Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves

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 Ca 2+ 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.

A Combination of a Genome-Wide Association Study and a Transcriptome Analysis Reveals circRNAs as New Regulators Involved in the Response to Salt Stress in Maize

“…Most circRNAs have been reported to regulate plant growth, development, and stress responses. For example, under a low-temperature treatment, 1759 circRNAs were induced in tomato leaves [ 52 ]. In maize, a total of 24 and 22 DECs obtained from the leaves and roots, respectively, were responsive to deficient nitrogen stress [ 53 ].…”

Comprehensive identification and analysis of circRNAs during hickory (Carya cathayensis Sarg.) flower bud differentiation

“…It then filtered the candidate circRNAs based on the global comparison, the reads support of circRNAs, and the annotation information to identify junction reads. Those with a read number larger than two were selected as the identified circRNA ( Gao et al., 2015 ; Ye et al., 2015 ; Tong et al., 2018 ; Zhang et al., 2019 ; Li et al., 2020 ; Philips et al., 2020 ; Yang et al., 2020 ; Jiang et al., 2021 ). The results that appeared in both find_circ and CIRI2 were selected as candidate circRNAs ( Xu et al., 2018 ; Liu et al., 2019 ; Li et al., 2020 ; Philips et al., 2020 ; Yang et al., 2020 ).…”

“…Those with a read number larger than two were selected as the identified circRNA ( Gao et al., 2015 ; Ye et al., 2015 ; Tong et al., 2018 ; Zhang et al., 2019 ; Li et al., 2020 ; Philips et al., 2020 ; Yang et al., 2020 ; Jiang et al., 2021 ). The results that appeared in both find_circ and CIRI2 were selected as candidate circRNAs ( Xu et al., 2018 ; Liu et al., 2019 ; Li et al., 2020 ; Philips et al., 2020 ; Yang et al., 2020 ).…”

Evolutionary Landscape of Tea Circular RNAs and Its Contribution to Chilling Tolerance of Tea Plant

“…Specifically, overexpression of the grape Vv-circATS1 , a circRNA derived from grape glycerol-3-Pacyltransferase gene, improved the cold tolerance of transgenic Arabidopsis plants [ 16 ]. To investigate the function of circRNAs in tomato leaves’ response to low-temperature stress, Yang et al identified 1759 low-temperature-induced circRNAs, and revealed that 383 differentially expressed circRNAs and their parental genes were functionally enriched in the regulation of metabolism, signal transduction, and environment adaptation pathways, revealing the vital roles of circRNA and its corresponding parental genes in response to low-temperature stress [ 22 ]. These studies demonstrated that circRNAs possess the abilities to respond to biotic and abiotic stresses by regulating the expression of stress-related genes.…”