Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1.
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.
Bos
Jorunn I B
JI
The Sainsbury Laboratory, John Innes Centre, Colney, Norwich NR4 7UH, UK.
Armstrong
Miles R
MR
Gilroy
Eleanor M
EM
Boevink
Petra C
PC
Hein
Ingo
I
Taylor
Rosalind M
RM
Zhendong
Tian
T
Engelhardt
Stefan
S
Vetukuri
Ramesh R
RR
Harrower
Brian
B
Dixelius
Christina
C
Bryan
Glenn
G
Sadanandom
Ari
A
Whisson
Stephen C
SC
Kamoun
Sophien
S
Birch
Paul R J
PR
D020418:Algal Proteins / Q000235:genetics / Q000276:immunology* / Q000378:metabolism*; D004795:Enzyme Stability; D054884:Host-Pathogen Interactions; D008969:Molecular Sequence Data; D055750:Phytophthora infestans / Q000235:genetics / Q000276:immunology* / Q000378:metabolism / Q000472:pathogenicity; D011198:Solanum tuberosum / Q000201:enzymology* / Q000276:immunology* / Q000469:parasitology; D044767:Ubiquitin-Protein Ligases / Q000378:metabolism*; D014774:Virulence
D020418:Algal Proteins; D044767:Ubiquitin-Protein Ligases
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