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Ultrastructure and anatomy of nematode-induced syncytia in roots of susceptible and resistant sugar beet

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Summary

Using susceptible and resistant sugar beet lines, comparative analyses of root histology and ultrastructure were made during invasion by nematodes and the induction and formation of specific feeding structures (syncytia).The resistant line carried the resistance geneHs1pro−1.Nematodes were able to invade and induce functional syncytia in roots of resistant and susceptible lines. However, syncytia in resistant roots were smaller and less hypertrophied. The vacuolar system of syncytia in susceptible plants contained many small vacuoles. In resistant plants vacuoles were larger but less numerous. Smooth endoplasmic reticulum prevailed in syncytial protoplasts of susceptible plants, whereas almost only rough endoplasmic reticulum occurred in syncytia in resistant plants. The most conspicuous and hitherto undescribed trait of syncytia in resistant roots was the initial appearance of loose, and later compact, aggregations of the endomembrane system which composed most of the endoplasmicreticulum system of syncytia at later stages. Syncytia in resistant plants usually degraded before the nematodes reached their adult stage. The appearance of membrane aggregations and the other resistance-specific features are discussed in relation to their possible effects on syncytium function and role in nematode resistance.

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Abbreviations

DAI:

days after inoculation

ER:

endoplasmic reticulum

ISC:

initial syncytial cell

J2:

second-stage juvenile

MA:

membrane aggregations

RER:

rough endoplasmic reticulum

SER:

smooth endoplasmic reticulum

References

  • Artschwager E (1926) Anatomy of the vegetative organs of the sugar beet. J Agric Res 33: 143–176

    Google Scholar 

  • Bleve-Zacheo T, Zacheo G (1987) Cytological studies of the susceptible reaction of sugarbeet roots toHeterodem schachtii. Physiol Mol Plant Pathol 30: 13–25

    Google Scholar 

  • Cai D, Kleine M, Kifle S, Harloff H-J, Sandal NN, Marcker KA, Klein-Langhorst RM, Salentijn EMJ, Lange W, Stiekema WJ, Wyss U, Grundler FMW, Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275: 832–834

    PubMed  Google Scholar 

  • Endo BY (1991) Ultrastructure of initial response of susceptible and resistant soybean roots to infection byHeterodem glycines. Rev Nematol 14: 73–94

    Google Scholar 

  • Gipson I, Kim KS, Riggs RD (1970) An ultrastructural study of syncytium development in soybean roots infected withHeterodera glycines. Phytopathology 61: 347–353

    Google Scholar 

  • Golinowski W, Magnusson C (1991) Tissue response induced byHeterodera schachtii (Nematoda) in susceptible and resistant white mustard cultivars. Can J Bot 69: 53–62

    Google Scholar 

  • —, Grundler FMW, Sobczak M (1996) Changes in the structure ofArabidopsis thaliana during female development of the plantparasitic nematodeHeterodera schachtii. Protoplasma 194: 103–116

    Google Scholar 

  • Grundler FMW (1989) Untersuchungen zur Geschlechtsdetermination des RübenzystennematodenHeterodera schachtii Schmidt. PhD thesis, Kiel University, Kiel, Federal Republic of Germany

    Google Scholar 

  • Grundler FMW, Sobczak M, Lange S (1997) Defense responses ofArabidopsis thaliana during invasion and feeding site induction by the plant-parasitic nematodeHeterodera glycines. Physiol Mol Plant Pathol 50: 419–429

    Google Scholar 

  • Grymaszewska G, Golinowski W (1987) Changes in the structure of wheat (Triticum aestivum L.) roots in varieties susceptible and resistant to infestation byHeterodera avenue Woll. Acta Soc Bot Pol 56: 381–389

    Google Scholar 

  • Jones MGK, Northcote DH (1972) Nematode-induced syncytium: a multinucleate transfer cell. J Cell Sci 10: 789–809

    PubMed  Google Scholar 

  • Jung C, Cai D, Kleine M (1998) Engineering nematode resistance in crop species. Trends Plant Sci 3: 266–271

    Google Scholar 

  • Kim YH, Riggs RD, Kim KS (1987) Structural changes associated with resistance of soybean toHeterodera glycines. J Nematol 19: 177–187

    Google Scholar 

  • Kleine M, Voss H, Cai D, Jung C (1998) Evaluation of nematode resistant sugar beet (Beta vulgaris L.) lines by molecular analysis. Theor Appl Genet 97: 896–904

    Google Scholar 

  • Mahaligam R, Skorupska HT (1996) Cytological expression of early response to infection byHeterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39: 986–998

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15: 473–497

    Google Scholar 

  • Paulson RE, Webster JM (1972) Ultrastructure of hypersensitive reaction in roots of tomato,Lycopersicon esculentum L., to infection by the root-knot nematodeMeloidogyne incognita. Physiol Plant Pathol 2: 227–234

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17: 208–212

    PubMed  Google Scholar 

  • Rice SL, Leadbeater BSC, Stone AR (1985) Changes in cell structure in roots of resistant potatoes parasitized by potato cystnematodes 1: potatoes with resistance geneH1 derived fromSolanum tuberosum ssp.andigena. Physiol Plant Pathol 27: 219–234

    Google Scholar 

  • —, Stone AR, Leadbeater BSC (1987) Changes in cell structure in roots of resistant potatoes parasitized by potato cyst nematodes 2: potatoes with resistance derived fromSolanum vernei. Physiol Mol Plant Pathol 31: 1–14

    Google Scholar 

  • Sobczak M (1996) Investigations on the structure of syncytia in roots ofArabidopsis thaliana induced by the beet cyst nematodeHeterodera schachtii and its relevance to the sex of the nematode. PhD thesis, Kiel University, Kiel, Federal Republic of Germany

    Google Scholar 

  • —, Golinowski W, Grundler FMW (1996) Changes in the structure ofArabidopsis thaliana roots induced during development of males of the plant parasitic nematodeHeterodera schachtii. Eur J Plant Pathol 103: 113–124

    Google Scholar 

  • —, Golinowski W, Grundler FMW (1999) Ultrastructure of feeding plugs and feeding tubes formed byHeterodera schachtii. Nematology 1: 363–374

    Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31–43

    PubMed  Google Scholar 

  • Wyss U (1992) Observations on the feeding behavior ofHeterodera schachtii throughout development, including events during moulting. Fund Appl Nematol 15: 75–89

    Google Scholar 

  • —, Stender C, Lehmann H (1984) Ultrastructure of feeding sites of the cyst nematodeHeterodera schachtii Schmidt in roots of susceptible and resistantRaphanus sativus L. var.oleiformis Pers. cultivars. Physiol Plant Pathol 25: 21–37

    Google Scholar 

  • Yu MH, Steele AE (1981) Host-parasite interaction of resistant sugarbeet andHeterodera schachtii. J Nematol 13: 206–212

    Google Scholar 

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Holtmann, B., Kleine, M. & Grundler, F.M.W. Ultrastructure and anatomy of nematode-induced syncytia in roots of susceptible and resistant sugar beet. Protoplasma 211, 39–50 (2000). https://doi.org/10.1007/BF01279898

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