A KH-Domain RNA-Binding Protein Interacts with FIERY2/CTD Phosphatase-Like 1 and Splicing Factors and Is Important for Pre-mRNA Splicing in Arabidopsis

Handle URI:
http://hdl.handle.net/10754/325278
Title:
A KH-Domain RNA-Binding Protein Interacts with FIERY2/CTD Phosphatase-Like 1 and Splicing Factors and Is Important for Pre-mRNA Splicing in Arabidopsis
Authors:
Chen, Tao; Cui, Peng; Chen, Hao; Ali, Shahjahan; Zhang, ShouDong; Xiong, Liming ( 0000-0001-8099-0806 )
Abstract:
Eukaryotic genomes encode hundreds of RNA-binding proteins, yet the functions of most of these proteins are unknown. In a genetic study of stress signal transduction in Arabidopsis, we identified a K homology (KH)-domain RNA-binding protein, HOS5 (High Osmotic Stress Gene Expression 5), as required for stress gene regulation and stress tolerance. HOS5 was found to interact with FIERY2/RNA polymerase II (RNAP II) carboxyl terminal domain (CTD) phosphatase-like 1 (FRY2/CPL1) both in vitro and in vivo. This interaction is mediated by the first double-stranded RNA-binding domain of FRY2/CPL1 and the KH domains of HOS5. Interestingly, both HOS5 and FRY2/CPL1 also interact with two novel serine-arginine (SR)-rich splicing factors, RS40 and RS41, in nuclear speckles. Importantly, FRY2/CPL1 is required for the recruitment of HOS5. In fry2 mutants, HOS5 failed to be localized in nuclear speckles but was found mainly in the nucleoplasm. hos5 mutants were impaired in mRNA export and accumulated a significant amount of mRNA in the nuclei, particularly under salt stress conditions. Arabidopsis mutants of all these genes exhibit similar stress-sensitive phenotypes. RNA-seq analyses of these mutants detected significant intron retention in many stress-related genes under salt stress but not under normal conditions. Our study not only identified several novel regulators of pre-mRNA processing as important for plant stress response but also suggested that, in addition to RNAP II CTD that is a well-recognized platform for the recruitment of mRNA processing factors, FRY2/CPL1 may also recruit specific factors to regulate the co-transcriptional processing of certain transcripts to deal with environmental challenges. © 2013 Chen et al.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Chen T, Cui P, Chen H, Ali S, Zhang S, et al. (2013) A KH-Domain RNA-Binding Protein Interacts with FIERY2/CTD Phosphatase-Like 1 and Splicing Factors and Is Important for Pre-mRNA Splicing in Arabidopsis. PLoS Genet 9: e1003875. doi:10.1371/journal.pgen.1003875.
Publisher:
Public Library of Science
Journal:
PLoS Genetics
Issue Date:
17-Oct-2013
DOI:
10.1371/journal.pgen.1003875
PubMed ID:
24146632
PubMed Central ID:
PMC3798263
Type:
Article
ISSN:
15537390
Appears in Collections:
Articles; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorChen, Taoen
dc.contributor.authorCui, Pengen
dc.contributor.authorChen, Haoen
dc.contributor.authorAli, Shahjahanen
dc.contributor.authorZhang, ShouDongen
dc.contributor.authorXiong, Limingen
dc.date.accessioned2014-08-27T09:44:34Zen
dc.date.available2014-08-27T09:44:34Zen
dc.date.issued2013-10-17en
dc.identifier.citationChen T, Cui P, Chen H, Ali S, Zhang S, et al. (2013) A KH-Domain RNA-Binding Protein Interacts with FIERY2/CTD Phosphatase-Like 1 and Splicing Factors and Is Important for Pre-mRNA Splicing in Arabidopsis. PLoS Genet 9: e1003875. doi:10.1371/journal.pgen.1003875.en
dc.identifier.issn15537390en
dc.identifier.pmid24146632en
dc.identifier.doi10.1371/journal.pgen.1003875en
dc.identifier.urihttp://hdl.handle.net/10754/325278en
dc.description.abstractEukaryotic genomes encode hundreds of RNA-binding proteins, yet the functions of most of these proteins are unknown. In a genetic study of stress signal transduction in Arabidopsis, we identified a K homology (KH)-domain RNA-binding protein, HOS5 (High Osmotic Stress Gene Expression 5), as required for stress gene regulation and stress tolerance. HOS5 was found to interact with FIERY2/RNA polymerase II (RNAP II) carboxyl terminal domain (CTD) phosphatase-like 1 (FRY2/CPL1) both in vitro and in vivo. This interaction is mediated by the first double-stranded RNA-binding domain of FRY2/CPL1 and the KH domains of HOS5. Interestingly, both HOS5 and FRY2/CPL1 also interact with two novel serine-arginine (SR)-rich splicing factors, RS40 and RS41, in nuclear speckles. Importantly, FRY2/CPL1 is required for the recruitment of HOS5. In fry2 mutants, HOS5 failed to be localized in nuclear speckles but was found mainly in the nucleoplasm. hos5 mutants were impaired in mRNA export and accumulated a significant amount of mRNA in the nuclei, particularly under salt stress conditions. Arabidopsis mutants of all these genes exhibit similar stress-sensitive phenotypes. RNA-seq analyses of these mutants detected significant intron retention in many stress-related genes under salt stress but not under normal conditions. Our study not only identified several novel regulators of pre-mRNA processing as important for plant stress response but also suggested that, in addition to RNAP II CTD that is a well-recognized platform for the recruitment of mRNA processing factors, FRY2/CPL1 may also recruit specific factors to regulate the co-transcriptional processing of certain transcripts to deal with environmental challenges. © 2013 Chen et al.en
dc.language.isoenen
dc.publisherPublic Library of Scienceen
dc.rightsThis is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.en
dc.rightsArchived with thanks to PLoS Geneticsen
dc.subjectdouble stranded RNAen
dc.subjectFIERY2 RNA polymerase 2 carboxyl terminal domain phosphatase like 1 poteinen
dc.subjecthigh osmotic stress gene expression 5en
dc.subjectK homology domain RNA binding proteinen
dc.subjectmembrane proteinen
dc.subjectRNA binding proteinen
dc.subjectRNA polymerase IIen
dc.subjectunclassified drugen
dc.subjectamino terminal sequenceen
dc.subjectArabidopsisen
dc.subjectcarboxy terminal sequenceen
dc.subjectcontrolled studyen
dc.subjectenvironmental stressen
dc.subjectgene controlen
dc.subjectgene frequencyen
dc.subjectgene mappingen
dc.subjectgenetic transcriptionen
dc.subjectgenetic transformationen
dc.subjectin vitro studyen
dc.subjectin vivo studyen
dc.subjectintronen
dc.subjectmolecular recognitionen
dc.subjectphenotypeen
dc.subjectplant growthen
dc.subjectpolyadenylationen
dc.subjectpromoter regionen
dc.subjectprotein bindingen
dc.subjectprotein localizationen
dc.subjectprotein phosphorylationen
dc.subjectprotein protein interactionen
dc.subjectprotein structureen
dc.subjectprotoplasten
dc.subjectreporter geneen
dc.subjectreverse transcription polymerase chain reactionen
dc.subjectRNA sequenceen
dc.subjectRNA splicingen
dc.subjectsalt stressen
dc.subjectsignal transductionen
dc.subjectstressen
dc.subjectArabidopsisen
dc.subjectArabidopsis Proteinsen
dc.subjectCell Nucleusen
dc.subjectGene Expression Regulation, Planten
dc.subjectMutationen
dc.subjectPhosphoprotein Phosphatasesen
dc.subjectProtein Bindingen
dc.subjectProtein Structure, Tertiaryen
dc.subjectRNA Precursorsen
dc.subjectRNA Splicingen
dc.subjectRNA, Double-Strandeden
dc.subjectRNA-Binding Proteinsen
dc.subjectSalinityen
dc.subjectSignal Transductionen
dc.subjectTranscription Factorsen
dc.subjectTranscription, Geneticen
dc.titleA KH-Domain RNA-Binding Protein Interacts with FIERY2/CTD Phosphatase-Like 1 and Splicing Factors and Is Important for Pre-mRNA Splicing in Arabidopsisen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalPLoS Geneticsen
dc.identifier.pmcidPMC3798263en
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.authorAli, Shahjahanen
kaust.authorZhang, ShouDongen
kaust.authorXiong, Limingen
kaust.authorChen, Taoen
kaust.authorChen, Haoen

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