Regulation of RNA-Dependent RNA Polymerase 1 and Isochorismate Synthase Gene Expression in Arabidopsis

Abstract

BackgroundRNA-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 FindingsIn 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- defense-related 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 (β-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.

Abscisic Acid Induces Resistance against Bamboo Mosaic Virus through Argonaute2 and 3

“…Promoters of AGO Genes Contain Several ABREs, and Their Expression Levels Are Affected by Exogenous ABA Some reports indicated that ABA regulates several components of the sRNA pathway, such as AGO1 and its regulator miR168 as well as RdR1 (Li et al, 2012;Hunter et al, 2013;Alazem and Lin, 2015). We hypothesized that ABA-mediated resistance is achieved by positive regulation of the RNA-silencing pathway and that such regulation also may affect members of the AGO family because several of these proteins have antiviral properties (Carbonell and Carrington, 2015).…”

“…While it is well established that salicylic acid (SA) controls plant resistance to virus infection via R gene resistance (Baebler et al, 2014), it also has been suggested that SA regulates a few genes in the RNA-silencing pathway (Alamillo et al, 2006;Hunter et al, 2013). In fact, the regulation of defense responses has been demonstrated to be a hormonetuned process in many cases.…”

“…For instance, miR168a, which posttranscriptionally regulates the ARGONAUTE (AGO) gene AGO1 and is specifically induced in virusinfected tissues, possesses a few abscisic acid-responsive elements (ABREs) in the promoter region that make it regulated by ABA (Liu et al, 2008;Laubinger et al, 2010;Li et al, 2012). RNA-dependent RNA polymerase (RdRP) is positively regulated by ABA as well (Hunter et al, 2013). Furthermore, abiotic stresses, of which some, such as severe drought, are controlled by ABA, also showed altered expression of some genes involved in the sRNA pathway, such as AGO1, AGO4, and AGO7, in Medicago truncatula (Capitao et al, 2011).…”

Modulation of host plant immunity by Tobamovirus proteins

“…More recent findings demonstrated that Cauliflower mosaic virus (CaMV) P6 alters the expression and sub-cellular localization of NPR1 and inhibits the SAdependent defence responses (Love et al, 2012). Moreover, another recent report showed that SA-induced RDR1 expression is dependent on NPR1 (Hunter et al, 2013). Thus, although NPR1 does not seem to be involved in SA-mediated resistance, its role during compatible viral interactions cannot be ruled out at this stage.…”

“…Interestingly; we observed that the expression of RDR1 was downregulated in mutant plants carrying a 17 amino acid deletion within the DELLA domain of GAI which are insensitive to GA treatment. Given that SA-induced RDR1 expression is dependent on NPR1 protein and is enhanced by H 2 O 2 (Hunter et al, 2013;Liao et al, 2013), it was proposed that DELLA could be attenuating RDR1 expression by its impact on SA signalling and ROS pathways (Rodriguez et al, 2014). Moreover, when viral accumulation was analysed in plants carrying a quadruple DELLA mutation, a reduced viral accumulation was observed in the quadruple DELLA mutants with respect to wild-type plants.…”