MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress

MicroRNAs (miRNAs) are major regulators of gene expression during plant development under normal and stress conditions. In this study, we analyzed the expression of 150 conserved miRNAs during drought stress applied to barley ready to flower. The dynamics of miRNAs expression was also observed after...

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Main Authors: Aleksandra Swida-Barteczka, Andrzej Pacak, Katarzyna Kruszka, Przemyslaw Nuc, Wojciech M. Karlowski, Artur Jarmolowski, Zofia Szweykowska-Kulinska
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1124785/full
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author Aleksandra Swida-Barteczka
Andrzej Pacak
Katarzyna Kruszka
Przemyslaw Nuc
Wojciech M. Karlowski
Artur Jarmolowski
Zofia Szweykowska-Kulinska
author_facet Aleksandra Swida-Barteczka
Andrzej Pacak
Katarzyna Kruszka
Przemyslaw Nuc
Wojciech M. Karlowski
Artur Jarmolowski
Zofia Szweykowska-Kulinska
author_sort Aleksandra Swida-Barteczka
collection DOAJ
description MicroRNAs (miRNAs) are major regulators of gene expression during plant development under normal and stress conditions. In this study, we analyzed the expression of 150 conserved miRNAs during drought stress applied to barley ready to flower. The dynamics of miRNAs expression was also observed after rewatering. Target messenger RNA (mRNAs) were experimentally identified for all but two analyzed miRNAs, and 41 of the targets were not reported before. Drought stress applied to barley induced accelerated flowering coordinated by a pair of two differently expressed miRNAs originating from a single precursor: hvu-miR172b-3p and hvu-miR172b-5p. Increased expression of miRNA172b-3p during drought leads to the downregulation of four APETALA2(AP2)-like genes by their mRNA cleavage. In parallel, the downregulation of the miRNA172b-5p level results in an increased level of a newly identified target, trehalose-6-phosphate synthase, a key enzyme in the trehalose biosynthesis pathway. Therefore, drought-treated plants have higher trehalose content, a known osmoprotectant, whose level is rapidly dropping after watering. In addition, trehalose-6-phosphate, an intermediate of the trehalose synthesis pathway, is known to induce flowering. The hvu-miRNA172b-5p/trehalose-6-phosphate synthase and hvu-miRNA172b-3p/AP2-like create a module leading to osmoprotection and accelerated flowering induction during drought.
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spelling doaj.art-92fbcb6afafe46ab81b8eb226b7091ab2023-03-06T05:45:23ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-03-011410.3389/fpls.2023.11247851124785MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stressAleksandra Swida-Barteczka0Andrzej Pacak1Katarzyna Kruszka2Przemyslaw Nuc3Wojciech M. Karlowski4Artur Jarmolowski5Zofia Szweykowska-Kulinska6Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandDepartment of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandDepartment of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandDepartment of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandDepartment of Computational Biology, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandDepartment of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandDepartment of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, PolandMicroRNAs (miRNAs) are major regulators of gene expression during plant development under normal and stress conditions. In this study, we analyzed the expression of 150 conserved miRNAs during drought stress applied to barley ready to flower. The dynamics of miRNAs expression was also observed after rewatering. Target messenger RNA (mRNAs) were experimentally identified for all but two analyzed miRNAs, and 41 of the targets were not reported before. Drought stress applied to barley induced accelerated flowering coordinated by a pair of two differently expressed miRNAs originating from a single precursor: hvu-miR172b-3p and hvu-miR172b-5p. Increased expression of miRNA172b-3p during drought leads to the downregulation of four APETALA2(AP2)-like genes by their mRNA cleavage. In parallel, the downregulation of the miRNA172b-5p level results in an increased level of a newly identified target, trehalose-6-phosphate synthase, a key enzyme in the trehalose biosynthesis pathway. Therefore, drought-treated plants have higher trehalose content, a known osmoprotectant, whose level is rapidly dropping after watering. In addition, trehalose-6-phosphate, an intermediate of the trehalose synthesis pathway, is known to induce flowering. The hvu-miRNA172b-5p/trehalose-6-phosphate synthase and hvu-miRNA172b-3p/AP2-like create a module leading to osmoprotection and accelerated flowering induction during drought.https://www.frontiersin.org/articles/10.3389/fpls.2023.1124785/fullbarleydroughtMicroRNAsfloweringtrehalose-6-phosphate synthaseAPETALA2
spellingShingle Aleksandra Swida-Barteczka
Andrzej Pacak
Katarzyna Kruszka
Przemyslaw Nuc
Wojciech M. Karlowski
Artur Jarmolowski
Zofia Szweykowska-Kulinska
MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress
Frontiers in Plant Science
barley
drought
MicroRNAs
flowering
trehalose-6-phosphate synthase
APETALA2
title MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress
title_full MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress
title_fullStr MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress
title_full_unstemmed MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress
title_short MicroRNA172b-5p/trehalose-6-phosphate synthase module stimulates trehalose synthesis and microRNA172b-3p/AP2-like module accelerates flowering in barley upon drought stress
title_sort microrna172b 5p trehalose 6 phosphate synthase module stimulates trehalose synthesis and microrna172b 3p ap2 like module accelerates flowering in barley upon drought stress
topic barley
drought
MicroRNAs
flowering
trehalose-6-phosphate synthase
APETALA2
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1124785/full
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