The non-coding RNA SVALKA locus produces a cis-natural antisense transcript that negatively regulates the expression of CBF1 and biomass production at normal temperatures.


Journal

Plant communications
ISSN: 2590-3462
Titre abrégé: Plant Commun
Pays: China
ID NLM: 101769147

Informations de publication

Date de publication:
10 07 2023
Historique:
received: 12 12 2022
revised: 17 01 2023
accepted: 18 01 2023
medline: 13 7 2023
pubmed: 23 1 2023
entrez: 22 1 2023
Statut: ppublish

Résumé

Non-coding transcription is present in all eukaryotic genomes, but we lack fundamental knowledge about its importance for an organism's ability to develop properly. In plants, emerging evidence highlights the essential biological role of non-coding transcription in the regulation of coding transcription. However, we have few molecular insights into this regulation. Here, we show that a long isoform of the long non-coding RNA SVALKA-L (SVK-L) forms a natural antisense transcript to the host gene CBF1 and negatively regulates CBF1 mRNA levels at normal temperatures in the model plant Arabidopsis thaliana. Furthermore, we show detailed evidence for the specific mode of action of SVK-L. This pathway includes the formation of double-stranded RNA that is recognized by the DICER proteins and subsequent downregulation of CBF1 mRNA levels. Thus, the CBF1-SVK regulatory circuit is not only important for its previously known role in cold temperature acclimation but also for biomass production at normal temperatures. Our study characterizes the developmental role of SVK-L and offers mechanistic insight into how biologically important overlapping natural antisense transcripts can act on and fine-tune the steady-state levels of their host gene's mRNA.

Identifiants

pubmed: 36681861
pii: S2590-3462(23)00049-4
doi: 10.1016/j.xplc.2023.100551
pmc: PMC10363475
pii:
doi:

Substances chimiques

RNA, Untranslated 0
RNA, Messenger 0
CBF1 protein, Arabidopsis 0
Trans-Activators 0
Arabidopsis Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

100551

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Références

PLoS Biol. 2004 May;2(5):E104
pubmed: 15024409
Dev Cell. 2018 Feb 5;44(3):348-361.e7
pubmed: 29290588
EMBO J. 2020 Jul 1;39(13):e103630
pubmed: 32449547
Nat Commun. 2018 Nov 1;9(1):4561
pubmed: 30385760
Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11928-33
pubmed: 16081530
Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5424-9
pubmed: 19289849
Curr Biol. 2017 Jan 23;27(2):243-249
pubmed: 28041792
Plant Physiol. 1999 Feb;119(2):463-70
pubmed: 9952441
Cell. 2005 Dec 29;123(7):1279-91
pubmed: 16377568
Plant Physiol. 2020 Feb;182(2):685-691
pubmed: 31843802
Genome Biol. 2005;6(4):R30
pubmed: 15833117
Nat Commun. 2016 Oct 07;7:13031
pubmed: 27713408
Plant Cell. 2010 Feb;22(2):481-96
pubmed: 20190077
Nature. 2009 Dec 10;462(7274):799-802
pubmed: 20010688
Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12984-9
pubmed: 16129836
ScientificWorldJournal. 2013 Jun 26;2013:219798
pubmed: 23878522
Plant Cell. 2009 Mar;21(3):972-84
pubmed: 19270186
Plant Physiol. 2005 Mar;137(3):961-8
pubmed: 15728337
Proc Natl Acad Sci U S A. 2018 Feb 13;115(7):E1485-E1494
pubmed: 29386391
Science. 2010 Jan 1;327(5961):94-7
pubmed: 19965720
Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:571-599
pubmed: 15012220
Nat Rev Mol Cell Biol. 2017 Jan;18(1):18-30
pubmed: 27677860
DNA Res. 2015 Jun;22(3):233-43
pubmed: 25922535
Plant Physiol. 2016 Jun;171(2):1392-406
pubmed: 27208227
Mol Genet Genomics. 2007 May;277(5):533-54
pubmed: 17285309
Genome Biol. 2021 Dec 15;22(1):340
pubmed: 34911561
J Biol Chem. 2008 Feb 22;283(8):4930-42
pubmed: 18096702
Genes Dev. 2005 Sep 1;19(17):2030-40
pubmed: 16140984
Plant Cell. 2006 Sep;18(9):2157-71
pubmed: 16891401
PLoS Genet. 2014 Aug 21;10(8):e1004564
pubmed: 25144737
Genome Res. 2013 Oct;23(10):1730-9
pubmed: 23816784
Trends Plant Sci. 2021 Nov;26(11):1104-1115
pubmed: 34303604
Plant Mol Biol. 2004 Mar;54(5):767-81
pubmed: 15356394
Science. 2003 Aug 1;301(5633):653-7
pubmed: 12893945
Plant J. 2023 Feb;113(3):460-477
pubmed: 36495314
PLoS Genet. 2012;8(11):e1003091
pubmed: 23209442
Plant Cell. 2012 Dec;24(12):4930-47
pubmed: 23221597
Plant Biol (Stuttg). 2011 Mar;13(2):362-7
pubmed: 21309983
New Phytol. 2017 Nov;216(3):854-867
pubmed: 28758689
EMBO J. 2006 Jul 26;25(14):3347-56
pubmed: 16810317
Nature. 2019 May;569(7755):265-269
pubmed: 31043738
Plant Cell Physiol. 2006 Jan;47(1):141-53
pubmed: 16284406
Plant Cell Environ. 2006 Jul;29(7):1259-72
pubmed: 17080948
PLoS One. 2014 Apr 10;9(4):e94270
pubmed: 24722185
EMBO Rep. 2006 Dec;7(12):1216-22
pubmed: 17139297
Genome Biol. 2012;13(3):R20
pubmed: 22439910
PLoS Genet. 2016 Feb 01;12(2):e1005817
pubmed: 26828932
Curr Biol. 2015 Jan 19;25(2):187-193
pubmed: 25557667
Plant Cell. 2014 May 30;26(5):2168-2183
pubmed: 24879427
Science. 1998 Apr 3;280(5360):104-6
pubmed: 9525853
Mol Plant. 2013 May;6(3):704-15
pubmed: 23505223
Mol Cell. 2011 Aug 19;43(4):624-37
pubmed: 21855801
Plant Mol Biol. 2014 Aug;85(6):541-50
pubmed: 24874772
Plant Cell Environ. 2008 Apr;31(4):562-74
pubmed: 18208512
Genome Res. 2014 Mar;24(3):444-53
pubmed: 24402519
Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):E7846-E7855
pubmed: 27856735
Plant Cell. 2008 Aug;20(8):2117-29
pubmed: 18757556
Plant Cell. 2020 Jun;32(6):1845-1867
pubmed: 32213639
Annu Rev Plant Biol. 2014;65:473-503
pubmed: 24579988
Mol Plant. 2020 Jun 1;13(6):894-906
pubmed: 32311530
Plant Physiol. 2003 Oct;133(2):910-8
pubmed: 14500791
Science. 2006 Jul 7;313(5783):68-71
pubmed: 16741077
Science. 2016 Sep 2;353(6303):989-990
pubmed: 27701102
Nucleic Acids Res. 2020 Mar 18;48(5):2332-2347
pubmed: 31863587
Immunity. 2020 Jun 16;52(6):1007-1021.e8
pubmed: 32497523
Plant Cell. 2013 Oct;25(10):4166-82
pubmed: 24096344

Auteurs

Vasiliki Zacharaki (V)

Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90187 Umeå, Sweden.

Shiv Kumar Meena (SK)

Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90187 Umeå, Sweden.

Peter Kindgren (P)

Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90187 Umeå, Sweden. Electronic address: peter.kindgren@slu.se.

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Classifications MeSH