Diagnosis and Control132
isoform-3 (AtCRT-3) function through gene deletion was identied in Arabidopsis plants [120].
Plant transformants with repressed AtCRT-3 gene activity were impaired in perception of M/
PAMP-associated e-18 and decient in EFR protein expression and anthocyanin content.
Furthermore, they concluded that AtCRT-3 may be involved in the unfolding and activation
of EFR based on its primary molecular function and recognition of EFR N-glycosyl binding
sites. Recently, studies have shown that root-knot nematodes secrete calreticulin, which plays
an important role in infection [121].
7.2. Plant proteinase inhibitors
Plants utilize an arsenal of defensive mechanisms to evade infection from nematodes. One
important strategy involves limiting nematode feeding capabilities. Plant proteinase inhibitors
are involved in many physiological processes including protein turnover and proteolysis dur-
ing metabolism however; other evidence has supported an alternative role in defense against
plant pathogens [122]. Plant proteinase inhibitors degrade nematode proteases preventing
the breakdown of food material which reduces nutrient absorption in the nematode. As early
as 1947, the idea of proteinaceous protease inhibitors was formulated as Mickel and Standish
observed dierences in larval development on soybean cultivars [123]. The applicability of
proteinase-inhibitors in nematode resistance was initially demonstrated in transgenic potato
expressing a serine proteinase-inhibitor cowpea trypsin inhibitor (CpTI) [124]. CpTI expres-
sion directly inuenced the sexual fate of G. pallida toward a higher ratio of smaller males with
reduced damage observed on roots. Out of the four major classes of plant proteinases inhibi-
tors (cysteine, serine, aspartic, metallo-proteinases) cysteine and serine proteinase inhibitors
have gained considerable interest as eective defense molecules nematodes due to their speci-
city in the degradation of the major digestive enzymes (proteases) in plant-parasitic nema-
todes [125].The eectiveness of proteinase inhibitors can be aributed to its small size, which
benets its inclusion with nutrient molecules absorbed by some plant-parasitic nematodes. In
tomato, overexpression of phytocystatin gene, CeCPI isolated from taro (Colocasia esculenta)
showed enhanced resistance to root-knot nematodes demonstrated by reduced galling and
an inuence on sex determination [126]. In sweetpotato, sporamin which is classied as a
Kuni-type trypsin inhibitor, accounts for 60–80% of total soluble protein. Sporamin is consti-
tutively expressed in the tuberous root in comparison to in the stem or leaves and is expressed
systemically in response to wounding and other abiotic stresses [127]. In previous studies,
three forms of sweetpotato sporamin showed strong trypsin inhibitory activity invitro [128].
Additional research has resulted in the identication of sporamin-mediated resistance to cyst
nematodes [129]. Decreased nematode development correlated with trypsin inhibitor activity
of sporamin which was the critical factor for inhibition of growth and development of cyst
nematodes on sugar beet roots. Plant genotypes that produce high sporamin levels may have
a selective advantage in defense to plant-parasitic nematodes.
7.3. Plant hormones
The roles of plant developmental hormones, ethylene, jasmonic acid and salicylic acid have
been well established during plant immunity [130, 131]. Jasmonic acid (JA) and ethylene (ET)
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
signaling pathways work synergistically while the salicylic acid (SA) pathway is antagonistic
to JA/ET pathways [132]. In a prior study, exogenous ethyhlene (ethephon) and jasmonic
acid (methyl jasmonate) application triggered the induction of PR proteins and the activa-
tion of systemic defense against root-knot nematodes on rice [133] These ndings suggest a
critical role of an active intact jasmonic acid pathway during the activation of systemically
induced resistance. The combination of exogenous jasmonic acid and biogenic elicitor arachi-
donic acid, decreased galling on tomato roots two-fold in comparison to controls [134]. The
role of salicylic acid has been well documented in the ecacy of host resistance to root-knot
nematodes. Pathogenesis-related protein expression was associated with salicylic acid-depen-
dent systemic required resistance in tomatoes pretreated with salicylic acid under root-knot
nematode challenge [109]. Expression of a NahG which encodes for an enzyme that degrades
salicylic acid to catechol, reduced Mi-1 gene- mediated root-knot nematode resistance in
transgenic tomatoes [135].
8. Disease management of plant-parasitic nematodes
8.1. Cultural control
For many years, crop rotation and cover cropping are often utilized in integrated pest manage-
ment protocols to reduce plant-parasitic nematode incidence and replenish soil nutrient levels.
Soil nematode levels have been eectively decreased by rotational cultivation of non-host cul-
tivars however, the wide host range of Meloidogyne spp. often diminishes the eectiveness of
crop rotation [136]. Planting corn as a rotational crop has been shown to reduce northern root-
knot nematode (M. hapla) incidence however; population densities of other Meloidogyne spp.
may increase with persistent cultivation. Plant species with resistance to mixed Meloidogyne
populations have been identied. Leguminous cover crops Mucuna pruriens L., and Crotalaria
spectabilis showed multiple resistance to three species of root-knot nematodes (Meloidogyne
arenaria, M. incognita, M. javanica) [137]. In certain cases, the very nature of crop production
may suppress the magnitude of infection. Rice is cultivated under ooding conditions which
does not favor the nematode lifestyle. In Taiwan, crop rotations with rice or taro combined
with cultural control methods including ooding and bare fallowing was shown to decrease
nematode soil populations and increase strawberry yields [138].
8.2. Plant extracts
Plant extracts often contain a myriad of compounds which demonstrate nematode suppressive
properties. Ethanolic extracts of Azadirachta indica (neem), Withania somnifera (ashwagandha),
Tagetes erecta (marigold) and Eucalyptus citriodora (eucalyptus) were reported to show nema-
ticidial activity against Meloidogyne incognita, Helicotylenchus multicinctus and Hoplolaimus
which was comparable to chemical nematicide controls [139]. In other reports, increased plant
growth and development were shown in plants propagated with the addition of a variety of
extracts. Root-knot nematode egg hatch and larval development was dramatically reduced
by leaf extracts from Hunteria umbellata and Mallotus oppositifolius which coincided with
Nematology - Concepts, Diagnosis and Control134
increased growth of cashew seedlings [140]. Plant height, fruit production and weights of M.
incognita-infected tomato were signicantly increased by the addition of ethanol extracts from
Azadirachta indica leaves, Capsicum annuum fruits, Zingiber ocinale rhizomes and Parkia biglo-
bosa seeds in comparison to non-treated controls [141].
8.3. Biological control
With increasing demands in organic agriculture and concerns for environmental welfare,
the use of chemical pesticides has decreased. Alternative means of pest management such as
the use of biological controls are of great interest for crop producers. The ecacy of nema-
tophagous bacteria and fungi in the control some nematode pests, including cyst and root-
knot nematodes has been well-documented [142, 143]. Parasitic bacteria of Pasteuria spp. have
been reported to infect 323 nematode species including both plant-parasitic nematodes and
free-living nematodes [144]. Three methods of application for P. penetrans were evaluated
for nematode control including seed, transplant, and post-plant treatments [145]. In green-
house studies involving cucumber, all three Pasteuria treatments were shown to reduce gall-
ing caused by M. incognita as well as soil nematode numbers and nematode reproduction.
In other reports, M. incognita suppression was observed in eld soil treated with P. penetrans
in comparison to untreated soil [146]. Other genera of bacteria including Bacillus spp. have
shown great promise in nematode management. B. cereus strain S2 treatment resulted in a
mortality of 90.96% to M. incognita [147]. B. rmus YBf-10 exhibited nematicidal activity against
M. incognita, which was clearly demonstrated by an inhibition of egg hatch and motility [148].
Nematophagous fungi Pochonia chlamydosporia has potential as a biological control agent for
M. incognita in vegetable crops. Along with crop rotational methods, P. chlamydosporia was
shown to reduce nematode levels in soil previously used for root-knot nematode susceptible
tomato [149]. Nematophagous fungal products including chitinases show great potential for
the development of biopesticides. Certain root-knot nematode species have transparent pro-
tective chitin-containing shells. Puried chitinase LPCHI1 from Lecanicillium psalliotae was
shown to degrade M. incognita eggs [150].
8.4. Host resistance
Chemical nematicides are often used in the management of root-knot nematodes however;
EPA restrictions in some soil fumigants due to increased environmental toxicity coupled
with the expensive costs associated new nematicide development limit their availability. The
very nature of these mammalian pesticides poses a signicant risk to humans. Plant-parasitic
nematodes often reside in plant tissue which makes soil delivery applications of the chemical
challenging. The incorporation of plant varieties that harbor multiple resistance to an array
of plant pathogens is an aractive and practical approach for plant breeders. However, the
conserved use of specic genotypes of disease resistant cultivars may contribute to increased
pathogen aggressiveness resulting in epiphytotic conditions; therefore the identication
of additional resistant varieties becomes increasingly necessary for long term control. For
many years crops have been articially selected for their inherent disease-resistant proper-
ties through phenotypic screenings and genetic analyses. Nematode-resistant genes found
The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
in gene pools of a variety of plant species have been introgressed into the genomes of eco-
nomically important crops with natural susceptibility through transgenic technologies such
as agrobacterium-mediated transformation [151, 152].
Plants synthesize and release an array of volatile organic compounds in response to damage.
Plant terpenes/terpenoids are secondary metabolites produced by terpene synthases in plants
and are involved plant survival and biotic and abiotic stress responses. Functional character-
ization of one member of the soybean TPS gene family, designated GmAFS suggested an anti-
nematode role [153]. Transgenic hairy roots overexpressing GmAFS were generated in an H.
avenae-susceptible soybean line. Plants showed signicantly higher resistance to H. avenae burden
than controls.
RNA interference (RNAi) is a method of gene silencing observed in a wide range of organ-
isms. This method of gene silencing has become a useful tool for biologists to study biological
processes and has been developed into a novel control strategy for engineering plants with
nematode resistance. First identied in plants [154] the mechanism of action was elucidated
in the nematode model organism C. elegans [155]. RNAi involves the suppression of specic
transcripts to minimum expression levels as a method of post-transcriptional gene silencing
during developmental processes and is believed to be a response to double-stranded viral
entry. RNAi is premised on the cell’s ability to recognize and degrade double-stranded RNA
(dsRNA). The dsRNA is processed into small interfering RNA (siRNA) by the enzyme Dicer,
a ribosome III-like enzyme. Double-stranded siRNA is unwound into two single-stranded
RNAs and one strand serves as a guide which associates with the RNA-induced silencing
complex (RISC). This complex associate with the specic complementary mRNA expressed
in the cell where the RNAse H enzyme Argonaute degrades the mRNA resulting in gene
silencing. Since the discovery of RNA-interference, researchers have developed transgenic
constructs that specically target genes for functional characterizations. More recently, plants
have been engineered to expresses double-stranded RNA that silence important genes in
plant-parasitic nematodes [156, 157]. As nematodes feed on the plant cytoplasm, the uptake
of the siRNA triggers the endogenous RNAi mechanism within the nematode, silencing the
target gene involved in infection [158]. The RNAi approach was applied, using sequence
fragments from M. incognita genes that encode for two heat-shock protein 90 (HSP90) and
isocitrate lyase (ICL). Heterologous expression of RNAi constructs in tobacco plants corre-
lated to a signicant level of resistance against M. incognita. Delayed galling and decreased
egg production was observed in plants expressing HSP90 dsRNA. The 16D10 eector gene
encodes for a secretory peptide synthesized in the subventral esophageal glands of root-knot
nematodes which plays an important role in giant cell formation cells [156]. In planta expres-
sion of 16D10 dsRNA in Arabidopsis conferred in resistance eective against the four major
root-knot nematode species [156]. In transgenic lines of potato expressing a 16D10 RNAi
construct (Mc16D10L), the number of M. chitwoodi egg masses and eggs was signicantly
decreased in comparison to empty vector controls [159]. Mc16D10L expression was reduced
in eggs and juveniles developed on transgenic potato which suggest a stable heritability of
the construct. Decreased egg production was also observed in transgenic grape lines express-
ing 16D10L [160].
Nematology - Concepts, Diagnosis and Control136
The use of site-specic DNA endonucleases including Zinc nger nucleases (ZFNs), [161]
transcription activator-like eector nucleases (TALENs) [162] and now clustered regularly
interspaced short palindromic repeats (CRISPR)/Cas9 [163] have equipped researchers
with the ability to specically inactivate genes and target genetic regions for homologous
recombination of input DNA. In general, double-stranded breaks introduced by nucleases
activates DNA repair mechanisms which generate mutations in the target sequence con-
ferring a loss of expression i.e., gene editing. Homologous recombination of exogenously
supplied sequences can result in genetic modications (knock-ins). CRISPR technology has
important advantages over TALENS and ZFNs including; ease of use [164] target site selec-
tion [165] and overall eciency, although o-target eects remains an important issue of
concern [166]. CRISPR/Cas9 system may be used to alter the expression of resistance genes
for constitutive expression against plant-parasitic nematodes. For example, point muta-
tions in the snc1 (suppressor of npr1-1, constitutive 1) locus in Arabidopsis plants resulted
in constitutive expression of pathogenesis-related proteins and enhanced disease resistance
against two plant pathogens [167]. The mutation was mapped to a single nucleotide change
in 120-kb region on chromosome 4 which contains a cluster of resistance genes. In a recent
sweetpotato study, putative disease resistance gene DRL23 showed elevated expression
in resistant sweetpotato genotypes when compared to susceptible plants at days 14 and
46 post-inoculation with Meloidogyne incognita inoculum [168]. To identify any polymor-
phisms in amino sequences between DRL23 from resistant and susceptible cultivars, protein
alignments using the NCBI BLAST (Basic Local Alignment Search Tool) was performed.
Interestingly, variations in amino acid sequences occurred between resistant (positions 187–
231) and susceptible (positions 57–102) which corresponded to the NBS domain. Mutations
in the NB-ARC domain often abolish R-protein function, indicative of the functional rel-
evance of this domain [169]. Precise targeting by CRISPR may be useful in restoring gene
function by sequence replacement in defense-related genes thereby enhancing resistance to
nematode infection.
The authors would like to acknowledge the IBREED program under USDA-NIFA Grant
#2014-38821-22448 and the Tuskegee University George Washington Carver Agricultural
Experiment Station.
Author details
Gregory C. Bernard*, Marceline Egnin and Conrad Bonsi
Address all correspondence to:
Tuskegee University, Tuskegee, Alabama, United States
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The Impact of Plant-Parasitic Nematodes on Agriculture and Methods of Control
... In general, farmers cultivate important cereal crops like rice, wheat, maize, oats, barley, sorghum, millet, etc. in most parts of the world, yet more or less than $80 billion has been predicted to be lost each year owing to PPNs globally. The impacts of nematodes are huge on the food chain in the tropical and subtropical ecology (Bernard et al. 2017;Sikora et al. 2018a). Here are a few effects of nematodes on rice, wheat, and maize, and the biomanagement of ectoparasitic nematodes affecting cereals is discussed below. ...
... In addition, cover crops can control PPNs density as a component of IPM. Bernard et al. (2017) demonstrated cover crops namely Crotalaria spectabilis and Mucuna pruriens being resistant to various species of Meloidogyne. Additionally, Xiphinema and Trichodorus abundance in maize-cover crop intercrop were regulated by use of cover crops and tillage systems (Jibrin et al. 2014). ...
Ectoparasitic nematode damage to agricultural crops has received little attention from researchers due to difficulty in estimating individual nematode impacts. This is because the degree of damage depends on the nematode pathotype, crop species, nematode population densities, nematode management practices, soil attributes, and climatic conditions. Furthermore, damage symptoms and effects are sometimes mistaken for those caused by drought, nutrient deficiencies, and other factors, and are not necessarily immediately associated with the nematodes. Limited investigations conducted so far have revealed damage to important crops such as maize, soybean, cowpea, sugarcane, rice, sugarcane, grapevine, sugar beet, potato, yam, strawberry, bermudagrass, woody vines, and vegetables, with Xiphinema, Trichodorus, Paratrichodorus, Helicotylenchus, Tylenchorhynchus, and Belonolaimus being the most economically important ectoparasitic nematode genera. Generally, impacts on crops may also be challenging to predict or grossly understated as plant-parasitic nematodes (PPNs) may damage plants in several ways. These include direct feeding action characterized by root galls, root stunting, or direct injury. In specific, ectoparasitic nematodes primarily injure plants by interacting with other soil pests namely fungi, bacteria, and other PPNs developing disease complexes through synergistic relations. Notably, Longidorus spp., Xiphinema spp., Paratrichodorus spp., Paralongidorus spp., and Trichodorus spp. can transmit some significant plant viruses. This chapter thus aims to highlight the threat posed by ectoparasitic nematodes to the agricultural crops including legumes/pulses, cereals and tubers as well as their potential management strategies.
... Others are parasitic on plant parts above the soil surface, such as stems, leaves, buds, flowers, and seeds. infection site depends on the type of nematode and the plant host, and even on the size of the nematode (Bernard et al., 2017). ...
... 2. Many of the losses attributed to infection with other pathogens may, in fact, be due to previous infection with nematodes, which leads to weakening the plant and preparing it for infection with other diseases, or it may be the main and effective participant in these losses, and this thus leads to difficulty in obtaining real changes (Bernard et al., 2017). As for the indirect losses, they are numerous and varied. ...
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Plant pathogenic nematode science is a relatively recent science that is related to many applied and research sciences. It is closely related to zoology and botany, which are the origin of all biological sciences. The study of plant-pathogenic nematodes requires a great understanding and knowledge of general zoology, invertebrate zoology, parasitology, and animal behavior science, which helps understand the nutritional behavior of nematodes on their plant hosts and thus the effects of different control methods on nematodes, as well as being familiar with botany and its various branches, especially the functions of organs, appearance, and internal anatomy, especially of the root system, and these are requirements for understanding the different and mutual influences between nematodes and plants.
... Plant parasitic nematodes found in association with plants pose a major threat to the agriculture sector and are responsible for approximately $80-$118 billion dollars loss globally [1]. They are obligate parasites of plants which derive their nutrition from them by using their specialized structure viz., stylet. ...
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Plant parasitic nematodes are major pests of the agricultural industry in developing countries. This group is associated with different parts viz., flower, leaves, buds, roots, trunk etc., of approximately all crucial crops of agronomy due to their omnipresent nature. They are categorized as endo, ecto and semi-endoparasite based on the feeding habits. PPNs possess remarkable characteristics especially, parasitic adaptations which help in combating adverse conditions. Furthermore, they interact with other microorganisms (pathogens) forming complex diseases in crops. For effective management of the PPNs through biological control, it is essential to understand their parasitic mechanism, adaptation of J2 stages, feeding mechanism, host-nematode relationship and identification of associated microbiota. This review focuses on the basic biology of PPN, feeding habits, parasitic potential, molecular insights for understanding host-nematode relationship and their management by exploiting the inherent abilities of biocontrol agents.
... Plant-parasitic nematodes are called plant-parasitic since supplements they get come straight forwardly from plants. They have a needle-like structure called a stylet that helps them to penetrate the plant cell wall and reach the juicy substance on which they nourish (Bernard et al., 2017). Correct identification of nematode species is fundamental for choosing the right strategies of control. ...
Plant-parasitic nematodes are a high-priced burden in agricultural crop manufacturing. Over 4100 species of plant-parasitic nematodes have been recognized. Together, they represent an envisioned $80–$118 billion dollars annually in damage to crops. Plant-parasitic nematodes are identified as one of the finest threats to vegetation globally. The most damaging plant-parasitic nematodes (PPNs) are taken into consideration to be the root knot nematodes (RKNs), Meloidogyne sp., which are accountable for losses in vegetable plants throughout the world and determine the common use of chemical pesticides. The major genera of phytoparasitic nematodes discovered to cause crop losses were Heterodera, Hoplolaimus, Meloidogyne, Pratylenchus, Rotylenchulus, and Xiphinema. In different reports, M. incognita suppression turned into observed in field soil treated with P. penetrans in contrast to untreated soil. Opportunity means of pest control consisting of the use of biological controls are great interest for crop producers.
... As the world soil temperature continues to increase due to climate change, it will likely alter the biology of PPN. While PPN belong to the oldest living organisms on earth 29,30 and they have been successful in co-evolving with the changing environment over the past millions of years 31 , it is not clear whether their ability to damage crops will remain the same or increase in the currently changing environment. Additionally, as the effect of climate change is not uniform across the globe, some regions may experience extreme weather such as heat waves which can have further consequences in nematode biology. ...
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Food security has become one of the greatest challenges of the millennium and it is predicted to be exacerbated by climate change due to the adverse effects of soil temperature on crop productivity. Although plant-parasitic nematodes are one of the most important limiting factors of agricultural production, the fate of soil temperature in their biology is not fully understood. Here we present the effects of soil temperature on survival, reproduction, virulence, and disease severity from the perspective of two nematode species Rotylenchulus reniformis and Meloidogyne floridensis. The two nematode species were purposefully selected to represent a significant threat to annual and perennial crops. We employed novel approaches of direct as well as indirect heat exposure to evaluate nematode biology. The direct heat exposure assay involved the exposure of nematodes to hot water in a heating block at 32, 33, and 34 °C for 7 h, and subsequent evaluation of their survival after 18 h. The indirect exposure assay employed a commercial heat mat to raise soil temperatures to 32, 33, and 34 °C for 7 h during the daytime, and subsequent evaluation of nematode reproduction, virulence, and/or disease severity over the period of 6 weeks after inoculation. When directly exposed to hot water at 34 °C, the survival of R. reniformis increased by 10% while the survival of M. floridensis decreased by 12% relative to that at 32 °C. Upon increasing soil temperatures from 32 to 34 °C, the reproduction of R. reniformis and M. floridensis decreased by 49% and 53%, respectively. A significant reduction in the reproduction of M. floridensis occurred when soil temperature was increased from 33 to 34 °C, however, the same condition did not significantly affect R. reniformis reproduction suggesting the latter species has a greater ability to adapt to increasing soil temperature. Additionally, the virulence of R. reniformis was greater at 33 and 34 °C relative to that at 30 °C indicating increased aggressiveness of the nematode at higher soil temperatures. The virulence of M. floridensis appeared to be decreased as evident from increased root biomass when soil temperature was increased from 32 to 34 °C, however, the greater root biomass may have resulted from increased root galling at the higher temperatures. Results of the current study suggest that while higher soil temperatures due to climate change may lead to reduced nematode reproduction, crop losses will likely increase due to increased nematode virulence. Through the current study, we report practical evidence of the quantitative impact of climate change on the biology of plant-parasitic nematodes. Further studies involving a wider range of temperature and exposure time are needed to better understand nematode biology under climate change. Plant-parasitic nematodes (PPN) are microscopic non-segmented pseudocoelomic worms that are cosmopolitan in distribution and feed on plants as obligatory pathogens. More than 4000 species of PPN have been described, and they are responsible for approximately $358 billion in crop losses worldwide every year 1. Among several species of PPN, the reniform nematode (Rotylenchulus reniformis) is one of the most economically important nematode species specifically in the US where approximately 168 thousand bales of cotton and 2 million bushels of soybean are lost to this nematode annually 2,3. The presence of as few as two R. reniformis in a cubic centimeter of soil early in the crop growing season is enough to elicit economic crop loss by the end of the crop growing season 4. Similarly, a new and emerging peach root-knot nematode (Meloidogyne floridensis) is becoming an increasing threat to tree crop industries in the US as management options available for other species of Meloi-dogyne are not effective against this nematode 5. Management of these nematodes will continue to be a challenge because of (i) the lack of host-plant resistance or preference of growers towards high-yielding cultivars with little OPEN
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Worldwide, scientists and farmers are struggling to increase productivity and agriculture sustainability to produce more food for people. Vegetable plants are of great importance for human and animal nutrition. The Meloidogyne species are one of the most widespread plant parasitic nematodes (PPNs), considered a serious global threat to vegetable crops and causing significant losses. Research scientists reported that using nematode-resistant plant cultivars is a much more significant and environmentally safe alternative than chemical nematicides. Little is known about the effectiveness of breeding for resistance methods to manage Meloidogyne populations. Resistant vegetable cultivars are available and have been well documented in their use against Meloidogyne species. In this chapter, we have discussed different breeding methods and enumerated some of plant cultivars found to be resistant to root-knot nematodes (RKNs) causing root gall disease. The specific breeding approaches for Meloidogyne species-vegetable crop resistance have been used to study the resistance mechanisms among the various varieties of vegetable crops.
Biotic stress refers to stress triggered by other living creatures like fungi, bacteria, viruses, parasitic organisms, nematodes, parasitic mites, insects, animals, noxious weeds, and farmed or natural plants wrecking an organism. Because of the enormous financial damages imposed on fruit and lucrative crops, biotic stresses are the primary focus of agricultural studies. Plants and their disease-causative agents evolved alongside one another over hundreds of millions of years of age. Such a coevolutionary dynamic has culminated in the development of a diverse variety of plant defenses toward their parasites, all of which serve to reduce the incidence and extent of assault. These defenses comprise both anatomical and physiological modifications, which can be exhibited persistently or, in numerous instances, only after being attacked. Microbe-associated or pathogen-associated molecular patterns (MAMPs/PAMPs) deemed to be ubiquitous across microbial groups are principally instrumental in inducing a defense outcome following biotic or abiotic duress. The plant’s core immune apparatus operates to identify and generate defenses against these patterns, but constantly shifting microorganisms articulate an assortment of effectors that are race or species-specific and help promote parasite infectiousness by dampening these adaptations. In response to this, plants express specialized receptors known as R proteins which sense pathogenic effectors and launch powerful defenses. Infectious agents can then modify or eliminate their recognized effectors to evade defense stimulation, at the risk of incurring an adaptation cost as a result of the depletion of their recognized effectors. Plant resistance may be activated by both eliciting agents and effectors, which are referred to as PAMP-triggered and effector-triggered immunity (PTI and ETI, correspondingly). Salicylic acid, jasmonic acid, and ethylene are important drivers of interrelated channels of signaling of plant defense systems that help plants resist adversity. Cellular redox shifts, ion channel gating, oxidative burst, or protein kinase signaling cascades that right away stimulate cellular alterations like cell wall stimulation, secretion of antimicrobials, boosting the amount of reactive oxygen species (ROS) within the cell, and elevating the level of calcium inside the cell in question, leading to apoptosis, promote shifts in the expression of genes that subsequently upgrade phytoanticipins and phytoalexin levels. Current studies are increasingly concentrating on the secondary metabolite foundation of retaliation to parasites, and investigators employ metabolomic techniques to explore the defense-related compounds synthesized as a reaction to elicitors, effectors, and other stressful situations.
Cyst nematodes are obligate sedentary endoparasites characterized by developing pear or lemon-shaped protective structures for their eggs. Cyst-forming nematodes embrace nearly 100 known species across six genera, but Heterodera and Globodera represent the main genera of cyst-forming plant parasitic nematodes world over. Novel biological and genetic-based management practices are discussed for Heterodera glycines (soybean cyst nematode), Heterodera avenae (cereal cyst nematode), Heterodera schachtii (sugar beet cyst nematode), Heterodera zeae (corn cyst nematode), and Globodera pallida and Globodera rostochiensis (potato cyst nematodes).
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Trichoderma, a well-known fungal genus and opportunistic plant symbiont, is a quintessential alternative to chemicals with great potential to minimize disease incidence. The mycoparasitic ability along with antibiosis and induction of host immunity are the main mechanisms of biocontrol by this fungus. Fungi belonging to genus Trichoderma have been identified as potential biocontrol agents due to majority of isolated antifungal bioactive compounds. This review summarizes the biological control activity exerted by Trichoderma spp. against plant pathogenic fungi, bacteria, viruses, nematodes and insect pests. In addition, the research on formulations advocates that encapsulation could be a promising tool for increasing efficacy and durability of these fungi under field conditions. Further, advances in different areas of science and technology would strengthen the future research on Trichoderma-based products for its efficient use in agriculture.
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Twelve cultivars of sweet potato ( Ipomoea batatas (L.) Lam) evaluated for resistance to Meloidogyne incognita (Chitwood) and M. javanica (Chitwood) using “greenhouse bed, ” “greenhouse cylinder, ” and “field” methods. Comparable results were obtained irrespective of the method used; however, the cylinder methods confined roots to an area readily accessible to the nematodes, permitted periodic root observations without destroying the root system, and was more conducive to effective evaluations at an earlier stage.
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The potato cyst nematodes Globodera pallida and G. rostochiensis are economically important plant pathogens causing losses to UK potato harvests estimated at £50m/ year. Implications of climate change on their future pest status have not been fully considered. Here, we report growth of female G. pallida and G. rostochiensis over the range 15 to 25 °C. Females per plant and their fecundity declined progressively with temperatures above 17.5 °C for G. pallida, whilst females per plant were optimal between 17.5 and 22.5 °C for G. rostochiensis. Relative reproductive success with temperature was confirmed on two potato cultivars infected with either species at 15, 22.5 and 25 °C. The reduced reproductive success of G. pallida at 22.5 °C relative to 15 °C was also recorded for a further seven host cultivars studied. The differences in optimal temperatures for reproductive success may relate to known differences in the altitude of their regions of origin in the Andes. Exposure of G. pallida to a diurnal temperature stress for one week during female growth significantly suppressed subsequent growth for one week at 17.5 °C but had no effect on G. rostochiensis. However, after two weeks of recovery female size was not significantly different from that for the control treatment. Future soil temperatures were simulated for medium and high emissions scenarios and combined with nematode growth data to project future implications of climate change for the two species. Increased soil temperatures associated with climate change may reduce the pest status of G. pallida but benefit G. rostochiensis especially in southern UK. We conclude that plant breeders may be able to exploit the thermal limits of G. pallida by developing potato cultivars able to grow under future warm summer conditions. Existing widely deployed resistance to G. rostochiensis is an important characteristic to retain for new potato cultivars. This article is protected by copyright. All rights reserved.
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Cereal cyst nematodes are sedentary biotrophic endoparasites that maintain a complex interaction with their host plants. Nematode effector proteins are synthesized in the oesophageal glands and are secreted into plant tissues through the stylet. To understand the function of nematode effectors in parasitic plants, we cloned predicted effectors genes from Heterodera avenae and transiently expressed them in Nicotiana benthamiana. Infiltration assays showed that HaEXPB2, a predicted expansin-like protein, caused cell death in N. benthamiana. In situ hybridization showed that HaEXPB2 transcripts were localised within the subventral gland cells of the pre-parasitic second-stage nematode. HaEXPB2 had the highest expression levels in parasitic second-stage juveniles. Subcellular localization assays revealed that HaEXPB2 could be localized in the plant cell wall after H. avenae infection.This The cell wall localization was likely affected by its N-terminal and C-terminal regions. In addition, we found that HaEXPB2 bound to cellulose and its carbohydrate-binding domain was required for this binding. The infectivity of H. avenae was significantly reduced when HaEXPB2 was knocked down by RNA interference in vitro. This study indicates that HaEXPB2 may play an important role in the parasitism of H. avenae through targeting the host cell wall.
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Targeted DNA integration into known locations in the genome has potential advantages over the random insertional events typically achieved using conventional means of genetic modification. Specifically integrated transgenes are guaranteed to co-segregate, and expression level is more predictable, which makes downstream characterization and line selection more manageable. Because the site of DNA integration is known, the steps to deregulation of transgenic crops may be simplified. Here we describe a method that combines transcription activator-like effector nuclease (TALEN)-mediated induction of double strand breaks (DSBs) and non-autonomous marker selection to insert a transgene into a pre-selected, transcriptionally active region in the potato genome. In our experiment, TALEN was designed to create a DSB in the genome sequence following an endogenous constitutive promoter. A cytokinin vector was utilized for TALENs expression and prevention of stable integration of the nucleases. The donor vector contained a gene of interest cassette and a promoter-less plant-derived herbicide resistant gene positioned near the T-DNA left border which was used to select desired transgenic events. Our results indicated that TALEN induced T-DNA integration occurred with high frequency and resulting events have consistent expression of the gene of interest. Interestingly, it was found that, in most lines integration took place through one sided homology directed repair despite the minimal homologous sequence at the right border. An efficient transient assay for TALEN activity verification is also described.
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Plant terpene synthase genes (TPSs) have roles in diverse biological processes. Here we report the functional characterization of one member of the soybean TPS gene family, which was designated GmAFS. Recombinant GmAFS produced in Escherichia coli catalyzed the formation of a sesquiterpene (E,E)-α-farnesene. GmAFS is closely related to (E,E)-α-farnesene synthase gene from apple, both phylogenetically and structurally. GmAFS was further investigated for its biological role in defense against nematodes and insects. Soybean cyst nematode (SCN) is the most important pathogen of soybean. The expression of GmAFS in a SCN-resistant soybean was significantly induced by SCN infection compared to the control, whereas its expression in a SCN-susceptible soybean was not changed by SCN infection. Transgenic hairy roots overexpressing GmAFS under the control of the CaMV 35S promoter were generated in an SCN-susceptible soybean line. The transgenic lines showed significantly higher resistance to SCN, which indicates that GmAFS contributes to the resistance of soybean to SCN. In soybean leaves, the expression of GmAFS was found to be induced by Tetranychus urticae (two-spotted spider mites). Exogenous application of methyl jasmonate to soybean plants also induced the expression of GmAFS in leaves. Using headspace collection combined with gas chromatography-mass spectrometry analysis, soybean plants that were infested with T. urticae emitted a mixture of volatiles with (E,E)-α-farnesene as one of the most abundant constituents. In summary, this study showed GmAFS has defense roles in both below-ground and above-ground organs of soybean against nematodes and insects, respectively. This article is protected by copyright. All rights reserved.
Root-knot nematodes are soil-borne pathogens that invade and establish feeding sites in plant roots. They have an extremely broad host range, including most vascular plants. During infection of a susceptible host, root-knot nematodes secrete molecules called effectors that help them establish an intimate interaction with the plant and, at the same time, allow them to evade or suppress plant immune responses. Despite the fact that Meloidogyne hapla is a significant pest on several food crops, no effectors have been characterized from this root-knot nematode species thus far. Using the published genome and proteome from M. hapla, we have identified and characterized two genes, MhTTL2 and Mh265. MhTTL2 encodes a predicted secreted protein containing a transthyretin-like protein domain. The expression of MhTTL2 was up-regulated during parasitic life stages of the nematode, and in situ hybridization showed that MhTTL2 was expressed in the amphids, suggesting it has a role in the nematode nervous system during parasitism. We also studied the gene Mh265. The Mh265 transcript was localized to the subventral esophageal glands. An upregulation in Mh265 expression coincided with the pre- and early-parasitic life stages of the nematode. When Mh265 was constitutively expressed in plants, it enhanced their susceptibility to nematodes. These transgenic plants were also compromised in flg22-induced callose deposition, suggesting the Mh265 is modulating plant basal immune responses.
The root-knot nematode (RKN) Meloidogyne incognita reproduces on the roots of tobacco (Nicotiana tabacum), damaging crops, reducing crop yield, and causing economic losses annually. The development of resistant genotypes is an alternative strategy to effectively control these losses. However, the molecular mechanism responsible for host pathogenesis and defense responses in tobacco specifically against RKNs remain poorly understood. Here, root transcriptome analysis of resistant (Yuyan12) and susceptible (Changbohuang) tobacco varieties infected with RKNs was performed. Moreover, 2623 and 545 differentially expressed genes (DEGs) in RKN-infected roots were observed in Yuyan12 and Changbohuang, respectively, compared to those in non-infected roots, including 289 DEGs commonly expressed in the two genotypes. Among these DEGs, genes encoding cell wall modifying proteins, auxin-related proteins, the ROS scavenging system, and transcription factors involved in various biological and physiochemical processes were significantly expressed in both the resistant and susceptible genotypes. This work is thus the first report on the relationships in the RKN-tobacco interaction using transcriptome analysis, and the results provide important information on the mechanism of RKN resistance in tobacco.
Resistance conferred by the Mi-1 gene from Solanum peruvianum is effective and widely used for controlling root-knot nematodes (RKNs, Meloidogyne spp.). However, breakdown of resistance by RKNs seriously threatens the durable application of the resistance resource. Here, a resistance-breaking population of M. incognita was selected from an avirulent population by continuously inoculating on Mi-1-carrying tomato. Histological observations showed the resistance-breaking population would not induce hypersensitive response (HR) when infecting Mi-1-carrying tomato, while avirulent population did. A total of 308 differentially expressed genes (DEGs) were identified from Mi-1-carrying tomato upon infection with resistance-breaking versus avirulent populations by RNA-seq. The expression patterns of 23 selected DEGs were validated by quantitative real-time PCR (qRT-PCR). Subsequently, seven out of nine highly up-regulated DEGs were successfully knocked down in Mi-1-carrying tomato by tobacco rattle virus (TRV) mediated RNAi. The TRV line targeting a peroxidase gene showed a much higher magnitude of reactive oxygen species (ROS) and distinct reduction of pathogenicity upon infection of the resistance-breaking population compared with that of TRV::gfp line. Our results suggested that plant peroxidase might be exploited by resistance-breaking population of M. incognita to scavenge ROS, so as to overcome Mi-1-mediated resistance.