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Disruption of Two Defensive Signaling Pathways by a Viral RNA Silencing Suppressor

July 2010 , Volume 23 , Number  7
Pages  835 - 845

Mathew G. Lewsey,1 Alex M. Murphy,1 Daniel MacLean,2 Neil Dalchau,1 Jack H. Westwood,1 Keith Macaulay,1 Mark H. Bennett,3 Michael Moulin,1 David E. Hanke,1 Glen Powell,3 Alison G. Smith,1 and John P. Carr1

1Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, U.K.; 2Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, U.K.; 3Imperial College London, South Kensington Campus, London, SW7 2AZ, U.K.

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Accepted 16 March 2010.

The Cucumber mosaic virus (CMV) 2b counter-defense protein disrupts plant antiviral mechanisms mediated by RNA silencing and salicylic acid (SA). We used microarrays to investigate defensive gene expression in 2b-transgenic Arabidopsis thaliana plants. Surprisingly, 2b inhibited expression of few SA-regulated genes and, in some instances, enhanced the effect of SA on certain genes. Strikingly, the 2b protein inhibited changes in the expression of 90% of genes regulated by jasmonic acid (JA). Consistent with this, infection of plants with CMV, but not the 2b gene-deletion mutant CMVΔ2b, strongly inhibited JA-inducible gene expression. JA levels were unaffected by infection with either CMV or CMVΔ2b. Although the CMV--Arabidopsis interaction is a compatible one, SA accumulation, usually considered to be an indicator of plant resistance, was increased in CMV-infected plants but not in CMVΔ2b-infected plants. Thus, the 2b protein inhibits JA signaling at a step downstream of JA biosynthesis but it primes induction of SA biosynthesis by another CMV gene product or by the process of infection itself. Like many plant viruses, CMV is aphid transmitted. JA is important in plant defense against insects. This raises the possibility that disruption of JA-mediated gene expression by the 2b protein may influence CMV transmission by aphids.

© 2010 The American Phytopathological Society