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Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions

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Abstract

We used video microscopy techniques as a tool for live examination of the dynamic aspects of plant/fungus interactions. Early, dynamic responses of epidermal midrib cells of leaves from a potato cultivar (Solanum tuberosum L. cv. Datura) carrying resistance gene R1 to Phytophthora infestans (race 1: compatible interaction, race 4: incompatible interaction) were monitored. Similar responses were observed in both types of interaction, ranging from no visible reaction of invaded plant cells to hypersensitive cell death. The overall defense response of each individual cell exhibited a highly dynamic behavior that appeared to be tightly coordinated with the growth of the fungus. Initial localized reactions, including major rearrangements within the cytoplasm, occurred directly at the fungal penetration site, where rapid apposition of autofluorescent material and callose took place. If fungal invasion stopped at this stage, the host cell restored its normal cytoplasmic activity and survived. Hypersensitive cell death occurred only when fungal growth had proceeded to the formation of a clearly identifiable haustorium. In such cases, cytoplasm and nucleus conglomerated around the intracellular fungal structure, followed by a sudden collapse of the whole conglomerate and an instantaneous collapse of the fungal haustorium. Only small quantitative differences between the compatible and incompatible interactions of the two fungal races were observed for these early responses of epidermal cells. In the incompatible interaction, a slightly larger number of epidermal cells responded to fungal attack. More pronounced quantitative differences between compatible and incompatible interactions occurred upon fungal invasion of the mesophyll. These differences in the number of responding cells were not reflected at the level of gene expression: the spatial and temporal activation patterns of two defense-related genes, encoding phenylalanine ammonia-lyase and pathogenesis-related protein 1, were similar in both types of interaction.

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Abbreviations

PAL:

phenylalanine ammonia-lyase

PR1:

pathogenesis-related protein 1

FITC:

fluorescein isothiocyanate

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Authors and Affiliations

  1. Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, D-50829, Köln, Germany

    Sibylle Freytag, Nikolaos Arabatzis, Klaus Hahlbrock & Elmon Schmelzer

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  1. Sibylle Freytag
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  2. Nikolaos Arabatzis
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  3. Klaus Hahlbrock
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  4. Elmon Schmelzer
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Dedicated to Professor Peter Sitte, Freiburg, Germany, on the occasion of his 65th birthday

It is a great pleasure to thank W. Sacks, W. Knogge and D. Scheel, Max-Planck-Institut für Züchtungsforschung, Köln, Germany, for critically reading the manuscript. This work was supported in part by Bundesministerium für Forschung und Technologie and Fonds der chemischen Industrie.

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Freytag, S., Arabatzis, N., Hahlbrock, K. et al. Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta 194, 123–135 (1994). https://doi.org/10.1007/BF00201043

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  • DOI: https://doi.org/10.1007/BF00201043

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