TaZIM-A1 negatively regulates flowering time in common wheat(Triticum aestivum L.)
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摘要
Flowering time is a critical determinant of regional adaptation for crops and has strong effects on crop yields. Here, we report that TaZIM-A1, an atypical GATAlike transcription factor, is a negative regulator of flowering in wheat. TaZIM-A1 possessed weak transcriptional repression activity, with its CCT domain functioning as the major inhibitory region. TaZIM-A1 expression exhibited a typical circadian oscillation pattern under various light regimes.Overexpression of TaZIM-A1 caused a delay in flowering time and a decrease in thousand-kernel weight(TKW) in wheat under long-day conditions. Moreover, TaZIM-A1 directly bound to the promoters of TaCO-1 and TaFT-1 and downregulated their expression. Sequence analysis of a collection of common wheat cultivars identified three and two haplotypes for TaZIM-A1 and TaZIM-B1, respectively. Association analysis revealed that TaZIM-A1-HapI/-HapIII and TaZIMB1-HapI have undergone strong positive selection during modern wheat breeding, likely due to their association with earlier heading and higher TKW. Diagnostic markers were developed for these haplotypes that can be used for wheat cultivar improvement, via marker-assisted breeding.
Flowering time is a critical determinant of regional adaptation for crops and has strong effects on crop yields. Here, we report that TaZIM-A1, an atypical GATAlike transcription factor, is a negative regulator of flowering in wheat. TaZIM-A1 possessed weak transcriptional repression activity, with its CCT domain functioning as the major inhibitory region. TaZIM-A1 expression exhibited a typical circadian oscillation pattern under various light regimes.Overexpression of TaZIM-A1 caused a delay in flowering time and a decrease in thousand-kernel weight(TKW) in wheat under long-day conditions. Moreover, TaZIM-A1 directly bound to the promoters of TaCO-1 and TaFT-1 and downregulated their expression. Sequence analysis of a collection of common wheat cultivars identified three and two haplotypes for TaZIM-A1 and TaZIM-B1, respectively. Association analysis revealed that TaZIM-A1-HapI/-HapIII and TaZIMB1-HapI have undergone strong positive selection during modern wheat breeding, likely due to their association with earlier heading and higher TKW. Diagnostic markers were developed for these haplotypes that can be used for wheat cultivar improvement, via marker-assisted breeding.
Flowering time is a critical determinant of regional adaptation for crops and has strong effects on crop yields. Here, we report that TaZIM-A1, an atypical GATAlike transcription factor, is a negative regulator of flowering in wheat. TaZIM-A1 possessed weak transcriptional repression activity, with its CCT domain functioning as the major inhibitory region. TaZIM-A1 expression exhibited a typical circadian oscillation pattern under various light regimes.Overexpression of TaZIM-A1 caused a delay in flowering time and a decrease in thousand-kernel weight(TKW) in wheat under long-day conditions. Moreover, TaZIM-A1 directly bound to the promoters of TaCO-1 and TaFT-1 and downregulated their expression. Sequence analysis of a collection of common wheat cultivars identified three and two haplotypes for TaZIM-A1 and TaZIM-B1, respectively. Association analysis revealed that TaZIM-A1-HapI/-HapIII and TaZIMB1-HapI have undergone strong positive selection during modern wheat breeding, likely due to their association with earlier heading and higher TKW. Diagnostic markers were developed for these haplotypes that can be used for wheat cultivar improvement, via marker-assisted breeding.
引文
An HL,Roussot C,Suarez-Lopez P,Corbesler L,Vincent C,Pineiro M,Hepworth S,Mouradov A,Justin S,Turnbull C,Coupland G(2004)CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis.Development 131:3615-3626
Arguello-Astorga G,Herrera-Estrella L(1998)Evolution of light-regulated plant promoters.Annu Rev Plant Physiol49:525-555
Beales J,Turner A,Griffiths S,Snape JW,Laurie DA(2007)A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat(Triticum aestivum L.).Theor Appl Genet 115:721-733
Bi HH,Sun YW,Xiao YG,Xia LQ(2014)Characterization of DFRallelic variations and their associations with pre-harvest sprouting resistance in a set of red-grained Chinese wheat germplasm.Euphytica 195:197-207
Bowler C,Benvenuto G,Laflamme P,Molino D,Probst AV,Tariq M,Paszkowski J(2004)Chromatin techniques for plant cells.Plant J 39:776-789
Campoli C,Drosse B,Searle I,Coupland G,Korff M(2012)Functional characterisation of HvCO1,the barley(Hordeum vulgare)flowering time ortholog of CONSTANS.Plant J 69:868-880
Chen A,Dubcovsky J(2012)Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering.PLoS Genet 8:e1003134
Chen A,Li C,Hu W,Lau MY,Lin H,Rockwell NC,Martin SS,Jernstedt JA,Lagarias JC,Dubcovsky J(2014)PHYTO-CHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod.Proc Natl Acad Sci USA 111:10037-10044
Christiansen P,Andersen CH,Didion T,Folling M,Nielsen KK(2005)A rapid and efficient transformation protocol for the grass Brachypodium distachyon.Plant Cell Rep 23:751-758
Clavijo BJ,Venturini L,Schudoma C,Accinelli GG,Kaithakottil G,Wright J,Borrill P,Kettleborough G,Heavens D,Chapman H(2017)An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations.Genome Res27:885-896
Cockram J,Jones H,Leigh FJ,O’Sullivan D,Powell W,Laurie DA,Greenland AJ(2007)Control of flowering time in temperate cereals:Genes,domestication,and sustainable productivity.J Exp Bot 58:1231-1244
Corbesier L,Vincent C,Jang S,Fornara F,Fan Q,Searle I,Giakountis A,Farrona S,Gissot L,Turnbull C,Coupland G(2007)FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis.Science 316:1030-1033
Crooks GE,Hon G,Chandonia JM,Brenner SE(2004)WebLogo:A sequence logo generator.Genome Res 14:1188-1190
Distelfeld A,Li C,Dubcovsky J(2009)Regulation of flowering in temperate cereals.Curr Opin Plant Biol 12:178-184
Dubcovsky J,Dvorak J(2007)Genome plasticity a key factor in the success of polyploid wheat under domestication.Science 316:1862-1866
Doebley JF,Gaut BS,Smith BD(2006)The molecular genetics of crop domestication.Cell 127:1309-1321
Dyck JA,Matus-Ca?diz MA,Hucl P,Talbert L,Hunt T,Dubuc JP,Nass H,Clayton G,Dobb J,Quick J(2004)Agronomic performance of hard red spring wheat isolines sensitive and insensitive to photoperiod.Crop Sci 44:1976-1981
Feng Y,Wang K,Ma C,Zhao Y,Yin J(2015)Virus-induced gene silencing-based functional verification of six genes associated with vernalization in wheat.Biochem Biophys Res Commun 458:928-933
Fornara F,de Montaigu A,Coupland G(2010)SnapShot:Control of flowering in Arabidopsis.Cell 141:550-550
Greenup A,Peacock WJ,Dennis ES,Trevaskis B(2009)The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals.Ann Bot 103:1165-1172
Hao C,Wang L,Ge H,Dong Y,Zhang X(2011)Genetic diversity and linkage disequilibrium in Chinese common wheat(Triticum aestivum L.)revealed by SSR markers.PLoS ONE6:e17279
Jung C,M€uller AE(2009)Flowering time control and applications in plant breeding.Trends Plant Sci 14:563-573
Kamran A,Iqbal M,Spaner D(2014)Flowering time in wheat(Triticum aestivum L.):A key factor for global adaptability.Euphytica 197:1-26
Kardailsky I,Shukla VK,Ahn JH,Dagenais N,Christensen SK,Nguyen JT,Chory J,Harrison MJ,Weigel D(1999)Activation tagging of the floral inducer FT.Science 286:1962-1965
Kato K,Miura H,Sawada S(1999)QTL mapping of genes controlling ear emergence time and plant height on chromosome 5A of wheat.Theor Appl Genet 98:472-477
Kitagawa S,Shimada S,Murai K(2012)Effect of Ppd-1 on the expression of flowering-time genes in vegetative and reproductive growth stages of wheat.Genes Genet Syst87:161-168
Khan MR,Ai XY,Zhang JZ(2014)Genetic regulation of flowering time in annual and perennial plants.Wiley Interdiscip Rev RNA 5:347-359
Li T,Wu X,Li H,Song J,Liu J(2016)A dual-function transcription factor,AtYY1,is a novel negative regulator of the Arabidopsis ABA response network.Mol Plant 9:650-661
Li T,Ma L,Geng Y,Hao C,Chen X,Zhang X(2015)Small RNAand degradome sequencing reveal complex roles of miRNAs and their targets in developing wheat grains.PLoS ONE 10:e0139658
Liu J,Zhang T,Jia J,Sun J(2016)The wheat mediator subunit TaMED25 interacts with the transcription factor TaEIL1 to negatively regulate disease resistance against powdery mildew.Plant Physiol 170:1799-1816
Luo XM,Lin WH,Zhu S,Zhu JY,Sun Y,Fan XY,Cheng M,Hao Y,Oh E,Tian M,Liu L,Zhang M,Xie Q,Chong K,Wang ZY(2010)Integration of light-and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis.Dev Cell 19:872-883
Manfield IW,Devlin PF,Jen C,Westhead DR,Gilmartin PM(2007)Conservation,convergence,and divergence of light-responsive,circadian-regulated,and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family.Plant Physiol 143:941-958
Martinic ZF(1975)Life cycle of common wheat varieties in natural environments as related to their response to shortened photoperiod.J Plant Breed 75:237-251
Miralles DJ,Richards RA(2000)Responses of leaf and tiller emergence and primordium initiation in wheat and barley to interchanged photoperiod.Ann Bot 85:655-663
Nakagawa T,Kurose T,Hino T,Tanaka K,Kawamukai M,Niwa Y,Toyooka K,Matsuoka K,Jinbo T,Kimura T(2007)Development of series of gateway binary vectors,pGWBs,for realizing efficient construction of fusion genes for plant transformation.J Biosci Bioeng 104:34-41
Nemoto Y,Kisaka M,Fuse T,Yano M,Ogihara Y(2003)Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice.Plant J 36:82-93
Oliver SN,Finnegan EJ,Dennis ES,Peacock WJ,Trevaskis B(2009)Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene.Proc Natl Acad Sci USA 106:8386-8391
Reyes JC,Muro-Pastor MI,Florencio FJ(2004)The GATAfamily of transcription factors in Arabidopsis and rice.Plant Physiol 134:1718-1732
Shaikhali J,Barajas-Lopez JDD,Otvos K,Kremnev D,Garcia AS,Srivastava V,Wingsle G,Bako L,Strand A(2012)The CRYPTOCHROME1 dependent response to excess light is mediated through the transcriptional activators ZINCFINGER PROTEIN EXPRESSED IN INFLORESCENCE MERI-STEM LIKE1 and ZML2 in Arabidopsis.Plant Cell 24:3009-3025
Shaw LM,Turner AS,Laurie DA(2012)The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat(Triticum aestivum).Plant J 71:71-84
Shikata M,Takemura M,Yokota A,Kohchi T(2003)Arabidopsis ZIM,a plant-specific GATA factor,can function as a transcriptional activator.Biosci Biotechnol Biochem 67:2495-2497
Shikata M,Matsuda Y,Ando K,Nishii A,Takemura M,Yokota A,Kohchi T(2004)Characterization of Arabidopsis ZIM,a member of a novel plant-specific GATA factor gene family.J Exp Bot 55:631-639
Shimada S,Ogawa T,Kitagawa S,Suzuki T,Ikari C,Shitsukawa N,Abe T,Kawahigashi H,Kikuchi R,Handa H,Murai K(2009)A genetic network of flowering-time genes in wheat leaves,in which an APETALA1/FRUITFULL-like gene,VRN1,is upstream of FLOWERING LOCUS T.Plant J 58:668-681
Song YH,Ito S,Imaizumi T(2010)Similarities in the circadian clock and photoperiodism in plants.Curr Opin Plant Biol13:594-603
Song YH,Shim JS,Kinmonth-Schultz HA,Imaizumi T(2015)Photoperiodic flowering:time measurement mechanisms in leaves.Annu Rev Plant Biol 66:441-464
Stelmakh AF(1990)Geographic distribution of Vrn genes in landraces and improved varieties of spring bread wheat.Euphytica 45:113-118
Suarez-Lopez P,Wheatley K,Robson F,Onouchi H,Valverde F,Coupland G(2001)CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.Nature 410:1116-1120
Tamaki S,Matsuo S,Wong HL,Yokoi S,Shimamoto K(2007)Hd3a protein is a mobile flowering signal in rice.Science316:1033-1036
Takada S,Goto K(2003)TERMINAL FLOWER2,an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1,counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time.Plant Cell 15:2856-2865
Tiwari SB,Shen Y,Chang HC,Hou Y,Harris A,Ma SF,McPartland M,Hymus GJ,Adam L,Marion C,Belachew A,Repetti PP,Reuber TL,Ratcliffe OJ(2010)The flowering time regulator CONSTANS is recruited to the FLOWERINGLOCUS T promoter via a unique cis-element.New Phytol187:57-66
Wang L,Yin H,Qian Q,Yang J,Huang C,Hu X,Luo D(2009)NECK LEAF 1,a GATA type transcription factor,modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice.Cell Res 19:598-611
Wang M,Tu L,Lin M,Lin Z,Wang P,Yang Q,Ye Z,Shen C,Li J,Zhang L(2017)Asymmetric subgenome selection and cisregulatory divergence during cotton domestication.Nat Genet 49:579
Wei W,Zhang Y,Tao J,Chen H,Li Q,Zhang W,Ma B,Lin Q,Zhang J,Chen S(2015)The Alfin-like homeodomain finger protein AL5 suppresses multiple negative factors to confer abiotic stress tolerance in Arabidopsis.Plant J 81:871-883
Worland AJ,Appendino ML,Sayers EJ(1994)The distribution,in European winter wheats,of genes that influence ecoclimatic adaptability whist determining photoperiodic insensitivity and plant height.Euphytica 80:219-228
Xiao J,Xu S,Li C,Xu Y,Xing L,Niu Y,Huan Q,Tang Y,Zhao C,Wagner D,Gao C,Chong K(2014)O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1m RNA accumulation during vernalization in winter wheat.Nat Commun 5:4572
Yan LL,Fu D,Li C,Blechl A,Tranquilli G,Bonafede M,Sanchez A,Valarik M,Yasuda S,Dubcovsky J(2006)The wheat and barley vernalization gene VRN3 is an orthologue of FT.Proc Natl Acad Sci USA 103:19581-19586
Yan LL,Loukoianov A,Blechl A,Tranquilli G,Ramakrishna W,SanMiguel P,Bennetzen JL,Echenique V,Dubcovsky J(2004b)The wheat VRN2 gene is a flowering repressor downregulated by vernalization.Science 303:1640-1644
Yan L,Loukoianov A,Tranquilli G,Helguera M,Fahima T,Dubcovsky J(2003)Positional cloning of the wheat vernalization gene VRN1.Proc Natl Acad Sci USA 100:6263-6268
Yan L,Helguera M,Kato K,Fukuyama S,Sherman J,Dubcovsky J(2004a)Allelic variation at the VRN-1 promoter region in polyploid wheat.Theor Appl Genet 109:1677-1686
Zhao XY,Hong P,Wu JY,Bin Chen X,Ye XG,Pan YY,Wang J,Zhang XS(2016)The tae-miR408-Mediated control of TaTOC1 genes transcription is required for the regulation of heading time in wheat.Plant Physiol170:1578-1594
Zheng J,Liu H,Wang Y,Wang L,Chang X,Jing R,Hao C,Zhang X(2014)TEF-7A,a transcript elongation factor gene,influences yield-related traits in bread wheat(Triticum aestivum L.).J Exp Bot 65:5351-5365
Arguello-Astorga G,Herrera-Estrella L(1998)Evolution of light-regulated plant promoters.Annu Rev Plant Physiol49:525-555
Beales J,Turner A,Griffiths S,Snape JW,Laurie DA(2007)A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat(Triticum aestivum L.).Theor Appl Genet 115:721-733
Bi HH,Sun YW,Xiao YG,Xia LQ(2014)Characterization of DFRallelic variations and their associations with pre-harvest sprouting resistance in a set of red-grained Chinese wheat germplasm.Euphytica 195:197-207
Bowler C,Benvenuto G,Laflamme P,Molino D,Probst AV,Tariq M,Paszkowski J(2004)Chromatin techniques for plant cells.Plant J 39:776-789
Campoli C,Drosse B,Searle I,Coupland G,Korff M(2012)Functional characterisation of HvCO1,the barley(Hordeum vulgare)flowering time ortholog of CONSTANS.Plant J 69:868-880
Chen A,Dubcovsky J(2012)Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering.PLoS Genet 8:e1003134
Chen A,Li C,Hu W,Lau MY,Lin H,Rockwell NC,Martin SS,Jernstedt JA,Lagarias JC,Dubcovsky J(2014)PHYTO-CHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod.Proc Natl Acad Sci USA 111:10037-10044
Christiansen P,Andersen CH,Didion T,Folling M,Nielsen KK(2005)A rapid and efficient transformation protocol for the grass Brachypodium distachyon.Plant Cell Rep 23:751-758
Clavijo BJ,Venturini L,Schudoma C,Accinelli GG,Kaithakottil G,Wright J,Borrill P,Kettleborough G,Heavens D,Chapman H(2017)An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations.Genome Res27:885-896
Cockram J,Jones H,Leigh FJ,O’Sullivan D,Powell W,Laurie DA,Greenland AJ(2007)Control of flowering time in temperate cereals:Genes,domestication,and sustainable productivity.J Exp Bot 58:1231-1244
Corbesier L,Vincent C,Jang S,Fornara F,Fan Q,Searle I,Giakountis A,Farrona S,Gissot L,Turnbull C,Coupland G(2007)FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis.Science 316:1030-1033
Crooks GE,Hon G,Chandonia JM,Brenner SE(2004)WebLogo:A sequence logo generator.Genome Res 14:1188-1190
Distelfeld A,Li C,Dubcovsky J(2009)Regulation of flowering in temperate cereals.Curr Opin Plant Biol 12:178-184
Dubcovsky J,Dvorak J(2007)Genome plasticity a key factor in the success of polyploid wheat under domestication.Science 316:1862-1866
Doebley JF,Gaut BS,Smith BD(2006)The molecular genetics of crop domestication.Cell 127:1309-1321
Dyck JA,Matus-Ca?diz MA,Hucl P,Talbert L,Hunt T,Dubuc JP,Nass H,Clayton G,Dobb J,Quick J(2004)Agronomic performance of hard red spring wheat isolines sensitive and insensitive to photoperiod.Crop Sci 44:1976-1981
Feng Y,Wang K,Ma C,Zhao Y,Yin J(2015)Virus-induced gene silencing-based functional verification of six genes associated with vernalization in wheat.Biochem Biophys Res Commun 458:928-933
Fornara F,de Montaigu A,Coupland G(2010)SnapShot:Control of flowering in Arabidopsis.Cell 141:550-550
Greenup A,Peacock WJ,Dennis ES,Trevaskis B(2009)The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals.Ann Bot 103:1165-1172
Hao C,Wang L,Ge H,Dong Y,Zhang X(2011)Genetic diversity and linkage disequilibrium in Chinese common wheat(Triticum aestivum L.)revealed by SSR markers.PLoS ONE6:e17279
Jung C,M€uller AE(2009)Flowering time control and applications in plant breeding.Trends Plant Sci 14:563-573
Kamran A,Iqbal M,Spaner D(2014)Flowering time in wheat(Triticum aestivum L.):A key factor for global adaptability.Euphytica 197:1-26
Kardailsky I,Shukla VK,Ahn JH,Dagenais N,Christensen SK,Nguyen JT,Chory J,Harrison MJ,Weigel D(1999)Activation tagging of the floral inducer FT.Science 286:1962-1965
Kato K,Miura H,Sawada S(1999)QTL mapping of genes controlling ear emergence time and plant height on chromosome 5A of wheat.Theor Appl Genet 98:472-477
Kitagawa S,Shimada S,Murai K(2012)Effect of Ppd-1 on the expression of flowering-time genes in vegetative and reproductive growth stages of wheat.Genes Genet Syst87:161-168
Khan MR,Ai XY,Zhang JZ(2014)Genetic regulation of flowering time in annual and perennial plants.Wiley Interdiscip Rev RNA 5:347-359
Li T,Wu X,Li H,Song J,Liu J(2016)A dual-function transcription factor,AtYY1,is a novel negative regulator of the Arabidopsis ABA response network.Mol Plant 9:650-661
Li T,Ma L,Geng Y,Hao C,Chen X,Zhang X(2015)Small RNAand degradome sequencing reveal complex roles of miRNAs and their targets in developing wheat grains.PLoS ONE 10:e0139658
Liu J,Zhang T,Jia J,Sun J(2016)The wheat mediator subunit TaMED25 interacts with the transcription factor TaEIL1 to negatively regulate disease resistance against powdery mildew.Plant Physiol 170:1799-1816
Luo XM,Lin WH,Zhu S,Zhu JY,Sun Y,Fan XY,Cheng M,Hao Y,Oh E,Tian M,Liu L,Zhang M,Xie Q,Chong K,Wang ZY(2010)Integration of light-and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis.Dev Cell 19:872-883
Manfield IW,Devlin PF,Jen C,Westhead DR,Gilmartin PM(2007)Conservation,convergence,and divergence of light-responsive,circadian-regulated,and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family.Plant Physiol 143:941-958
Martinic ZF(1975)Life cycle of common wheat varieties in natural environments as related to their response to shortened photoperiod.J Plant Breed 75:237-251
Miralles DJ,Richards RA(2000)Responses of leaf and tiller emergence and primordium initiation in wheat and barley to interchanged photoperiod.Ann Bot 85:655-663
Nakagawa T,Kurose T,Hino T,Tanaka K,Kawamukai M,Niwa Y,Toyooka K,Matsuoka K,Jinbo T,Kimura T(2007)Development of series of gateway binary vectors,pGWBs,for realizing efficient construction of fusion genes for plant transformation.J Biosci Bioeng 104:34-41
Nemoto Y,Kisaka M,Fuse T,Yano M,Ogihara Y(2003)Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice.Plant J 36:82-93
Oliver SN,Finnegan EJ,Dennis ES,Peacock WJ,Trevaskis B(2009)Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene.Proc Natl Acad Sci USA 106:8386-8391
Reyes JC,Muro-Pastor MI,Florencio FJ(2004)The GATAfamily of transcription factors in Arabidopsis and rice.Plant Physiol 134:1718-1732
Shaikhali J,Barajas-Lopez JDD,Otvos K,Kremnev D,Garcia AS,Srivastava V,Wingsle G,Bako L,Strand A(2012)The CRYPTOCHROME1 dependent response to excess light is mediated through the transcriptional activators ZINCFINGER PROTEIN EXPRESSED IN INFLORESCENCE MERI-STEM LIKE1 and ZML2 in Arabidopsis.Plant Cell 24:3009-3025
Shaw LM,Turner AS,Laurie DA(2012)The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat(Triticum aestivum).Plant J 71:71-84
Shikata M,Takemura M,Yokota A,Kohchi T(2003)Arabidopsis ZIM,a plant-specific GATA factor,can function as a transcriptional activator.Biosci Biotechnol Biochem 67:2495-2497
Shikata M,Matsuda Y,Ando K,Nishii A,Takemura M,Yokota A,Kohchi T(2004)Characterization of Arabidopsis ZIM,a member of a novel plant-specific GATA factor gene family.J Exp Bot 55:631-639
Shimada S,Ogawa T,Kitagawa S,Suzuki T,Ikari C,Shitsukawa N,Abe T,Kawahigashi H,Kikuchi R,Handa H,Murai K(2009)A genetic network of flowering-time genes in wheat leaves,in which an APETALA1/FRUITFULL-like gene,VRN1,is upstream of FLOWERING LOCUS T.Plant J 58:668-681
Song YH,Ito S,Imaizumi T(2010)Similarities in the circadian clock and photoperiodism in plants.Curr Opin Plant Biol13:594-603
Song YH,Shim JS,Kinmonth-Schultz HA,Imaizumi T(2015)Photoperiodic flowering:time measurement mechanisms in leaves.Annu Rev Plant Biol 66:441-464
Stelmakh AF(1990)Geographic distribution of Vrn genes in landraces and improved varieties of spring bread wheat.Euphytica 45:113-118
Suarez-Lopez P,Wheatley K,Robson F,Onouchi H,Valverde F,Coupland G(2001)CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.Nature 410:1116-1120
Tamaki S,Matsuo S,Wong HL,Yokoi S,Shimamoto K(2007)Hd3a protein is a mobile flowering signal in rice.Science316:1033-1036
Takada S,Goto K(2003)TERMINAL FLOWER2,an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1,counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time.Plant Cell 15:2856-2865
Tiwari SB,Shen Y,Chang HC,Hou Y,Harris A,Ma SF,McPartland M,Hymus GJ,Adam L,Marion C,Belachew A,Repetti PP,Reuber TL,Ratcliffe OJ(2010)The flowering time regulator CONSTANS is recruited to the FLOWERINGLOCUS T promoter via a unique cis-element.New Phytol187:57-66
Wang L,Yin H,Qian Q,Yang J,Huang C,Hu X,Luo D(2009)NECK LEAF 1,a GATA type transcription factor,modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice.Cell Res 19:598-611
Wang M,Tu L,Lin M,Lin Z,Wang P,Yang Q,Ye Z,Shen C,Li J,Zhang L(2017)Asymmetric subgenome selection and cisregulatory divergence during cotton domestication.Nat Genet 49:579
Wei W,Zhang Y,Tao J,Chen H,Li Q,Zhang W,Ma B,Lin Q,Zhang J,Chen S(2015)The Alfin-like homeodomain finger protein AL5 suppresses multiple negative factors to confer abiotic stress tolerance in Arabidopsis.Plant J 81:871-883
Worland AJ,Appendino ML,Sayers EJ(1994)The distribution,in European winter wheats,of genes that influence ecoclimatic adaptability whist determining photoperiodic insensitivity and plant height.Euphytica 80:219-228
Xiao J,Xu S,Li C,Xu Y,Xing L,Niu Y,Huan Q,Tang Y,Zhao C,Wagner D,Gao C,Chong K(2014)O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1m RNA accumulation during vernalization in winter wheat.Nat Commun 5:4572
Yan LL,Fu D,Li C,Blechl A,Tranquilli G,Bonafede M,Sanchez A,Valarik M,Yasuda S,Dubcovsky J(2006)The wheat and barley vernalization gene VRN3 is an orthologue of FT.Proc Natl Acad Sci USA 103:19581-19586
Yan LL,Loukoianov A,Blechl A,Tranquilli G,Ramakrishna W,SanMiguel P,Bennetzen JL,Echenique V,Dubcovsky J(2004b)The wheat VRN2 gene is a flowering repressor downregulated by vernalization.Science 303:1640-1644
Yan L,Loukoianov A,Tranquilli G,Helguera M,Fahima T,Dubcovsky J(2003)Positional cloning of the wheat vernalization gene VRN1.Proc Natl Acad Sci USA 100:6263-6268
Yan L,Helguera M,Kato K,Fukuyama S,Sherman J,Dubcovsky J(2004a)Allelic variation at the VRN-1 promoter region in polyploid wheat.Theor Appl Genet 109:1677-1686
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