Abstract
Infective second stage juveniles of the cyst forming genera of plant parasitic nematodes (Heterodera and Globodera) induce the formation of feeding sites in roots of resistant and susceptible plants. Under special experimental conditions in Arabidopsis thaliana, future males select the initial syncytial cell (ISC) in the pericycle and future females select their ISC in the procambium. After a preparation phase the nematode feeding site is still unicellular. Cytoplasmic streaming and cytoplasm density, amount of endoplasmic reticulum (ER) and volume of nucleus are increased while the volume of central vacuole is decreased and new small cytoplasmic vacuoles are formed. The cell walls are thickened and covered by a layer of callose-like material. The developing syncytia expand along the vascular cylinder. The expansion of the syncytium triggers the proliferation of cambial and peridermal tissues, in a manner similar to secondary growth. Compared with syncytia associated with females, syncytia of males are less hypertrophied and are composed of more cells. Distinctive cell wall openings are mostly found between the few strongly hypertrophied pericyclic syncytial elements. The ultrastructure of both types of syncytia is very similar but shows conspicuous differences in the structure and localisation of cell wall ingrowths.
Cultivars resistant to nematodes share some common reactions upon nematode infection. At the stage of migration and ISC selection there are no essential differences between susceptible and resistant plants. However, at the stage of syncytium induction some resistant plants show a very quick defence based on the hypersensitive response (HR). Many other resistant plants do not exhibit the HR. In these cases resistance develops more gradually during syncytium formation. The resistance can be correlated with changes in symplast and apoplast. In the symplast they usually deal with the ER. Another characteristic change is gradual reduction of cytoplasm density indicating loss of its physiological activity. Changes in apoplast can be responsible for the obstruction of syncytial development. The syncytial cell walls are abnormally thickened and restructured. The cell wall openings are smaller and less numerous. The syncytia are often surrounded by a conspicuous layer of necrotic cells. Syncytia developing in roots of resistant plants necrotise prematurely.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Bingefors, S. (1982) Nature of inherited nematode resistance in plants, in Harris, K.F. and K. Maramorosch (eds.), Pathogens, Vectors, and Plant Diseases: Approaches to Control, Academic Press, N. Y., pp. 187–219.
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.
Bleve-Zacheo, T., Melillo, M.T. and Zacheo, G. (1990) Syncytia development in germplasm pea accessions infected with Heterodera goettingiana. Nematol. mediter. 18, 93–102.
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.
Di Vito, M. and Vovlas, N. (1990) Differential histological response of selected Cicer bijugum and C. arietinum lines to Heterodera ciceri, Nematol. mediter. 18, 165–167.
Endo, B.Y. (1964) Penetration and development of Heterodera glycines in soybean roots and related anatomical changes, Phytopathology 54, 79–88.
Endo, B.Y. (1965) Histological responses of resistant and susceptible varieties and backcross progeny to entry and development of Heterodera glycines, Phytopathology 55, 375–381.
Endo, B.Y. (1971) Nematode-induced syncytia (giant cells). Host-parasite relationships of Heteroderidae, in B.M. Zukerman, W.F. Mai and R.A. Rohde (eds.), Plant Parasitic Nematodes, vol. 2, Academic Press, N.Y., pp. 91–117.
Endo, B.Y. (1975) Pathogenesis of nematode-infected plants, Annu. Rev. Phytopathol. 13, 213–238.
Endo, B.Y. (1978) Feeding plug formation in soybean roots infected with the soybean cyst nematode, Phytopathology 68, 1022–1031.
Endo, B.Y. (1991) Ultrastructure of initial responses of susceptible and resistant soybean roots to infection by Heterodera glycines, Rev. Nématol. 14, 73–94.
Endo, B.Y. and Veech, J.A. (1970) Morphology and histochemistry of soybean infected with Heterodera glycines, Phytopathology 60, 1493–1498.
Gipson, I., Kim, K.S. and Riggs, R.D. (1971) An ultrastructural study of syncytium development in soybean roots infected with Heterodera glycines, Phytopathology 61, 253–346.
Golinowski, W., Grundler, F.M.W. and Sobczak, M. (1996) Changes in the structure of Arabidopsis thaliana induced during development of females of the plant parasitic nematode Heterodera schachtii, Protoplasma, 194, 103–116.
Golinowski, W. and Magnusson, C. (1991) Tissue response induced by Heterodera schachtii (Nematoda) in susceptible and resistant white mustard cultivars, Can. J. Bot. 69, 53–62.
Grundler, F.M.W. (1989) Untersuchungen zur Geschlechtsdetermination des Rübenzystennematoden Heterodera schachtii Schmidt, PhD thesis, University of Kiel.
Grundler, F.M.W., Böckenhoff, A., Schmidt, K.-P., Sobczak, M., Golinowski, W. and Wyss, U. (1994a) Arabidopsis thaliana and Heterodera schachtii, a versatile model to characterize the interaction between host plants and cyst nematodes, in F. Lamberti, C. De Giorgi, and D.McK. Bird (eds.), Advances in Molecular Plant Nematology, NATO ASI Series A: no. 268, Plenum Press, N.Y., pp. 171–180.
Grundler, F.M.W. and Wyss, U. (1995) Strategies of root parasitism by sedentary plant parasitic nematodes, in U.S. Singh, K. Kohmoto and R.P. Singh (eds.), Pathogenesis and Host Specificity in Plant Diseases, vol. II. Pergamon Press, Oxford, UK, pp. 309–319.
Grundler, F.M.W., Wyss, U. and Golinowski, W. (1994b) Sedentary endoparasitic nematodes in Arabidopsis thaliana, in J. Bowman (ed.), Arabidopsis, an Atlas of Morphology and Development, Springer, N.Y., pp. 418–423.
Grymaszewska, G. and Golinowski, W. (1987) Changes in the structure of wheat (Triticum aestivum L.) roots in varieties susceptible and resistant to infection by Heterodera avenae Woll., Acta Soc. Bot. Pol. 56, 381–383.
Grymaszewska, G. and Golinowski, W. (1991) Structure of syncytia induced by Heterodera avenae Woll. in roots of susceptible and resistant wheat (Triticum aestivum L.), J. Phytopathol. 133, 307–319.
Hoopes, R.W., Anderson, R.E. and Mai, W.F. (1978) Internal response of resistant and susceptible potato clones to invasion by potato cyst nematode Heterodera rostochiensis, Nematropica 8, 13–20.
Hussey, R.S. (1989) Disease-inducing secretions of plant parasitic nematodes. Annu. Rev. Phytopathol, 27, 123–141.
Hussey, R.S., Davis, E.L. and Ray, C. (1994) Meloidogyne stylet secretions, in F. Lamberti, C. De Giorgi, and D.McK. Bird (eds.), Advances in Molecular Plant Nematology, NATO ASI Series A: no. 268, Plenum Press, N.Y., pp. 233–248.
Jones, A.M. and Dangl, J.L. (1996) Longjam at the Styx: programmed cell death in plants, Trends Plant Sci. 1, 114–119.
Jones, M.G.K. (1981a) Host cell responses to endoparasitic nematode attack: Structure and function of giant cells and syncytia, Ann. Appl. Biol. 97, 353–372.
Jones, M.G.K. (1981b) The development and function of plant cells modified by endoparasitic nematodes, in B.M. Zukerman and R.A. Rohde (eds.) Plant Parasitic Nematodes, vol. III, Academic Press, N.Y., pp. 255–279.
Jones, M.G.K. and Dropkin, V.H. (1975) Scanning electron microscopy of syncytial transfer cells induced in roots by cyst nematodes, Physiol. Plant Pathol. 7, 259–263.
Jones, M.G.K. and Northcote, D.H. (1972) Nematode-induced syncytium-a multinucleate transfer cell, J. Cell Sci. 10, 789–809.
Kim, Y.H., Riggs, R.D. and Kim, K.S. (1987) Structural changes associated with resistance of soybean to Heterodera glycines, J. Nematol. 19, 177–187.
Luc, M., Maggenti, A.R. and Fortuner, R. (1988) A reappraisal of Tylenchina (Nemata). 9. The family Heteroderidae Filip’ev & Schuurmans Stekhoven, 1941, Rev. N (matol. 11, 159–176.
Magnusson, C. and Golinowski, W. (1991) Ultrastructural relationships of the developing syncytium induced by Heterodera schachtii (Nematoda) in root tissue of rape, Can. J. Bot. 69, 44–52.
Melillo, M.T., Bleve-Zacheo, T. and Zacheo, G. (1990a) Ultrastructural response of potato roots susceptible to cyst nematode Globodera pallida pathotype Pa3, Rev. N(matol. 13, 17–28.
Melillo, M.T., Bleve-Zacheo, T., Zacheo, G. and Perrino, P. (1990b) Morphology and enzyme histochemistry in germplasm pea roots attacked by Heterodera goettingiana, Nematol. mediter. 18, 83–91.
Mittler, R. and Lam, E. (1996) Sacrifice in the face of foes: pathogen-induced programmed cell death in plants, Trends Microbiol. 4, 10–15.
Mugniery, D. and Bossis, M. (1985) Influence de l’hote, de la compétition et de l’état physiologique des juvéniles sur la pénétration, le développement et la sexe d’Heterodera carotae Jones. Nematologica 31, 335–343.
Mugniery, D. and Fayet, G. (1981) Determination du sexe chez Globodera pallida Stone, Rev. N(matol. 4, 41–45.
Mugniery, D. and Fayet, G. (1984) Détermination du sexe de Globodera rostochiensis Woll. et influence des niveaux d’infestacion sur la pénétration le développement et le sexe de ce nématode, Rev. N(matol. 7, 233–238.
Raski, D.J. (1950) The life history and morphology of the sugar beet nematode, Heterodera schachtii Schmidt, Phytopathology 40, 135–150.
Rice, S.L., Leadbeater, B.S.C. and Stone, A.R. (1985) Changes in cell structure in roots of resistant potatoes parasitized by potato cyst nematodes. 1. Potatoes with resistance gene H1 derived from Solanum tuberosum ssp. andigena, Physiol. Plant Pathol. 27, 219–234.
Rice, S.L., Stone, A.R. and Leadbeater, B.S.C. (1987) Changes in cell structure in roots of resistant potatoes parasitized by potatoes cyst nematodes. 2. Potatoes with resistance derived from Solanum vernei, Physiol. Mol. Plant Pathol. 31, 1–14.
Riggs, R.D., Kim, K.S. and Gipson, I. (1973) Ultrastructural changes in Peking soybeans infected with Heterodera glycines, Phytopathology 63, 76–84.
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.
Sijmons, P.C., Atkinson, H.J. and Wyss, U. (1994) Parasitic strategies of root nematodes and associated host cell responses, Annu. Rev. Phytopaihol 32, 235–259.
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. PhD Thesis, University of Kiel.
Sobczak, M., Golinowski, W. and Grundler, F.M.W. (1996) Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii, Europ. J. Plant Pathol. in press.
Stender, C. Lehmann, H. and Wyss, U. (1982) Feinstrukturelle Untersuchungen zur Entwicklung von Wurzelriesenzellen (Syncytien) induziert durch Rübenzystennematoden Heterodera schachtii, Flora 172, 223–233.
Williams, K.J. and Fisher, J.M. (1993) Development of Heterodera avenae Woll. and host cellular responses in susceptible and resistant wheat, Fundam. Appl. Nematol. 16, 417–423.
Wilski, A. (1977) M1twik zbo¿owy Heterodera avenae Woll. (1924), PAN, Komitet Ochrony Roœlin.
Wyss, U. (1992) Observations on the feeding behaviour of Heterodera schachtii throughout development, including events during moulting, Fundam. Appl. Nematol. 15, 75–89.
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.
Wyss, U. and Zunke, U. (1986) Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots, Rev. Nématol. 9, 153–165.
Yu, M.H. and Steele, A.E. (1981) Host-parasite interaction of resistant sugarbeet and Heterodera schachtii, J. Nematol. 13, 206–212.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1997 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Golinowski, W., Sobczak, M., Kurek, W., Grymaszewska, G. (1997). The Structure of Syncytia. 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_7
Download citation
DOI: https://doi.org/10.1007/978-94-011-5596-0_7
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-010-6360-9
Online ISBN: 978-94-011-5596-0
eBook Packages: Springer Book Archive