Viroid pathogenesis: a critical appraisal of the role of RNA silencing in triggering the initial molecular lesion

ABSTRACT The initial molecular lesions through which viroids, satellite RNAs and viruses trigger signal cascades resulting in plant diseases are hotly debated. Since viroids are circular non-protein-coding RNAs of ∼250–430 nucleotides, they appear very convenient to address this issue. Viroids are t...

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Veröffentlicht in:FEMS microbiology reviews Jg. 44; H. 3; S. 386 - 398
Hauptverfasser: Flores, Ricardo, Navarro, Beatriz, Delgado, Sonia, Serra, Pedro, Di Serio, Francesco
Format: Journal Article
Sprache:Englisch
Veröffentlicht: England Oxford University Press 01.05.2020
Schlagworte:
Cascades
Catalytic RNA
Cause-effect relationships
Chloroplasts
Host-Pathogen Interactions
Lesions
Nucleotides
Pathogenesis
Phenotypes
Plant diseases
Plant Diseases - virology
Plant viruses
Plants - genetics
Plants - virology
Plastids
Pospiviroidae
Potatoes
Proteins
Replication
RNA Interference
RNA viruses
RNA-mediated interference
Satellite RNA
Sexually transmitted diseases
Signs and symptoms
STD
Viroids
Viroids - genetics
Viroids - physiology
Viruses
pathogenesis
plant viruses
RNA silencing
catalytic RNAs
plant satellite RNAs
viroids
hammerhead ribozymes
ISSN:0168-6445, 1574-6976, 1574-6976
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Zusammenfassung:ABSTRACT The initial molecular lesions through which viroids, satellite RNAs and viruses trigger signal cascades resulting in plant diseases are hotly debated. Since viroids are circular non-protein-coding RNAs of ∼250–430 nucleotides, they appear very convenient to address this issue. Viroids are targeted by their host RNA silencing defense, generating viroid-derived small RNAs (vd-sRNAs) that are presumed to direct Argonaute (AGO) proteins to inactivate messenger RNAs, thus initiating disease. Here, we review the existing evidence. Viroid-induced symptoms reveal a distinction. Those attributed to vd-sRNAs from potato spindle tuber viroid and members of the family Pospiviroidae (replicating in the nucleus) are late, non-specific and systemic. In contrast, those attributed to vd-sRNAs from peach latent mosaic viroid (PLMVd) and other members of the family Avsunviroidae (replicating in plastids) are early, specific and local. Remarkably, leaf sectors expressing different PLMVd-induced chloroses accumulate viroid variants with specific pathogenic determinants. Some vd-sRNAs containing such determinant guide AGO1-mediated cleavage of mRNAs that code for proteins regulating chloroplast biogenesis/development. Therefore, the initial lesions and the expected phenotypes are connected by short signal cascades, hence supporting a cause-effect relationship. Intriguingly, one virus satellite RNA initiates disease through a similar mechanism, whereas in the Pospiviroidae and in plant viruses the situation remains uncertain. Comparison of symptoms and molecular pathways supports that viroids replicating in chloroplasts initiate disease (specific plant chloroses) by RNA silencing mRNAs encoding proteins involved in chloroplast biogenesis/development, while the situation is unclear for those replicating in nuclei (inducing non-specific alterations like stunting).
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ISSN:0168-6445
1574-6976
1574-6976
DOI:10.1093/femsre/fuaa011