Genome-wide identification of long non-coding RNAs and circular RNAs reveal their ceRNA networks in response to cucumber green mottle mosaic virus infection in watermelon

Long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) play vital roles in plant defense responses against viral infections. However, there is no systematic understanding of lncRNAs and circRNAs and their competing endogenous RNA (ceRNA) networks in watermelon under cucumber green mottle mosaic virus (CGMMV) stress. Here, we present the characterization and expression profiles of lncRNAs and circRNAs in watermelon leaves 48-h post-inoculation (48 hpi) with CGMMV, with mock inoculation as a control. Deep sequencing analysis revealed 2373 lncRNAs and 606 circRNAs in the two libraries. Among them, 67 lncRNAs (40 upregulated and 27 downregulated) and 548 circRNAs (277 upregulated and 271 downregulated) were differentially expressed (DE) in the 48 hpi library compared with the control library. Furthermore, 263 cis-acting matched lncRNA-mRNA pairs were detected for 49 of the DE-lncRNAs. KEGG pathway analysis of the cis target genes of the DE-lncRNAs revealed significant associations with phenylalanine metabolism, the citrate cycle (TCA cycle), and endocytosis. Additionally, 30 DE-lncRNAs were identified as putative target mimics of 33 microRNAs (miRNAs), and 153 DE-circRNAs were identified as putative target mimics of 88 miRNAs. Furthermore, ceRNA networks of lncRNA/circRNA-miRNA-mRNA in response to CGMMV infection are described, with 12 DE-lncRNAs and 65 DE-circRNAs combining with 22 miRNAs and competing for the miRNA binding sites on 29 mRNAs. The qRT-PCR validation of selected lncRNAs and circRNAs showed a general correlation with the high-throughput sequencing results. This study provides a valuable resource of lncRNAs and circRNAs involved in the response to CGMMV infection in watermelon.