Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia

Retention of RNA in the nucleus precisely regulates the time and rate of translation and controls transcriptional bursts that can generate profound variability in mRNA levels among identical cells in tissues. In this study, we investigated the function of Cajal bodies (CBs) in RNA retention in <i...

Full description

Bibliographic Details
Main Authors: Sylwia Górka, Dawid Kubiak, Małgorzata Ciesińska, Katarzyna Niedojadło, Jarosław Tyburski, Janusz Niedojadło
Format: Article
Language:English
Published: MDPI AG 2022-07-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/14/7568
_version_ 1797433518011187200
author Sylwia Górka
Dawid Kubiak
Małgorzata Ciesińska
Katarzyna Niedojadło
Jarosław Tyburski
Janusz Niedojadło
author_facet Sylwia Górka
Dawid Kubiak
Małgorzata Ciesińska
Katarzyna Niedojadło
Jarosław Tyburski
Janusz Niedojadło
author_sort Sylwia Górka
collection DOAJ
description Retention of RNA in the nucleus precisely regulates the time and rate of translation and controls transcriptional bursts that can generate profound variability in mRNA levels among identical cells in tissues. In this study, we investigated the function of Cajal bodies (CBs) in RNA retention in <i>A. thaliana</i> leaf nuclei during hypoxia stress was investigated. It was observed that in <i>ncb-1</i> mutants with a complete absence of CBs, the accumulation of poly(A<sup>+</sup>) RNA in the leaf nuclei was lower than that in wt under stress. Moreover, unlike in root cells, CBs store less RNA, and RNA retention in the nuclei is much less intense. Our results reveal that the function of CBs in the accumulation of RNA in nuclei under stress depends on the plant organ. Additionally, in <i>ncb-1</i>, retention of introns of mRNA RPB1 (largest subunit of RNA polymerase II) mRNA was observed. However, this isoform is highly accumulated in the nucleus. It thus follows that intron retention in transcripts is more important than CBs for the accumulation of RNA in nuclei. Accumulated mRNAs with introns in the nucleus could escape transcript degradation by NMD (nonsense-mediated mRNA decay). From non-fully spliced mRNAs in <i>ncb-1</i> nuclei, whose levels increase during hypoxia, introns are removed during reoxygenation. Then, the mRNA is transferred to the cytoplasm, and the RPB1 protein is translated. Despite the accumulation of isoforms in nuclei with retention of introns in reoxygenation, <i>ncb-1</i> coped much worse with long hypoxia, and manifested faster yellowing and shrinkage of leaves.
first_indexed 2024-03-09T10:18:06Z
format Article
id doaj.art-2fea331ca7c7437c82a0cb39a1fcf595
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-09T10:18:06Z
publishDate 2022-07-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-2fea331ca7c7437c82a0cb39a1fcf5952023-12-01T22:14:02ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-07-012314756810.3390/ijms23147568Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to HypoxiaSylwia Górka0Dawid Kubiak1Małgorzata Ciesińska2Katarzyna Niedojadło3Jarosław Tyburski4Janusz Niedojadło5Department of Cellular and Molecular Biology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń, PolandDepartment of Cellular and Molecular Biology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń, PolandDepartment of Cellular and Molecular Biology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń, PolandDepartment of Cellular and Molecular Biology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń, PolandChair of Plant Physiology and Biotechnology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń, PolandDepartment of Cellular and Molecular Biology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń, PolandRetention of RNA in the nucleus precisely regulates the time and rate of translation and controls transcriptional bursts that can generate profound variability in mRNA levels among identical cells in tissues. In this study, we investigated the function of Cajal bodies (CBs) in RNA retention in <i>A. thaliana</i> leaf nuclei during hypoxia stress was investigated. It was observed that in <i>ncb-1</i> mutants with a complete absence of CBs, the accumulation of poly(A<sup>+</sup>) RNA in the leaf nuclei was lower than that in wt under stress. Moreover, unlike in root cells, CBs store less RNA, and RNA retention in the nuclei is much less intense. Our results reveal that the function of CBs in the accumulation of RNA in nuclei under stress depends on the plant organ. Additionally, in <i>ncb-1</i>, retention of introns of mRNA RPB1 (largest subunit of RNA polymerase II) mRNA was observed. However, this isoform is highly accumulated in the nucleus. It thus follows that intron retention in transcripts is more important than CBs for the accumulation of RNA in nuclei. Accumulated mRNAs with introns in the nucleus could escape transcript degradation by NMD (nonsense-mediated mRNA decay). From non-fully spliced mRNAs in <i>ncb-1</i> nuclei, whose levels increase during hypoxia, introns are removed during reoxygenation. Then, the mRNA is transferred to the cytoplasm, and the RPB1 protein is translated. Despite the accumulation of isoforms in nuclei with retention of introns in reoxygenation, <i>ncb-1</i> coped much worse with long hypoxia, and manifested faster yellowing and shrinkage of leaves.https://www.mdpi.com/1422-0067/23/14/7568Cajal bodiesnuclear retentionintron retentionhypoxia
spellingShingle Sylwia Górka
Dawid Kubiak
Małgorzata Ciesińska
Katarzyna Niedojadło
Jarosław Tyburski
Janusz Niedojadło
Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia
International Journal of Molecular Sciences
Cajal bodies
nuclear retention
intron retention
hypoxia
title Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia
title_full Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia
title_fullStr Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia
title_full_unstemmed Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia
title_short Function of Cajal Bodies in Nuclear RNA Retention in <i>A. thaliana</i> Leaves Subjected to Hypoxia
title_sort function of cajal bodies in nuclear rna retention in i a thaliana i leaves subjected to hypoxia
topic Cajal bodies
nuclear retention
intron retention
hypoxia
url https://www.mdpi.com/1422-0067/23/14/7568
work_keys_str_mv AT sylwiagorka functionofcajalbodiesinnuclearrnaretentioniniathalianaileavessubjectedtohypoxia
AT dawidkubiak functionofcajalbodiesinnuclearrnaretentioniniathalianaileavessubjectedtohypoxia
AT małgorzataciesinska functionofcajalbodiesinnuclearrnaretentioniniathalianaileavessubjectedtohypoxia
AT katarzynaniedojadło functionofcajalbodiesinnuclearrnaretentioniniathalianaileavessubjectedtohypoxia
AT jarosławtyburski functionofcajalbodiesinnuclearrnaretentioniniathalianaileavessubjectedtohypoxia
AT januszniedojadło functionofcajalbodiesinnuclearrnaretentioniniathalianaileavessubjectedtohypoxia