Dissecting conserved cis-regulatory modules of Glu-1 promoters which confer the highly active endosperm-specific expression via stable wheat transformation
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摘要
Wheat high-molecular-weight glutenin subunits(HMW-GS) determine dough elasticity and play an essential role in processing quality. HMW-GS are encoded by Glu-1 genes and controlled primarily at transcriptional level, implemented through the interactions between cis-acting elements and trans-acting factors. However, transcriptional mechanism of Glu-1 genes remains elusive. Here we made a comprehensive analysis of cis-regulatory elements within 1-kb upstream of the Glu-1 start codon(-1000 to-1) and identified 30 conserved motifs. Based on motif distribution pattern, three conserved cis-regulatory modules(CCRMs), CCRM1(-300 to-101), CCRM2(-650 to-400), and CCRM3(-950 to-750), were defined, and their functions were characterized in wheat stable transgenic lines transformed with progressive 5′ deletion promoter::GUS fusion constructs. GUS staining, qP CR and enzyme activity assays indicated that CCRM2 and CCRM3 could enhance the expression level of Glu-1, whereas the 300-bp promoter(-300 to-1), spanning CCRM1 and core region(-100 to-1), was enough to ensure accurate Glu-1 initiation at 7 days after flowering(DAF) and shape its spatiotemporal expression pattern during seed development. Further transgenic assays demonstrated that CCRM1-2(-300 to-209) containing Complete HMW Enhancer(-246 to-209) was important for expression level but had no effect on expression specificity in the endosperm. In contrast, CCRM1-1(-208 to-101) was critical for both expression specificity and level of Glu-1. Our findings not only provide new insights to uncover Glu-1 transcription regulatory machinery but also lay foundations for modifying Glu-1 expression.
Wheat high-molecular-weight glutenin subunits(HMW-GS) determine dough elasticity and play an essential role in processing quality. HMW-GS are encoded by Glu-1 genes and controlled primarily at transcriptional level, implemented through the interactions between cis-acting elements and trans-acting factors. However, transcriptional mechanism of Glu-1 genes remains elusive. Here we made a comprehensive analysis of cis-regulatory elements within 1-kb upstream of the Glu-1 start codon(-1000 to-1) and identified 30 conserved motifs. Based on motif distribution pattern, three conserved cis-regulatory modules(CCRMs), CCRM1(-300 to-101), CCRM2(-650 to-400), and CCRM3(-950 to-750), were defined, and their functions were characterized in wheat stable transgenic lines transformed with progressive 5′ deletion promoter::GUS fusion constructs. GUS staining, qP CR and enzyme activity assays indicated that CCRM2 and CCRM3 could enhance the expression level of Glu-1, whereas the 300-bp promoter(-300 to-1), spanning CCRM1 and core region(-100 to-1), was enough to ensure accurate Glu-1 initiation at 7 days after flowering(DAF) and shape its spatiotemporal expression pattern during seed development. Further transgenic assays demonstrated that CCRM1-2(-300 to-209) containing Complete HMW Enhancer(-246 to-209) was important for expression level but had no effect on expression specificity in the endosperm. In contrast, CCRM1-1(-208 to-101) was critical for both expression specificity and level of Glu-1. Our findings not only provide new insights to uncover Glu-1 transcription regulatory machinery but also lay foundations for modifying Glu-1 expression.
Wheat high-molecular-weight glutenin subunits(HMW-GS) determine dough elasticity and play an essential role in processing quality. HMW-GS are encoded by Glu-1 genes and controlled primarily at transcriptional level, implemented through the interactions between cis-acting elements and trans-acting factors. However, transcriptional mechanism of Glu-1 genes remains elusive. Here we made a comprehensive analysis of cis-regulatory elements within 1-kb upstream of the Glu-1 start codon(-1000 to-1) and identified 30 conserved motifs. Based on motif distribution pattern, three conserved cis-regulatory modules(CCRMs), CCRM1(-300 to-101), CCRM2(-650 to-400), and CCRM3(-950 to-750), were defined, and their functions were characterized in wheat stable transgenic lines transformed with progressive 5′ deletion promoter::GUS fusion constructs. GUS staining, qP CR and enzyme activity assays indicated that CCRM2 and CCRM3 could enhance the expression level of Glu-1, whereas the 300-bp promoter(-300 to-1), spanning CCRM1 and core region(-100 to-1), was enough to ensure accurate Glu-1 initiation at 7 days after flowering(DAF) and shape its spatiotemporal expression pattern during seed development. Further transgenic assays demonstrated that CCRM1-2(-300 to-209) containing Complete HMW Enhancer(-246 to-209) was important for expression level but had no effect on expression specificity in the endosperm. In contrast, CCRM1-1(-208 to-101) was critical for both expression specificity and level of Glu-1. Our findings not only provide new insights to uncover Glu-1 transcription regulatory machinery but also lay foundations for modifying Glu-1 expression.
引文
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[2]P.R.Shewry,Wheat,J.Exp.Bot.60(2009)1537-1553.
[3]G.Branlard,M.Dardevet,Diversity of grain protein and bread wheat quality,J.Cereal Sci.3(1985)345-354.
[4]P.I.Payne,M.A.Nightingale,A.F.Krattiger,L.M.Holt,The relationship between HMW glutenin subunit composition and the bread-making quality of British-grown wheat varieties,J.Sci.Food Agric.40(1987)51-65.
[5]N.G.Halford,J.M.Field,H.Blair,P.Urwin,K.Moore,L.Robert,R.Thompson,R.B.Flavell,A.S.Tatham,P.R.Shewry,Analysis of HMW glutenin subunits encoded by chromosome 1A of bread wheat(Triticum aestivum L.)indicates quantitative effects on grain quality,Theor.Appl.Genet.83(1992)373-378.
[6]Z.H.He,L.Liu,X.C.Xia,J.J.Liu,R.J.Pe?a,Composition of HMWand LMW glutenin subunits and their effects on dough properties,pan bread,and noodle quality of Chinese bread wheats,Cereal Chem.82(2005)345-350.
[7]P.I.Payne,Genetics of wheat storage proteins and the effect of allelic variation on bread-making quality,Annu.Rev.Plant Physiol.38(1987)141-153.
[8]A.Rasheed,X.C.Xia,Y.M.Yan,R.Appels,T.Mahmood,Z.H.He,Wheat seed storage proteins:advances in molecular genetics,diversity and breeding applications,J.Cereal Sci.60(2014)11-24.
[9]C.Lamacchia,P.R.Shewry,N.Di Fonzo,J.L.Forsyth,N.Harris,P.A.Lazzeri,J.A.Napier,N.G.Halford,P.Barcelo,Endospermspecific activity of a storage protein gene promoter in transgenic wheat seed,J.Exp.Bot.52(2001)243-250.
[10]P.R.Shewry,C.Underwood,Y.F.Wan,A.Lovegrove,D.Bhandari,G.Toole,E.N.C.Mills,K.Denyer,R.A.C.Mitchell,Storage product synthesis and accumulation in developing grains of wheat,J.Cereal Sci.50(2009)106-112.
[11]J.Verdier,R.D.Thompson,Transcriptional regulation of storage protein synthesis during dicotyledon seed filling,Plant Cell Physiol.49(2008)1263-1271.
[12]T.Kawakatsu,F.Takaiwa,Cereal seed storage protein synthesis:fundamental processes for recombinant protein production in cereal grains,Plant Biotechnol.J.8(2010)939-953.
[13]R.J.Schmidt,M.Ketudat,M.J.Aukerman,G.Hoschek,Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes,Plant Cell 4(1992)689-700.
[14]J.Vicente-Carbajosa,S.P.Moose,R.L.Parsons,R.J.Schmidt,Amaize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2,Proc.Natl.Acad.Sci.U.S.A.94(1997)7685-7690.
[15]M.A.Moreno-Risueno,N.Gonzalez,I.Diaz,F.Parcy,P.Carbonero,J.Vicente-Carbajosa,FUSCA3 from barley unveils a common transcriptional regulation of seedspecific genes between cereals and Arabidopsis,Plant J.53(2008)882-894.
[16]C.Ravel,S.Fiquet,J.Boudet,M.Dardevet,J.Vincent,M.Merlino,R.Michard,P.Martre,Conserved cis-regulatory modules in promoters of genes encoding wheat high-molecular-weight glutenin subunits,Front.Plant Sci.5(2014)621.
[17]W.W.Guo,H.Yang,Y.Q.Liu,Y.J.Gao,Z.F.Ni,H.R.Peng,M.M.Xin,Z.R.Hu,Q.X.Sun,Y.Y.Yao,The wheat transcription factor TaGAMyb recruits histone acetyltransferase and activates the expression of a high molecular weight glutenin subunit gene,Plant J.84(2015)347-359.
[18]F.S.Sun,X.Y.Liu,Q.H.Wei,J.N.Liu,T.X.Yang,L.Y.Jia,Y.S.Wang,G.X.Yang,G.Y.He,Functional characterization of TaFUSCA3,a B3-superfamily transcription factor gene in the wheat,Front.Plant Sci.8(2017)1133.
[19]J.C.Kridl,J.Vieira,I.Rubenstein,J.Messing,Nucleotide sequence analysis of a zein genomic clone with a short open reading frame,Gene 28(1984)113-118.
[20]B.G.Forde,A.Heyworth,J.Pywell,M.Kreis,Nucleotide sequence of a B1 hordein gene and the identification of possible upstream regulatory elements in endosperm storage protein genes from barley,wheat and maize,Nucleic Acids Res.13(1985)7327-7339.
[21]M.Kreis,P.R.Shewry,B.Forde,B.J.Miflin,Structure and evolution of seed storage proteins and their genes with particular reference to those of wheat,barley and rye,Oxford Surv.Plant Mol.Cell Biol.2(1985)253-317.
[22]H.Hartings,N.Lazzaroni,P.A.Marsan,A.Aragay,R.Thompson,F.Salamini,N.Di Fonzo,J.Palau,M.Motto,The b-32 protein from maize endosperm:characterization of genomic sequences encoding two alternative central domains,Plant Mol.Biol.14(1990)1031-1040.
[23]C.Y.Wu,A.Suzuki,H.Washida,F.Takaiwa,The GCN4 motif in a rice glutelin gene is essential for endosperm-specific gene expression and is activated by Opaque-2 in transgenic rice plants,Plant J.14(1998)673-683.
[24]C.Y.Wu,H.Washida,Y.Onodera,K.Harada,F.Takaiwa,Quantitative nature of the Prolamin-box,ACGT and AACAmotifs in a rice glutelin gene promoter:minimal cis-element requirements for endosperm-specific gene expression,Plant J.23(2000)415-421.
[25]F.Takaiwa,U.Yamanouchi,T.Yoshihara,H.Washida,F.Tanabe,A.Kato,K.Yamada,Characterization of common cisregulatory elements responsible for the endosperm-specific expression of members of the rice glutelin multigene family,Plant Mol.Biol.30(1996)1207-1221.
[26]H.Baumlein,I.Nagy,R.Villarroel,D.Inze,U.Wobus,Cisanalysis of a seed protein gene promoter:the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene,Plant J.2(1992)233-239.
[27]J.M.Lelievre,L.Oliveira,N.C.Nielsen,5'-CATGCAT-3′elements modulate the expression of glycinin genes,Plant Physiol.98(1992)387-391.
[28]T.Fujiwara,R.N.Beachy,Tissue-specific and temporal regulation of aβ-conglycinin gene:roles of the RY repeat and other cis-acting elements,Plant Mol.Biol.24(1994)261-272.
[29]M.S.Thomas,R.B.Flavell,Identification of an enhancer element for the endosperm-specific expression of high molecular weight glutenin,Plant Cell 2(1990)1171-1180.
[30]F.Norre,C.Peyrot,C.Garcia,I.Rance,J.Drevet,M.Theisen,V.Gruber,Powerful effect of an atypical bifactorial endosperm box from wheat HMWG-Dx5 promoter in maize endosperm,Plant Mol.Biol.50(2002)699-712.
[31]Y.K.Geng,B.S.Pang,C.Y.Hao,S.J.Tang,X.Y.Zhang,T.Li,Expression of wheat high molecular weight glutenin subunit1Bx is affected by large insertions and deletions located in the upstream flanking sequences,PLoS One 9(2014),e105363.
[32]R.Thilmony,M.E.Guttman,J.Lin,A.E.Blechl,The wheat HMW-glutenin 1Dy10 gene promoter controls endosperm expression in Brachypodium distachyon,GM Crops Food 5(2014)36-43.
[33]A.Furtado,R.J.Henry,F.Takaiwa,Comparison of promoters in transgenic rice,Plant Biotechnol.J.6(2008)679-693.
[34]J.S.Michaloski,P.A.Galante,B.Malnic,Identification of potential regulatory motifs in odorant receptor genes by analysis of promoter sequences,Genome Res.16(2006)1091-1098.
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