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

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 i...

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Main Authors: Xuedong Yang, Yahui Liu, Hui Zhang, Jinyu Wang, Gaurav Zinta, Shangbo Xie, Weimin Zhu, Wen-Feng Nie
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2020.591806/full
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author Xuedong Yang
Yahui Liu
Hui Zhang
Jinyu Wang
Gaurav Zinta
Shangbo Xie
Weimin Zhu
Wen-Feng Nie
Wen-Feng Nie
author_facet Xuedong Yang
Yahui Liu
Hui Zhang
Jinyu Wang
Gaurav Zinta
Shangbo Xie
Weimin Zhu
Wen-Feng Nie
Wen-Feng Nie
author_sort Xuedong Yang
collection DOAJ
description 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.
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spelling doaj.art-83371a9b141f4e16b73107934cf25b722022-12-21T18:14:21ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-11-011110.3389/fgene.2020.591806591806Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato LeavesXuedong Yang0Yahui Liu1Hui Zhang2Jinyu Wang3Gaurav Zinta4Shangbo Xie5Weimin Zhu6Wen-Feng Nie7Wen-Feng Nie8Shanghai Key Laboratory of Protected Horticulture Technology, The Protected Horticulture Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShanghai Key Laboratory of Protected Horticulture Technology, The Protected Horticulture Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShanghai Key Laboratory of Protected Horticulture Technology, The Protected Horticulture Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaDepartment of Horticulture, College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, ChinaBiotechnology Division, CSIR-Institute of Himalayan Bioresource Technology, Palampur, IndiaBGI-Shenzhen, Shenzhen, ChinaShanghai Key Laboratory of Protected Horticulture Technology, The Protected Horticulture Institute, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaDepartment of Horticulture, College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, ChinaJoint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou, ChinaAbiotic 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.https://www.frontiersin.org/articles/10.3389/fgene.2020.591806/fullcircRNAstomatocold stressmiRNA spongepost-transcriptional regulation
spellingShingle Xuedong Yang
Yahui Liu
Hui Zhang
Jinyu Wang
Gaurav Zinta
Shangbo Xie
Weimin Zhu
Wen-Feng Nie
Wen-Feng Nie
Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves
Frontiers in Genetics
circRNAs
tomato
cold stress
miRNA sponge
post-transcriptional regulation
title Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves
title_full Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves
title_fullStr Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves
title_full_unstemmed Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves
title_short Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves
title_sort genome wide identification of circular rnas in response to low temperature stress in tomato leaves
topic circRNAs
tomato
cold stress
miRNA sponge
post-transcriptional regulation
url https://www.frontiersin.org/articles/10.3389/fgene.2020.591806/full
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