A translocation signal for delivery of oomycete effector proteins into host plant cells

Stephen C. Whisson, Petra C. Boevink, Lucy Moleleki, Anna O. Avrova, Juan G. Morales, Eleanor M. Gilroy, Miles R. Armstrong, Severine Grouffaud, Pieter van West, Sean Chapman, Ingo Hein, Ian K. Toth, Leighton Pritchard, Paul R. J. Birch

Research output: Contribution to journalArticle

472 Citations (Scopus)

Abstract

Bacterial, oomycete and fungal plant pathogens establish disease by translocation of effector proteins into host cells, where they may directly manipulate host innate immunity. In bacteria, translocation is through the type III secretion system, but analogous processes for effector delivery are uncharacterized in fungi and oomycetes. Here we report functional analyses of two motifs, RXLR and EER, present in translocated oomycete effectors. We use the Phytophthora infestans RXLR-EER-containing protein Avr3a as a reporter for translocation because it triggers RXLR-EER-independent hypersensitive cell death following recognition within plant cells that contain the R3a resistance protein. We show that Avr3a, with or without RXLR-EER motifs, is secreted from P. infestans biotrophic structures called haustoria, demonstrating that these motifs are not required for targeting to haustoria or for secretion. However, following replacement of Avr3a RXLR-EER motifs with alanine residues, singly or in combination, or with residues KMIK-DDK - representing a change that conserves physicochemical properties of the protein - P. infestans fails to deliver Avr3a or an Avr3a-GUS fusion protein into plant cells, demonstrating that these motifs are required for translocation. We show that RXLR-EER-encoding genes are transcriptionally upregulated during infection. Bioinformatic analysis identifies 425 potential genes encoding secreted RXLR-EER class proteins in the P. infestans genome. Identification of this class of proteins provides unparalleled opportunities to determine how oomycetes manipulate hosts to establish infection.

LanguageEnglish
Pages115-118
Number of pages4
JournalNature
Volume450
DOIs
Publication statusPublished - 30 Sep 2007

Fingerprint

Oomycetes
Plant Cells
Phytophthora infestans
Proteins
Protein Transport
Infection
Computational Biology
Innate Immunity
Alanine
Genes
Fungi
Cell Death
Genome
Bacteria

Keywords

  • plant pathogens
  • host cells
  • bacteria
  • oomycete effector proteins

Cite this

Whisson, S. C., Boevink, P. C., Moleleki, L., Avrova, A. O., Morales, J. G., Gilroy, E. M., ... Birch, P. R. J. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450, 115-118. https://doi.org/10.1038/nature06203
Whisson, Stephen C. ; Boevink, Petra C. ; Moleleki, Lucy ; Avrova, Anna O. ; Morales, Juan G. ; Gilroy, Eleanor M. ; Armstrong, Miles R. ; Grouffaud, Severine ; van West, Pieter ; Chapman, Sean ; Hein, Ingo ; Toth, Ian K. ; Pritchard, Leighton ; Birch, Paul R. J. / A translocation signal for delivery of oomycete effector proteins into host plant cells. In: Nature. 2007 ; Vol. 450. pp. 115-118.
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Whisson, SC, Boevink, PC, Moleleki, L, Avrova, AO, Morales, JG, Gilroy, EM, Armstrong, MR, Grouffaud, S, van West, P, Chapman, S, Hein, I, Toth, IK, Pritchard, L & Birch, PRJ 2007, 'A translocation signal for delivery of oomycete effector proteins into host plant cells' Nature, vol. 450, pp. 115-118. https://doi.org/10.1038/nature06203

A translocation signal for delivery of oomycete effector proteins into host plant cells. / Whisson, Stephen C.; Boevink, Petra C.; Moleleki, Lucy; Avrova, Anna O.; Morales, Juan G.; Gilroy, Eleanor M.; Armstrong, Miles R.; Grouffaud, Severine; van West, Pieter; Chapman, Sean; Hein, Ingo; Toth, Ian K.; Pritchard, Leighton; Birch, Paul R. J.

In: Nature, Vol. 450, 30.09.2007, p. 115-118.

Research output: Contribution to journalArticle

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T1 - A translocation signal for delivery of oomycete effector proteins into host plant cells

AU - Whisson, Stephen C.

AU - Boevink, Petra C.

AU - Moleleki, Lucy

AU - Avrova, Anna O.

AU - Morales, Juan G.

AU - Gilroy, Eleanor M.

AU - Armstrong, Miles R.

AU - Grouffaud, Severine

AU - van West, Pieter

AU - Chapman, Sean

AU - Hein, Ingo

AU - Toth, Ian K.

AU - Pritchard, Leighton

AU - Birch, Paul R. J.

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Y1 - 2007/9/30

N2 - Bacterial, oomycete and fungal plant pathogens establish disease by translocation of effector proteins into host cells, where they may directly manipulate host innate immunity. In bacteria, translocation is through the type III secretion system, but analogous processes for effector delivery are uncharacterized in fungi and oomycetes. Here we report functional analyses of two motifs, RXLR and EER, present in translocated oomycete effectors. We use the Phytophthora infestans RXLR-EER-containing protein Avr3a as a reporter for translocation because it triggers RXLR-EER-independent hypersensitive cell death following recognition within plant cells that contain the R3a resistance protein. We show that Avr3a, with or without RXLR-EER motifs, is secreted from P. infestans biotrophic structures called haustoria, demonstrating that these motifs are not required for targeting to haustoria or for secretion. However, following replacement of Avr3a RXLR-EER motifs with alanine residues, singly or in combination, or with residues KMIK-DDK - representing a change that conserves physicochemical properties of the protein - P. infestans fails to deliver Avr3a or an Avr3a-GUS fusion protein into plant cells, demonstrating that these motifs are required for translocation. We show that RXLR-EER-encoding genes are transcriptionally upregulated during infection. Bioinformatic analysis identifies 425 potential genes encoding secreted RXLR-EER class proteins in the P. infestans genome. Identification of this class of proteins provides unparalleled opportunities to determine how oomycetes manipulate hosts to establish infection.

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KW - plant pathogens

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KW - bacteria

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Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM et al. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature. 2007 Sep 30;450:115-118. https://doi.org/10.1038/nature06203