Pestalotiopsis trachicarpicola Y. M. Zhang & K. D. Hyde is a plant-pathogenic fungus which can cause leaf spot on tea (Camellia sinensis), seriously decreasing the production and quality of tea leaves. Competing endogenous RNAs (ceRNAs) include messenger RNAs (mRNAs), circular RNAs (circRNAs), and long non-coding RNAs (lncRNAs), which can regulate gene expression through binding to response elements in microRNAs (miRNAs) which, in turn, operate post-transcriptional regulation of target mRNAs. In the current study, ceRNAs and miRNAs originating from infected and uninfected leaves of tea (C. sinensis var. sinensis cv. Fuding-dabaicha) were sequenced and analyzed, and the interaction between individual ceRNAs and miRNAs was predicted, with target genes being identified. Thirty-one, 24, six, and two of the ceRNA interaction pairs were predicted in the form of miRNA-mRNA, miRNA-lncRNA, miRNA-circRNA, and mRNA-lncRNA interactions, respectively. Three types of interactions were predicted to occur in the regulation pairs of lncRNA/circRNA-miRNA-mRNA: circRNA-miRNA-mRNA (Type 1 interactions), lncRNA-miRNA-mRNA (Type 2 interactions), and circRNA-lncRNA-miRNA-mRNA (Type 3 interactions). Some interaction pairs in lncRNA/circRNA-miRNA-mRNA in infected tea leaves ultimately changed the abundance of mRNAs, such as TEA015316.1:TEA015316.1, TEA020085.1:TEA020085.1, TEA027239.1:TEA027239.1 and TEA001447.1:TEA001447.1. Analysis of the types and expression abundance of ceRNAs and miRNAs originating from tea leaves during infection by P. trachicarpicola, and their interactive relationship will provide a valuable resource for future research into this host–pathogen interaction.
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