Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection

Abstract Background Long Noncoding-RNAs (LncRNAs) are known to be involved in some biological processes, but their roles in plant-virus interactions remain largely unexplored. While circular RNAs (circRNAs) have been studied in animals, there has yet to be extensive research on them in a plant syste...

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Main Authors: Jinyan Wang, Yuwen Yang, Lamei Jin, Xitie Ling, Tingli Liu, Tianzi Chen, Yinghua Ji, Wengui Yu, Baolong Zhang
Format: Article
Language:English
Published: BMC 2018-06-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1332-3
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spelling doaj-8ce93812ed5d4694b0645c2defc039f62020-11-25T01:13:34ZengBMCBMC Plant Biology1471-22292018-06-0118111610.1186/s12870-018-1332-3Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infectionJinyan Wang0Yuwen Yang1Lamei Jin2Xitie Ling3Tingli Liu4Tianzi Chen5Yinghua Ji6Wengui Yu7Baolong Zhang8Provincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesInstitute of Plant Protection, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesProvincial Key Laboratory of Agrobiology, Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural SciencesAbstract Background Long Noncoding-RNAs (LncRNAs) are known to be involved in some biological processes, but their roles in plant-virus interactions remain largely unexplored. While circular RNAs (circRNAs) have been studied in animals, there has yet to be extensive research on them in a plant system, especially in tomato-tomato yellow leaf curl virus (TYLCV) interaction. Results In this study, RNA transcripts from the susceptible tomato line JS-CT-9210 either infected with TYLCV or untreated, were sequenced in a pair-end strand-specific manner using ribo-zero rRNA removal library method. A total of 2056 lncRNAs including 1767 long intergenic non-coding RNA (lincRNAs) and 289 long non-coding natural antisense transcripts (lncNATs) were obtained. The expression patterns in lncRNAs were similar in susceptible tomato plants between control check (CK) and TYLCV infected samples. Our analysis suggested that lncRNAs likely played a role in a variety of functions, including plant hormone signaling, protein processing in the endoplasmic reticulum, RNA transport, ribosome function, photosynthesis, glulathione metabolism, and plant-pathogen interactions. Using virus-induced gene silencing (VIGS) analysis, we found that reduced expression of the lncRNA S-slylnc0957 resulted in enhanced resistance to TYLCV in susceptible tomato plants. Moreover, we identified 184 circRNAs candidates using the CircRNA Identifier (CIRI) software, of which 32 circRNAs were specifically expressed in untreated samples and 83 circRNAs in TYLCV samples. Approximately 62% of these circRNAs were derived from exons. We validated the circRNAs by both PCR and Sanger sequencing using divergent primers, and found that most of circRNAs were derived from the exons of protein coding genes. The silencing of these circRNAs parent genes resulted in decreased TYLCV virus accumulation. Conclusion In this study, we identified novel lncRNAs and circRNAs using bioinformatic approaches and showed that these RNAs function as negative regulators of TYLCV infection. Moreover, the expression patterns of lncRNAs in susceptible tomato plants were different from that of resistant tomato plants, while exonic circRNAs expression positively associated with their respective protein coding genes. This work provides a foundation for elaborating the novel roles of lncRNAs and circRNAs in susceptible tomatoes following TYLCV infection.http://link.springer.com/article/10.1186/s12870-018-1332-3Susceptible tomatoLong non-coding RNAcircRNATYLCV
collection DOAJ
language English
format Article
sources DOAJ
author Jinyan Wang
Yuwen Yang
Lamei Jin
Xitie Ling
Tingli Liu
Tianzi Chen
Yinghua Ji
Wengui Yu
Baolong Zhang
spellingShingle Jinyan Wang
Yuwen Yang
Lamei Jin
Xitie Ling
Tingli Liu
Tianzi Chen
Yinghua Ji
Wengui Yu
Baolong Zhang
Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection
BMC Plant Biology
Susceptible tomato
Long non-coding RNA
circRNA
TYLCV
author_facet Jinyan Wang
Yuwen Yang
Lamei Jin
Xitie Ling
Tingli Liu
Tianzi Chen
Yinghua Ji
Wengui Yu
Baolong Zhang
author_sort Jinyan Wang
title Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection
title_short Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection
title_full Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection
title_fullStr Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection
title_full_unstemmed Re-analysis of long non-coding RNAs and prediction of circRNAs reveal their novel roles in susceptible tomato following TYLCV infection
title_sort re-analysis of long non-coding rnas and prediction of circrnas reveal their novel roles in susceptible tomato following tylcv infection
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2018-06-01
description Abstract Background Long Noncoding-RNAs (LncRNAs) are known to be involved in some biological processes, but their roles in plant-virus interactions remain largely unexplored. While circular RNAs (circRNAs) have been studied in animals, there has yet to be extensive research on them in a plant system, especially in tomato-tomato yellow leaf curl virus (TYLCV) interaction. Results In this study, RNA transcripts from the susceptible tomato line JS-CT-9210 either infected with TYLCV or untreated, were sequenced in a pair-end strand-specific manner using ribo-zero rRNA removal library method. A total of 2056 lncRNAs including 1767 long intergenic non-coding RNA (lincRNAs) and 289 long non-coding natural antisense transcripts (lncNATs) were obtained. The expression patterns in lncRNAs were similar in susceptible tomato plants between control check (CK) and TYLCV infected samples. Our analysis suggested that lncRNAs likely played a role in a variety of functions, including plant hormone signaling, protein processing in the endoplasmic reticulum, RNA transport, ribosome function, photosynthesis, glulathione metabolism, and plant-pathogen interactions. Using virus-induced gene silencing (VIGS) analysis, we found that reduced expression of the lncRNA S-slylnc0957 resulted in enhanced resistance to TYLCV in susceptible tomato plants. Moreover, we identified 184 circRNAs candidates using the CircRNA Identifier (CIRI) software, of which 32 circRNAs were specifically expressed in untreated samples and 83 circRNAs in TYLCV samples. Approximately 62% of these circRNAs were derived from exons. We validated the circRNAs by both PCR and Sanger sequencing using divergent primers, and found that most of circRNAs were derived from the exons of protein coding genes. The silencing of these circRNAs parent genes resulted in decreased TYLCV virus accumulation. Conclusion In this study, we identified novel lncRNAs and circRNAs using bioinformatic approaches and showed that these RNAs function as negative regulators of TYLCV infection. Moreover, the expression patterns of lncRNAs in susceptible tomato plants were different from that of resistant tomato plants, while exonic circRNAs expression positively associated with their respective protein coding genes. This work provides a foundation for elaborating the novel roles of lncRNAs and circRNAs in susceptible tomatoes following TYLCV infection.
topic Susceptible tomato
Long non-coding RNA
circRNA
TYLCV
url http://link.springer.com/article/10.1186/s12870-018-1332-3
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