Salicylic acid and gentisic acid induce RNA silencing-related genes and plant resistance to RNA pathogens

Campos, Laura; Granell, Pablo; Tárraga, Susana; López-Gresa, María Pilar; Conejero, Vicente; Bellés, José M.; Rodrigo, Ismael; Lisón, Purificación

doi:10.1016/j.plaphy.2014.01.016

Cited by 93 publications

(95 citation statements)

References 66 publications

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“…Moreover, it does not favor the idea that vd-sRNAs, as proposed previously for transgene siRNAs and endogenous siRNAs and miRNAs (68), could compete to bind to AGO1 and lead to a reduction in AGO1-miR168 complexes and an increase in AGO1 mRNA translation. However, recent data indicate that infection by citrus exocortis viroid, a close relative of PSTVd, induces the accumulation of other enzymes mediating RNA-silencing steps in tomato (69). Whether this accumulation is a direct or indirect effect, and what is the nature of the underlying mechanism, remains unknown.…”

Section: Discussionmentioning

confidence: 99%

Specific Argonautes Selectively Bind Small RNAs Derived from Potato Spindle Tuber Viroid and Attenuate Viroid Accumulation In Vivo

Minoia

Carbonell

Serio

et al. 2014

J Virol

100

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The identification of viroid-derived small RNAs (vd-sRNAs) of 21 to 24 nucleotides (nt) in plants infected by viroids (infectious non-protein-coding RNAs of just 250 to 400 nt) supports their targeting by Dicer-like enzymes, the first host RNA-silencing barrier. However, whether viroids, like RNA viruses, are also targeted by the RNA-induced silencing complex (RISC) remains controversial. At the RISC core is one Argonaute (AGO) protein that, guided by endogenous or viral sRNAs, targets complementary RNAs. To examine whether AGO proteins also load vd-sRNAs, leaves of Nicotiana benthamiana infected by potato spindle tuber viroid (PSTVd) were agroinfiltrated with plasmids expressing epitope-tagged versions of AGO1, AGO2, AGO3, AGO4, AGO5, AGO6, AGO7, AGO9, and AGO10 from Arabidopsis thaliana. Immunoprecipitation analyses of the agroinfiltrated halos revealed that all AGOs except AGO6, AGO7, and AGO10 associated with vd-sRNAs: AGO1, AGO2, and AGO3 preferentially with those of 21 and 22 nt, while AGO4, AGO5, and AGO9 additionally bound those of 24 nt. Deep-sequencing analyses showed that sorting of vd-sRNAs into AGO1, AGO2, AGO4, and AGO5 depended essentially on their 5=-terminal nucleotides, with the profiles of the corresponding AGO-loaded vd-sRNAs adopting specific hot spot distributions along the viroid genome. Furthermore, agroexpression of AGO1, AGO2, AGO4, and AGO5 on PSTVd-infected tissue attenuated the level of the genomic RNAs, suggesting that they, or their precursors, are RISC targeted. In contrast to RNA viruses, PSTVd infection of N. benthamiana did not affect miR168-mediated regulation of the endogenous AGO1, which loaded vd-sRNAs with specificity similar to that of its A. thaliana counterpart. V iroids, despite having minimal genomes restricted to a nonprotein-coding single-stranded RNA (ssRNA) of only ϳ250 to 400 nucleotides (nt), can parasitize the higher plants they infect and replicate, spread systemically, and frequently incite disease (1-3). Most of the approximately 30 viroids characterized so far, including the type species potato spindle tuber viroid (PSTVd) (4, 5), have been assigned to the family Pospiviroidae on the basis of a rod-like (or quasi-rod-like) secondary structure with a central conserved region (CCR) and replication in the nucleus through an asymmetric rolling-circle mechanism with double-stranded RNA (dsRNA) intermediates (6-10). This mechanism is catalyzed by the RNA polymerase II forced to transcribe RNA templates (11-13), an RNase most likely of class III (14), and the DNA ligase 1 redirected to act as an RNA ligase (15), with the CCR playing a critical role in the cleavage of the oligomeric plus strands generated by the rolling-circle mechanism (14) and in the ligation (circularization) of the resulting monomeric plus strands (16). The remaining four viroids, members of the family Avsunviroidae, display a quasi-rod-like or clearly branched secondary structure without a CCR but with hammerhead ribozymes in both polarity strands; these catalytic RNA motifs mediate se...

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Section: Discussionmentioning

confidence: 99%

Specific Argonautes Selectively Bind Small RNAs Derived from Potato Spindle Tuber Viroid and Attenuate Viroid Accumulation In Vivo

Minoia

Carbonell

Serio

et al. 2014

J Virol

100

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“…The “Infectivity Index” consists of the total number of days that each plant presents symptoms, thus providing a measure of the delay in the onset of symptoms [37]. Data from a representative experiment from three independent assays were used to perform statistical analysis by using the Mann-Whitney non-parametric test.…”

Section: Methodsmentioning

confidence: 99%

Salicylic Acid Is Involved in the Basal Resistance of Tomato Plants to Citrus Exocortis Viroid and Tomato Spotted Wilt Virus

et al. 2016

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Tomato plants expressing the NahG transgene, which prevents accumulation of endogenous salicylic acid (SA), were used to study the importance of the SA signalling pathway in basal defence against Citrus Exocortis Viroid (CEVd) or Tomato Spotted Wilt Virus (TSWV). The lack of SA accumulation in the CEVd- or TSWV-infected NahG tomato plants led to an early and dramatic disease phenotype, as compared to that observed in the corresponding parental Money Maker. Addition of acibenzolar-S-methyl, a benzothiadiazole (BTH), which activates the systemic acquired resistance pathway downstream of SA signalling, improves resistance of NahG tomato plants to CEVd and TSWV. CEVd and TSWV inoculation induced the accumulation of the hydroxycinnamic amides p-coumaroyltyramine, feruloyltyramine, caffeoylputrescine, and feruloylputrescine, and the defence related proteins PR1 and P23 in NahG plants earlier and with more intensity than in Money Maker plants, indicating that SA is not essential for the induction of these plant defence metabolites and proteins. In addition, NahG plants produced very high levels of ethylene upon CEVd or TSWV infection when compared with infected Money Maker plants, indicating that the absence of SA produced additional effects on other metabolic pathways. This is the first report to show that SA is an important component of basal resistance of tomato plants to both CEVd and TSWV, indicating that SA-dependent defence mechanisms play a key role in limiting the severity of symptoms in CEVd- and TSWV-infected NahG tomato plants.

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“…2,5-DHBA accumulates in response to different types of plant-pathogen interactions in much higher levels than SA (Bellés et al, 1999(Bellés et al, , 2006Campos et al, 2014). The exogenous application of 2,5-DHBA to tomato (Solanum lycopersicum), cucumber (Cucumis sativus), and Gynura auriantiaca induces the expression of a distinct subset of PR genes compared with the genes induced by SA (Bellés et al, 1999(Bellés et al, , 2006; 2,5-DHBA also induces RNA silencing-related genes and resistance to RNA pathogens in tomato and G. auriantiaca (Campos et al, 2014). Moreover, 2,5-DHBA itself displays antibacterial activity in the harvested fruits (Lattanzio et al, 1996).…”

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confidence: 98%

“…Similar to other hydroxybenzoates, 2,5-DHBA accumulates as glycoconjugates in plants, primarily as 2,5-DHBA 5-O-b-D-glucosides, 2,5-DHBA 5-O-b-D-xylosides, or 2,5-DHBA 2-O-b-D-xylosides (Dean and Delaney, 2008;Tárraga et al, 2010;Li et al, 2014). 2,5-DHBA accumulates in response to different types of plant-pathogen interactions in much higher levels than SA (Bellés et al, 1999(Bellés et al, , 2006Campos et al, 2014). The exogenous application of 2,5-DHBA to tomato (Solanum lycopersicum), cucumber (Cucumis sativus), and Gynura auriantiaca induces the expression of a distinct subset of PR genes compared with the genes induced by SA (Bellés et al, 1999(Bellés et al, , 2006; 2,5-DHBA also induces RNA silencing-related genes and resistance to RNA pathogens in tomato and G. auriantiaca (Campos et al, 2014).…”

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confidence: 99%

S5H/DMR6 Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis

et al. 2017

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The phytohormone salicylic acid (SA) plays essential roles in biotic and abiotic responses, plant development, and leaf senescence. 2,5-Dihydroxybenzoic acid (2,5-DHBA or gentisic acid) is one of the most commonly occurring aromatic acids in green plants and is assumed to be generated from SA, but the enzymes involved in its production remain obscure. DMR6 (Downy Mildew Resistant6; At5g24530) has been proven essential in plant immunity of Arabidopsis (Arabidopsis thaliana), but its biochemical properties are not well understood. Here, we report the discovery and functional characterization of DMR6 as a salicylic acid 5-hydroxylase (S5H) that catalyzes the formation of 2,5-DHBA by hydroxylating SA at the C5 position of its phenyl ring in Arabidopsis. S5H/DMR6 specifically converts SA to 2,5-DHBA in vitro and displays higher catalytic efficiency (K cat /K m = 4. ) for SA. Interestingly, S5H/DMR6 displays a substrate inhibition property that may enable automatic control of its enzyme activities. The s5h mutant and s5hs3h double mutant overaccumulate SA and display phenotypes such as a smaller growth size, early senescence, and a loss of susceptibility to Pseudomonas syringae pv tomato DC3000. S5H/DMR6 is sensitively induced by SA/pathogen treatment and is expressed widely from young seedlings to senescing plants, whereas S3H is more specifically expressed at the mature and senescing stages. Collectively, our results disclose the identity of the enzyme required for 2,5-DHBA formation and reveal a mechanism by which plants fine-tune SA homeostasis by mediating SA 5-hydroxylation.

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Salicylic acid and gentisic acid induce RNA silencing-related genes and plant resistance to RNA pathogens

Cited by 93 publications

References 66 publications

Specific Argonautes Selectively Bind Small RNAs Derived from Potato Spindle Tuber Viroid and Attenuate Viroid Accumulation In Vivo

Specific Argonautes Selectively Bind Small RNAs Derived from Potato Spindle Tuber Viroid and Attenuate Viroid Accumulation In Vivo

Salicylic Acid Is Involved in the Basal Resistance of Tomato Plants to Citrus Exocortis Viroid and Tomato Spotted Wilt Virus

S5H/DMR6 Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis

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