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ZOOLOGY Biology of Parasitism Plant Parasitic Nematodes Development Paper No. : 08 Biology of Parasitism Module : 33 Plant Parasitic Nematodes Development Team Principal Investigator: Prof. Neeta Sehgal Head, Department of Zoology, University of Delhi Paper Coordinator: Dr. Pawan Malhotra ICGEB, New Delhi Content Writers: Dr. Vartika Mathur, Sri Venkateswara College, University of Delhi Dr. Tom O. G. Tytgat, Department of Molecular Plant Physiology, Institute for Water and Wetland Research, Radboud University Nijmege, The Netherlands Content Reviewer: Prof. Virender Kumar Bhasin Department of Zoology, University of Delhi 1 Biology of Parasitism ZOOLOGY Plant Parasitic Nematodes Description of Module Subject Name ZOOLOGY Paper Name Biology of Parasitism Module Name/Title Morphology, biology, life cycle and infection of crop plants by parasitic nematodes Module ID 33; Plant Parasitic Nematodes Keywords PPN, Triplonchida, Dorylaimida, Tylenchida, root parasitic nematodes, ecto-endoparasites Contents 1. Learning Outcomes 2. Introduction 3. Phylogeny 4. Biodiversity 4.1. Triplonchida 4.2. Dorylaimida 4.3. Tylenchida 4.3.1 Above Ground Feeders 4.3.2 Root Parasitic Nematodes 5. Summary 2 Biology of Parasitism ZOOLOGY Plant Parasitic Nematodes 1. Learning Outcomes After completing this module, you will be able to: understand the economic and ecological importance of plant parasitic nematodes. learn the phylogeny of the plant parasitic nematodes. understand their biodiversity. identify and classify them based on their morphological features and mode of parasitism. distinguish them based on their trophic niches. 2. Introduction Plant parasitic nematodes (PPN) nematodes are usually small, soil-borne pathogens and the symptoms they cause are often nonspecific. They are extremely diverse and abundant in all types of soil, and plants regularly encounter them during their lifetime (Sohlenius, 1980). There are more than 4100 described species of PPN (Decraemer & Hunt, 2006). With only a few exceptions, PPN are root feeders. Their presence is not only the key driving force of plant succession in natural environments (De Deyn et al., 2003), but they also collectively represent a significant constraint to the global food security with annual crop damages estimated to be more than $US80 billion per year (Nicol et al., 2011). Nematode infection affects the plant at different levels. Infested fields show a reduced number of plants, and infected plants have a lower biomass due to a disturbed physiology (Figure1). Crop damage is not only limited to the direct nematode-plant interaction itself, but very often nematode infected plants are more susceptible to fungal or bacterial infection (Abawi & Chen, 1998). Certain nematode species can serve as vectors for a number of important plant viruses (Brown et al., 1995), or may enhance crop losses associated with insect as well as weed pests (Alston et al., 1991). Figure 1: A healthy sugar beet versus a beet infected with the cyst nematode Heteroderas chachtii. 3 Biology of Parasitism ZOOLOGY Plant Parasitic Nematodes 3. Phylogeny Most of the nematode species are microscopic in size and lack obvious distinguishing characteristics. Therefore, classification within the phylum has been very difficult. Based on small-subunit ribosomal sequences of 53 species, Blaxter et al. (1998) proposed a molecular evolutionary framework for the Nematoda comprising five major clades, all of which including parasitic species (Figure 2). It suggests that animal parasitism arose independently at least four times, and plant parasitism three times. 4. Biodiversity Evolutionary adaptation to plant parasitism led to some striking morphological changes (Hussey, 1989). Almost all plant-parasitic nematodes possess a hollow, protrusible, hypodermic needle-like axial spear, which serves as the interface between the plant and the nematode. Figure 2: A phylogenetic hypothesis for the phylum Nematoda based on small subunit sequences (Blaxter et al., 1998). C+S indicates clade Chromadorida plus Secernentea; S+P indicates Secernentea plus Plectidae. Plant parasitism occurs in three widely separated orders. 4 Biology of Parasitism ZOOLOGY Plant Parasitic Nematodes It can be used to penetrate the plant cell wall, to withdraw nutrients from the cytoplasm, or to release secretions. These secretions are synthesised in the pharyngeal glands, which have enlarged considerably when nematodes adapted to parasitism. Two different types of pharyngeal glands are recognised: subventral and dorsal glands (Figure 3). Each gland is a single cell, with a long cytoplasmic extension terminating in an ampulla, which is connected to the pharyngeal lumen via a valve-like structure (Robertson & Wyss, 1979; Endo, 1984; Endo & Wergin, 1988). Secretory proteins are processed in the well-developed rough endoplasmic reticulum and Golgi-apparatus, and collected in secretory granules (Hussey & Mims, 1990) (Figure4). These granules are transported via microtubuli towards the ampulla, where the secretions are released into the pharyngeal lumen. Figure 3 : Diagram of the anterior region of a second-stage juvenile of a tylenchid plant-parasitic nematode (Hussey R.S., 1989). Two types of pharyngeal glands are recognized : one dorsal and two subventral. The subventral gland extensions end of the metacorpal pump chamber. The dorsal gland extension runs anteriorly until the ampulla, which is located closely behind the base of the stylet.Via a valve structure, the ampullae of both types of pharyngeal glands are connected to the pharyngeal (esophageal) lumen. The protrusible stylet has a narrow lumen throughout its length. Close to the tip, the lumen has a ventrally located orifice. The stylet isused to pierce cell walls, to release pharyngeal gland secretions, and to withdraw nutrients from the cytoplasm of a plant cell. 5 Biology of Parasitism ZOOLOGY Plant Parasitic Nematodes Plant-parasitic nematodes occur in three widely separated orders: Triplonchida, Dorylaimida and Tylenchida (Blaxter et al., 1998), with the majority being in the latter. Although there are some similarities between these taxa, it is evident that evolution to plant parasitism occurred convergently in the three orders. Figure 4: Diagram of a pharyngeal gland cell dissected from a cyst nematode (Smant G., 1998). mRNA, coding for secreted proteins, is translated on the rough endoplasmic reticulum. The precursor proteins are modified in the lumen of the endoplasmic reticulum, and transported to the golgi-bodies for further processing. Small vesicles, containing the mature secretory proteins, bud from the golgi–bodies and fuse thereafter to form large secretory granules. The secretory granules are transported via microtubuli through the cell extension towards the ampulla. Probably by the process of exocytosis, the contents of the secetory granules are released via the valve into the pharyngeal (oesophageal) lumen. 4.1. Triplonchida All triplonchid plant-parasitic nematodes are migratory ectoparasites on roots (Wyss, 1997).The species of the family Trichodoridae have five secretory gland cells, one dorsal and two anterior and two posterior subventral glands, which end in the basal bulb of the pharynx. Their stylet (onchiostyle) is a modified mural tooth. Trichodoridae (Figure 5.1) explore the surface of the root, and feed on epidermis cells. During feeding, which rarely exceeds a few minutes, the ventrally curved stylet is continuously thrust into the perforated cells (Wyss, 1981).Injection of secretions results in the formation of a feeding tube (Wyss et al., 1979). Due to the relatively large width of the feeding tube, they are the only root parasitic nematodes capable of removing large organelles from the cytoplasm. If 6 Biology of Parasitism ZOOLOGY Plant Parasitic Nematodes the epidermis cells survive the feeding, Tobraviruses can be successfully transmitted by the nematodes. Trichodorids are considered to be little advanced in their mode of parasitism as the cytoplasm of several hundred cells has to be withdrawn to produce a few eggs within a week (Wyss, 1981). 4.2. Dorylaimida The axial spear of the Longidoridae is composed of an odontostyle and an odontophore; the former is thought to have evolved from a mural tooth and has a dorsal aperture.It is formed in the anterior part of the pharynx and moves forward during moulting to replace the previous odontostyle, at the same time the odontophore is reformed in situ (Coomans & De Coninck, 1963).The length of the stylet enables the Longidoridae to feed deeper inside the root tissue.They have three pharyngeal glands, one dorsal and two subventral. Most of the time, root tips are selected as feeding sites, and root tip galls develop (Wyss, 1997). Xiphinema index (Figure 5.3) feeds on a column of cells: it starts feeding for a few minutes on one cell, and afterwards progresses to deeper laying cells.Dorsal gland secretions are injected into the cells and seem to liquefy the cytoplasm (Robertson & Wyss, 1979).After ingestion of the solutes by the nematode, the cells die of necrosis.Probably also in response to the secretions, the neighbouring cells become hypertrophied and binucleate (Wyss et al., 1988). In case of Longidorus (Figure 5.2), stylet secretions seem to induce a gall-like structure containing uninucleate hypertrophied cells surrounding the necrotic feeding cells (Griffiths & Robertson, 1984). Figure 5: Schematic representation of feeding sites of some selected migratory root-parasitic nematodes.1: Triplonchid nematodeTrichodorus sp.; 2: Dorylaimid nematode Longidorus elongatus; 3 : Dorylaimid nematode Xiphinema
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