Skip to main content

Structural Characterisation of the Interaction between Triticum aestivum and the Dothideomycete Pathogen Stagonospora nodorum

Abstract

The interaction between Stagonospora nodorum and a susceptible wheat cultivar was investigated using a range of microscopic techniques. Germination of pycnidiospores occurred approximately 3 h after making contact with the leaf surface and was followed by attempted penetration 8–12 h later. Penetration was observed through stomata and also directly through periclinal and anticlinal epidermal cell walls. Penetration down the anticlinal cell walls appeared to occur without a differentiated penetrating structure whilst structures identified as either lateral appressoria or hyphopodia were typically present when penetrating over a periclinal cell wall. Once inside the leaf, the fungus continued to grow for the next 4–5 days colonising all parts of the leaf except the vascular bundles. Only in the later phase of the infection was total host cell collapse apparent. Evidence of polyphenolic compounds was observed. The infection cycle was completed within 7 days as indicated by sporulation on the leaf surface. These results have allowed us to understand how the fungus physically interacts with the leaf and will help the overall understanding of the infection process.

This is a preview of subscription content, access via your institution.

References

  • L Adam SC Somerville (1996) ArticleTitleGenetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana The Plant Journal 9 341–356 Occurrence Handle8919911 Occurrence Handle1:CAS:528:DyaK28Xitl2ltr4%3D Occurrence Handle10.1046/j.1365-313X.1996.09030341.x

    PubMed  CAS  Article  Google Scholar 

  • EA Baker IM Smith (1978) ArticleTitleDevelopment of the susceptible and resistant reactions in wheat on inoculation with Septoria nodourm Transactions of the British Mycological Society 71 475–482 Occurrence Handle10.1016/S0007-1536(78)80076-X

    Article  Google Scholar 

  • JA Bathgate R Loughman (2001) ArticleTitleAcospores are a source of inoculum of Phaeosphaeria nodorum, P. avenaria f sp avenaria and Mycosphaerella graminicola in Western Australia Australasian Plant Pathology 30 317–322 Occurrence Handle10.1071/AP01043

    Article  Google Scholar 

  • O Bethenod JF Bousquet D Laffray P Louguet (1982) ArticleTitleReexamen des modalites d’action de l’ochracine sur la conductance stomatique des feuilles de plantules de ble, Triticum aestivum L cv “ Etoile de Choisy” Agronomie 2 99–101

    Google Scholar 

  • PM Bird JP Ride (1981) ArticleTitleThe resistance of wheat to Septoria nodorum: fungal development in relation to host lignification Physiological Plant Pathology 19 289–299

    Google Scholar 

  • JF Bousquet A Kollmann (1998) ArticleTitleVariation in metabolite production by Septoria nodorum isolates adapted to wheat or to barley Phytopathologische Zeitschrift 146 273–277 Occurrence Handle1:CAS:528:DyaK1cXlsVGqt7c%3D

    CAS  Google Scholar 

  • JP Brennan GM Murray (1998) Economic Importance of Wheat Diseases in Australia NSW Agriculture Wagga Wagga

    Google Scholar 

  • E Bruzzese S Hasan (1983) ArticleTitleA whole leaf clearing and staining technique for host specificity studies of rust fungi Plant Pathology 32 335–338

    Google Scholar 

  • Cunfer BM (1999) Stagonospora and Septoria pathogens of cereals: The infection process. In: van Ginkel M, McNab A and Krupinsky J (eds) Septoria and Stagonospora Diseases of Cereals: A Compilation of Global Research D.F CIMMYT, Mexico.

  • PJGM Wit ParticleDe (1977) ArticleTitleA light and scanning electron microscopic study of infection of tomato plants by virulent and avirulent races of Cladosporium fulvum Netherlands Journal of Plant Pathology 83 109–122 Occurrence Handle10.1007/BF01981556

    Article  Google Scholar 

  • HB Deising S Werner M Wernitz (2000) ArticleTitleThe role of fungal appressoria in plant infection Microbes and Infection 2 1631–1641 Occurrence Handle11113382 Occurrence Handle1:STN:280:DC%2BD3M%2Fps12htg%3D%3D Occurrence Handle10.1016/S1286-4579(00)01319-8

    PubMed  CAS  Article  Google Scholar 

  • MN Douaiher P Halama MC Janex-Favre (2004) ArticleTitleThe ontogeny of Stagonospora nodorum pynidia in culture Sydowia 56 39–50

    Google Scholar 

  • KE Duncan RJ Howard (2000) ArticleTitleCytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola Mycological Research 104 1074–1082 Occurrence Handle10.1017/S0953756299002294

    Article  Google Scholar 

  • RW Emmett DG Parbery (1975) ArticleTitleAppressoria Annual Reviews of Phytopathology 13 147–165 Occurrence Handle10.1146/annurev.py.13.090175.001051

    Article  Google Scholar 

  • S Essad JF Bousquet (1981) ArticleTitleAction de l’ochracine, phytotoxine de Septoria nodorum Berk., sur le cycle mitotique de Triticum aestivum L Agronomie 1 689–694

    Google Scholar 

  • RE Falloon PW Sutherland IC Hallett (1989) ArticleTitleMorphology of Erysiphe pisi on leaves of Pisum sativum Canadian Journal of Botany 67 3410–3416

    Google Scholar 

  • KE Hammond BG Lewis TM Musa (1985) ArticleTitleA systemic pathway in the infection of oilseed rape plants by Leptosphaeria maculans Plant Pathology 34 557–565

    Google Scholar 

  • C Heintz R Blaich (1990) ArticleTitleUltrastructural and histochemical studies on interactions between Vitis vinifera L and Uncinula necator (Schw.) Burr New Phytologist 115 107–117 Occurrence Handle1:CAS:528:DyaK3cXlvVyhtLc%3D Occurrence Handle10.1111/j.1469-8137.1990.tb00928.x

    CAS  Article  Google Scholar 

  • RJ Howard (1997) Breaching the outer barriers – cuticle and cell wall penetration GC Carrol P Tudzynski (Eds) The Mycota V. Plant Relationships Part A Springer Berlin/Heidelberg/New York 43–60

    Google Scholar 

  • JE King RJ Cook SC Melville (1983) ArticleTitleA review of Septoria diseases of wheat and barley Annals of Applied Biology 103 345–373 Occurrence Handle10.1111/j.1744-7348.1983.tb02773.x

    Article  Google Scholar 

  • PE Kolattukudy LM Rogers D Li C-S Hwang CA Flaishman (1995) ArticleTitleSurface signalling in pathogenesis Proceedings of the National Academy of Sciences of the United States of America 92 4080–4087 Occurrence Handle7753774 Occurrence Handle1:CAS:528:DyaK2MXls1altrw%3D Occurrence Handle10.1073/pnas.92.10.4080

    PubMed  CAS  Article  Google Scholar 

  • ZH Liu JD Faris SW Meinhardt S Ali JB Rasmussen TL Friesen (2004a) ArticleTitleGenetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum Phytopathology 94 1056–1060 Occurrence Handle1:CAS:528:DC%2BD2cXovVCjurw%3D

    CAS  Google Scholar 

  • ZH Liu TL Friesen JB Rasmussen S Ali SW Meinhardt JD Faris (2004b) ArticleTitleQuantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat Phytopathology 94 1061–1067 Occurrence Handle1:CAS:528:DC%2BD2cXovVCjur0%3D

    CAS  Google Scholar 

  • K Mendgen M Hahn H Deising (1996) ArticleTitleMorphogenesis and mechanisms of penetration by plant pathogenic fungi Annual Review of Phytopathology 34 367–386 Occurrence Handle15012548 Occurrence Handle1:CAS:528:DyaK28XlsFOhsLg%3D Occurrence Handle10.1146/annurev.phyto.34.1.367

    PubMed  CAS  Article  Google Scholar 

  • NP Money TC Caesar-TonThat B Frederick JM Henson (1998) ArticleTitleMelanin synthesis is associated with changes in hyphopodial turgor, permeability, and wall rigidity in Gaeumannomyces graminis var. graminis Fungal Genetics and Biology 24 240–251 Occurrence Handle9742204 Occurrence Handle1:CAS:528:DyaK1cXmslCitrs%3D Occurrence Handle10.1006/fgbi.1998.1052

    PubMed  CAS  Article  Google Scholar 

  • TP O’Brien ME McCully (1981) The Study of Plant Structure: Principles and Selected Methods Termarcarphi Pty. Ltd Melbourne

    Google Scholar 

  • P O’Reilly MJ Downes (1986) ArticleTitleForm of survival of Septoria nodorum on symptomless winter wheat Transactions of the British Mycological Society 86 381–385 Occurrence Handle10.1016/S0007-1536(86)80181-4

    Article  Google Scholar 

  • E Rodriguez-Galvez K Mendgen (1995) ArticleTitleThe infection process of Fusarium oxysporum in cotton root tips Protoplasma 189 61–72 Occurrence Handle10.1007/BF01280291

    Article  Google Scholar 

  • A Sesma AE Osbourn (2004) ArticleTitleThe rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi Nature 431 582–586 Occurrence Handle15457264 Occurrence Handle1:CAS:528:DC%2BD2cXnvFCntbs%3D Occurrence Handle10.1038/nature02880

    PubMed  CAS  Article  Google Scholar 

  • AC Sexton BJ Howlett (2001) ArticleTitleGreen fluorescent protein as a reporter in the Brassica-Leptosphaeria maculans interaction Physiological and Molecular Plant Pathology 58 13–21 Occurrence Handle1:CAS:528:DC%2BD3MXmtV2luw%3D%3D Occurrence Handle10.1006/pmpp.2000.0307

    CAS  Article  Google Scholar 

  • PJ Shipton WRJ Boyd AA Rosielle BL Shearer (1971) ArticleTitleThe common Septoria diseases of wheat Botanical Review 37 231–262 Occurrence Handle10.1007/BF02858957

    Article  Google Scholar 

  • WA Shipton JF Brown (1962) ArticleTitleA whole-leaf clearing and␣staining technique to demonstrate host-pathogen relationships of wheat stem rust Phytopathology 52 1313–1318

    Google Scholar 

  • PS Solomon RC Lee TJG Wilson RP Oliver (2004a) ArticleTitlePathogenicity of Stagonospora nodorum requires malate synthase Molecular Microbiology 53 1065–1073 Occurrence Handle1:CAS:528:DC%2BD2cXntFOnsbg%3D Occurrence Handle10.1111/j.1365-2958.2004.04178.x

    CAS  Article  Google Scholar 

  • PS Solomon RP Oliver (2004) ArticleTitleFunctional characterisation of glyoxalase I from the fungal wheat pathogen Stagonospora nodorum Current Genetics 46 115–121 Occurrence Handle15205912 Occurrence Handle1:CAS:528:DC%2BD2cXmtVOiurs%3D Occurrence Handle10.1007/s00294-004-0514-8

    PubMed  CAS  Article  Google Scholar 

  • PS Solomon K-C Tan RP Oliver (2005) ArticleTitleMannitol 1-phosphate metabolism is required for sporulation in planta of the wheat pathogen Stagonospora nodorum Molecular Plant-Microbe Interactions 18 110–115 Occurrence Handle15720079 Occurrence Handle1:CAS:528:DC%2BD2MXptFCksA%3D%3D

    PubMed  CAS  Google Scholar 

  • PS Solomon K-C Tan P Sanchez RM Cooper RP Oliver (2004b) ArticleTitleThe disruption of a G alpha subunit sheds new light on the pathogenicity of Stagonospora nodorum on wheat Molecular Plant-Microbe Interactions 17 456–466 Occurrence Handle1:CAS:528:DC%2BD2cXjs1Gks7o%3D

    CAS  Google Scholar 

  • PS Solomon SW Thomas P Spanu RP Oliver (2003) ArticleTitleThe utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection Physiological and Molecular Plant Pathology 63 191–199 Occurrence Handle1:CAS:528:DC%2BD2cXivVCqs74%3D Occurrence Handle10.1016/j.pmpp.2003.12.003

    CAS  Article  Google Scholar 

  • ML Straley AL Scharen (1979) ArticleTitleDevelopment of Septoria nodorum in resistant and susceptible wheat leaves Phytopathology 69 920–921

    Google Scholar 

  • NJ Talbot (2003) ArticleTitleOn the trail of a cereal killer: Exploring the biology of Magnaporthe grisea Annual Review of Microbiology 57 177–202 Occurrence Handle14527276 Occurrence Handle1:CAS:528:DC%2BD3sXptFWmu70%3D Occurrence Handle10.1146/annurev.micro.57.030502.090957

    PubMed  CAS  Article  Google Scholar 

  • E Thines RWS Weber NJ Talbot (2000) ArticleTitleMAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea Plant Cell 12 1703–1718 Occurrence Handle11006342 Occurrence Handle1:CAS:528:DC%2BD3cXnsVylt74%3D Occurrence Handle10.1105/tpc.12.9.1703

    PubMed  CAS  Article  Google Scholar 

  • J Walker (1980) ArticleTitleGaeumannomyces, Linocarpon, Ophiobolus and several other genera of scolecospred ascomycetes and Phialophora conidial states, with a note on hyphopodia Mycotaxon 11 1–129

    Google Scholar 

  • J Walker (1981) Taxonomy of take-all fungi and related genera and species MJC Asher PJ Shipton (Eds) Biology and Control of Take-all Academic Press London 15–74

    Google Scholar 

  • SS Xu TL Friesen A Mujeeb-Kazi (2004) ArticleTitleSeedling resistance to tan spot and Stagonospora nodorum blotch in␣synthetic hexaploid wheats Crop Science 44 2238–2245 Occurrence Handle10.2135/cropsci2004.2238

    Article  Google Scholar 

  • V Zinkernagel F Reiss M Wendland H-C Bartschere (1988) ArticleTitleInfektionsstrukturen von Septoria nodorum in Blattern anfalliger Weizensorten Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 95 169–175

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter S. Solomon.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Solomon, P.S., Wilson, T.J.G., Rybak, K. et al. Structural Characterisation of the Interaction between Triticum aestivum and the Dothideomycete Pathogen Stagonospora nodorum . Eur J Plant Pathol 114, 275–282 (2006). https://doi.org/10.1007/s10658-005-5768-6

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-005-5768-6

Keywords

  • hyphopodia
  • leaf and glume blotch
  • Stagonospora nodorum