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Part of the book series: Developments in Plant Pathology ((DIPP,volume 10))

Abstract

This overview emphasizes the present state of knowledge on the feeding behaviour of root parasitic nematodes and associated cell responses. Several unresolved questions related to this topic could recently be answered with the aid of high resolution video-enhanced contrast light microscopy, which enables direct observations of live nematodes within roots. Unlike in other plant pathogens, such as fungi, where cell wall surface molecules elicit a cascade in plant gene regulation, nematodes inject copious amounts of salivary secretions from oesophageal gland cells to transform root cells and tissues for their own reproductive success. Hence this chapter covers several examples of root cell responses to salivary secretions. As shown, Xiphinema index may be a good model. It has a huge dorsal gland cell and the effects of its secretions can be studied in detail. However, from an economic point of view, nearly all efforts in understanding the molecular bases for feeding structure establishment are currently devoted to the economically most important cyst and root-knot nematodes. In order to compare their feeding structures with those of other nematodes with different parasitic strategies, this introductory chapter gives also a general overview on the wide array of food cell modifications induced and maintained. These modifications are entirely nematode specific, irrespective of the host plant parasitized. Each is successful in its own to support development and reproduction of the nematode species involved. From an evolutionary point of view the uninucleate giant cells of some non-cyst-forming nematodes are for instance more primitive than the syncytia of cyst-forming nematodes, which ensure a higher reproductive capacity. Root-knot nematodes are generally regarded to have evolved the most advanced form of root parasitism. Multinucleate giant cells may therefore be considered torepresent the most advanced form of nurse cell systems. Hopefully, with rapid advances in molecular biology, we will finally find an answer to the intriguing question how nematode secretions regulate plant gene expression for their own benefit and how the specificity of the nurse cells or nurse cell systems induced by them can be explained.

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References

  1. Atkinson, H J., and Harris, P.D. (1989) Changes in nematode antigens recognized by monoclonal antibodies during early infections of soya beans with the cyst nematode Heterodera glycines, Parasitology 98, 479–487.

    Article  Google Scholar 

  2. B’Chir, M.M. (1988) Organisation ultrastructurale du site trophique induit par Tylenchulus semipenetrans dans les racines de citrus, Revue Nématol. 11, 213–222.

    Google Scholar 

  3. Baldwin, J.G. (1986) Testing hypotheses of phylogeny of Heteroderidae, in F. Lamberti and C. E. Taylor (eds.), Cyst nematodes, NATO ASI Series, Plenum, New York, pp. 75–100.

    Chapter  Google Scholar 

  4. Baldwin, J.G., and Bell, A.H. (1985) Cactodera eremica n.sp., Afenestrata africana (Luc et al., 1973) n. gen., n. comb., and an emended diagnosis of Sarisodera Wouts and Sher, 1971 (Heteroderidae), J. Nematol 17, 187–201.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Bleve-Zacheo, T., Lamberti, F., and Chinappen, M. (1987) Root cell response in rice attacked by Hemicycliophora typica, Nematol. medit, 5, 129–138.

    Google Scholar 

  6. Bleve-Zacheo, T., Melillo, M.T., Andres, M., Zacheo G., and Romero, M.D. (1995) Ultrastructure of initial response of graminaceous roots to infection by Heterodera avenae, Nematologica 41, 80–97.

    Article  Google Scholar 

  7. Bleve-Zacheo, T., and Zacheo, G. (1987) Cytological studies of the susceptible reaction of sugarbeet roots to Heterodera schachtii, Physiol. Mol. Plant Pathol. 30, 13–25.

    Article  Google Scholar 

  8. Böckenhoff, A (1995) Untersuchungen zur Physiologie der Nährstoffversorgung des Rübenzysten-nematoden Heterodera schachtii und der von ihm induzierten Nährzellen in Wurzeln von Arabidopsis thaliana unter Verwendung einer speziell adaptierten in situ Mikroinjektionstechnik, Ph.D. thesis, University of Kiel, 135 pp.

    Google Scholar 

  9. Böckenhoff, A., and Grundler, F.M.W. (1994) Studies on the nutrient uptake by the beet cyst nematode Heterodera schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana, Parasitology 109, 249–254.

    Article  Google Scholar 

  10. Cohn, E., and Kaplan, D.T. (1983) Parasitic habits of Trophotylenchulus floridensis (Tylenchulidae) and its taxonomic relationship to Tylenchulus semipenetrans and allied species, J. Nematol. 15, 514–523.

    CAS  PubMed Central  PubMed  Google Scholar 

  11. Cohn, E., Kaplan, D.T., and Esser, R.P. (1984) Observations on the mode of parasitism and histopathology of Meloidodera floridensis and Verutus volvingentis (Heteroderidae), J. Nematol. 16, 256–264.

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Cohn, E., and Mordechai, M. (1977) Uninucleate giant cell, induced in soybean by the nematode Rotylenchulus macrodoratus, Phytoparasitica 5, 85–93.

    Article  Google Scholar 

  13. Cohn, E., and Mordechai, M. (1982) Biology and host-parasite relations of a species of Meloidoderita (Nematoda: Criconematoidea), Revue Nématol. 5, 247–256.

    Google Scholar 

  14. Cohn, E., and Spiegel, Y. (1991) Root-nematode interactions, in Y. Waisel, A. Eshel and U. Kafkafi (eds.), Plant Roots; The Hidden Half, Marcel Dekker, Dordrecht, pp. 789–805.

    Google Scholar 

  15. Davis, E.L., Allen, R., and Hussey, R.S. (1994) Developmental expression of esophageal gland antigens and their detection in stylet secretions of Meloidogyne incognita, Fundam. appl. Nematol. 17, 255–262.

    Google Scholar 

  16. Endo, B.Y. (1984) Ultrastructure of the esophagus of larvae of the soybean cyst nematode, Heterodera glycines, Proc. Helminthol. Soc. Wash. 51, 1–24.

    Google Scholar 

  17. Endo, B.Y. (1987) Histopathology and ultrastructure of crops invaded by certain sedentary endoparasitic nematodes, in J. A, Veech and D.W. Dickson (eds.), Vistas on Nematology,, Soc. Nematol., Hyattsville, MD, pp. 196–210.

    Google Scholar 

  18. Endo, B.Y.(1990) Ultrastructure of nematode-plant interactions, in K. Mendgen and D.E. Lesemann (eds.), Electron Microscopy of Plant Pathogens, Springer, Berlin, pp. 291–305.

    Google Scholar 

  19. Endo, B.Y. (1991) Ultrastructure of initial responses of susceptible and resistant soybean roots to infection by Heterodera glycines, Revue Nématol. 14, 73–94.

    Google Scholar 

  20. Golinowski, W., Grundler, F.M.W., and Sobczak, M. (1996) Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii, Protoplasma, 194, 103–116.

    Article  Google Scholar 

  21. Goverse, A., Davis, E.L., and Hussey, R..S. (1994) Monoclonal antibodies to the esophageal glands and stylet secretions of Heterodera glycines, J. Nematol. 26, 251–259.

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Griffiths, B.S., and Robertson, W.M. (1984) Morphological and histochemical changes occurring during the life-span of root-tip galls on Lolium perenne induced by Longidorus elongatus. J. Nematol. 16, 223–229.

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Grundler, F. (1989) Untersuchungen zur Geschlechtsdetermination des Rübenzystennematoden Heterodera schachtii Schmidt, Ph.D. thesis, University of Kiel, 114 pp.

    Google Scholar 

  24. Grundler, F.M.W., Schnibbe, L., and Wyss, U. (1991) In vitro studies on the behaviour of second-stage juveniles of Heterodera schachtii (Nematoda: Heteroderidae) in response to host plant root exudates, Parasitology 103, 149–155.

    Article  Google Scholar 

  25. Grundler, F.M.W., Böckenhoff, A., Schmidt, K-P., Sobczak, M., Golinowski, W., and Wyss, U. (1994) Arabidopsis thaliana and Heterodera schachtii: a versatile model to characterize the interaction between host plants and cyst nematodes, in Advances in molecular Plant Nematology. NATO ASI Series, eds. F. Lamberti, C. De Giorgi, and D. McK Bird, pp. 171–180. New York, Plenum, 309 pp.

    Chapter  Google Scholar 

  26. Grundler, F.M.W., and Wyss, U. (1995) Strategies of root parasitism by sedentary plant parasitic nematodes, in K. Kohmoto, U.S. Singh and R.P. Singh (eds), Pathogenesis and Host Specificity in Plant Diseases, Histopathological, Biochemical, Genetic and Molecular Bases. Vol II Eukaryotes, Pergamon, Oxford, pp. 309–319.

    Google Scholar 

  27. Huang. C.S. (1985) Formation, anatomy and physiology of giant cells induced by root-knot nematodes, in J.N. Sasser and C.C. Carter (eds.), An Advanced Treatise on Meloidogyne, Vol. I, Biology and Control, NC State Univ. Graphics, Raleigh, NC, pp. 155–164.

    Google Scholar 

  28. Hussey, R.S. (1989) Disease-inducing secretions of plant-parasitic nematodes, Annu. Rev. Phytopathol. 27, 123–141.

    Article  Google Scholar 

  29. Hussey, R.S., and Mims, C.W. (1991) Ultrastructure of feeding tubes formed in giant cells induced in plants by the root-knot nematode Meloidogyne incognita, Protoplasma 162, 99–107.

    Article  Google Scholar 

  30. Hussey, R.S., Mims, C.W., and Westcott, S.W. (1992) Ultrastructure of root cortical cells parasitized by the ring nematode Criconemella xenoplax, Protoplasma 167, 55–65.

    Article  Google Scholar 

  31. Hussey, R.S., Mims, C.W., and Westcott, S.W. (1992) Immunocytochemical localization of callose in root cortical cells parasitized by the ring nematode Criconemella xenoplax, Protoplasma 171, 1–6.

    Article  CAS  Google Scholar 

  32. Inserra, R.N., Vovlas, N., and O’Bannon, J.H. (1988) Morphological and biological characters of diagnostic significance in Tylenchulus and Trophotylenchulus species, Nematologica 34, 412–421.

    Article  Google Scholar 

  33. Jones, M.G.K. (1981) Host cell responses to endoparasitic nematode attack: structure and function of giant cells and syncytia, Ann. appl. Biol. 97, 353–372.

    Article  CAS  Google Scholar 

  34. Jones, M.G.K., and Payne, H.L. (1977) The structure of syncytia induced by the phytoparasitic nematode Nacobbus aberrans in tomato roots, and the possible role of plasmodesmata in their nutrition, J. Cell Sci. 23, 299–313.

    CAS  PubMed  Google Scholar 

  35. Jones, R.K. (1978) Histological and ultrastructural changes in cereal roots caused by feeding of Helicotylenchus spp., Nematologica 24, 393–397.

    Article  Google Scholar 

  36. Linford, M.B. (1942) The transient feeding of root-knot nematode larvae, Phytopathology 32, 580–589.

    Google Scholar 

  37. Maggenti, A.R. (1981) General Nematology. Springer, New York, 372 pp.

    Book  Google Scholar 

  38. Maggenti, A.R. (1991) Nemata: higher classification, in W.R. Nickle (ed.), Manual of Agricultural Nematology, M. Dekker, New York, pp. 147–187.

    Google Scholar 

  39. Magnusson, C., and Golinowski, W. (1991) Ultrastructural relationships of the developing syncytium induced by Heterodera schachtii (Nematoda) in root tissues of rape, Can. J. Bot. 69, 44–52.

    Article  Google Scholar 

  40. Melillo, M.T., Bleve-Zacheo, T., and Zacheo, G. (1990) Ultrastructural response of potato roots susceptible to cyst nematode Globodera pallida pathotype Pa 3, Revue Nématol. 13, 17–28.

    Google Scholar 

  41. Mundo-Ocampo, M., and Baldwin, J.G. (1984) Comparison of host response of Cryphodera utahensis with other Heteroderidae, and a discussion of phylogeny, Proc. Helminthol. Soc. Wash. 51, 25–31.

    Google Scholar 

  42. Rebois, R.V. (1980) Ultrastructure of a feeding peg and tube associated with Rotylenchulus reniformis in cotton, Nematologica 26, 396–405.

    Article  Google Scholar 

  43. Rhoades, H.L., and Linford, M.B. (1961) A study of the parasitic habit of Paratylenchus projectus and P. dianthus, Proc. Helminthol. Soc. Wash. 28, 185–190.

    Google Scholar 

  44. Robertson, W.M., Trudgill, D.L., and Griffiths, B.S. (1984) Feeding of Longidorus elongatus and L. leptocephalus on root-tip galls of perennial ryegrass (Lolium perenne), Nematologica 30, 222–229.

    Article  Google Scholar 

  45. Robertson, W.M., and Wyss, U. (1979) Observations on the ultrastructure and function of the dorsal oesophageal gland cell in Xiphinema index, Nematologica 25, 391–396.

    Article  Google Scholar 

  46. Robertson, W.M., and Wyss, U. (1983) Feeding processes of virus-transmitting nematodes, in K.F. Harris (ed.), Current Topics in Vector Research Vol 1, Praeger, New York, 325 pp.

    Google Scholar 

  47. Rumpenhorst, H.J. (1984) Intracellular feeding tubes associated with sedentary plant parasitic nematodes, Nematologica 30, 77–85.

    Article  Google Scholar 

  48. Rumpenhorst, H.J., and Weischer, B. (1978) Histopathological and histochemical studies on grapevine roots damaged by Xiphinema index, Revue Nématol. 1, 217–225.

    CAS  Google Scholar 

  49. Schuerger, A.C., and McClure, M.A. (1983) Ultrastructural changes induced by Scutellonema brachyurum in potato roots, Phytopathology 73, 70–81.

    Article  Google Scholar 

  50. Sijmons, P. C. (1993) Plant nematode interactions, Plant Mol. Biol. 23, 917–931.

    Article  CAS  PubMed  Google Scholar 

  51. Sijmons, P.C., Atkinson, H.J., and Wyss, U. (1994) Parasitic strategies of root nematodes and associated host cell responses, Annu. Rev. Phytopathol. 32, 235–259.

    Article  CAS  Google Scholar 

  52. Sijmons, P.C., Grundler, F.M.W., von Mende, N., Burrows, P.R., and Wyss, U. (1991) Arabidopsis thaliana as a new model host for plant-parasitic nematodes, Plant J. 1, 245–254.

    Article  Google Scholar 

  53. Sobczak, M. (1996) Investigations on the structure of syncytia in roots of Arabidopsis thaliana induced by the beet cyst nematode Heterodera schachtii and its relevance to the sex of the nematode, Ph.D. thesis, University of Kiel.

    Google Scholar 

  54. Steinbach, P. (1973) Untersuchungen über das Verhalten von Larven des Kartoffelzystenälchens (Heterodera rostochiensis Wollenweber, 1923) an und in Wurzeln der Wirtspflanze Lycopersicon esculentum Mill). III. Die Nahrungsaufnahme von Kartoffelnematodenlarven, Biol. Zbl. 92, 563–582.

    Google Scholar 

  55. Suarez, Z., Sosa Moss, C., and Inserra, R.N. (1985) Anatomical changes induced by Punctodera chalcoensis in corn roots, J. Nematol. 17, 242–244.

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Subbotin, S.A. (1993) Evolution of modified food cells induced by sedentary nematodes in plant roots, Russian J. Nematol. 1, 17–26.

    Google Scholar 

  57. Taylor, D.P., Cadet, P., and Luc, M. (1978) An unique host-parasite relationship between Hylonema ivorense (Nematoda: Heteroderidae) and the roots of a tropical rainforest tree, Revue Nématol. 1, 99–108.

    Google Scholar 

  58. Townshend, J.L., Stobbs, L., and Carter, R. (1989) Ultrastructural pathology of cells affected by Pratylenchus penetrans in alfalfa roots, J. Nematol. 21, 530–539.

    CAS  PubMed Central  PubMed  Google Scholar 

  59. Vovlas, N. (1987) Parasitism of Trophotylenchulus obscurus on coffee roots, Revue Nématol. 10, 337–342.

    Google Scholar 

  60. Vovlas, N., and Inserra, R.N. (1986) Morphometrics, illustration, and histopathology of Sphaeronema rumicis on cottonwood in Utah, J. Nematol. 18, 239–246.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Wiggers, R.J., Starr, J.L., and Price, H.J. (1990) DNA content and variation in chromosome number in plant cells affected by Meloidogyne incognita and M.arenaria, Phytopathology 80, 1391–1395.

    Article  Google Scholar 

  62. Wyss, U. (1981) Ectoparasitc root nematodes: Feeding behavior and plant cell responses, in B.M. Zuckerman and R.A. Rhode (eds.), Plant Parasitic Nematodes. Vol. III, Academic, New York, pp. 325–351.

    Chapter  Google Scholar 

  63. Wyss, U. (1987) Video assessment of root cell responses to dorylaimid and tylenchid nematodes, in J. A, Veech and D.W. Dickson (eds.), Vistas on Nematology,, Soc. Nematol., Hyattsville, MD, pp. 211–220.

    Google Scholar 

  64. Wyss, U. (1988) Pathogenesis and host-parasite specificity in nematodes, in R.S. Singh, U.S. Singh W.M. Hess and D.J. Weber (eds.), Experimental and Conceptual Plant Pathology, Vol. 2. Pathogenesis and Host-Parasite Specificity, Gordon and Breach, New York, pp. 417–432.

    Google Scholar 

  65. Wyss, U. (1992) Observations on the feeding behaviour of Heterodera schachtii throughout development, including events during moulting, Fundam. appl. Nematol. 15, 75–89.

    Google Scholar 

  66. Wyss, U., and Grundler, F.M.W. (1992) Seminar: Heterodera schachtii and Arabidopsis thaliana, a model host-parasite interaction, Nematologica 38, 488–493.

    Article  Google Scholar 

  67. Wyss, U., Grundler, F.M.W. and Münch, A. (1992) The parasitic behaviour of second-stage juveniles of Meloidogyne incognita in roots of Arabidopsis thaliana, Nematologica 38, 98–111.

    Article  Google Scholar 

  68. Wyss, U., and Inst. Wiss. Film (1974) Trichodorus similis (Nematoda) — Response of protoplasts in root hairs (Nicotiana tabacum) to feeding, Film E 2045, IWF Göttingen, 19 pp.

    Google Scholar 

  69. Wyss, U., and Inst. Wiss. Film (1988) Responses of root-tip cells (Ficus carica) ) to feeding of the nematode Xiphinema index, Film D 1657, IWF Göttingen, 22 pp.

    Google Scholar 

  70. Wyss, U., Jank-Ladwig, R., and Lehmann, H. (1979) On the formation and ultrastructure of feeding tubes produced by trichodorid nematodes, Nematologica 25, 385–390.

    Article  Google Scholar 

  71. Wyss, U., Lehmann, H., and Jank-Ladwig, R. (1980) Ultrastructure of modified root-tip cells in Ficus carica, induced by the ectoparasitic nematode Xiphinema index, J. Cell Sci. 41, 193–208.

    CAS  PubMed  Google Scholar 

  72. Wyss, U., Robertson, W.M., and Trudgill, D.L. (1988) Oesophageal bulb function of Xiphinema index and associated root cell responses, assessed by video-enhanced contrast light microscopy, Revue Nématol. 11, 253–261.

    Google Scholar 

  73. Wyss, U., Stender, C., and Lehmann, H. (1984) Ultrastructure of feeding sites of the cyst nematode Heterodera schachtii Schmidt in roots of susceptible and resistant Raphanus sativus L. var. oleiformis Pers. cultivars, Physiol. Plant Pathol. 25, 21–37.

    Article  Google Scholar 

  74. Wyss, U., and Zunke, U. (1986) Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots, Revue Nématol. 9, 153–165.

    Google Scholar 

  75. Wyss, U., Zunke, U., and Inst. Wiss. Film. (1986) Heterodera schachtii (Nematoda) — Behaviour inside the root (rape)., Film E 2904, IWF Göttingen, 21 pp.

    Google Scholar 

  76. Zacheo, G., and Bleve-Zacheo, T. (1995) Plant-nematode interactions: histological, physiological and biochemical interactions, in K. Kohmoto, U.S. Singh and R.P. Singh (eds.), Pathogenesis and Host Specificity in Plant Diseases. Histo-pathological, Biochemical, Genetic and Molecular Bases, Vol.II Eukaryotes, Pergamon, Oxford, pp.321–353.

    Google Scholar 

  77. Zunke, U. (1990) Ectoparasitic feeding behaviour of the root lesion nematode, Pratylenchus penetrans, on root hairs of different host plants, Revue Nématol. 13, 331–337.

    Google Scholar 

  78. Zunke, U. (1990) Observations on the invasion and endoparasitic behavior of the root lesion nematode Pratylenchus penetrans, J. Nematol. 22, 309–320.

    CAS  PubMed Central  PubMed  Google Scholar 

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Wyss, U. (1997). Root Parasitic Nematodes: An Overview. In: Fenoll, C., Grundler, F.M.W., Ohl, S.A. (eds) Cellular and Molecular Aspects of Plant-Nematode Interactions. Developments in Plant Pathology, vol 10. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5596-0_2

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