Abstract
Viroids are plant-pathogenic non-coding RNAs able to interfere with as yet poorly known host-regulatory pathways and to cause alterations recognized as diseases. The way in which these RNAs coerce the host to express symptoms remains to be totally deciphered. In recent years, diverse studies have proposed a close interplay between viroid-induced pathogenesis and RNA silencing, supporting the belief that viroid-derived small RNAs mediate the post-transcriptional cleavage of endogenous mRNAs by acting as elicitors of symptoms expression. Although the evidence supporting the role of viroid-derived small RNAs in pathogenesis is robust, the possibility that this phenomenon can be a more complex process, also involving viroid-induced alterations in plant gene expression at transcriptional levels, has been considered. Here we show that plants infected with the ‘Hop stunt viroid’ accumulate high levels of sRNAs derived from ribosomal transcripts. This effect was correlated with an increase in the transcription of ribosomal RNA (rRNA) precursors during infection. We observed that the transcriptional reactivation of rRNA genes correlates with a modification of DNA methylation in their promoter region and revealed that some rRNA genes are demethylated and transcriptionally reactivated during infection. This study reports a previously unknown mechanism associated with viroid (or any other pathogenic RNA) infection in plants providing new insights into aspects of host alterations induced by the viroid infectious cycle.
Highlights
Impelled by their need to optimize a humble (250–400 nt) non-protein-coding genome to guarantee their infectious cycle, viroids have evolved into versatile molecular entities capable of interacting with the host-cell machinery at diverse functional levels [1]
The 23and 25-nt-sized classes showed similar accumulation levels in both the control and HSVd-infected small RNA (sRNA) populations. This scenario was in general reproduced when the unique sequences recovered from both datasets were analyzed (Figure 1A, right), indicating that HSVd infection is associated with changes in the endogenous sRNA population levels, being the 21-and 24-nt species up- and downregulated in infected plants, respectively
When plant endogenous sRNAs recovered from infected and healthy plants were analyzed by pairwise alignment against the cucumber transcript database, we observed that the sRNAs derived from 45S ribosomal RNA were the most differentially accumulated population of sRNAs in viroid-infected plants (Figure 1B)
Summary
Impelled by their need to optimize a humble (250–400 nt) non-protein-coding genome to guarantee their infectious cycle, viroids have evolved into versatile molecular entities capable of interacting with the host-cell machinery at diverse functional levels [1]. In some cases, this crosstalk can affect key host-regulatory pathways and cause phenotypic alterations recognized as plant diseases [2,3].
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