A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato

Anna O. Avrova, Petra C. Boevink, Vanessa Young, Laura J. Grenville-Briggs, Pieter van West, Paul R. J. Birch, Stephen C. Whisson

Research output: Contribution to journalArticle

48 Citations (Scopus)

Abstract

Phytophthora infestans causes late-blight, a devastating and re-emerging disease of potato crops. During the early stages of infection, P. infestans differentiates infection-specific structures such as appressoria for host epidermal cell penetration, followed by infection vesicles, and haustoria to establish a biotrophic phase of interaction. Here we report the cloning, from a suppression subtractive hybridization library, of a P. infestans gene called Pihmp1 encoding a putative glycosylated protein with four closely spaced trans-membrane helices. Pihmp1 expression is upregulated in germinating cysts and in germinating cysts with appressoria, and significantly upregulated throughout infection of potato. Transient gene silencing of Pihmp1 led to loss of pathogenicity and indicated involvement of this gene in the penetration and early infection processes of P. infestans. P. infestans transformants expressing a Pihmp1::monomeric red fluorescent protein (mRFP) fusion demonstrated that Pihmp1 was translated in germinating sporangia, germinating cysts and appressoria, accumulated in the appressorium, and was located at the haustorial membrane during infection. Furthermore, we discovered that haustorial structures are formed over a 3 h period, maturing for up to 12 h, and that their formation is initiated only at sites on the surface of intercellular hyphae where Pihmp1::mRFP is localized. We propose that Pihmp1 is an integral membrane protein that provides physical stability to the plasma membrane of P. infestans infection structures. We have provided the first evidence that the surface of oomycete haustoria possess proteins specific to these biotrophic structures, and that formation of biotrophic structures (infection vesicles and haustoria) is essential to successful host colonization by P. infestans.

Original languageEnglish
Pages (from-to)2271-2284
Number of pages14
JournalCellular Microbiology
Volume10
Issue number11
Early online date15 Jul 2008
DOIs
Publication statusPublished - Nov 2008

Keywords

  • fungus uromyces-fabae
  • host-plant cells
  • pathogen phytophithora
  • ultrastructural characterization
  • appressorium formation
  • functional expression
  • arabidopsis-thaliana
  • effector proteins
  • zoospore motility
  • gene family

Cite this

Avrova, A. O., Boevink, P. C., Young, V., Grenville-Briggs, L. J., van West, P., Birch, P. R. J., & Whisson, S. C. (2008). A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cellular Microbiology, 10(11), 2271-2284. https://doi.org/10.1111/j.1462-5822.2008.01206.x

A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. / Avrova, Anna O.; Boevink, Petra C.; Young, Vanessa; Grenville-Briggs, Laura J.; van West, Pieter; Birch, Paul R. J.; Whisson, Stephen C.

In: Cellular Microbiology, Vol. 10, No. 11, 11.2008, p. 2271-2284.

Research output: Contribution to journalArticle

Avrova, AO, Boevink, PC, Young, V, Grenville-Briggs, LJ, van West, P, Birch, PRJ & Whisson, SC 2008, 'A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato', Cellular Microbiology, vol. 10, no. 11, pp. 2271-2284. https://doi.org/10.1111/j.1462-5822.2008.01206.x
Avrova, Anna O. ; Boevink, Petra C. ; Young, Vanessa ; Grenville-Briggs, Laura J. ; van West, Pieter ; Birch, Paul R. J. ; Whisson, Stephen C. / A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. In: Cellular Microbiology. 2008 ; Vol. 10, No. 11. pp. 2271-2284.
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abstract = "Phytophthora infestans causes late-blight, a devastating and re-emerging disease of potato crops. During the early stages of infection, P. infestans differentiates infection-specific structures such as appressoria for host epidermal cell penetration, followed by infection vesicles, and haustoria to establish a biotrophic phase of interaction. Here we report the cloning, from a suppression subtractive hybridization library, of a P. infestans gene called Pihmp1 encoding a putative glycosylated protein with four closely spaced trans-membrane helices. Pihmp1 expression is upregulated in germinating cysts and in germinating cysts with appressoria, and significantly upregulated throughout infection of potato. Transient gene silencing of Pihmp1 led to loss of pathogenicity and indicated involvement of this gene in the penetration and early infection processes of P. infestans. P. infestans transformants expressing a Pihmp1::monomeric red fluorescent protein (mRFP) fusion demonstrated that Pihmp1 was translated in germinating sporangia, germinating cysts and appressoria, accumulated in the appressorium, and was located at the haustorial membrane during infection. Furthermore, we discovered that haustorial structures are formed over a 3 h period, maturing for up to 12 h, and that their formation is initiated only at sites on the surface of intercellular hyphae where Pihmp1::mRFP is localized. We propose that Pihmp1 is an integral membrane protein that provides physical stability to the plasma membrane of P. infestans infection structures. We have provided the first evidence that the surface of oomycete haustoria possess proteins specific to these biotrophic structures, and that formation of biotrophic structures (infection vesicles and haustoria) is essential to successful host colonization by P. infestans.",
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AB - Phytophthora infestans causes late-blight, a devastating and re-emerging disease of potato crops. During the early stages of infection, P. infestans differentiates infection-specific structures such as appressoria for host epidermal cell penetration, followed by infection vesicles, and haustoria to establish a biotrophic phase of interaction. Here we report the cloning, from a suppression subtractive hybridization library, of a P. infestans gene called Pihmp1 encoding a putative glycosylated protein with four closely spaced trans-membrane helices. Pihmp1 expression is upregulated in germinating cysts and in germinating cysts with appressoria, and significantly upregulated throughout infection of potato. Transient gene silencing of Pihmp1 led to loss of pathogenicity and indicated involvement of this gene in the penetration and early infection processes of P. infestans. P. infestans transformants expressing a Pihmp1::monomeric red fluorescent protein (mRFP) fusion demonstrated that Pihmp1 was translated in germinating sporangia, germinating cysts and appressoria, accumulated in the appressorium, and was located at the haustorial membrane during infection. Furthermore, we discovered that haustorial structures are formed over a 3 h period, maturing for up to 12 h, and that their formation is initiated only at sites on the surface of intercellular hyphae where Pihmp1::mRFP is localized. We propose that Pihmp1 is an integral membrane protein that provides physical stability to the plasma membrane of P. infestans infection structures. We have provided the first evidence that the surface of oomycete haustoria possess proteins specific to these biotrophic structures, and that formation of biotrophic structures (infection vesicles and haustoria) is essential to successful host colonization by P. infestans.

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KW - functional expression

KW - arabidopsis-thaliana

KW - effector proteins

KW - zoospore motility

KW - gene family

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