Dek42 encodes an RNA-binding protein that affects alternative pre-m RNA splicing and maize kernel development
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摘要
RNA-binding proteins(RBPs) play an important role in post-transcriptional gene regulation. However, the functions of RBPs in plants remain poorly understood.Maize kernel mutant dek42 has small defective kernels and lethal seedlings. Dek42 was cloned by Mutator tag isolation and further confirmed by an independent mutant allele and clustered regularly interspaced short palindromic repeats(CRISPR)-CRISPR-associated protein9 materials. Dek42 encodes an RRM_RBM48 type RNA-binding protein that localizes to the nucleus. Dek42 is constitutively expressed in various maize tissues.The dek42 mutation caused a significant reduction in the accumulation of DEK42 protein in mutant kernels.RNA-seq analysis showed that the dek42 mutation significantly disturbed the expression of thousands of genes during maize kernel development. Sequenceanalysis also showed that the dek42 mutation significantly changed alternative splicing in expressed genes, which were especially enriched for the U12-type intron-retained type. Yeast two-hybrid screening identified SF3 a1 as a DEK42-interacting protein. DEK42 also interacts with the spliceosome component U1-70 K. These results suggested that DEK42 participates in the regulation of pre-messenger RNA splicing through its interaction with other spliceosome components. This study showed the function of a newly identified RBP and provided insights into alternative splicing regulation during maize kernel development.
RNA-binding proteins(RBPs) play an important role in post-transcriptional gene regulation. However, the functions of RBPs in plants remain poorly understood.Maize kernel mutant dek42 has small defective kernels and lethal seedlings. Dek42 was cloned by Mutator tag isolation and further confirmed by an independent mutant allele and clustered regularly interspaced short palindromic repeats(CRISPR)-CRISPR-associated protein9 materials. Dek42 encodes an RRM_RBM48 type RNA-binding protein that localizes to the nucleus. Dek42 is constitutively expressed in various maize tissues.The dek42 mutation caused a significant reduction in the accumulation of DEK42 protein in mutant kernels.RNA-seq analysis showed that the dek42 mutation significantly disturbed the expression of thousands of genes during maize kernel development. Sequenceanalysis also showed that the dek42 mutation significantly changed alternative splicing in expressed genes, which were especially enriched for the U12-type intron-retained type. Yeast two-hybrid screening identified SF3 a1 as a DEK42-interacting protein. DEK42 also interacts with the spliceosome component U1-70 K. These results suggested that DEK42 participates in the regulation of pre-messenger RNA splicing through its interaction with other spliceosome components. This study showed the function of a newly identified RBP and provided insights into alternative splicing regulation during maize kernel development.
RNA-binding proteins(RBPs) play an important role in post-transcriptional gene regulation. However, the functions of RBPs in plants remain poorly understood.Maize kernel mutant dek42 has small defective kernels and lethal seedlings. Dek42 was cloned by Mutator tag isolation and further confirmed by an independent mutant allele and clustered regularly interspaced short palindromic repeats(CRISPR)-CRISPR-associated protein9 materials. Dek42 encodes an RRM_RBM48 type RNA-binding protein that localizes to the nucleus. Dek42 is constitutively expressed in various maize tissues.The dek42 mutation caused a significant reduction in the accumulation of DEK42 protein in mutant kernels.RNA-seq analysis showed that the dek42 mutation significantly disturbed the expression of thousands of genes during maize kernel development. Sequenceanalysis also showed that the dek42 mutation significantly changed alternative splicing in expressed genes, which were especially enriched for the U12-type intron-retained type. Yeast two-hybrid screening identified SF3 a1 as a DEK42-interacting protein. DEK42 also interacts with the spliceosome component U1-70 K. These results suggested that DEK42 participates in the regulation of pre-messenger RNA splicing through its interaction with other spliceosome components. This study showed the function of a newly identified RBP and provided insights into alternative splicing regulation during maize kernel development.
引文
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Burd CG,Dreyfuss G(1994)Conserved structures and diversity of functions of RNA-binding proteins.Science 265:615-621
Burge CB,Padgett RA,Sharp PA(1998)Evolutionary fates and origins of U12-type introns.Mol Cell 2:773-785
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Chen XZ,Feng F,Qi WW,Xu LM,Yao DS,Wang Q,Song RT(2017)Dek35 encodes a PPR protein that affects cissplicing of mitochondrial nad4 intron 1 and seed development in maize.Mol Plant 10:427-441
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Jeong S(2017)SR Proteins:Binders,regulators,and connectors of RNA.Mol Cells 40:1-9
Jia HY,Suzuki M,Mc Carty DR(2014)Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks.Wiley Interdiscip Rev Dev Biol 3:135-145
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Antic D,Keene JD(1997)Embryonic lethal abnormal visual RNA-binding proteins involved in growth,differentiation,and posttranscriptional gene expression.Am J Hum Genet61:273-278
Arvidsson S,Kwasniewski M,Ria?opachón DM,Muellerroeber B(2008)Quant Prime-a flexible tool for reliable highthroughput primer design for quantitative PCR.BMCBioinfo 9:465
Barta A,Kalyna M,Lorkovi c ZJ(2008)Plant SR proteins and their functions.Curr Top Microbiol 326:83-102
Bhave MR,Lawrence S,Barton C,Hannah LC(1990)Identification and molecular characterization of Shrunken2c DNA clones of maize.Plant Cell 2:581-588
Brust H,Orzechowski S,Fettke J,Steup M(2013)Starch synthesizing reactions and paths:In vitro and in vivo studies.J Appl Glycosci 60:3-20
Bul eon A,Colonna P,Planchot V,Ball SG(1998)Starch granules:Structure and biosynthesis.Int J Biol Macromol23:85-112
Burd CG,Dreyfuss G(1994)Conserved structures and diversity of functions of RNA-binding proteins.Science 265:615-621
Burge CB,Padgett RA,Sharp PA(1998)Evolutionary fates and origins of U12-type introns.Mol Cell 2:773-785
Chamala S,Feng GQ,Chavarro C,Barbazuk WB(2015)Genome-wide identification of evolutionarily conserved alternative splicing events in flowering plants.Front Bioeng Biotechnol 3:33
Chen XZ,Feng F,Qi WW,Xu LM,Yao DS,Wang Q,Song RT(2017)Dek35 encodes a PPR protein that affects cissplicing of mitochondrial nad4 intron 1 and seed development in maize.Mol Plant 10:427-441
Chung T,Kim CS,Nguyen HN,Meeley RB,Larkins BA(2007)The maize Zmsmu2 gene encodes a putative RNA-splicing factor that affects protein synthesis and RNA processing during endosperm development.Plant Physiol 144:821-835
Chung T,Wang FD,Kim CS,Yadegari R,Larkins BA(2009)Plant SMU-1 and SMU-2 homologues regulate pre-m RNAsplicing and multiple aspects of development.Plant Physiol 151:1498-1512
Cl ery A,Blatter M,Allain FH(2008)RNA recognition motifs:Boring?Not quite.Curr Opin Struct Biol 18:290-298
Day IS,Golovkin M,Palusa SG,Link A,Ali GS,Thomas J,Richardson DN,Reddy ASN(2012)Interactions of SR45,an SR-like protein,with spliceosomal proteins and an intronic sequence:Insights into regulated splicing.Plant J 71:936-947
Feng F,Qi WW,Lv YD,Yan SM,Xu LM,Yang WY,Yuan Y,Chen YH,Zhao H,Song RT(2018)Opaque11 is a central hub of the regulatory network for maize endosperm development and nutrient metabolism.Plant Cell 30:375-396
Feng LN,Zhu J,Wang G,Tang YP,Chen HJ,Jin WB,Wang F,Mei B,Xu ZK,Song RT(2009)Expressional profiling study revealed unique expressional patterns and dramatic expressional divergence of maize a-zein super gene family.Plant Mol Biol 69:649
Fouquet R,Martin F,Fajardo DS,Gault CM,G omez E,Tseung CW,Policht T,Hueros G,Settles AM(2012)Maize rough endosperm3 encodes an RNA splicing factor required for endosperm cell differentiation and has a nonautonomous effect on embryo development.Plant Cell 23:4280-4297
Frame B,Main M,Schick R,Wang K(2011)Genetic transformation using maize immature zygotic embryos.Methods Mol Biol 710:327-341
Gault CM,Martin F,Mei WB,Bai F,Black JB,Barbazuk WB,Settles AM(2017)Aberrant splicing in maize rough endosperm3 reveals a conserved role for U12 splicing in eukaryotic multicellular development.Proc Natl Acad Sci USA 114:E2195-E2204
Glisovic T,Bachorik JL,Yong J,Dreyfuss G(2008)RNA-binding proteins and post-transcriptional gene regulation.FEBSLett 582:1977-1986
Golovkin M,Reddy ASN(1998)The plant U1 small nuclear ribonucleoprotein particle 70K protein interacts with two novel serine/arginine-rich proteins.Plant Cell 10:1637-1647
Golovkin M,Reddy ASN(1999)An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1-70K protein.J Biol Chem 274:36428-36438
Gupta S,Ciungu A,Jameson N,Lal SK(2006)Alternative splicing expression of U1 sn RNP 70K gene is evolutionary conserved between different plant species.DNA Sequence 17:254-261
Hodges PE,Beggs JD(1994)RNA splicing.U2 fulfils a commitment.Curr Biol 4:264-267
Holding DR,Larkins BA(2006)The development and importance of zein protein bodies in maize endosperm.Maydica 51:243-254
Howitt CA,Pogson BJ(2006)Carotenoid accumulation and function in seeds and non-green tissues.Plant Cell Environ29:435-445
Jeong S(2017)SR Proteins:Binders,regulators,and connectors of RNA.Mol Cells 40:1-9
Jia HY,Suzuki M,Mc Carty DR(2014)Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks.Wiley Interdiscip Rev Dev Biol 3:135-145
Kim D,Pertea G,Trapnell C,Pimentel H,Kelley R,Salzberg SL(2013)Top Hat2:Accurate alignment of transcriptomes in the presence of insertions,deletions and gene fusions.Genome Biol 14:R36
Klein P,Oloko M,Roth F,Montel V,Malerba A,Jarmin S,Gidaro T,Popplewell L,Perie S,Guily LSJ,Grange PDL,Antoniou M,Dickson G,Butlerbrowne G,Bastide B,Mouly V,Trollet C(2016)Nuclear poly(A)-binding protein aggregates misplace a pre-m RNA outside of SC35 speckle causing its abnormal splicing.Nucleic Acids Res 44:10929-10945
Letunic I,Copley RR,Bork P(2002)Common exon duplication in animals and its role in alternative splicing.Hum Mol Genet 11:1561-1567
Li JK,Fu JJ,Chen Y,Fan KJ,He C,Zhang ZQ,Li L,Liu YJ,Zheng J,Ren DT,Wang GY(2017)The U6 biogenesis-like 1plays an important role in maize kernel and seedling development by affecting the 30end processing of U6sn RNA.Mol Plant 10:470-482
Livak KJ,Schmittgen TD(2001)Analysis of relative gene expression data using real-time quantitative PCR and the2 DDCTmethod.Methods 25:402-408
Lopato S,Forstner C,Kalyna M,Hilscher J,Langhammer U,Indrapichate K,Lorkovic ZJ,Barta A(2002)Network of interactions of a novel plant-specific Arg/Ser-rich protein,at RSZ33,with at SC35-like splicing factors.J Biol Chem 277:39989-39998
Lorkovi ZJ,Barta A(2002)Genome analysis:RNA recognition motif(RRM)and K homology(KH)domain RNA-binding proteins from the flowering plant Arabidopsis thaliana.Nucleic Acids Res 30:623-635
Lunde BM,Moore C,Varani G(2007)RNA-binding proteins:Modular design for efficient function.Nat Rev Mol Cell Bio8:479-490
Marquez Y,Brown JWS,Simpson CG,Barta A,Kalyna M(2012)Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis.Genome Res22:1184-1195
Marquez Y,H€opfler M,Ayatollahi Z,Barta A,Kalyna M(2015)Unmasking alternative splicing inside protein-coding exons defines exitrons and their role in proteome plasticity.Genome Res 25:995-1007
Matlin AJ,Clark F,Smith CWJ(2005)Understanding alternative splicing:Towards a cellular code.Nat Rev Mol Cell Bio6:386
Mei WB,Liu SZ,Schnable JC,Yeh C,Springer NM,Schnable PS,Barbazuk WB(2017)A comprehensive analysis of alternative splicing in paleopolyploid maize.Front Plant Sci 8:694
Mousavi A,Hotta Y(2005)Glycine-rich proteins.Appl Biochem Biotechnol 120:169-174
Nesic D,Kramer A(2001)Domains in human splicing factors SF3a60 and SF3a66 required for binding to SF3a120,assembly of the 17S U2 sn RNP,and prespliceosome formation.Mol Cell Biol 21:6406-6417
Neuffer MG,Sheridan WF(1980)Defective kernel mutants of maize.I.genetic and lethality studies.Genetics 95:929-944
Pan Q,Shai O,Lee LJ,Frey BJ,Blencowe BJ(2008)Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing.Nat Genet40:1413-1415
Pandit S,Zhou Y,Shiue L,Coutinhomansfield G,Li H,Qiu JS,Huang J,Yeo GW,Ares M,Fu XD(2013)Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing.Mol Cell 50:223-235
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