Plant Parasitic Nematodes: History
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Subjects: Agriculture, Dairy & Animal Science | Green & Sustainable Science & Technology
Contributor:
Anusha Pulavarty

Plant parasitic nematodes are a major problem for growers worldwide, causing severe crop losses. Several conventional strategies, such as chemical nematicides and biofumigation, have been employed in the past to manage their infection in plants and spread in soils. However, the search for the most sustainable and environmentally safe practices is still ongoing.

  • lant parasitic nematodes
  • microbial
  • fermentation
  • bionematicides

1. Introduction

There are nearly 4100 species of plant parasitic nematodes (PPN) reported to date that are considered to be a serious constraint for global food security [1]. Considering economic development and food preferences, the World Bank in 2008 estimated a 35% increase in world population by 2050, which will correspond to a 75% increase in food demand [2]. Therefore, it has become an environmental concern for relevant stakeholders worldwide to promote sustainable methods to enhance the efficiency of resource use [3].

2. Plant Parasitic Nematode Species and Their Distribution

In the UK alone, it is estimated that the cyst nematodes Globodera rostochiensis and Globodera pallida are responsible for approximately 9% of the total UK potato production losses [4]. Globodera pallida is the predominant potato cyst nematode (PCN) that is found in more than 90% of the nematode-infested fields of England and Wales, with an overall estimated cost of £26 million per year in crop yield [5] and an additional £10 million per year in nematicides [6]. In tropical and sub-tropical climates, 14.6% crop losses primarily occur due to nematodes, whereas these are estimated to be 8.8% in developed nations [1]. Fleming et al. [7] reported the prevalence and diversity of PPN in the cereals and grasslands of Northern Ireland; Meloidogyne spp., Heterodera spp. and Pratylenchus spp. were found above the threshold levels for economic damage. This increase in nematode populations was reported due to poor cropping practices and climate change [7]. Surveys conducted in 35 states of the USA reported a total of 25% crop loss due to PPN [8]. Loss in crop productivity due to soybean cyst nematodes have been calculated to be around $US1.5 billion each year in the USA alone [9]. Under favourable environmental conditions, cereal cyst nematodes (CCN) can destroy 90% of crop fields [1]. Potato cyst nematodes cause a 9% loss of total potato production worldwide [1]. These nematodes, originating from South America, are currently major quarantine pathogens and have widely spread to all the potato-growing regions of the world [10].
Nose and Shiraishi [11] have reported a total loss of 2 × 106 m3 of timber in Japan due to Bursaphelenchus xylophilus which has the potential to infect and kill all the pine trees in an infested area under favourable conditions. The Department of Agriculture, Food and the Marine (DAFM) in Ireland reported B. xylophilus, G. pallida, G. rostochiensis, Meloidogyne chitwoodi and Meloidogyne fallax as European Union quarantine pests [12].

3. Nematode Behaviour, Feeding and Host–Parasite Interactions

Plant parasitic nematodes demonstrate a wide variety of interactions with their host. They can be categorized into ecto or endoparasites depending on the plant tissues they feed on. Some PPN are migratory as they easily move from soil to plant tissues, whereas others are sedentary with an adult female being completely immobile and stuck to the roots of the plant. The sedentary endoparasites feed with the help of specialised cells present around the female head. Most species of PPN have a needle-like protrusible oral structure called a stylet, which helps to puncture the host plant tissues. They release specific enzymes into the tissues that help in partially digesting the plant cells for easy ingestion into the nematode gut [13]. The migratory adult female usually deposits its eggs in soil or plants, based on its position. On the other hand, the most economically important PPN, such as root-knot (Meloidogyne spp.), cyst (Globodera spp., Heterodera spp.), reniform (Rotylenchulus spp.), and citrus (Tylenchulus semipenetrans) species are biotrophic, sedentary in nature [14]. They lay a large cluster of eggs either inside their bodies or attached as masses to their body. Within the egg after embryogenesis, first stage juveniles (J1) moult to form the second stage infective juveniles (J2) that hatch from the eggs to infect the root tissues. The expanded root parts appear as galls, containing root-knot nematode females, or as pathological nodes on roots, induced by traumatic wounds done by the nematode stylets or spears puncturing the root surface.
The genus Meloidogyne consists of nearly 98 species with a wide host range and can parasitize many vascular plants [15]. Second stage juveniles adopt both physical and enzymatic approaches to penetrate the host. With the help of a stylet, they damage the plant cell wall and then release cellulolytic and pectolytic enzymes to completely digest it. Conversely, the cyst nematodes display an upward intercellular movement within the root cells and try to reach the zone of differentiation, via the root tip, the apical meristems and the vascular cylinder. The giant cells, generated due to repeated nuclear divisions, in this region act as permanent feeding sites for the sedentary J2, where they undergo third and fourth stage moults to form reproductive male and female adults [16].
De Waele, D. and Elsen [17] have reported the difficulty in mitigating the damage caused by Meloidogyne species due to their short life cycle and broad host range. Due to short life cycles, these organisms spread faster and infect nearby crop plants within a short time. These nematode species are well adapted to flood conditions, with the potential to attack both upland and lowland rice [18] and can cause up to 85% crop loss [19]. Meloidogyne incognita have a unique set of putative genes that reduce plant immunity, detoxification and defence mechanisms and that help them to survive inside the plant host [20]. The plant parasitic lifestyle of root-knot nematodes is mainly due to the abundance of plant-cell-wall-degrading genes in their genomes [21]. Meloidogyne species, being obligate biotrophs, have to continuously suppress host defence mechanisms for the survival of their feeding structures. Meloidogyne incognita have a defence mechanism similar to that of plant pathogenic bacteria, in which they secrete calreticulin, which helps in sequestering free calcium ions and therefore curbs calcium ion influx [22]. Root knot nematodes also interact with other pathogens like Fusarium wilt, Rhizoctonia solani and Thielaviopsis basicola, leading to complex plant diseases [23]. Meloidogyne species have a gene that mimics the rhizobial NodL gene, which induces nodular formation in legumes [24]. Though the nematode exudates potentially alter nodulation signalling in legumes, some mutant legumes that do not support normal nodulation are tolerant to nematode infections [25].
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 [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 [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 [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 [28]. The nematode remains attached to the feeding site for several weeks, wherein it undergoes two further moults to form a complete adult [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 [30]. Besides proteins that modify the host cell wall, many nematodes are reported to have effector molecules that suppress the host defensive mechanisms [31] and modify the host nucleus [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 [32]. Therefore, indirect nematode manipulation of the CLAVATA signalling pathway induces the feeding site [32]. In addition, an effector that modulates the auxin flow pattern into the feeding structures has been identified [33]. Moreover, various genes expressed within the syncytia have been studied through microarray analysis to understand the basis of the feeding site formation [34].
Many taxa of nematodes produce specific secretions that contain effectors and cell-wall degrading enzymes, such as cellulases [35], pectate lyases [36] and xylanases [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 [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 [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 [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 [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 [40]. Some Radopholus spp. manifest as toppling disease in infected banana host plants [41]. Reduction in crop yield is often monitored as a sign of nematode infestation, both in terms of quality and quantity [42]. The threshold level for nematode infestation could be one nematode egg per 100 cm3 of soil [43]. The rice-stem nematodes, Ditylenchus angustus, feed ecoparasitically on the leaves and stems of rice and cause ufra disease in rice plants [41]. Ditylenchus dipsaci primarily infects onion and garlic, leading to the discoloration of the infected bulbs and the stunted growth of the host plants [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

This entry is adapted from the peer-reviewed paper 10.3390/plants10112352

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