Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1

Jorunn Bos, Miles R. Armstrong, Eleanor M. Gilroy, Petra C. Boevink, Ingo Hein, Rosalind M. Taylor, Zhendong Tian, Stefan Engelhardt, Ramesh R. Vetukuri, Brian Harrower, Christina Dixelius, Glenn Bryan, Ari Sadanandom, Stephen C. Whisson, Sophien Kamoun (Lead / Corresponding author), Paul R. J. Birch (Lead / Corresponding author)

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    235 Citations (Scopus)

    Abstract

    Fungal and oomycete plant pathogens translocate effector proteins into host cells to establish infection. However, virulence targets and modes of action of their effectors are unknown. Effector AVR3a from potato blight pathogen Phytophthora infestans is translocated into host cells and occurs in two forms: AVR3a(KI), which is detected by potato resistance protein R3a, strongly suppresses infestin 1 (INF1)-triggered cell death (ICD), whereas AVR3a(EM), which evades recognition by R3a, weakly suppresses host ICD. Here we show that AVR3a interacts with and stabilizes host U-box E3 ligase CMPG1, which is required for ICD. In contrast, AVR3a(KI/Y147del), a mutant with a deleted C-terminal tyrosine residue that fails to suppress ICD, cannot interact with or stabilize CMPG1. CMPG1 is stabilized by the inhibitors MG132 and epoxomicin, indicating that it is degraded by the 26S proteasome. CMPG1 is degraded during ICD. However, it is stabilized by mutations in the U-box that prevent its E3 ligase activity. In stabilizing CMPG1, AVR3a thus modifies its normal activity. Remarkably, given the potential for hundreds of effector genes in the P. infestans genome, silencing Avr3a compromises P. infestans pathogenicity, suggesting that AVR3a is essential for virulence. Interestingly, Avr3a silencing can be complemented by in planta expression of Avr3a(KI) or Avr3a(EM) but not the Avr3a(KI/Y147del) mutant. Our data provide genetic evidence that AVR3a is an essential virulence factor that targets and stabilizes the plant E3 ligase CMPG1, potentially to prevent host cell death during the biotrophic phase of infection.

    Original languageEnglish
    Pages (from-to)9909-9914
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume107
    Issue number21
    DOIs
    Publication statusPublished - 25 May 2010

    Keywords

    • oomycete
    • plant disease resistance
    • programmed cell death
    • ubiquitin
    • CATHEPSIN-B
    • CELL-DEATH
    • HYPERSENSITIVE RESPONSE
    • NICOTIANA-BENTHAMIANA
    • FUNCTIONAL REDUNDANCY
    • PATHOGEN EFFECTORS
    • SIGNALING PATHWAYS
    • DISEASE RESISTANCE
    • GENE FAMILY
    • PROTEIN

    Cite this

    Bos, J., Armstrong, M. R., Gilroy, E. M., Boevink, P. C., Hein, I., Taylor, R. M., Tian, Z., Engelhardt, S., Vetukuri, R. R., Harrower, B., Dixelius, C., Bryan, G., Sadanandom, A., Whisson, S. C., Kamoun, S., & Birch, P. R. J. (2010). Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proceedings of the National Academy of Sciences of the United States of America, 107(21), 9909-9914. https://doi.org/10.1073/pnas.0914408107