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PMID:23071821

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Citation

Love, AJ, Geri, C, Laird, J, Carr, C, Yun, BW, Loake, GJ, Tada, Y, Sadanandom, A and Milner, JJ (2012) Cauliflower mosaic virus Protein P6 Inhibits Signaling Responses to Salicylic Acid and Regulates Innate Immunity. PLoS ONE 7:e47535

Abstract

Cauliflower mosaic virus (CaMV) encodes a multifunctional protein P6 that is required for translation of the 35S RNA and also acts as a suppressor of RNA silencing. Here we demonstrate that P6 additionally acts as a pathogenicity effector of an unique and novel type, modifying NPR1 (a key regulator of salicylic acid (SA)- and jasmonic acid (JA)-dependent signaling) and inhibiting SA-dependent defence responses We find that that transgene-mediated expression of P6 in Arabidopsis and transient expression in Nicotiana benthamiana has profound effects on defence signaling, suppressing expression of representative SA-responsive genes and increasing expression of representative JA-responsive genes. Relative to wild-type Arabidopsis P6-expressing transgenics had greatly reduced expression of PR-1 following SA-treatment, infection by CaMV or inoculation with an avirulent bacterial pathogen Pseudomonas syringae pv tomato (Pst). Similarly transient expression in Nicotiana benthamiana of P6 (including a mutant form defective in translational transactivation activity) suppressed PR-1a transcript accumulation in response to Agrobacterium infiltration and following SA-treatment. As well as suppressing the expression of representative SA-regulated genes, P6-transgenic Arabidopsis showed greatly enhanced susceptibility to both virulent and avirulent Pst (titres elevated 10 to 30-fold compared to non-transgenic controls) but reduced susceptibility to the necrotrophic fungus Botrytis cinerea. Necrosis following SA-treatment or inoculation with avirulent Pst was reduced and delayed in P6-transgenics. NPR1 an important regulator of SA/JA crosstalk, was more highly expressed in the presence of P6 and introduction of the P6 transgene into a transgenic line expressing an NPR1:GFP fusion resulted in greatly increased fluorescence in nuclei even in the absence of SA. Thus in the presence of P6 an inactive form of NPR1 is mislocalized in the nucleus even in uninduced plants. These results demonstrate that P6 is a new type of pathogenicity effector protein that enhances susceptibility to biotrophic pathogens by suppressing SA- but enhancing JA-signaling responses.

Links

PubMed Online version:10.1371/journal.pone.0047535

Keywords


Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

9VIRU:Q3HM11

GO:0019050: suppression by virus of host apoptotic process

ECO:0000315:

P

Figure 3 depicts necrosis in leaves not expressing the viral P6 protein.

complete
CACAO 5512

9VIRU:Q3HM11

GO:0009753: response to jasmonic acid stimulus

ECO:0000315:

P

Figure 4 shows there are higher levels of JA-responsive gene transcripts after JA is introduced.

complete
CACAO 5701

9VIRU:Q3HM11

GO:0010941: regulation of cell death

ECO:0000315:

P

Figure 3 shows leaves not expressing the viral P6 protein have necrosis. So the viral P6 protein plays a role in regulation of cell death.

complete
CACAO 5699

9VIRU:Q3HM11

GO:0071446: cellular response to salicylic acid stimulus

ECO:0000315:

P

Figure 2 shows there is a reduction of SA-responsive gene transcripts after introduction of SA.

complete
CACAO 5704

9VIRU:Q3HM11

GO:0043066: negative regulation of apoptotic process

ECO:0000315:

P

Figure 3 shows leaves not expressing the viral P6 protein have necrosis.

complete
CACAO 5696

9VIRU:Q3HM11

GO:0019056: modulation by virus of host transcription

ECO:0000315:

P

Figure 7B shows that plants that are transgenic for P6 have altered transcription, as measured by qPCR.

complete
CACAO 5677

9VIRU:Q3HM11

GO:0034504: suppression by virus of host DNA-dependent transcription

ECO:0000315:

P

Figure 7D demonstrates nuclear localization of NPR1 and P6 induced aggregation of NPR1.

complete
CACAO 5528

9VIRU:Q3HM11

involved_in

GO:0019050: suppression by virus of host apoptotic process

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

9VIRU:Q3HM11

involved_in

GO:0019056: modulation by virus of host transcription

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

9VIRU:Q3HM11

involved_in

GO:0043066: negative regulation of apoptotic process

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete


See also

References

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