Potato Spindle Tuber Viroid (PSTVd)-Plant Interactions: Molecular Mechanisms, Multi-Omics Reprogramming, and Emerging...

Viroids are the smallest known nucleic acid-based infectious agents of plants and consist of single-stranded, circular, non-coding RNAs that can cause significant crop diseases. The potato spindle tuber viroid (PSTVd), a model Pospiviroidae member, severely impacts Solanaceous hosts like potato and tomato, causing substantial yield reductions. Its 359-nucleotide, rod-like genome, with five functional domains, mediates nuclear replication, systemic movement via plasmodesmata and phloem, and evasion of host RNA silencing. High mutation rates generate diverse quasi-species, enhancing adaptability. Recent multi-omics studies reveal PSTVd reprogramming of host transcriptomes, epigenomes, and metabolomes, disrupting defence, hormone signalling, and photosynthesis. Within the plant holobiont, PSTVd modulates interactions with viruses, notably via RNA-directed DNA methylation, and may affect rhizosphere microbial communities indirectly via changes in host physiology, an area that remains poorly resolved. This review synthesises advances in PSTVd structure, infection mechanisms, and holobiont interactions, highlighting its role in uncovering RNA-mediated pathogenesis principles. Key knowledge gaps persist regarding host factors facilitating systemic spread and interactions with other organisms, such as microbial communities. Ongoing PSTVd research is essential to address this gap and guide strategies for viroid-resistant crops and sustainable control.