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Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity

Love, A.J., Geri, C., Laird, J., Carr, C., Yun, B.-W., Loake, G.J., Tada, Y., Sadanandom, A., and Milner, J.J. (2012) Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS ONE, 7 (10). e47535. ISSN 1932-6203 (doi:10.1371/journal.pone.0047535)

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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.

Item Type:Article
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Carr, Mr Craig and Milner, Dr Joel and Sadanandom, Dr Ari and Laird, Ms Janet and Love, Dr Andrew
Authors: Love, A.J., Geri, C., Laird, J., Carr, C., Yun, B.-W., Loake, G.J., Tada, Y., Sadanandom, A., and Milner, J.J.
Subjects:Q Science > QK Botany
Q Science > QR Microbiology
College/School:College of Medical Veterinary and Life Sciences > School of Life Sciences
Research Group:Plant Science
Journal Name:PLoS ONE
Publisher:Public Library of Science
ISSN:1932-6203
ISSN (Online):1932-6203
Published Online:11 October 2012
Copyright Holders:Copyright © 2012 Love et al.
First Published:First published in PLoS ONE 8(1):4-30
Publisher Policy:Reproduced under a Creative Commons Licence

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
0UNSPECIFIEDUNSPECIFIEDJoel MilnerUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
0UNSPECIFIEDUNSPECIFIEDJoel MilnerUNSPECIFIEDUNSPECIFIEDUNSPECIFIED

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