European Journal of Plant Pathology

, Volume 120, Issue 4, pp 383–396

Cytological and immunocytochemical studies on responses of wheat spikes of the resistant Chinese cv. Sumai 3 and the susceptible cv. Xiaoyan 22 to infection by Fusarium graminearum

  • Zhensheng Kang
  • Heinrich Buchenauer
  • Lili Huang
  • Qingmei Han
  • Hongchang Zhang
Full Research Paper
  • 255 Downloads

Abstract

Fusarium head blight (FHB), predominantly caused by Fusarium graminearum and F. culmorum, is one of the most destructive diseases of wheat, reducing grain yield and quality of kernels. In diseased kernels trichothecne mycotoxins accumulate, which are harmful to human and animal health. Pathogen development and host responses to infection by F. graminearum were investigated in wheat spikes of the resistant cv. Sumai 3 and susceptible cv. Xiaoyan 22 to infection by means of electron microscopy and immunogold labelling techniques. The infection process of the pathogen in wheat spikes was similar in both the resistant and susceptible cultivars, but the pathogen developed more slowly in the resistant cv. Sumai 3 compared to the susceptible cv. Xiaoyan 22, indicating that fungal spread was restricted to the spike tissues of the resistant cultivar. The formation of thick-layered appositions and papillae was essentially more pronounced in the infected host tissues of the resistant cultivar than in the susceptible one. ß-1,3-glucan was detected in the appositions and papillae. Immunogold labelling studies demonstrated that labelling densities for lignin, thionins and hydroxyproline-rich glycoproteins (HRGP) over the cell walls of the infected tissues of the susceptible wheat cv. Xiaoyan 22 only slightly increased whereas these compounds intensely accumulated in the host cell walls of the infected wheat spikes of the resistant cv. Sumai 3. The labelling densities for the two plant hydrolases, ß -1,3-glucanase and chitinase, increased slightly in the infected wheat spike tissues of the susceptible cv. Xiaoyan 22, whereas higher labelling densities of both enzymes were found in the infected wheat spikes from the resistant cv. Sumai 3. Immunogold labelling of the Fusarium toxin DON in the infected wheat spike tissues showed that labelling densities in spike tissues for DON in the resistant cv. Sumai 3 were significantly lower than those in the susceptible cv. Xiaoyan 22. The significance of the induced morphological (e.g. thick-layered wall appositions and papillae) and chemical defence constituents (e.g. ß -1,3-glucanase, chitinase, lignin, thionin and HRGP) in resistance to FHB as well as the possible role of DON as an aggressiveness factor in translation of transcripts of defence response genes and spreading of F. graminearum and F. culmorum are discussed.

Keywords

Triticum aestivum Fusarium graminearum Resistance Fusarium head blight Mycotoxins Cytology Immunocytochemistry DON Sumai 3 Xiaoyan 22 Electron microscopy 

Abbreviations

FHB

Fusarium head blight

DON

deoxynivalenol

TBS

Tris-buffered saline

HRGP

hydroxyproline-rich glycoproteins

TEM

transmission electron microscopy

References

  1. Aist, J. R. (1976). Papillae and related wound plugs of plant cells. Annual Review of Phytopathology, 14, 145–163.CrossRefGoogle Scholar
  2. Arlorio, M., Ludwig, A., Boller, T., & Bonfante, P. (1992). Inhibition of fungal growth by plant chitinases and β-1,3-glucanases: A morphological study. Protoplasma, 171, 34–43.CrossRefGoogle Scholar
  3. Bai, G. H., Desjardins, A. E., & Plattner, R. D. (2002). Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia, 153, 91–98.PubMedCrossRefGoogle Scholar
  4. Bai, G. H., & Shaner, G. (1994). Scab of wheat: Prospects for control. Plant Disease, 78, 760–766.CrossRefGoogle Scholar
  5. Ban, T., & Suenaga, K. (2000). Genetic analysis of resistance to Fusarium head blight caused by Fusarium graminearum in Chinese wheat cultivar Sumai 3 and Japanese cultivar Saikai 165. Euphytica, 113, 87–99.CrossRefGoogle Scholar
  6. Benhamou, N., Joosten, M. H. A. J., & De Wit, P. J. G. M. (1990). Subcellular localization of chitinase and of its potential substrate in tomato root tissues infected by Fusarium oxysporum f.sp. radicis-lycopersici. Plant Physiology, 92, 1108–1120.PubMedGoogle Scholar
  7. Benhamou, N., Mazau, D., Grenier, J., & Esquerré-Tugayé, M.-T. (1991). Time-course study of the accumulation of hydroxyproline-rich glycoproteins in root cells of susceptible and resistant tomato plants infected by Fusarium oxysporum f.sp. radicis-lycopersici. Planta, 184, 196–208.CrossRefGoogle Scholar
  8. Boller, T. (1987). Hydrolytic enzymes in plant disease resistance. In T. Kosuge, & E. W. Nester (Eds.) Plant-microbe interactions. Molecular and genetic perspectives, vol 2 (pp. 385–413). New York: Macmillan.Google Scholar
  9. Boyacioglu, D., & Hettiarachchy, N. S. (1995). Changes in some biochemical components of wheat grain that was infected with Fusarium graminearum. Journal of Cereal Science, 21, 57–62.CrossRefGoogle Scholar
  10. Desjardins, A. E., & Hohn, T. M. (1997). Mycotoxins in plant pathogenesis. Molecular Plant-Microbe Interactions, 10, 147–152.CrossRefGoogle Scholar
  11. Desjardins, A. E., Proctor, R. H., Bai, G., McCormick, S. P., Shaner, G., & Buechley, G., et al. (1996). Reduced virulence of trichothecene non-producing mutants of Gibberella zeae in wheat field tests. Molecular Plant-Microbe Interactions, 9, 775–781.Google Scholar
  12. Enkerli, K., Hahn, M. G., & Mims, C. W. (1997). Ultrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic oomycete Phytophthora sojae. Canadian Journal of Botany, 75, 1493–1508.CrossRefGoogle Scholar
  13. Epple, P., Apel, K., & Bohlmann, H. (1997). Overexpression of an endogenous thionin enhances resistance of arabidopsis against Fusarium oxysporum. Plant Cell, 9(4), 509–520.PubMedCrossRefGoogle Scholar
  14. Kang, Z., & Buchenauer, H. (1999). Immunocytochemical localization of Fusarium toxins in infected wheat spikes by Fusarium culmorum. Physiological and Molecular Plant Pathology, 55, 275–288.CrossRefGoogle Scholar
  15. Kang, Z., & Buchenauer, H. (2000a). Cytology and ultrastructure of the infection of wheat spikes by Fusarium culmorum. Mycological Research, 104, 1083–1093.CrossRefGoogle Scholar
  16. Kang, Z., & Buchenauer, H. (2000b). Ultrastructural and cytochemical studies on cellulose, xylan and pectin degradation in wheat spikes infected by Fusarium culmorum. Journal of Phytopathology, 148, 263–275.CrossRefGoogle Scholar
  17. Kang, Z., & Buchenauer, H. (2000c). Ultrastructural and immunocytochemical investigation of pathogen development and host responses in resistant and susceptible wheat spikes infected by Fusarium culmorum. Physiological and Molecular Plant Pathology, 57, 255–268.CrossRefGoogle Scholar
  18. Kang, Z., & Buchenauer, H. (2002). Immunocytochemical localization of ß-1,3-glucanase and chitinase in Fusarium culmorum-infected wheat spikes. Physiological and Molecular Plant Pathology, 60, 141–153.CrossRefGoogle Scholar
  19. Kang, Z., & Buchenauer, H. (2003). Immunocytochemical localization of cell wall-bound thionins and hydroxyproline-rich glycoproteins in Fusarium culmorum-infected wheat spikes. Journal of Phytopathology, 151(3), 120–129.CrossRefGoogle Scholar
  20. Kang, Z., Huang, L., & Buchenauer, H. (2004). Ultrastructural and cytochemical studies on infection of wheat spikes by Microdochium nivale. Journal of Plant Diseases and Protection, 111(4), 351–361.Google Scholar
  21. Kang, Z., Zingen-Sell, I., & Buchenauer, H. (2005). Infection of wheat spikes by Fusarium avenaceum and alteration of cell wall components in the infected tissue. European Journal of Plant Pathology, 111(1), 19–28.CrossRefGoogle Scholar
  22. Keen, N. T., & Yoshikawa, M. (1983). ß-1,3-Endoglucanases from soybean release elicitor-active carbohydrates from fungal cell walls. Plant Physiology, 71, 460–465.PubMedCrossRefGoogle Scholar
  23. Kombrink, E., Schröder, M., & Hahlbrock, K. (1988). Several pathogenesis-related proteins in potato are 1,3-ß-glucanases and chitinases. Proceedings of the National Academy of Sciences of the United States of America, 85, 782–786.PubMedCrossRefGoogle Scholar
  24. Langevin, F., Eudes, F., & Comeau, A. (2004). Effect of trichothecenes produced by Fusarium graminearum during Fusarium head blight development in six cereal species. European Journal of Plant Pathology, 110, 735–746.CrossRefGoogle Scholar
  25. McMullen, M., Jones, R., & Gallenberg, D. (1997). Scab of wheat and barley: A reemerging disease of devastating impact. Plant Disease, 81, 1340–1348.CrossRefGoogle Scholar
  26. Mesterházy, Á. (1995). Types and components of resistance against Fusarium head blight of wheat. Plant Breeding, 114, 377–386.CrossRefGoogle Scholar
  27. Mesterházy, Á., Bartók, T., Kászonyi, G., Varga, M., Tóth, B., & Varga, J. (2005). Common resistance to different Fusarium spp. causing Fusarium head blight in wheat. European Journal of Plant Pathology, 112, 267–281.CrossRefGoogle Scholar
  28. Miller, J. D., & Arnison, P. G. (1986). Degradation of deoxynivalenol by suspension cultures of the Fusarium head blight resistant wheat cultivar Frontana. Canadian Journal of Plant Pathology, 8, 147–150.CrossRefGoogle Scholar
  29. Miller, J. D., & Ewen, M. A. (1997). Toxic effects of deoxynivalenol on ribosomes and tissues of the spring wheat cultivars Frontana and Casavant. Natural Toxins, 5, 234–237.PubMedCrossRefGoogle Scholar
  30. Parry, D. W., Jenkinson, P., & McLeod, L. (1995). Fusarium ear blight (scab) in small grain cereals, a review. Plant Pathology, 44, 207–238.CrossRefGoogle Scholar
  31. Pritsch, C., Muehlbauer, G. J., Bushnell, W. R., Somers, D. A., & Vance, C. P. (2000). Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Molecular Plant-Microbe Interactions, 13, 159–169.PubMedCrossRefGoogle Scholar
  32. Proctor, R. H., Desjardins, A. E., McCormick, S. P., Plattner, R. D., Alexander, N. J., & Brown, D. W. (2002). Genetic analysis of the role of trichothecene and fumonisin mycotoxins in the virulence of Fusarium. European Journal of Plant Pathology, 108, 691–698.CrossRefGoogle Scholar
  33. Schroeder, H. W., & Christensen, J. J. (1963). Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology, 53, 831–818.Google Scholar
  34. Snijders, C. H. (2004). Resistance of wheat to Fusarium infection and trichothecene formation. Toxicology Letter, 153, 37–46.CrossRefGoogle Scholar
  35. Snijders, C. H. A., & Krechting, C. F. (1992). Inhibition of deoxynivalenol translocation and fungal colonization in Fusarium head blight resistant wheat. Canadian Journal Botany, 70, 1570–1576.Google Scholar
  36. Snijders, C. H. A., & Perkowski, J. (1990). Effects of head blight caused by Fusarium culmorum on toxin content and weight of wheat kernels. Phytopathology, 80, 566–570.CrossRefGoogle Scholar
  37. Usleber, E., Märtlbauer, E., Dietrich, R., & Terplan, G. (1991). Direct enzyme-linked immunosorbent assays for the detection of the 8-ketotrichothecene mycotoxins deoxynivalenol, 3-acetyldeoxynivalenol and 15-acetyldeoxynivalenol, in buffer solutions. Journal of Agricultural and Food Chemistry, 39, 2091–2095.CrossRefGoogle Scholar
  38. Van Ginkel, M., Van der Schaar, W., Zhuping, Y., & Rajaram, S. (1996). Inheritance of resistance to scab in two wheat cultivars from Brazil and China. Plant Disease, 80, 863–867.CrossRefGoogle Scholar
  39. Wang, Y. Z., & Miller, J. D. (1988). Effects of Fusarium graminearum metabolites on wheat tissue in relation to fusarium head blight resistance. Journal of Phytopathology, 122, 118–125.Google Scholar
  40. Wanyoike, M. W., Kang, Z., & Buchenauer, H. (2002). Importance of cell wall degrading enzymes produced by Fusarium graminearum during infection of wheat heads. European Journal of Plant Pathology, 108(1), 803–810.Google Scholar
  41. Wessels, J. G. H., & Sietsma, J. H. (1981). Fungal cell walls: A survey. In W. Tanner, & F. A. Loewus (Eds.) Plant carbohydrates II. Extracellular carbohydrates. Encyclopedia of plant physiology, new series vol. 13B (pp. 352–395). Berlin, Germany: Springer Verlag.Google Scholar
  42. Wubben, J., Joosten, M. H. A. J., Van Kan, J. A. L., & De Wit, P. J. G. M. (1992). Subcellular localization of plant chitinases and 1,3-β-gluanases in Cladosporium fulvum (syn. Fulvia fulva)-infected tomato leaves. Physiological and Molecular Plant Pathology, 41, 23–32.CrossRefGoogle Scholar
  43. Zadoks, J. C., Chang, T., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.CrossRefGoogle Scholar
  44. Zhou, W. C., Kolb, F. L., Bai, G. H., Domier, L. L., & Yao, J. B. (2002). Effect of individual Sumai 3 chromosomes on resistance to scab spread within spikes and deoxynivalenol accumulation with kernels in wheat. Hereditas, 137(2), 81–89.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  • Zhensheng Kang
    • 1
    • 3
  • Heinrich Buchenauer
    • 2
  • Lili Huang
    • 1
  • Qingmei Han
    • 1
  • Hongchang Zhang
    • 1
  1. 1.College of Plant Protection and Shaanxi Key Laboratory of Molecular Biology for AgricultureNorthwestern A&F UniversityYanglingPeoples’ Republic of China
  2. 2.Institute of Phytomedicine (360)University HohenheimStuttgartGermany
  3. 3.Plant Protection CollegeNorthwest A&F UniversityYanglingPeoples’ Republic of China

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