Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis

Handle URI:
http://hdl.handle.net/10754/325272
Title:
Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis
Authors:
Cui, Peng ( 0000-0003-3076-0070 ) ; Zhang, ShouDong; Ding, Feng ( 0000-0001-8237-4062 ) ; Ali, Shahjahan; Xiong, Liming ( 0000-0001-8099-0806 )
Abstract:
Background: Sm-like proteins are highly conserved proteins that form the core of the U6 ribonucleoprotein and function in several mRNA metabolism processes, including pre-mRNA splicing. Despite their wide occurrence in all eukaryotes, little is known about the roles of Sm-like proteins in the regulation of splicing.Results: Here, through comprehensive transcriptome analyses, we demonstrate that depletion of the Arabidopsis supersensitive to abscisic acid and drought 1 gene (SAD1), which encodes Sm-like protein 5 (LSm5), promotes an inaccurate selection of splice sites that leads to a genome-wide increase in alternative splicing. In contrast, overexpression of SAD1 strengthens the precision of splice-site recognition and globally inhibits alternative splicing. Further, SAD1 modulates the splicing of stress-responsive genes, particularly under salt-stress conditions. Finally, we find that overexpression of SAD1 in Arabidopsis improves salt tolerance in transgenic plants, which correlates with an increase in splicing accuracy and efficiency for stress-responsive genes.Conclusions: We conclude that SAD1 dynamically controls splicing efficiency and splice-site recognition in Arabidopsis, and propose that this may contribute to SAD1-mediated stress tolerance through the metabolism of transcripts expressed from stress-responsive genes. Our study not only provides novel insights into the function of Sm-like proteins in splicing, but also uncovers new means to improve splicing efficiency and to enhance stress tolerance in a higher eukaryote. 2014 Cui et al.; licensee BioMed Central Ltd.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Cui P, Zhang S, Ding F, Ali S, Xiong L (2014) Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis. Genome Biology 15: R1. doi:10.1186/gb-2014-15-1-r1.
Publisher:
Springer Nature
Journal:
Genome Biology
Issue Date:
7-Jan-2014
DOI:
10.1186/gb-2014-15-1-r1
PubMed ID:
24393432
PubMed Central ID:
PMC4053965
Type:
Article
ISSN:
1474760X
Appears in Collections:
Articles; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorCui, Pengen
dc.contributor.authorZhang, ShouDongen
dc.contributor.authorDing, Fengen
dc.contributor.authorAli, Shahjahanen
dc.contributor.authorXiong, Limingen
dc.date.accessioned2014-08-27T09:44:09Z-
dc.date.available2014-08-27T09:44:09Z-
dc.date.issued2014-01-07en
dc.identifier.citationCui P, Zhang S, Ding F, Ali S, Xiong L (2014) Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis. Genome Biology 15: R1. doi:10.1186/gb-2014-15-1-r1.en
dc.identifier.issn1474760Xen
dc.identifier.pmid24393432en
dc.identifier.doi10.1186/gb-2014-15-1-r1en
dc.identifier.urihttp://hdl.handle.net/10754/325272en
dc.description.abstractBackground: Sm-like proteins are highly conserved proteins that form the core of the U6 ribonucleoprotein and function in several mRNA metabolism processes, including pre-mRNA splicing. Despite their wide occurrence in all eukaryotes, little is known about the roles of Sm-like proteins in the regulation of splicing.Results: Here, through comprehensive transcriptome analyses, we demonstrate that depletion of the Arabidopsis supersensitive to abscisic acid and drought 1 gene (SAD1), which encodes Sm-like protein 5 (LSm5), promotes an inaccurate selection of splice sites that leads to a genome-wide increase in alternative splicing. In contrast, overexpression of SAD1 strengthens the precision of splice-site recognition and globally inhibits alternative splicing. Further, SAD1 modulates the splicing of stress-responsive genes, particularly under salt-stress conditions. Finally, we find that overexpression of SAD1 in Arabidopsis improves salt tolerance in transgenic plants, which correlates with an increase in splicing accuracy and efficiency for stress-responsive genes.Conclusions: We conclude that SAD1 dynamically controls splicing efficiency and splice-site recognition in Arabidopsis, and propose that this may contribute to SAD1-mediated stress tolerance through the metabolism of transcripts expressed from stress-responsive genes. Our study not only provides novel insights into the function of Sm-like proteins in splicing, but also uncovers new means to improve splicing efficiency and to enhance stress tolerance in a higher eukaryote. 2014 Cui et al.; licensee BioMed Central Ltd.en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.rightsThis is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.en
dc.rights.urihttp://creativecommons.org/licenses/by/2.0en
dc.subjectArabidopsis proteinen
dc.subjectLSm5 proteinen
dc.subjectmessenger RNA precursoren
dc.subjectSm like proteinen
dc.subjectunclassified drugen
dc.subjectalternative RNA splicingen
dc.subjectArabidopsisen
dc.subjectcontrolled studyen
dc.subjectexonen
dc.subjectgene mappingen
dc.subjectgene overexpressionen
dc.subjectintronen
dc.subjectphenotypeen
dc.subjectplant geneen
dc.subjectplant genomeen
dc.subjectplant stressen
dc.subjectprotein functionen
dc.subjectreverse transcription polymerase chain reactionen
dc.subjectRNA sequenceen
dc.subjectRNA splicingen
dc.subjectsalt stressen
dc.subjectsalt toleranceen
dc.subjectsequence alignmenten
dc.subjectsequence analysisen
dc.subjectsupersensitive to abscisic acid and drought 1 geneen
dc.subjecttransgenic planten
dc.titleDynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsisen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalGenome Biologyen
dc.identifier.pmcidPMC4053965en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionUnidad Académica de Sistemas Arrecifales (Puerto Morelos), Instituto de Ciencias Del Mar y Limnología, Universidad Nacional Autõnoma de México, Puerto Morelos, QR 77580, Mexicoen
dc.contributor.institutionSchool of Natural Sciences, University of California Merced, 5200 North Lake Road, Merced, CA 95343, United Statesen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorCui, Pengen
kaust.authorZhang, ShouDongen
kaust.authorDing, Fengen
kaust.authorAli, Shahjahanen
kaust.authorXiong, Limingen

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