Cyst nematodes are obligate biotrophs, and the most devastating species among them are: soybean cyst nematodes (SCN;
H. glycines), PCN (
G. pallida and
G. rostochiensis) and CCN (including
Heterodera avenae and
Heterodera filipjevi). It is nearly impossible to eradicate potato cyst nematodes due to their prolonged survival of up to 20 years in the soil, even in the absence of a host, and their tolerance to extremely low temperatures
[39][26]. The dormant second-stage juveniles (J2) hatch from the eggs in the presence of a host-derived chemical that is abundant in root diffusates
[40][27]. The released second-stage juveniles invade the host intercellularly and reach the inner cortex. This juvenile has a peculiar behaviour; it keeps inserting its stylet into various cells until it finds a cell that does not collapse its protoplast and does not cover the stylet with a layer of callose- like material. Finally, it finds a suitable cell that becomes the initial syncytial cell (ISC). Subsequently, the cell walls of the ISC surrounding cells are dissolved and protoplasts fuse to form the large multinucleate feeding cell called the syncytium
[29][16]. All the cells surrounding the ISC cells contribute to the formation of the syncytium, where DNA is synthesised and metabolism is enhanced to provide a nutrient-rich medium to the infecting nematode
[41][28]. The nematode remains attached to the feeding site for several weeks, wherein it undergoes two further moults to form a complete adult
[42][29]. The male adults remain vermiform and leave the root cells, whereas the female adults grow, get fertilised and finally die to form a tanned body wall that converts into a cyst, which bears the next generation of eggs
[43][30]. Besides proteins that modify the host cell wall, many nematodes are reported to have effector molecules that suppress the host defensive mechanisms
[44][31] and modify the host nucleus
[43][30]. Significant efforts have been made to understand syncytium formation in the biology of cyst nematodes. These nematodes initiate the production of a peptide that has complete similarity with the plant peptide CLAVATA3 (CLE3). The stem cells in shoot and floral meristems of
Arabidopsis secrete CLV3, which is the founding member of the CLE protein family, which eventually restricts the size of the stem cell population
[45][32]. Therefore, indirect nematode manipulation of the CLAVATA signalling pathway induces the feeding site
[45][32]. In addition, an effector that modulates the auxin flow pattern into the feeding structures has been identified
[46][33]. Moreover, various genes expressed within the syncytia have been studied through microarray analysis to understand the basis of the feeding site formation
[47][34].
Many taxa of nematodes produce specific secretions that contain effectors and cell-wall degrading enzymes, such as cellulases
[48][35], pectate lyases
[49][36] and xylanases
[48][35]; these degrade the cell walls of infected cells. The effectors also have the potential to suppress the host immune system by altering its defence mechanisms. The species
Ditylenchus dipsaci cause malformations in the infected plant tissues by withdrawing the cell contents through the nematode stylet
[50][37]. This nematode has the unique property of resistance to dry conditions and freeze tolerance, due to the outer lipid layer of the fourth generation juvenile, which prevents water loss from its body
[51][38]. The reniform nematodes have a unique way of interacting with their host plant. Initially, the adult female inserts one-third of its anterior body into the host root and establishes a feeding site to form a syncytium. After continuous feeding for about 2–3 days, the posterior part of the body outside the roots starts swelling near the vulval region to attain a kidney shape. Subsequently, within 7–9 days of thriving in environmentally favourable conditions, 40–100 eggs are laid within the gelatinous matrix produced by the uterine glands
[52][39]. Under favourable conditions, PPN also interacts with other soil-borne pathogens like bacteria, fungi and viruses to suppress plants defence mechanisms or to cause a breakdown of plant resistance against infection
[43][30].
4. Plant Responses to Nematode Infection
Based on plant cultivar and species, different plants react differently to nematode infections. Temperature, soil moisture content, nematode type, soil characteristics and crop rotations also affect the damage levels. Typical and most peculiar plant symptoms range from premature wilting, chlorosis, nutrient deficiency leading to stunted growth, fragile roots and swollen root areas due to gall formation. The
Pratylenchus species cause lesions in roots leading to cell necrosis, browning and death, and root rotting due to secondary attachment by fungi and bacteria that thrive in soil. Infected plant roots undergo discolouration, and become stubby and stunted, making the plant susceptible to water stress conditions
[53][40]. Some
Radopholus spp. manifest as toppling disease in infected banana host plants
[54][41]. Reduction in crop yield is often monitored as a sign of nematode infestation, both in terms of quality and quantity
[55][42]. The threshold level for nematode infestation could be one nematode egg per 100 cm
3 of soil
[56][43]. The rice-stem nematodes,
Ditylenchus angustus, feed ecoparasitically on the leaves and stems of rice and cause ufra disease in rice plants
[54][41].
Ditylenchus dipsaci primarily infects onion and garlic, leading to the discoloration of the infected bulbs and the stunted growth of the host plants
[50][37].
Ditylenchus dipsaci is a migratory endoparasite, whereas
Ditylenchus angustus is a migratory ectoparasite. The host plant resistance (HPR) mode can be easily incorporated in the case of endoparasites, as they spend more than half of their life-cycle within the host. However, ectoparasitic nematodes cannot be strongly selected to develop HPR, due to their reduced specific feeding requirements. Different types of PPN and their mode of action are listed in
Table 1.
Table 1. Classification of PPN groups according to genus, feeding type, physical manifestations and mode of action.
Nematode Groups |
Genus |
Feeding Type |
Physical Manifestations |
Mode of Action |
Root-Knot |
Meloidogyne | spp. |
Obligate |
Forms galls (root-knots) on infected roots |
Feeds on giant cells of the root and suppresses the host defence mechanisms |
Cyst |
Heterodera | and | Globodera | spp. |
Obligate biotrophs |
Forms cysts (enclosing eggs) due to a large multinucleate feeding structure called the syncytium |
Dissolves plant cell walls and fuses protoplasts Effectors target the host cell nucleus and suppress plant defence mechanisms. |
Root lesion |
Pratylenchus | spp. |
Polyphagous, migratory, intercellular root endoparasites |
Formation of lesions, necrotic areas, browning and plant cell death, often followed by root rotting. |
Secretions from pharyngeal glands have effectors that degrade plant cell walls. |
Burrowing |
Radopholus similis |
Migratory endoparasite |
Weakens the root system, forms dark lesions, root rotting and causes toppling disease |
The effectors contain plant-cell-wall-degrading enzymes like cellulases, pectate lyases and xylanases. |
Stem and bulb |
Ditylenchus dipsaci |
Migratory endoparasite |
Causes stunted growth, twisted stems and the discoloration of bulbs |
Feeds on the parenchymatous cells of the cortex and produces cell-wall-softening enzymes and effectors such as expansins |
Pine wilt |
Bursaphelencus xylophilus |
Migratory endoparasite |
Completely infects and kills all the pine trees growing in an area |
Parasitizes plants with the help of cellulose-degrading proteins like glycoside hydrolase It is carried with the help of insect vector, | Monochamus | beetles. |
Reniform |
Rotylenchulus reniformis |
Sedentary Semi-endoparasite |
Leads to moisture and nutrient deficiency in infected host along with root necrosis, chlorosis and stunted growth |
Feeds on pericycle and endodermal root cells by inserting 1/3 of their anterior body Cell walls break to form a two-cell-deep syncytium. |
Large plant parasitic species |
Xiphinema index |
Ectoparasite |
Infection retards root extension, causes swelling and gall formation |
Have feeding mechanisms similar to root-knot nematodes |
False-root knot |
Nacobbus aberrans |
Migratory juveniles Sedentary adult female |
Causes cavities and lesions on root tissues; root galls are formed around feeding sites |
Induces the partial dissolution the of cell wall and the fusion of protoplasts to form a syncytium |
White tip disease variety |
Aphelenchoides besseyi |
Ecto/endo parasite Fungivorous |
Infected plants have stunted growth, and other symptoms include chlorotic white tips on leaves, leaf necrosis, reduction in rice grain size and number |
Does not induce re-differentiation of plant cells Local cell damage, tissue disintegration and browning in epidermal cells and palisade parenchyma |