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Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis

Sexual reproduction in angiosperms requires the production and delivery of two male gametes by a three-celled haploid male gametophyte. This demands synchronized gene expression in a short developmental window to ensure double fertilization and seed set. While transcriptomic changes in developing po...

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Autores principales: Klodová, Božena, Potěšil, David, Steinbachová, Lenka, Michailidis, Christos, Lindner, Ann-Cathrin, Hackenberg, Dieter, Becker, Jörg D., Zdráhal, Zbyněk, Twell, David, Honys, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10363097/
https://www.ncbi.nlm.nih.gov/pubmed/36282332
http://dx.doi.org/10.1007/s00497-022-00452-5
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author Klodová, Božena
Potěšil, David
Steinbachová, Lenka
Michailidis, Christos
Lindner, Ann-Cathrin
Hackenberg, Dieter
Becker, Jörg D.
Zdráhal, Zbyněk
Twell, David
Honys, David
author_facet Klodová, Božena
Potěšil, David
Steinbachová, Lenka
Michailidis, Christos
Lindner, Ann-Cathrin
Hackenberg, Dieter
Becker, Jörg D.
Zdráhal, Zbyněk
Twell, David
Honys, David
author_sort Klodová, Božena
collection PubMed
description Sexual reproduction in angiosperms requires the production and delivery of two male gametes by a three-celled haploid male gametophyte. This demands synchronized gene expression in a short developmental window to ensure double fertilization and seed set. While transcriptomic changes in developing pollen are known for Arabidopsis, no studies have integrated RNA and proteomic data in this model. Further, the role of alternative splicing has not been fully addressed, yet post-transcriptional and post-translational regulation may have a key role in gene expression dynamics during microgametogenesis. We have refined and substantially updated global transcriptomic and proteomic changes in developing pollen for two Arabidopsis accessions. Despite the superiority of RNA-seq over microarray-based platforms, we demonstrate high reproducibility and comparability. We identify thousands of long non-coding RNAs as potential regulators of pollen development, hundreds of changes in alternative splicing and provide insight into mRNA translation rate and storage in developing pollen. Our analysis delivers an integrated perspective of gene expression dynamics in developing Arabidopsis pollen and a foundation for studying the role of alternative splicing in this model. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00497-022-00452-5.
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spelling pubmed-103630972023-07-24 Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis Klodová, Božena Potěšil, David Steinbachová, Lenka Michailidis, Christos Lindner, Ann-Cathrin Hackenberg, Dieter Becker, Jörg D. Zdráhal, Zbyněk Twell, David Honys, David Plant Reprod Original Article Sexual reproduction in angiosperms requires the production and delivery of two male gametes by a three-celled haploid male gametophyte. This demands synchronized gene expression in a short developmental window to ensure double fertilization and seed set. While transcriptomic changes in developing pollen are known for Arabidopsis, no studies have integrated RNA and proteomic data in this model. Further, the role of alternative splicing has not been fully addressed, yet post-transcriptional and post-translational regulation may have a key role in gene expression dynamics during microgametogenesis. We have refined and substantially updated global transcriptomic and proteomic changes in developing pollen for two Arabidopsis accessions. Despite the superiority of RNA-seq over microarray-based platforms, we demonstrate high reproducibility and comparability. We identify thousands of long non-coding RNAs as potential regulators of pollen development, hundreds of changes in alternative splicing and provide insight into mRNA translation rate and storage in developing pollen. Our analysis delivers an integrated perspective of gene expression dynamics in developing Arabidopsis pollen and a foundation for studying the role of alternative splicing in this model. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00497-022-00452-5. Springer Berlin Heidelberg 2022-10-25 2023 /pmc/articles/PMC10363097/ /pubmed/36282332 http://dx.doi.org/10.1007/s00497-022-00452-5 Text en © The Author(s) 2022, corrected publication 2023 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/) .
spellingShingle Original Article
Klodová, Božena
Potěšil, David
Steinbachová, Lenka
Michailidis, Christos
Lindner, Ann-Cathrin
Hackenberg, Dieter
Becker, Jörg D.
Zdráhal, Zbyněk
Twell, David
Honys, David
Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis
title Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis
title_full Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis
title_fullStr Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis
title_full_unstemmed Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis
title_short Regulatory dynamics of gene expression in the developing male gametophyte of Arabidopsis
title_sort regulatory dynamics of gene expression in the developing male gametophyte of arabidopsis
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10363097/
https://www.ncbi.nlm.nih.gov/pubmed/36282332
http://dx.doi.org/10.1007/s00497-022-00452-5
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