Salicylic acid perturbs sRNA-gibberellin regulatory network in immune response of potato toPotato virus Yinfection

Abstract

Potato virus Y is the most economically important potato viral pathogen. We aimed at unraveling the roles of small RNAs (sRNAs) in the complex immune signaling network controlling the establishment of tolerant response of potato cv. Désirée to the virus. We constructed a sRNA regulatory network connecting sRNAs and their targets to link sRNA level responses to physiological processes. We discovered an interesting novel sRNAs-gibberellin regulatory circuit being activated as early as 3 days post inoculation before viral multiplication can be detected. Increased levels of miR167 and phasiRNA931 were reflected in decreased levels of transcripts involved in gibberellin biosynthesis. Moreover, decreased concentration of gibberellin confirmed this regulation. The functional relation between lower activity of gibberellin signaling and reduced disease severity was previously confirmed in Arabidopsis-virus interaction using knockout mutants. We further showed that this regulation is salicylic acid-dependent as the response of sRNA network was attenuated in salicylic acid-depleted transgenic counterpart NahG-Désirée expressing severe disease symptoms. Besides downregulation of gibberellin signaling, regulation of several other parts of sRNA network in tolerant Désirée revealed similarities to responses observed in mutualistic symbiotic interactions. The intertwining of different regulatory networks revealed shows how developmental signaling, disease symptom development and stress signaling can be balanced.

Precision transcriptomics of viral foci reveals the spatial regulation of immune‐signaling genes and identifies RBOHD as an important player in the incompatible interaction between potato virus Y and potato

“…Hormones were isolated and measured by gas chromatography coupled with mass spectrometry (GC‐MS) as described by Križnik et al . (2017).…”

Roles of small RNAs in the establishment of tolerant interaction between plants and viruses

“…This is not surprising since auxin levels are crucial for proper legume nodule and arbuscule development [49,50]. Interestingly, many miRNAs, namely miR160, miR164, miR167, miR390, miR393 were found to be similarly regulated during tolerance response of potato to PVY [36]. Also, decreased GA levels were shown to be regulated by a miRNA/phasiRNA circuit in the potato tolerance response [36] and shown to be involved in rhizobial and mycorrhizal signalling network [51][52][53].…”

“…Moreover, miR482, which targets NBS-LRR transcripts was reported to be induced during establishment of symbiosis between soybean and Bradyrhizobium japonicum [47]. Notably, miR482 which targets NBS-LRR transcripts was upregulated following PVY infection in the tolerant potato-PVY interaction [36]. Similarity in regulation of certain sRNAs should not be so unexpected because in both, the tolerant response to viruses and mutualistic interactions, plants need to tolerate the presence of microorganisms (Figure 2).…”

“…Furthermore, sRNAs link immune signalling with growth. In response to PVY infection, tolerant potato plants exhibited increased levels of miR167 and a secondary siRNA (phasiRNA931) that target transcripts encoding two gibberellin (GA) biosynthesis genes, and miR319 (closely related to Arabidopsis miR159), which targets MYB33, which encodes a GAMYB transcription factor involved in GA signal transduction [36]. In Arabidopsis, a GAMYB-targeting miR159 was reported to be involved in limiting disease symptoms in response to a severe strain of CMV.…”

“…Additionally, there is a link between GA signalling and R gene expression, supporting the hypothesis that viral perception is actively modulated in tolerant interactions. In the potato-PVY interaction, downregulation of miR6022 (targeting LRR-RLKs) occurs, which is linked to downregulation of GA signalling as GAMYB binding sites were discovered in the MIR6022 promoter region [36]. The miR159/miR319 family also targets Teosinte branched1/cycloidea/proliferating (TCP) bHLH transcription factor which targets lipoxygenase 2 (LOX2) involved in JA biosynthesis [39] (Figure 1).…”