Viroid Pathogenesis in Host Plants

Viroids are the smallest known plant pathogens, comprising single-stranded, circular RNAs of a few hundred nucleotides and lacking any protein-coding capacity. They are classified into two families based on their replication sites: Pospiviroidae, which replicate in the nucleus via an asymmetric rolling-circle mechanism, and Avsunviroidae, which replicate in chloroplasts using hammerhead ribozymes. Infection begins with entry into a host cell, followed by recruitment of host RNA polymerases and accessory factors to synthesise multimeric RNA strands. These oligomers are cleaved and ligated to produce mature viroid circles, which move cell to cell through plasmodesmata and systemically via the phloem. Pathogenesis arises from complex interactions with host RNA-silencing pathways, leading to the production of viroid-derived small RNAs that can target endogenous transcripts, disrupt transcriptional and post-transcriptional regulation, and alter DNA methylation patterns. The resulting transcriptional reprogramming and developmental dysregulation manifest as stunting, leaf deformation, chlorosis and yield loss. Study of viroid pathogenesis not only informs crop protection strategies but also offers a window into RNA-based regulation and the evolutionary origins of minimal infectious agents.

Research from Nature Portfolio

Recent studies have uncovered a wealth of previously unrecognised viroid-like elements across diverse biological niches. In particular, novel circular RNAs in fungi, termed ambiviruses, display hybrid features of viroid-like genomes and viruses by encoding their own RNA-dependent RNA polymerase alongside self-cleaving ribozymes. These ambiviruses undergo rolling-circle replication akin to classical viroids, yet their polymerase genes blur the boundary between subviral agents and RNA viruses. The discovery of related circular RNAs in mitochondria and other organelles suggests a broad evolutionary continuum and deep co-evolution of minimal infectious RNAs. This expanding catalogue of viroid-like elements informs our understanding of the molecular evolution, host recruitment of replication machinery and potential cross-kingdom movement of pathogenic RNAs.

Viroid Pathogenesis in Host Plants publication trend

The graph below shows the total number of articles in viroid pathogenesis in host plants across all publications each year (not limited to Nature Index journals).

Technical terms

Viroid: A small, circular non-coding RNA pathogen of plants that relies entirely on host machinery for replication.

Rolling-circle replication: A mechanism where circular RNA templates are repetitively transcribed into multimeric strands, which are subsequently cleaved and circularised.

Quasispecies: A population of closely related RNA variants generated by error-prone replication, among which structural stability dictates dominance.

Hammerhead ribozyme: A self-cleaving RNA motif in some viroids that mediates site-specific cleavage of multimeric transcripts.

RNA silencing: A defence pathway in plants whereby small RNAs guide sequence-specific degradation or translational repression of target RNAs.

References

1. Hybrids of RNA viruses and viroid-like elements replicate in fungi. Nature Communications (2023).
2. RNA three-dimensional structure drives the sequence organization of potato spindle tuber viroid quasispecies. PLOS Pathogens (2024).
3. “Pathomorphogenic” Changes Caused by Citrus Bark Cracking Viroid and Transcription Factor TFIIIA-7ZF Variants Support Viroid Propagation in Tobacco. International Journal of Molecular Sciences (2023).
4. Viroid Replication: Rolling-Circles, Enzymes and Ribozymes. Viruses (2009).
5. ICTV Virus Taxonomy Profile: Pospiviroidae. Journal of General Virology (2020).
6. Advances in Viroid-Host Interactions. Annual Review of Virology (2021).
7. A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Research (2013).
8. Deep Sequencing of Viroid-Derived Small RNAs from Grapevine Provides New Insights on the Role of RNA Silencing in Plant-Viroid Interaction. PLOS ONE (2009).
9. Small RNA Derived from the Virulence Modulating Region of the Potato spindle tuber viroid Silences callose synthase Genes of Tomato Plants. The Plant Cell (2015).