Skip to main content
SpringerLink
Log in

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

  • Full Research Paper
  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

FHB:

Fusarium head blight

DON:

deoxynivalenol

TBS:

Tris-buffered saline

HRGP:

hydroxyproline-rich glycoproteins

TEM:

transmission electron microscopy

References

  • Aist, J. R. (1976). Papillae and related wound plugs of plant cells. Annual Review of Phytopathology, 14, 145–163.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bai, G. H., & Shaner, G. (1994). Scab of wheat: Prospects for control. Plant Disease, 78, 760–766.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Desjardins, A. E., & Hohn, T. M. (1997). Mycotoxins in plant pathogenesis. Molecular Plant-Microbe Interactions, 10, 147–152.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kang, Z., & Buchenauer, H. (2000a). Cytology and ultrastructure of the infection of wheat spikes by Fusarium culmorum. Mycological Research, 104, 1083–1093.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • McMullen, M., Jones, R., & Gallenberg, D. (1997). Scab of wheat and barley: A reemerging disease of devastating impact. Plant Disease, 81, 1340–1348.

    Article  Google Scholar 

  • Mesterházy, Á. (1995). Types and components of resistance against Fusarium head blight of wheat. Plant Breeding, 114, 377–386.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Parry, D. W., Jenkinson, P., & McLeod, L. (1995). Fusarium ear blight (scab) in small grain cereals, a review. Plant Pathology, 44, 207–238.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Schroeder, H. W., & Christensen, J. J. (1963). Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology, 53, 831–818.

    Google Scholar 

  • Snijders, C. H. (2004). Resistance of wheat to Fusarium infection and trichothecene formation. Toxicology Letter, 153, 37–46.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Zadoks, J. C., Chang, T., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr. E. Usleber (Institute for Hygiene and Technology, University Munich, Germany), Dr. Ruel (Centre de Recherches sur les Macromolécules Végétales, Université Joseph Fourier, France), Dr. K. Apel (Institut für Pflanzenwissenschaften, Swiss Institute of Technology (ETH), Zürich, Switzerland), and Dr. E. Hood (Department of Bichemistry and Biophysics, Texas A&M University, USA) for kindly supplying antibodies. This study has been financially supported by the National Basic Research Programme of China (No.2006CB101901), Key Research Project, Ministry of Education of China (03158), Nature Science Foundation of China (No.30125031), the Programme for Changjiang Scholars and Innovative Research Teams in Universities, Ministry of Education of China (No.200558) and the 111 Project from Ministry of Education of China (B07049).

Author information

Authors and Affiliations

  1. College of Plant Protection and Shaanxi Key Laboratory of Molecular Biology for Agriculture, Northwestern A&F University, Yangling, Shaanxi, 712100, Peoples’ Republic of China

    Zhensheng Kang, Lili Huang, Qingmei Han & Hongchang Zhang

  2. Institute of Phytomedicine (360), University Hohenheim, Stuttgart, Germany

    Heinrich Buchenauer

  3. Plant Protection College, Northwest A&F University, Yangling, Shaanxi, 712100, Peoples’ Republic of China

    Zhensheng Kang

Authors
  1. Zhensheng Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heinrich Buchenauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lili Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qingmei Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongchang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhensheng Kang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kang, Z., Buchenauer, H., Huang, L. et al. 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 . Eur J Plant Pathol 120, 383–396 (2008). https://doi.org/10.1007/s10658-007-9230-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-007-9230-9

Keywords

Search

Navigation