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Ultrastructural characterisation of the host–pathogen interface in white blister-infected Arabidopsis leaves

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Abstract

In this study transmission electron microscopy (TEM) was used to examine details of the host–pathogen interface in Arabidopsis thaliana cotyledons infected by Albugo candida, causal agent of white blister. After successful entry through stomatal pores, the pathogen developed a substomatal vesicle and subsequently produced intercellular hyphae. TEM observations revealed that coenocytic intercellular hyphae ramified and spread intercellularly throughout the host tissue forming several haustoria in host mesophyll cells. Intracellular haustoria were spherical and 4.5 μm in diameter. Each haustorium was connected to intercellular hyphae by a narrow, slender haustorium neck. The cytoplasm of the haustorium included the organelles characteristic of the pathogen. No obvious response was observed in host cells following formation of haustoria. Most of the mesophyll cells contained normal haustoria and the host cytoplasm displayed a high degree of structural integrity. Absence of host cell wall alteration and cell death in penetrated host cells suggest that the pathogen exerts considerable control over basic cellular processes and in this respect, response to this biotrophic Oomycete differs considerably from responses to other pathogens such as necrotrophs. Modification of the host plasma membrane (PM) along the cell wall and around the haustoria, was detected by applying the periodic acid-chromic acid-phosphotungstic acid (PACP) staining technique. After staining with PACP, the host PM was found to be intensely electron dense where it was adjacent to the host cell wall and the distal region of the haustorial neck. By contrast, the extrahaustorial membrane, where the host PM surrounded the haustorium, was consistently very lightly stained.

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References

  • B Kunkel (1996) ArticleTitleA useful weed put to work: genetic analysis of disease resistance in Arabidopsis thaliana Trends Genet 2 64–69

    Google Scholar 

  • EB Holub JL Beynon (1997) ArticleTitleSymbiology of mouse ear cress ( Arabidopsis thaliana) and oomycetes. Adv Bot Res 24 228–273

    Google Scholar 

  • DE Harder (1991) Chong J. Rust haustoria K Mendgen DE Lesemann (Eds) Electron microscopy of plant pathogen Springer Verlag Berlin 235–250

    Google Scholar 

  • JR Green J Mackie AM Roberts JA Callow (1992) Molecular differentiation and development of the host–parasite interface in powdery mildew of pea JA Callow JR Green (Eds) Perspectives in plant cell recognition Cambridge University Press Cambridge 193–212

    Google Scholar 

  • MC Heath D Skalamera (1997) ArticleTitleCellular interactions between plants and biotrophic fungal parasites. Adv Bot Res 24 195–225

    Google Scholar 

  • PTN Spencer-Phillips (1997) ArticleTitleFunction of fungal haustoria in epiphytic and endophytic infections. Adv Bot Res 24 309–333

    Google Scholar 

  • K Mendgen C Struck RT Voegele M Hahn (2000) ArticleTitleBiotrophy and rust haustoria Physiol Mol Plant Pathol 56 141–145 Occurrence Handle10.1006/pmpp.2000.0264

    Article  Google Scholar 

  • RT Voegele C Struck M Hahn K Mendgen (2001) ArticleTitleThe role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae Proc Natl Acad Sci 98 8133–8138 Occurrence Handle10.1073/pnas.131186798 Occurrence Handle11390980

    Article  PubMed  Google Scholar 

  • EB Holub E Brose M Tör C Clay IR Crute JL Beynon (1995) ArticleTitlePhenotypic and genotypic variation in the interaction between Arabidopsis thaliana and Albugo candida Mol Plant–Microbe Interact 8 916–928 Occurrence Handle8664502

    PubMed  Google Scholar 

  • EM Soylu S Soylu (2003) ArticleTitleLight and electron microscopy of the compatible interaction between Arabidopsis and the downy mildew pathogen Peronospora parasitica J Phytopathol 151 300–306 Occurrence Handle10.1046/j.1439-0434.2003.00723.x

    Article  Google Scholar 

  • S Soylu M Keshavarzi I Brown JW. Mansfield (2003) ArticleTitleUltrastructural characterisation of interactions between Arabidopsis thaliana and Albugo candida Physiol Mol Plant Pathol 2003; 63 201–211

    Google Scholar 

  • CS Bestwick MH Bennett JW Mansfield (1995) ArticleTitleHrp mutant of Pseudomonas syringae pv. phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol 108 503–516 Occurrence Handle12228488

    PubMed  Google Scholar 

  • JC Roland CA Lembi DJ Morrè (1972) ArticleTitlePhosphotungstic acid-chromic acid as a selective electron-dense stain for plasma membranes of plant cells Stain Technol 47 195–200 Occurrence Handle4113996

    PubMed  Google Scholar 

  • MD Coffey (1975) ArticleTitleUltrastructural features of the haustorial apparatus of the white blister fungus Albugo candida Can J Bot 53 1285–1299

    Google Scholar 

  • JD Berlin CC Bowen (1964) ArticleTitleThe host-parasite interface of Albugo candida on Raphanus sativus Am J Bot 51 445–452

    Google Scholar 

  • AM Woods JL Gay (1983) ArticleTitleEvidence for a neckband delimiting structural and physiological regions of the host plasma membrane associated with haustoria of Albugo candida Physiol Plant Pathol 23 73–88

    Google Scholar 

  • EL Hickey MD Coffey (1977) ArticleTitleA fine-structural study of the pea downy mildew fungus Peronospora pisi in its host Pisum sativum Can J Bot 55 2845–2858

    Google Scholar 

  • Y Cohen H Eyal J Hanania Z Malik (1989) ArticleTitleUltrastructure of Pseudoperonospora cubensis in muskmelon genotype susceptible and resistant to downy mildew Physiol Mol Plant Pathol 34 27–40 Occurrence Handle10.1016/0885-5765(89)90014-3

    Article  Google Scholar 

  • MD Coffey (1976) ArticleTitleFlax rust resistance involving the K gene: An ultrastructural survey. Can J Bot 54 1443–1457

    Google Scholar 

  • ZAM Baka (2002) ArticleTitleUltrastructure of intercellular hypha and haustorium of the rust fungus, Uromyces euphorbiae Mycopathologia 156 215–221 Occurrence Handle12749586

    PubMed  Google Scholar 

  • Y Cohen H Eyal J Hanania (1990) ArticleTitleUltrastructure, autofluorescence, callose deposition and lignification in susceptible and resistant muskmelon leaves infected with the powdery mildew fungus Sphaerotheca fuliginea Physiol Mol Plant Pathol 36 191–204 Occurrence Handle10.1016/0885-5765(90)90025-S

    Article  Google Scholar 

  • RD Pares AD Greenwood (1981) ArticleTitleUltrastructure of Pseudoperonospora humuli mycelium. New Phytol 89 289–294

    Google Scholar 

  • HR Hohl E Suter (1976) ArticleTitleHost-parasite interfaces in a resistant and susceptible cultivar of Solanum tuberosum inoculated with Phytophthora infestans: leaf tissue Can J Bot 54 1956–1970

    Google Scholar 

  • JA. Sargent (1981) The fine structure of the downy mildews DM Spencer (Eds) The downy mildews Academic Press London 183–236

    Google Scholar 

  • AM Woods F Didehvar JL Gay JW Mansfield (1988) ArticleTitleModification of the host plasmalemma in haustorial infections of Lactuca sativa by Bremia lactucae Physiol Mol Plant Pathol 33 299–310 Occurrence Handle10.1016/0885-5765(88)90030-6

    Article  Google Scholar 

  • K Enkerli MG Hahn CW Mims (1997) ArticleTitleUltrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic Oomycete Phytophthora sojae Can J Bot 75 1493–1508

    Google Scholar 

  • MC Heath IB Heath (1971) ArticleTitleUltrastructure of an immune and a susceptible reaction of cowpea leaves to rust infection. Physiol Plant Pathol 1 277–287

    Google Scholar 

  • MD Coffey F Allen (1983) ArticleTitleA quantitative histochemical and ultrastructural analysis of interactions between the flax rust and near-isogenic host lines varying in their degree of incompatibility Can J Bot 61 1831–1850

    Google Scholar 

  • AM Woods JL Gay (1987) ArticleTitleThe interface between haustoria of Puccinia poarum (monokaryon) and Tussilago farfara Physiol Mol Plant Pathol 33 299–310 Occurrence Handle10.1016/0885-5765(88)90030-6

    Article  Google Scholar 

  • NV Hardwick AD Greenwood RKS Wood (1971) ArticleTitleThe fine structure of the haustorium of Uromyces appendiculatus in Phaseolus vulgaris. Can J Bot 49 383–390

    Google Scholar 

  • MC Heath (1976) ArticleTitleUltrastructural and functional similarity of the haustorial neckband of rust fungi and the Casparian strip of vascular plants. Can J Bot 54 2484–2489

    Google Scholar 

  • MD Coffey (1983) ArticleTitleCytochemical specialisation at the haustorial interface of a biotrophic fungal parasite, Albugo candida Can J Bot 61 2004–2014

    Google Scholar 

  • MC Heath FHE Allen (1985) ArticleTitleMorphology, element composition, and response to acids and oxidizing agents, of the haustorial neckband of Uromyces phaseoli var vignae. Can J Bot 63 463–473

    Google Scholar 

  • F Gil JL Gay (1977) ArticleTitleUltrastructural and physiological properties of the host interfacial components of haustoria of Erysiphe pisi in vitro and in vivo Physiol Plant Pathol 10 1–12

    Google Scholar 

  • EL Hickey MD Coffey (1978) ArticleTitleA cytochemical investigation of the host-parasite interface in Pisum sativum infected by the downy mildew fungus Peronospora pisi Protoplasma 97 201–220 Occurrence Handle10.1007/BF01276694

    Article  Google Scholar 

  • DE Harder R Rohringer DJ Samborski WK Kim J Chong (1978) ArticleTitleElectron microscopy of susceptible and near-isogenic sr6/Sr6 lines of wheat infected by Puccinia graminis tritici I. The host–pathogen interface in the compatible (sr6/P6) interaction. Can J Bot 56 2955–2966

    Google Scholar 

  • AM Roberts AJ Mackie V Hathaway JA Callow JR Green (1993) ArticleTitleMolecular differentiation in the extrahaustorial membrane of pea powdery mildew haustoria at early and late stages of development Physiol Mol Plant Pathol 43 147–160 Occurrence Handle10.1006/pmpp.1993.1047

    Article  Google Scholar 

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  1. Department of Plant Protection, Faculty of Agriculture, University of Mustafa Kemal, 31034, Antakya, Hatay, Turkey

    Soner Soylu

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  1. Soner Soylu
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Correspondence to Soner Soylu.

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Soylu, S. Ultrastructural characterisation of the host–pathogen interface in white blister-infected Arabidopsis leaves. Mycopathologia 158, 457–464 (2004). https://doi.org/10.1007/s11046-004-2453-9

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  • DOI: https://doi.org/10.1007/s11046-004-2453-9

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