The Role of Hydrogen Peroxide and Nitric Oxide in the Induction of Plant-Encoded RNA-Dependent RNA Polymerase 1 in the Basal Defense against Tobacco Mosaic Virus

Abstract

Plant RNA-dependent RNA Polymerase 1 (RDR1) is an important element of the RNA silencing pathway in the plant defense against viruses. RDR1 expression can be elicited by viral infection and salicylic acid (SA), but the mechanisms of signaling during this process remains undefined. The involvement of hydrogen peroxide (H2O2) and nitric oxide (NO) in RDR1 induction in the compatible interactions between Tobacco mosaic tobamovirus (TMV) and Nicotiana tabacum, Nicotiana benthamiana, and Arabidopsis thaliana was examined. TMV inoculation onto the lower leaves of N. tabacum induced the rapid accumulation of H2O2 and NO followed by the increased accumulation of RDR1 transcripts in the non-inoculated upper leaves. Pretreatment with exogenous H2O2 and NO on upper leaf led to increased RDR1 expression and systemic TMV resistance. Conversely, dimethylthiourea (an H2O2 scavenger) and 2-(4-carboxyphenyl)- 4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (an NO scavenger) partly blocked TMV- and SA-induced RDR1 expression and increased TMV susceptibility, whereas pretreatment with exogenous H2O2 and NO failed to diminish TMV infection in N. benthamiana plants with naturally occurring RDR1 loss-of-function. Furthermore, in N. tabacum and A. thaliana, TMV-induced H2O2 accumulation was NO-dependent, whereas NO generation was not affected by H2O2. These results suggest that, in response to TMV infection, H2O2 acts downstream of NO to mediate induction of RDR1, which plays a critical role in strengthening RNA silencing to restrict systemic viral infection.

The relationship between the plant-encoded RNA-dependent RNA polymerase 1 and alternative oxidase in tomato basal defense against Tobacco mosaic virus

“…2), as well as the upregulation of SlRDR1 expression at 1 dpi (Fig. 2), results that are supported by previous studies reporting the TMV-induced induction of AOX1a in tomato (Fu et al 2010) andof RDR1 in N. tabacum, N. benthamiana andArabidopsis (Xie et al 2001;Yu et al 2003;Liao et al 2013). These results imply a possible connection between TMV-induced RDR1 upregulation and AOX pathway induction.…”

“…It has been reported that AOX and antioxidant systems limit H 2 O 2 formation after TMV attack in tomato (Liao et al 2012). In the present study, the silencing of SlAOX1a may have resulted in increased antioxidant systems as a compensation for lower AOX activity after TMV challenge, restricting the accumulation of H 2 O 2 , which might decrease the TMV-induced SlRDR1 transcript level (Liao et al 2013). Therefore, our results suggest that SlAOX1a may be involved in the induction of SlRDR1 in response to TMV infection.…”

“…Indeed, there is evidence supporting the overlap of the regulation of RDR1 expression and the AOX pathway (Lennon et al 1997;Yang et al 2004;Fu et al 2010;Liao et al 2013). In a study of N. tabacum, N. benthamiana and Arabidopsis, hydrogen peroxide (H 2 O 2 ) was shown to interact with nitric oxide (NO) and to mediate the TMV-and SA-induced RDR1 gene expression (Liao et al 2013).…”

Molecular mechanisms behind the accumulation of ATP and H2O2 in citrus plants in response to ‘Candidatus Liberibacter asiaticus’ infection

“…36,[50][51][52] Briefly, citrus leaf discs were collected from either the Las-infected citrus trees or non-infected trees Figure 1. Las-infected and non-infected sample leaves used in the study.…”

Modulation of host plant immunity by Tobamovirus proteins

“…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.…”