Salicylic acid perturbs sRNA-gibberellin regulatory network in immune response of potato to Potato virus Y infection

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. Desiree 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-Desiree expressing severe disease symptoms. Besides downregulation of gibberellin signaling, regulation of several other parts of sRNA network in tolerant Desiree 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.