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Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice

Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive pests of rice. Non-coding RNA plays an important regulatory role in various biological processes. However, comprehensive identification and characterization of long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs)...

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Autores principales: Wu, Yan, Zha, Wenjun, Qiu, Dongfeng, Guo, Jianping, Liu, Gang, Li, Changyan, Wu, Bian, Li, Sanhe, Chen, Junxiao, Hu, Liang, Shi, Shaojie, Zhou, Lei, Zhang, Zaijun, Du, Bo, You, Aiqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10457010/
https://www.ncbi.nlm.nih.gov/pubmed/37636117
http://dx.doi.org/10.3389/fpls.2023.1242089
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author Wu, Yan
Zha, Wenjun
Qiu, Dongfeng
Guo, Jianping
Liu, Gang
Li, Changyan
Wu, Bian
Li, Sanhe
Chen, Junxiao
Hu, Liang
Shi, Shaojie
Zhou, Lei
Zhang, Zaijun
Du, Bo
You, Aiqing
author_facet Wu, Yan
Zha, Wenjun
Qiu, Dongfeng
Guo, Jianping
Liu, Gang
Li, Changyan
Wu, Bian
Li, Sanhe
Chen, Junxiao
Hu, Liang
Shi, Shaojie
Zhou, Lei
Zhang, Zaijun
Du, Bo
You, Aiqing
author_sort Wu, Yan
collection PubMed
description Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive pests of rice. Non-coding RNA plays an important regulatory role in various biological processes. However, comprehensive identification and characterization of long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) in BPH-infested rice have not been performed. Here, we performed a genome-wide analysis of lncRNAs and circRNAs in BPH6-transgenic (resistant, BPH6G) and Nipponbare (susceptible, NIP) rice plants before and after BPH feeding (early and late stage) via deep RNA-sequencing. A total of 310 lncRNAs and 129 circRNAs were found to be differentially expressed. To reveal the different responses of resistant and susceptible rice to BPH herbivory, the potential functions of these lncRNAs and circRNAs as competitive endogenous RNAs (ceRNAs) were predicted and investigated using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analyses. Dual-luciferase reporter assays revealed that miR1846c and miR530 were targeted by the lncRNAs XLOC_042442 and XLOC_028297, respectively. In responsive to BPH infestation, 39 lncRNAs and 21 circRNAs were predicted to combine with 133 common miRNAs and compete for miRNA binding sites with 834 mRNAs. These mRNAs predictably participated in cell wall organization or biogenesis, developmental growth, single-organism cellular process, and the response to stress. This study comprehensively identified and characterized lncRNAs and circRNAs, and integrated their potential ceRNA functions, to reveal the rice BPH-resistance network. These results lay a foundation for further study on the functions of lncRNAs and circRNAs in the rice-BPH interaction, and enriched our understanding of the BPH-resistance response in rice.
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spelling pubmed-104570102023-08-26 Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice Wu, Yan Zha, Wenjun Qiu, Dongfeng Guo, Jianping Liu, Gang Li, Changyan Wu, Bian Li, Sanhe Chen, Junxiao Hu, Liang Shi, Shaojie Zhou, Lei Zhang, Zaijun Du, Bo You, Aiqing Front Plant Sci Plant Science Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive pests of rice. Non-coding RNA plays an important regulatory role in various biological processes. However, comprehensive identification and characterization of long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) in BPH-infested rice have not been performed. Here, we performed a genome-wide analysis of lncRNAs and circRNAs in BPH6-transgenic (resistant, BPH6G) and Nipponbare (susceptible, NIP) rice plants before and after BPH feeding (early and late stage) via deep RNA-sequencing. A total of 310 lncRNAs and 129 circRNAs were found to be differentially expressed. To reveal the different responses of resistant and susceptible rice to BPH herbivory, the potential functions of these lncRNAs and circRNAs as competitive endogenous RNAs (ceRNAs) were predicted and investigated using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analyses. Dual-luciferase reporter assays revealed that miR1846c and miR530 were targeted by the lncRNAs XLOC_042442 and XLOC_028297, respectively. In responsive to BPH infestation, 39 lncRNAs and 21 circRNAs were predicted to combine with 133 common miRNAs and compete for miRNA binding sites with 834 mRNAs. These mRNAs predictably participated in cell wall organization or biogenesis, developmental growth, single-organism cellular process, and the response to stress. This study comprehensively identified and characterized lncRNAs and circRNAs, and integrated their potential ceRNA functions, to reveal the rice BPH-resistance network. These results lay a foundation for further study on the functions of lncRNAs and circRNAs in the rice-BPH interaction, and enriched our understanding of the BPH-resistance response in rice. Frontiers Media S.A. 2023-08-10 /pmc/articles/PMC10457010/ /pubmed/37636117 http://dx.doi.org/10.3389/fpls.2023.1242089 Text en Copyright © 2023 Wu, Zha, Qiu, Guo, Liu, Li, Wu, Li, Chen, Hu, Shi, Zhou, Zhang, Du and You https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Wu, Yan
Zha, Wenjun
Qiu, Dongfeng
Guo, Jianping
Liu, Gang
Li, Changyan
Wu, Bian
Li, Sanhe
Chen, Junxiao
Hu, Liang
Shi, Shaojie
Zhou, Lei
Zhang, Zaijun
Du, Bo
You, Aiqing
Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice
title Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice
title_full Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice
title_fullStr Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice
title_full_unstemmed Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice
title_short Comprehensive identification and characterization of lncRNAs and circRNAs reveal potential brown planthopper-responsive ceRNA networks in rice
title_sort comprehensive identification and characterization of lncrnas and circrnas reveal potential brown planthopper-responsive cerna networks in rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10457010/
https://www.ncbi.nlm.nih.gov/pubmed/37636117
http://dx.doi.org/10.3389/fpls.2023.1242089
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