Anatomical Alterations in Plant Tissues Induced by Plant-Parasitic Nematodes

Abstract

Plant-parasitic nematodes (PPNs) interact with plants in different ways, for example, through subtle feeding behavior, migrating destructively through infected tissues, or acting as virus-vectors for nepoviruses. They are all obligate biotrophic parasites as they derive their nutrients from living cells which they modify using pharyngeal gland secretions prior to food ingestion. Some of them can also shield themselves against plant defenses to sustain a relatively long lasting interaction while feeding. This paper is centered on cell types or organs that are newly induced in plants during PPN parasitism, including recent approaches to their study based on molecular biology combined with cell biology-histopathology. This issue has already been reviewed extensively for major PPNs (i.e., root-knot or cyst nematodes), but not for other genera (viz. Nacobbus aberrans, Rotylenchulus spp.). PPNs have evolved with plants and this co-evolution process has allowed the induction of new types of plant cells necessary for their parasitism. There are four basic types of feeding cells: (i) non-hypertrophied nurse cells; (ii) single giant cells; (iii) syncytia; and (iv) coenocytes. Variations in the structure of these cells within each group are also present between some genera depending on the nematode species viz. Meloidogyne or Rotylenchulus. This variability of feeding sites may be related in some way to PPN life style (migratory ectoparasites, sedentary ectoparasites, migratory ecto-endoparasites, migratory endoparasites, or sedentary endoparasites). Apart from their co-evolution with plants, the response of plant cells and roots are closely related to feeding behavior, the anatomy of the nematode (mainly stylet size, which could reach different types of cells in the plant), and the secretory fluids produced in the pharyngeal glands. These secretory fluids are injected through the stylet into perforated cells where they modify plant cytoplasm prior to food removal. Some species do not produce specialized feeding sites (viz. Ditylenchus, Subanguina), but may develop a specialized modification of the root system (e.g., unspecialized root galls or a profusion of roots). This review introduces new data on cell types and plant organs stimulated by PPNs using sources varying from traditional histopathology to new holistic methodologies.

Keywords: Ditylenchus; Globodera; Heterodera; Meloidogyne; Rotylenchulus; Xiphinema; giant cell; syncytium.

Figure 1

Morphogenesis caused by stem, leaf, seed and root gall nematodes. Ditylenchus gigas (A–D): (A) Necrotic area on stem (arrowed). (B–D) Cross sections of parenchymatic tissues of the stem showing under-epidermic cavities surrounded by necrotic cells and nematode body portions (Vovlas et al., ; with permission of John Wiley and Sons). Ditylenchus oncogenus (E–G): (E) Leaf midrib nematode-induced galls, showing different deformation degrees. (F) Longitudinal section of parenchyma of a stem portion showing sub-epidermal cavities (ca) surrounded by necrotic cells. (G) Cross-section of flower parenchyma showing a nematode (n), and hypertrophied nuclei (hn) in the attacked cells (Vovlas et al., ; with permission of Cambridge University Press). Anguina tritici (H–J): (H) Healthy (left) and infected (right) spike and seed galls of wheat. (I,J) Cross-sections of wheat-seed showing severe infection induced by the nematode (n) and the high number of nematodes inside the grain (Source: N. Vovlas). Root-galls caused by Subanguina radicicola (K) on Poa annua (Source: N. Vovlas). Subanguina moxae (L,M): Cross-sections of foliar galls from Artemisia sp. showing cavities (ca), nematodes (n), and a layer of nutritious cells (lnc) (Source: N. Vovlas). ca, cavity; ec, epidermic cell layer; hn, hypertrophied nuclei; lnc, layer of nutritious cells; n, nematode. Scale bars: A,F,H,K = 1,000 μm; B,E = 500 μm; C,D,G,J = 50 μm; I,L,M = 100 μm.

Figure 2

Morphogenesis caused by ectoparasite root nematodes. Paratrichodorus teres (A,B): (A) Apical-root galls on wheat. (B) Cross-section of apical-root wheat gall (Source: N. Vovlas). Xiphinema index (C–F): (C, D) Apical-root galls in grapevine. (E,F) Cross-sections showing multinucleate cells with hypertrophied nucleus (hn) induced by nematode parasitism (Gutiérrez-Gutiérrez et al., ; with permission of John Wiley and Sons). Helicotylenchus oleae (G,H): Cross-sections of olive roots showing the nematode feeding on a parenchymatic feeding cell (fc) with hypertrophied nucleus (hn) (Source: N. Vovlas). fc, feeding cell; hn, hypertrophied nucleus; n, nematode; st, stylet. Scale bars: A,D = 1,000 μm; B = 200 μm; E = 10 μm; F,H = 20 μm; G = 100 μm.

Figure 3

Morphogenesis in root knot nematodes forming galls. Meloidogyne spp. (A–I): (A) Egg mass (eg) protruding from a gall in a Cucumis sativus root infected by Meloidogyne javanica. (B) Longitudinal section of a gall from Arabidopsis thaliana showing multinucleate giant cells (^*) and anterior region of the nematode (n). (C) Vascular tissue of a gall with GUS intense signal from an Arabidopsis transgenic marker line. (D) 3D reconstruction of giant cells (^*) from Arabidopsis thaliana (Source: C. Escobar). Meloidogyne artiellia (E–I): (E) Healthy and M. artiellia-infected chickpea roots, showing the prominent adult female covered by the egg mass. (F) Cross-section of M. artiellia-infected root showing the typical feeding site with giant cells (Palomares-Rius et al., ; with permission of Elsevier). (G–I) Detail of multinucleate giant cells induced by M. artiellia, M. arenaria, and M. javanica in chickpea roots, respectively (Vovlas et al., ; with permission of The American Phytopathological Society). ^*, multinucleate giant cell; eg, egg-mass; hn, hypertrophied nucleus; n, nematode. Scale bars: A–C,E = 100 μm; F–I = 20 μm.

Figure 4

Morphogenesis in cyst nematodes forming syncytia. Heterodera spp. (A–I): Heterodera cruciferae (A–F) Transverse sections of cabbage roots infected by H. cruciferae showing the semi-endoparasitic adult female (n) inducing the cortical and stellar syncytium (s) with fused syncytial cells with dense cytoplasm and hypertrophic nuclei (hn) ((Sasanelli et al., 2013); with permission of The American Phytopathological Society). Heterodera daverti (G,H) Cross-sections of white clover roots showing the semi-endoparasitic adult female (n) inducing the cortical and stellar syncytium (s) with fused syncytial cells presenting dense cytoplasm and hypertrophic nuclei (hn) (Vovlas et al., ; with permission of Springer). Heterodera filipjevi (I) Detail of syncytial cells in wheat roots showing hypertrophic nuclei (hn) (Source: N. Vovlas). Scale bars: A = 1,000 μm; B,G,H = 500 μm; C–F,I = 100 μm.

Figure 5

Morphogenesis in root nematodes: other root endoparasites (A–N). Trophotylenchulus obscurus (A,B): (A) Nematode (n) parasitizing coffee root. (B) Cross section of coffee root showing feeding cells (fc) with no evident increase in size and the nematode (Source: N. Vovlas). Tylenchulus semipenetrans (C,D): (C) Nematode (n) parasitizing citrus root. (D) Cross section showing induced nurse cells (nc) with dense cytosols (Source: N. Vovlas). Nacobbus aberrans (E–H). (E,F) Tomato roots infected by the nematode showing knobs. (G,H) Cross sections of tomato roots showing the nematode (n) and the induced syncytium (s) (Vovlas et al., ; with permission of Journal of Nematology). Cryphodera brinkmani (I–L): (I) Root segment of pine with the posterior portion of the body of a white female (n) protruding from the root surface. (J–L) Cross sections of pine roots showing nematode female body (n) embedded in the cortical parenchyma and an uninucleate giant cell (ugc) with hypertrophied nucleus (hn) (Vovlas et al., ; with permission of Springer). (M) Cross section of corn root infected by Meloidodera charis showing the single nurse cell (nc) (Source: N. Vovlas). (N) Cross section of Mentha aquatica root infected by Meloidoderita kirjanovae showing the syncytial formation (s) (Vovlas et al., ; with permission of Journal of Nematology). Fc, feeding cell; hn, hypertrophied nucleus; n, nematode; nc, nurse cell; s, syncytium; ugc, uninucleate giant cell. Scale bars: A,I = 500 μm; B,G,H,N = 50 μm; C,D,J–M = 100 μm.