Profiling plant circRNAs as a guide for expression of plant genes involved in viral infection

Abstract

In this study, we explore the changes in the expression of plant circRNAs as a guide to trace plant gene expression during viral/viral component infections, focusing on the circRNAs dysregulation and their role in triggering plant cell responses. Our investigation distinguishes host-virus (TRoV) determinants versus non-host virus (RYMV) in Arabidopsis thaliana (A. thalian) plants. We iden-tified 760 plant circRNAs with varying abundances, primarily encoded in exonic regions, and fur-ther analyzed their distribution across all A. thaliana chromosomes. Notably, the chloroplast chromosome exhibits the highest number of circRNAs compared to other chromosomes, sug-gesting the chloroplast as a circRNA hotspot in response to viruses and/or viral genes. Gene ontology (GO) analysis indicates that most host genes encoding these circRNAs are primarily asso-ciated with plant development and protein binding activity, suggesting a potential role for circR-NAs in the regulation of their host genes. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis highlights photosynthesis as the most enriched pathway among the identified circRNAs. While some circRNAs are anticipated to function as decoys for miRNA binding, such as circRNA AT1G01520 targeting ath-miR396b-5p, it is noteworthy that the majority of identified circRNAs do not correspond with miRNA sequences. Additionally, the non-coding exogenous circular sat-ellite RNA (scLTSV) (virusoid) is shown to affect specific genes. Our results demonstrate that numerous cellular circRNAs (e.g., ATCG00030 (ciRNA106) and ATCG00130 (ciRNA11)) are induced solely by scLTSV. One circRNA (circRNA2) with an open reading frame (ORF) codes for a protein similar to a described wheat protein with monooxygenase activity. CircRNA205, displaying significant expression changes between non-host and host viruses, also contains a translatable ORF. RYMV genomic RNA is transcribed in transgenic A. thaliana by the 35S promoter but is unable to replicate (non-host), impacting host eIF4G expression (AT3G60240). Intriguingly, expression of transgenic scLTSV (satellite RNA) in A. thaliana enhances plant resistance to TRoV infection. These findings contribute to our understanding of circRNA mediated mechanisms in plant-virus interactions, shedding light on potential avenues for improving plant resistance to viral infections.