Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis

Lydia J. R. Hunter, Jack H. Westwood, Geraldine Heath, Keith Macaulay, Alison G. Smith, Stuart A. MacFarlane, Peter Palukaitis, John P. Carr

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    43 Citations (Scopus)

    Abstract

    Background: RNA-dependent RNA polymerases (RDRs) function in anti-viral silencing in Arabidopsis thaliana and other plants. Salicylic acid (SA), an important defensive signal, increases RDR1 gene expression, suggesting that RDR1 contributes to SA-induced virus resistance. In Nicotiana attenuata RDR1 also regulates plant-insect interactions and is induced by another important signal, jasmonic acid (JA). Despite its importance in defense RDR1 regulation has not been investigated in detail.

    Methodology/Principal Findings: In Arabidopsis, SA-induced RDR1 expression was dependent on 'NON-EXPRESSER OF PATHOGENESIS-RELATED GENES 1', indicating regulation involves the same mechanism controlling many other SA-defenserelated genes, including pathogenesis-related 1 (PR1). Isochorismate synthase 1 (ICS1) is required for SA biosynthesis. In defensive signal transduction RDR1 lies downstream of ICS1. However, supplying exogenous SA to ics1-mutant plants did not induce RDR1 or PR1 expression to the same extent as seen in wild type plants. Analysing ICS1 gene expression using transgenic plants expressing ICS1 promoter: reporter gene (beta-glucuronidase) constructs and by measuring steady-state ICS1 transcript levels showed that SA positively regulates ICS1. In contrast, ICS2, which is expressed at lower levels than ICS1, is unaffected by SA. The wound-response hormone JA affects expression of Arabidopsis RDR1 but jasmonate-induced expression is independent of CORONATINE-INSENSITIVE 1, which conditions expression of many other JA-responsive genes. Transiently increased RDR1 expression following tobacco mosaic virus inoculation was due to wounding and was not a direct effect of infection. RDR1 gene expression was induced by ethylene and by abscisic acid (an important regulator of drought resistance). However, rdr1-mutant plants showed normal responses to drought.

    Conclusions/Significance: RDR1 is regulated by a much broader range of phytohormones than previously thought, indicating that it plays roles beyond those already suggested in virus resistance and plant-insect interactions. SA positively regulates ICS1.

    Original languageEnglish
    Article numbere66530
    Number of pages10
    JournalPLoS ONE
    Volume8
    Issue number6
    DOIs
    Publication statusPublished - 2013

    Keywords

    • ANTIVIRAL DEFENSE
    • DROUGHT TOLERANCE
    • ABSCISIC-ACID
    • SYSTEMIC ACQUIRED-RESISTANCE
    • POTATO-VIRUS-X
    • SILENCING SUPPRESSOR
    • DICER-LIKE PROTEINS
    • SMALL INTERFERING RNAS
    • NICOTIANA-BENTHAMIANA
    • SALICYLIC-ACID

    Cite this

    Hunter, L. J. R., Westwood, J. H., Heath, G., Macaulay, K., Smith, A. G., MacFarlane, S. A., Palukaitis, P., & Carr, J. P. (2013). Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLoS ONE, 8(6), [e66530]. https://doi.org/10.1371/journal.pone.0066530