Abstract

Abiotic stress adversely inhibits the growth and development of plants, by changing the expression of multiple genes. Circular RNAs (circRNAs), as a class of non-coding RNAs, function in transcriptional and posttranscriptional regulation. Yet, the involvement of circRNAs in abiotic stress response is rarely reported. In this study, the participation and function of circRNAs in low-temperature (LT)-induced stress response were investigated in tomato leaves. We generated genome-wide profiles of circRNAs and mRNAs in tomato leaves grown at 25°C room temperature (RT) and 12°C LT. Our results show that 1,830 circRNAs were identified in tomato leaves in both RT and LT treatments, among which 1,759 were differentially induced by the LT treatment. We find that the identified circRNAs are mainly located at exons of genes, but less distributed at introns of genes or intergenic regions. Our results suggest that there are 383 differentially expressed circRNAs predicted to function as putative sponges of 266 miRNAs to target 4,476 mRNAs in total. Moreover, Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis assays indicate that multiple pathways were enriched in both differentially expressed genes induced by LT and parental genes of differentially expressed circRNAs induced by LT, revealing the key functions of circRNAs and the corresponding targeted genes in response to LT stress. Our results suggest that circRNAs may be involved in regulating metabolism (i.e., carbohydrate, amino acid, lipid, and energy), signal transduction, and environmental adaptation-related pathways and that these circRNAs were predicted to regulate the expression of transcription factors, genes in signal transduction pathways, and genes related to the Ca2+ channel through targeting the corresponding proteins, such as WRKY, NAC, cytochrome P450, and calmodulin binding protein. Taken together, our study uncovers that multiple circRNAs are isolated and differently regulated in response to LT stress and provides the resource and potential networks of circRNA–miRNA–mRNA under LT stress for further investigations in tomato leaves.

Highlights

  • Most of the genomes in eukaryotes generate RNA transcripts that do not code for proteins

  • The circRNAs identified in room temperature (RT) treatment and LT treatment displayed similar expression patterns on tomato chromosomes (Figure 1D)

  • These results indicated that circRNAs in tomato leaves were generated from different genomic regions and chromosomes, showing the characterization of various lengths

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Summary

Introduction

Most of the genomes in eukaryotes generate RNA transcripts that do not code for proteins. Long non-coding RNAs (lncRNAs) regulate multiple gene expressions that are enriched in various biological processes in eukaryotes (Zaynab et al, 2018). Circular RNAs (circRNAs) are recently discovered endogenous non-coding RNAs (Salzman et al, 2012; Memczak et al, 2013; Wang et al, 2014). The circRNAs are derived from linear precursor mRNAs, which can be generated from circularization of lariat-driven and intron-pairing-driven, alternative splicing, and protein factors associated circulation (Zhang et al, 2014; Starke et al, 2015; Chen, 2016; Liu J. et al, 2017). Recent studies reveal that circRNAs are conserved among species and are mainly expressed in a cell-, tissue-, and developmental stage-dependent manner (Jeck et al, 2013; Memczak et al, 2013; Salzman et al, 2013; Szabo et al, 2015; Venø et al, 2015)

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