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An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development

BACKGROUND: Light switches on the photomorphogenic development of young plant seedlings, allowing young seedlings to acquire photosynthetic capacities and gain survival fitness. Light regulates gene expression at all levels of the central dogma, including alternative splicing (AS) during the photomo...

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Autores principales: Huang, Chun-Kai, Lin, Wen-Dar, Wu, Shu-Hsing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8827149/
https://www.ncbi.nlm.nih.gov/pubmed/35139889
http://dx.doi.org/10.1186/s13059-022-02620-2
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author Huang, Chun-Kai
Lin, Wen-Dar
Wu, Shu-Hsing
author_facet Huang, Chun-Kai
Lin, Wen-Dar
Wu, Shu-Hsing
author_sort Huang, Chun-Kai
collection PubMed
description BACKGROUND: Light switches on the photomorphogenic development of young plant seedlings, allowing young seedlings to acquire photosynthetic capacities and gain survival fitness. Light regulates gene expression at all levels of the central dogma, including alternative splicing (AS) during the photomorphogenic development. However, accurate determination of full-length (FL) splicing variants has been greatly hampered by short-read RNA sequencing technologies. RESULT: In this study, we adopt PacBio isoform sequencing (Iso-seq) to overcome the limitation of the short-read RNA-seq technologies. Normalized cDNA libraries used for Iso-seq allows for comprehensive and effective identification of FL AS variants. Our analyses reveal more than 30,000 splicing variant models from approximately 16,500 gene loci and additionally identify approximately 700 previously unannotated genes. Among the variants, approximately 12,000 represent new gene models. Intron retention (IR) is the most frequently observed form of variants, and many IR-containing AS variants show evidence of engagement in translation. Our study reveals the formation of heterodimers of transcription factors composed of annotated and IR-containing AS variants. Moreover, transgenic plants overexpressing the IR forms of two B-BOX DOMAIN PROTEINs exhibits light-hypersensitive phenotypes, suggesting their regulatory roles in modulating optimal light responses. CONCLUSIONS: This study provides an accurate and comprehensive portrait of full-length transcript isoforms and experimentally confirms the presence of de novo synthesized AS variants that impose regulatory functions in photomorphogenic development in Arabidopsis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02620-2.
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spelling pubmed-88271492022-02-10 An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development Huang, Chun-Kai Lin, Wen-Dar Wu, Shu-Hsing Genome Biol Research BACKGROUND: Light switches on the photomorphogenic development of young plant seedlings, allowing young seedlings to acquire photosynthetic capacities and gain survival fitness. Light regulates gene expression at all levels of the central dogma, including alternative splicing (AS) during the photomorphogenic development. However, accurate determination of full-length (FL) splicing variants has been greatly hampered by short-read RNA sequencing technologies. RESULT: In this study, we adopt PacBio isoform sequencing (Iso-seq) to overcome the limitation of the short-read RNA-seq technologies. Normalized cDNA libraries used for Iso-seq allows for comprehensive and effective identification of FL AS variants. Our analyses reveal more than 30,000 splicing variant models from approximately 16,500 gene loci and additionally identify approximately 700 previously unannotated genes. Among the variants, approximately 12,000 represent new gene models. Intron retention (IR) is the most frequently observed form of variants, and many IR-containing AS variants show evidence of engagement in translation. Our study reveals the formation of heterodimers of transcription factors composed of annotated and IR-containing AS variants. Moreover, transgenic plants overexpressing the IR forms of two B-BOX DOMAIN PROTEINs exhibits light-hypersensitive phenotypes, suggesting their regulatory roles in modulating optimal light responses. CONCLUSIONS: This study provides an accurate and comprehensive portrait of full-length transcript isoforms and experimentally confirms the presence of de novo synthesized AS variants that impose regulatory functions in photomorphogenic development in Arabidopsis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02620-2. BioMed Central 2022-02-09 /pmc/articles/PMC8827149/ /pubmed/35139889 http://dx.doi.org/10.1186/s13059-022-02620-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Huang, Chun-Kai
Lin, Wen-Dar
Wu, Shu-Hsing
An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development
title An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development
title_full An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development
title_fullStr An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development
title_full_unstemmed An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development
title_short An improved repertoire of splicing variants and their potential roles in Arabidopsis photomorphogenic development
title_sort improved repertoire of splicing variants and their potential roles in arabidopsis photomorphogenic development
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8827149/
https://www.ncbi.nlm.nih.gov/pubmed/35139889
http://dx.doi.org/10.1186/s13059-022-02620-2
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