Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato

Laura J. Grenville-Briggs, Victoria L. Anderson, Johanna Fugelstad, Anna O. Avrova, Jamel Bouzenzana, Alison Williams, Stephan Wawra, Stephen C. Whisson, Paul R. J. Birch, Vincent Bulone, Pieter van West

Research output: Contribution to journalArticle

83 Citations (Scopus)

Abstract

Cellulose, the important structural compound of cell walls, provides strength and rigidity to cells of numerous organisms. Here, we functionally characterize four cellulose synthase genes (CesA) in the oomycete plant pathogen Phytophthora infestans, the causal agent of potato (Solanum tuberosum) late blight. Three members of this new protein family contain Pleckstrin homology domains and form a distinct phylogenetic group most closely related to the cellulose synthases of cyanobacteria. Expression of all four genes is coordinately upregulated during pre- and early infection stages of potato. Inhibition of cellulose synthesis by 2,6-dichlorobenzonitrile leads to a dramatic reduction in the number of normal germ tubes with appressoria, severe disruption of the cell wall in the preinfection structures, and a complete loss of pathogenicity. Silencing of the entire gene family in P. infestans with RNA interference leads to a similar disruption of the cell wall surrounding appressoria and an inability to form typical functional appressoria. In addition, the cellulose content of the cell walls of the silenced lines is >50% lower than in the walls of the nonsilenced lines. Our data demonstrate that the isolated genes are involved in cellulose biosynthesis and that cellulose synthesis is essential for infection by P. infestans.

Original languageEnglish
Pages (from-to)720-738
Number of pages19
JournalThe Plant Cell
Volume20
Issue number3
DOIs
Publication statusPublished - Mar 2008

Keywords

  • fungus saprolegnia-monoica
  • V chitin synthase
  • cell-walls
  • sequence alignment
  • plant interactions
  • in-vitro
  • biosynthesis
  • oomycete
  • gene
  • enzymes

Cite this

Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. / Grenville-Briggs, Laura J.; Anderson, Victoria L.; Fugelstad, Johanna; Avrova, Anna O.; Bouzenzana, Jamel; Williams, Alison; Wawra, Stephan; Whisson, Stephen C.; Birch, Paul R. J.; Bulone, Vincent; van West, Pieter.

In: The Plant Cell, Vol. 20, No. 3, 03.2008, p. 720-738.

Research output: Contribution to journalArticle

Grenville-Briggs, LJ, Anderson, VL, Fugelstad, J, Avrova, AO, Bouzenzana, J, Williams, A, Wawra, S, Whisson, SC, Birch, PRJ, Bulone, V & van West, P 2008, 'Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato', The Plant Cell, vol. 20, no. 3, pp. 720-738. https://doi.org/10.1105/tpc.107.052043
Grenville-Briggs, Laura J. ; Anderson, Victoria L. ; Fugelstad, Johanna ; Avrova, Anna O. ; Bouzenzana, Jamel ; Williams, Alison ; Wawra, Stephan ; Whisson, Stephen C. ; Birch, Paul R. J. ; Bulone, Vincent ; van West, Pieter. / Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. In: The Plant Cell. 2008 ; Vol. 20, No. 3. pp. 720-738.
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abstract = "Cellulose, the important structural compound of cell walls, provides strength and rigidity to cells of numerous organisms. Here, we functionally characterize four cellulose synthase genes (CesA) in the oomycete plant pathogen Phytophthora infestans, the causal agent of potato (Solanum tuberosum) late blight. Three members of this new protein family contain Pleckstrin homology domains and form a distinct phylogenetic group most closely related to the cellulose synthases of cyanobacteria. Expression of all four genes is coordinately upregulated during pre- and early infection stages of potato. Inhibition of cellulose synthesis by 2,6-dichlorobenzonitrile leads to a dramatic reduction in the number of normal germ tubes with appressoria, severe disruption of the cell wall in the preinfection structures, and a complete loss of pathogenicity. Silencing of the entire gene family in P. infestans with RNA interference leads to a similar disruption of the cell wall surrounding appressoria and an inability to form typical functional appressoria. In addition, the cellulose content of the cell walls of the silenced lines is >50{\%} lower than in the walls of the nonsilenced lines. Our data demonstrate that the isolated genes are involved in cellulose biosynthesis and that cellulose synthesis is essential for infection by P. infestans.",
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AU - Avrova, Anna O.

AU - Bouzenzana, Jamel

AU - Williams, Alison

AU - Wawra, Stephan

AU - Whisson, Stephen C.

AU - Birch, Paul R. J.

AU - Bulone, Vincent

AU - van West, Pieter

N1 - On authors website and institutional repository State that pre-print is under review/accepted Remove pre-print on publication and replace with toll-free link to publisher version If funding agency rules apply, authors may post articles in PubMed Central after a 12 month embargo Must link to publisher version Publisher's version/PDF must be used, but publisher's toll-free option preferred

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N2 - Cellulose, the important structural compound of cell walls, provides strength and rigidity to cells of numerous organisms. Here, we functionally characterize four cellulose synthase genes (CesA) in the oomycete plant pathogen Phytophthora infestans, the causal agent of potato (Solanum tuberosum) late blight. Three members of this new protein family contain Pleckstrin homology domains and form a distinct phylogenetic group most closely related to the cellulose synthases of cyanobacteria. Expression of all four genes is coordinately upregulated during pre- and early infection stages of potato. Inhibition of cellulose synthesis by 2,6-dichlorobenzonitrile leads to a dramatic reduction in the number of normal germ tubes with appressoria, severe disruption of the cell wall in the preinfection structures, and a complete loss of pathogenicity. Silencing of the entire gene family in P. infestans with RNA interference leads to a similar disruption of the cell wall surrounding appressoria and an inability to form typical functional appressoria. In addition, the cellulose content of the cell walls of the silenced lines is >50% lower than in the walls of the nonsilenced lines. Our data demonstrate that the isolated genes are involved in cellulose biosynthesis and that cellulose synthesis is essential for infection by P. infestans.

AB - Cellulose, the important structural compound of cell walls, provides strength and rigidity to cells of numerous organisms. Here, we functionally characterize four cellulose synthase genes (CesA) in the oomycete plant pathogen Phytophthora infestans, the causal agent of potato (Solanum tuberosum) late blight. Three members of this new protein family contain Pleckstrin homology domains and form a distinct phylogenetic group most closely related to the cellulose synthases of cyanobacteria. Expression of all four genes is coordinately upregulated during pre- and early infection stages of potato. Inhibition of cellulose synthesis by 2,6-dichlorobenzonitrile leads to a dramatic reduction in the number of normal germ tubes with appressoria, severe disruption of the cell wall in the preinfection structures, and a complete loss of pathogenicity. Silencing of the entire gene family in P. infestans with RNA interference leads to a similar disruption of the cell wall surrounding appressoria and an inability to form typical functional appressoria. In addition, the cellulose content of the cell walls of the silenced lines is >50% lower than in the walls of the nonsilenced lines. Our data demonstrate that the isolated genes are involved in cellulose biosynthesis and that cellulose synthesis is essential for infection by P. infestans.

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KW - plant interactions

KW - in-vitro

KW - biosynthesis

KW - oomycete

KW - gene

KW - enzymes

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