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Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development

BACKGROUND: Long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) can play important roles in many biological processes. However, no study of the influence of epigenetics factors or the 3D structure of the genome in their regulation is available in plants. RESULTS: In the current analysis, we...

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Autores principales: Zhou, Run, Sanz-Jimenez, Pablo, Zhu, Xi-Tong, Feng, Jia-Wu, Shao, Lin, Song, Jia-Ming, Chen, Ling-Ling
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843763/
https://www.ncbi.nlm.nih.gov/pubmed/33507446
http://dx.doi.org/10.1186/s12284-021-00455-2
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author Zhou, Run
Sanz-Jimenez, Pablo
Zhu, Xi-Tong
Feng, Jia-Wu
Shao, Lin
Song, Jia-Ming
Chen, Ling-Ling
author_facet Zhou, Run
Sanz-Jimenez, Pablo
Zhu, Xi-Tong
Feng, Jia-Wu
Shao, Lin
Song, Jia-Ming
Chen, Ling-Ling
author_sort Zhou, Run
collection PubMed
description BACKGROUND: Long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) can play important roles in many biological processes. However, no study of the influence of epigenetics factors or the 3D structure of the genome in their regulation is available in plants. RESULTS: In the current analysis, we identified a total of 15,122 lncRNAs and 7902 circRNAs in three tissues (root, leaf and panicle) in the rice varieties Minghui 63, Zhenshan 97 and their hybrid Shanyou 63. More than 73% of these lncRNAs and parental genes of circRNAs (P-circRNAs) are shared among Oryza sativa with high expression specificity. We found that, compared with protein-coding genes, the loci of these lncRNAs have higher methylation levels and the loci of circRNAs tend to locate in the middle of genes with high CG and CHG methylation. Meanwhile, the activated lncRNAs and P-circRNAs are mainly transcribed from demethylated regions containing CHH methylation. In addition, ~ 53% lncRNAs and ~ 15% P-circRNAs are associated with transposable elements (TEs), especially miniature inverted-repeat transposable elements and RC/Helitron. We didn’t find correlation between the expression of lncRNAs and histone modifications; however, we found that the binding strength and interaction of RNAPII significantly affects lncRNA expression. Interestingly, P-circRNAs tend to combine active histone modifications. Finally, we found that lncRNAs and circRNAs acting as competing-endogenous RNAs have the potential to regulate the expression of genes, such as osa-156 l-5p (related to yield) and osa-miR444a-3p (related to N/P metabolism) confirmed through dual-luciferase reporter assays, with important roles in the growth and development of rice, laying a foundation for future rice breeding analyses. CONCLUSIONS: In conclusion, our study comprehensively analyzed the important regulatory roles of lncRNA/circRNA in the tissue development of Indica rice from multiple perspectives. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-021-00455-2.
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spelling pubmed-78437632021-01-29 Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development Zhou, Run Sanz-Jimenez, Pablo Zhu, Xi-Tong Feng, Jia-Wu Shao, Lin Song, Jia-Ming Chen, Ling-Ling Rice (N Y) Original Article BACKGROUND: Long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) can play important roles in many biological processes. However, no study of the influence of epigenetics factors or the 3D structure of the genome in their regulation is available in plants. RESULTS: In the current analysis, we identified a total of 15,122 lncRNAs and 7902 circRNAs in three tissues (root, leaf and panicle) in the rice varieties Minghui 63, Zhenshan 97 and their hybrid Shanyou 63. More than 73% of these lncRNAs and parental genes of circRNAs (P-circRNAs) are shared among Oryza sativa with high expression specificity. We found that, compared with protein-coding genes, the loci of these lncRNAs have higher methylation levels and the loci of circRNAs tend to locate in the middle of genes with high CG and CHG methylation. Meanwhile, the activated lncRNAs and P-circRNAs are mainly transcribed from demethylated regions containing CHH methylation. In addition, ~ 53% lncRNAs and ~ 15% P-circRNAs are associated with transposable elements (TEs), especially miniature inverted-repeat transposable elements and RC/Helitron. We didn’t find correlation between the expression of lncRNAs and histone modifications; however, we found that the binding strength and interaction of RNAPII significantly affects lncRNA expression. Interestingly, P-circRNAs tend to combine active histone modifications. Finally, we found that lncRNAs and circRNAs acting as competing-endogenous RNAs have the potential to regulate the expression of genes, such as osa-156 l-5p (related to yield) and osa-miR444a-3p (related to N/P metabolism) confirmed through dual-luciferase reporter assays, with important roles in the growth and development of rice, laying a foundation for future rice breeding analyses. CONCLUSIONS: In conclusion, our study comprehensively analyzed the important regulatory roles of lncRNA/circRNA in the tissue development of Indica rice from multiple perspectives. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-021-00455-2. Springer US 2021-01-28 /pmc/articles/PMC7843763/ /pubmed/33507446 http://dx.doi.org/10.1186/s12284-021-00455-2 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Original Article
Zhou, Run
Sanz-Jimenez, Pablo
Zhu, Xi-Tong
Feng, Jia-Wu
Shao, Lin
Song, Jia-Ming
Chen, Ling-Ling
Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development
title Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development
title_full Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development
title_fullStr Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development
title_full_unstemmed Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development
title_short Analysis of Rice Transcriptome Reveals the LncRNA/CircRNA Regulation in Tissue Development
title_sort analysis of rice transcriptome reveals the lncrna/circrna regulation in tissue development
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843763/
https://www.ncbi.nlm.nih.gov/pubmed/33507446
http://dx.doi.org/10.1186/s12284-021-00455-2
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