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Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis
Leaf senescence, the last stage of leaf development, is essential for whole-plant fitness as it marks the relocation of nutrients from senescing leaves to reproductive or other developing organs. Temporally coordinated physiological and functional changes along leaf aging are fine-tuned by a highly...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9753222/ https://www.ncbi.nlm.nih.gov/pubmed/36531391 http://dx.doi.org/10.3389/fpls.2022.1068163 |
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author | Kim, Jung Yeon Lee, Juhyeon Kang, Myeong Hoon Trang, Tran Thi My Lee, Jusung Lee, Heeho Jeong, Hyobin Lim, Pyung Ok |
author_facet | Kim, Jung Yeon Lee, Juhyeon Kang, Myeong Hoon Trang, Tran Thi My Lee, Jusung Lee, Heeho Jeong, Hyobin Lim, Pyung Ok |
author_sort | Kim, Jung Yeon |
collection | PubMed |
description | Leaf senescence, the last stage of leaf development, is essential for whole-plant fitness as it marks the relocation of nutrients from senescing leaves to reproductive or other developing organs. Temporally coordinated physiological and functional changes along leaf aging are fine-tuned by a highly regulated genetic program involving multi-layered regulatory mechanisms. Long noncoding RNAs (lncRNAs) are newly emerging as hidden players in many biological processes; however, their contribution to leaf senescence has been largely unknown. Here, we performed comprehensive analyses of RNA-seq data representing all developmental stages of leaves to determine the genome-wide lncRNA landscape along leaf aging. A total of 771 lncRNAs, including 232 unannotated lncRNAs, were identified. Time-course analysis revealed 446 among 771 developmental age-related lncRNAs (AR-lncRNAs). Intriguingly, the expression of AR-lncRNAs was regulated more dynamically in senescing leaves than in growing leaves, revealing the relevant contribution of these lncRNAs to leaf senescence. Further analyses enabled us to infer the function of lncRNAs, based on their interacting miRNA or mRNA partners. We considered functionally diverse lncRNAs including antisense lncRNAs (which regulate overlapping protein-coding genes), competitive endogenous RNAs (ceRNAs; which regulate paired mRNAs using miRNAs as anchors), and mRNA-interacting lncRNAs (which affect the stability of mRNAs). Furthermore, we experimentally validated the senescence regulatory function of three novel AR-lncRNAs including one antisense lncRNA and two mRNA-interacting lncRNAs through molecular and phenotypic analyses. Our study provides a valuable resource of AR-lncRNAs and potential regulatory networks that link the function of coding mRNA and AR-lncRNAs. Together, our results reveal AR-lncRNAs as important elements in the leaf senescence process. |
format | Online Article Text |
id | pubmed-9753222 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-97532222022-12-16 Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis Kim, Jung Yeon Lee, Juhyeon Kang, Myeong Hoon Trang, Tran Thi My Lee, Jusung Lee, Heeho Jeong, Hyobin Lim, Pyung Ok Front Plant Sci Plant Science Leaf senescence, the last stage of leaf development, is essential for whole-plant fitness as it marks the relocation of nutrients from senescing leaves to reproductive or other developing organs. Temporally coordinated physiological and functional changes along leaf aging are fine-tuned by a highly regulated genetic program involving multi-layered regulatory mechanisms. Long noncoding RNAs (lncRNAs) are newly emerging as hidden players in many biological processes; however, their contribution to leaf senescence has been largely unknown. Here, we performed comprehensive analyses of RNA-seq data representing all developmental stages of leaves to determine the genome-wide lncRNA landscape along leaf aging. A total of 771 lncRNAs, including 232 unannotated lncRNAs, were identified. Time-course analysis revealed 446 among 771 developmental age-related lncRNAs (AR-lncRNAs). Intriguingly, the expression of AR-lncRNAs was regulated more dynamically in senescing leaves than in growing leaves, revealing the relevant contribution of these lncRNAs to leaf senescence. Further analyses enabled us to infer the function of lncRNAs, based on their interacting miRNA or mRNA partners. We considered functionally diverse lncRNAs including antisense lncRNAs (which regulate overlapping protein-coding genes), competitive endogenous RNAs (ceRNAs; which regulate paired mRNAs using miRNAs as anchors), and mRNA-interacting lncRNAs (which affect the stability of mRNAs). Furthermore, we experimentally validated the senescence regulatory function of three novel AR-lncRNAs including one antisense lncRNA and two mRNA-interacting lncRNAs through molecular and phenotypic analyses. Our study provides a valuable resource of AR-lncRNAs and potential regulatory networks that link the function of coding mRNA and AR-lncRNAs. Together, our results reveal AR-lncRNAs as important elements in the leaf senescence process. Frontiers Media S.A. 2022-12-01 /pmc/articles/PMC9753222/ /pubmed/36531391 http://dx.doi.org/10.3389/fpls.2022.1068163 Text en Copyright © 2022 Kim, Lee, Kang, Trang, Lee, Lee, Jeong and Lim 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 Kim, Jung Yeon Lee, Juhyeon Kang, Myeong Hoon Trang, Tran Thi My Lee, Jusung Lee, Heeho Jeong, Hyobin Lim, Pyung Ok Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis |
title | Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis
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title_full | Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis
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title_fullStr | Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis
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title_full_unstemmed | Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis
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title_short | Dynamic landscape of long noncoding RNAs during leaf aging in Arabidopsis
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title_sort | dynamic landscape of long noncoding rnas during leaf aging in arabidopsis |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9753222/ https://www.ncbi.nlm.nih.gov/pubmed/36531391 http://dx.doi.org/10.3389/fpls.2022.1068163 |
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