Integrating transcriptomic and proteomic analyses of photoperiod-sensitive in near isogenic maize line under long-day conditions
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摘要
As a short-day plant species, maize requires an optimal photoperiod for inducing reproductive growth. However, there is a lack of information regarding photoperiod-induced changes in maize mRNA and protein levels. In this study, a photoperiod-insensitive maize inbred line and its near isogenic photoperiod-sensitive line were used. By integrating RNAbased transcriptomic and iTRAQ LC-MS/MS-based proteomic approaches, we generated a comprehensive inventory of the transcripts and proteins with altered abundances in response to a long photoperiod(LP) during growth stage transitions. We detected 22 000 transcripts in RNA-sequence runs and 5 259 proteins from an iTRAQ-based analysis. A weak correlation between mRNA-and protein-level changes was observed, suggesting the LP-induced transition between maize growth stages is largely regulated post-transcriptionally. Differentially expressed genes influenced by LP conditions were associated with several regulatory processes in both maize inbred lines, especially phosphate ion transport and the circadian rhythm. Additionally, 31 transcripts and six proteins related to photoperiodic flowering in maize were identified by comparing transcriptomic and proteomic data. This transcriptomic and proteomic analysis represents the first comprehensive and comparative study of gene/protein-level changes occurring in photoperiod-sensitive and-insensitive maize inbred lines during growth stage transitions under LP conditions.
As a short-day plant species, maize requires an optimal photoperiod for inducing reproductive growth. However, there is a lack of information regarding photoperiod-induced changes in maize mRNA and protein levels. In this study, a photoperiod-insensitive maize inbred line and its near isogenic photoperiod-sensitive line were used. By integrating RNAbased transcriptomic and iTRAQ LC-MS/MS-based proteomic approaches, we generated a comprehensive inventory of the transcripts and proteins with altered abundances in response to a long photoperiod(LP) during growth stage transitions. We detected 22 000 transcripts in RNA-sequence runs and 5 259 proteins from an iTRAQ-based analysis. A weak correlation between mRNA-and protein-level changes was observed, suggesting the LP-induced transition between maize growth stages is largely regulated post-transcriptionally. Differentially expressed genes influenced by LP conditions were associated with several regulatory processes in both maize inbred lines, especially phosphate ion transport and the circadian rhythm. Additionally, 31 transcripts and six proteins related to photoperiodic flowering in maize were identified by comparing transcriptomic and proteomic data. This transcriptomic and proteomic analysis represents the first comprehensive and comparative study of gene/protein-level changes occurring in photoperiod-sensitive and-insensitive maize inbred lines during growth stage transitions under LP conditions.
As a short-day plant species, maize requires an optimal photoperiod for inducing reproductive growth. However, there is a lack of information regarding photoperiod-induced changes in maize mRNA and protein levels. In this study, a photoperiod-insensitive maize inbred line and its near isogenic photoperiod-sensitive line were used. By integrating RNAbased transcriptomic and iTRAQ LC-MS/MS-based proteomic approaches, we generated a comprehensive inventory of the transcripts and proteins with altered abundances in response to a long photoperiod(LP) during growth stage transitions. We detected 22 000 transcripts in RNA-sequence runs and 5 259 proteins from an iTRAQ-based analysis. A weak correlation between mRNA-and protein-level changes was observed, suggesting the LP-induced transition between maize growth stages is largely regulated post-transcriptionally. Differentially expressed genes influenced by LP conditions were associated with several regulatory processes in both maize inbred lines, especially phosphate ion transport and the circadian rhythm. Additionally, 31 transcripts and six proteins related to photoperiodic flowering in maize were identified by comparing transcriptomic and proteomic data. This transcriptomic and proteomic analysis represents the first comprehensive and comparative study of gene/protein-level changes occurring in photoperiod-sensitive and-insensitive maize inbred lines during growth stage transitions under LP conditions.
引文
Alabadi D,Oyama T,Yanovsky M J,Harmon F G,Mas P,Kay S A.2001.Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.Science,293,880-883.
An H,Roussot C,Suárez-López P,Corbesier L,Vincent C,Pi?eiro M,Hepworth S,Mouradov A,Justin S,Turnbull C.2004.CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis.Development,131,3615.
Bindea G,Galon J,Mlecnik B.2013.CluePedia Cytoscape plugin:pathway insights using integrated experimental and in silico data.Bioinformatics,29,661.
Bindea G,Mlecnik B,Hackl H,Charoentong P,Tosolini M,Kirilovsky A,Fridman W H,Pagès F,Trajanoski Z,Galon J.2009.ClueGO:A Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks.Bioinformatics,25,1091-1093.
Brambilla V,Fornara F.2016.Y flowering regulation and activity of CONSTANS and CCT-domain proteins in Arabidopsis and crop species.Biochimica et Biophysica Acta-Gene Regulatory Mechanisms,5,655-660.
Buckler E S,Holland J B,Bradbury P J,Acharya C B,Brown P J,Browne C,Ersoz E,Flintgarcia S,Garcia A,Glaubitz J C.2009.The genetic architecture of maize flowering time.Science,325,714-718.
Choudhary M K,Nomura Y,Shi H,Nakagami H,Somers D E.2016.Circadian profiling of the Arabidopsis proteome using2D-DIGE.Frontiers in Plant Science,7,1007.
Colasanti J,Yuan Z,Sundaresan V.1998.The indeterminate gene encodes a zinc finger protein and regulates a leafgenerated signal required for the transition to flowering in maize.Cell,93,593-603.
Coles N D,Mcmullen M D,Balint P J,Pratt R C,Holland J B.2010.Genetic control of photoperiod sensitivity in maize revealed by joint multiple population analysis.Genetics,184,799-812.
Corbesier L,Vincent C,Jang S,Fornara F,Fan Q,Searle I,Giakountis A,Farrona S,Gissot L,Turnbull C.2007.FTprotein movement contributes to long-distance signaling in floral induction of Arabidopsis.Science,316,1030.
David K M,Armbruster U,Tama N,Putterill J.2006.Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark.FEBS Letters,580,1193-1197.
Ding Y,Liu N,Virlouvet L,Riethoven J J,Fromm M,Avramova Z.2013.Four distinct types of dehydration stress memory genes in Arabidopsis thaliana.BMC Plant Biology,13,229.
Ding Y,Virlouvet L,Liu N,Riethoven J J,Fromm M,Avramova Z.2014.Dehydration stress memory genes of Zea mays;comparison with Arabidopsis thaliana.BMC Plant Biology,14,141.
Fernández V,Takahashi Y,Legourrierec J,Coupland G.2016.Photoperiodic and thermosensory pathways interact through CONSTANS to promote flowering at high temperature under short days.The Plant Journal,86,426.
Fornara F,Panigrahi K C,Gissot L,Sauerbrunn N,Rühl M,Jarillo J A,Coupland G.2009.Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response.Developmental Cell,17,75.
Fournier M L,Paulson A,Pavelka N,Mosley A L,Gaudenz K,Bradford W D,Glynn E,Li H,Sardiu M E,Fleharty B.2010.Delayed correlation of mRNA and protein expression in rapamycin-treated cells and a role for Ggc1 in cellular sensitivity to rapamycin.Molecular&Cellular Proteomics,9,271.
Ghatak A,Chaturvedi P,Weckwerth W.2017.Cereal crop proteomics:Systemic analysis of crop drought stress responses towards marker-assisted selection breeding.Frontiers in Plant Science,8,757.
Gil K E,Park M J,Lee H J,Park Y J,Han S H,Kwon Y J,Seo PJ,Jung J H,Park C M.2016.Alternative splicing provides a proactive mechanism for the diurnal CONSTANS dynamics in Arabidopsis photoperiodic flowering.The Plant Journal,89,128-140.
Gnanasekaran T,Karcher D,Nielsen A Z,Martens H J,Ruf S,Kroop X,Olsen C E,Motawie M S,Pribil M,Moller BL,Bock R,Jensen P E.2016.Transfer of the cytochrome P450-dependent dhurrin pathway from Sorghum bicolor into Nicotiana tabacum chloroplasts for light-driven synthesis.Journal of Experimental Botany,67,2495-2506.
Graf A,Coman D,Uhrig R G,Walsh S,Flis A,Stitt M,Gruissem W.2017.Parallel analysis of Arabidopsis circadian clock mutants reveals different scales of transcriptome and proteome regulation.Open Biology,7,160333.
Greenup A,Peacock W J,Dennis E S,Trevaskis B.2009.The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals.Annals of Botany,103,1165-1172.
van Heerwaarden J,Doebley J,Briggs W H,Glaubitz J C,Goodman M M,Gonzalez J,Ross J.2011.Genetic signals of origin,spread,and introgression in a large sample of maize landraces.Proceedings of the National Academy of Sciences of the United States of America,108,1088-1092.
Hoenicka H,Lautner S,Klingberg A,Koch G,El-Sherif F,Lehnhardt D,Zhang B,Burgert I,Odermatt J,Melzer S,Fromm J,Fladung M.2012.Influence of over-expression of the flowering promoting factor 1 gene(FPF1)from arabidopsis on wood formation in hybrid poplar(Populus tremula L.×P.tremuloides Michx.).Planta,235,359-373.
Ito S,Song Y H,Josephson-Day A R,Miller R J,Breton G,Olmstead R G,Imaizumi T.2012.FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis.Proceedings of the National Academy of Sciences of the United States of America,109,3582.
Itoh H,Izawa T.2013.The coincidence of critical day length recognition for florigen gene expression and floral transition under long-day conditions in rice.Molecular Plant,6,635-649.
Jackson S D.2009.Plant responses to photoperiod.New Phytologist,181,517-531.
Kim S J,Hong S M,Yoo S J,Moon S,Jung H S,Ahn J H.2016.Post-translational regulation of FLOWERING LOCUS Tprotein in Arabidopsis.Molecular Plant,9,308-311.
Ku L,Tian L,Su H,Wang C,Wang X,Wu L,Shi Y,Li G,Wang Z,Wang H.2016.Dual functions of the ZmCCT-associated quantitative trait locus in flowering and stress responses under long-day conditions.BMC Plant Biology,16,239.
Kumimoto R W,Zhang Y,Siefers N,Holt B F.2010.NF-YC3,NF-YC4 and NF-YC9 are required for CONSTANS-mediated,photoperiod-dependent flowering in Arabidopsis thaliana.The Plant Journal,63,379-391.
Langmead B,Trapnell C,Pop M,Salzberg S L.2009.Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.Genome Biology,10,R25.
Liron S.2015.Post-translational Regulation of CONSTANSProtein in the Photoperiod Pathway of Arabidopsis thaliana.[2018-01-06].http://kups.ub.uni-koeln.de/6204/
Liu L,Adrian J,Pankin A,Hu J,Dong X,von Korff M,Turck F.2014.Induced and natural variation of promoter length modulates the photoperiodic response of FLOWERINGLOCUS T.Nature Communications,5,4558.
Ma Q,Wu M,Pei W,Li H,Li X,Zhang J,Yu J,Yu S.2014.Quantitative phosphoproteomic profiling of fiber differentiation and initiation in a fiberless mutant of cotton.BMC Genomics,15,466.
Mathieu J,Warthmann N,Küttner F,Schmid M.2007.Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis.Current Biology,17,1055-1060.
Matsuoka Y,Vigouroux Y,Goodman M M,Sanchez G J,Buckler E,Doebley J.2002.A single domestication for maize shown by multilocus microsatellite genotyping.Proceedings of the National Academy of Sciences of the United States of America,99,6080-6084.
Michael T P,Mockler T C,Ghislain B,Connor M E,Amanda B,Trout J D,Hazen S P,Shen R,Priest H D,Sullivan C M.2008.Network discovery pipeline elucidates conserved time-ofday-specific cis-regulatory modules.PLo S Genetics,4,e14.
Noh Y S,Bizzell C M,Noh B,Schomburg F M,Amasino R M.2004.EARLY FLOWERING 5 acts as a floral repressor in Arabidopsis.The Plant Journal,38,664-672.
Ponnala L,Wang Y,Sun Q,Wijk K J.2014.Correlation of mRNAand protein abundance in the developing maize leaf.The Plant Journal,78,424-440.
Putterill J,Robson F,Lee K,Simon R,Coupland G.1995.The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors.Cell,80,847-857.
Seo E,Yu J,Ryu K H,Lee M M,Lee I.2011.WEREWOLF,a regulator of root hair pattern formation,controls flowering time through the regulation of FT mRNA stability.Plant Physiology,156,1867-1877.
Song Y H,Estrada D A,Johnson R S,Kim S K,Lee S Y,Maccoss M J,Imaizumi T.2014.Distinct roles of FKF1,GIGANTEA,and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering.Proceedings of the National Academy of Sciences of the United States of America,111,17672.
Tian L,Wang S,Song X,Zhang J,Liu P,Chen Z,Chen Y,Wu L.2018.Long photoperiod affects the maize transition from vegetative to reproductive stages:A proteomic comparison between photoperiod-sensitive inbred line and its recurrent parent.Amino Acids,50,149-161.
Valverde F,Mouradov A,Soppe W,Ravenscroft D,Samach A,Coupland G.2004.Photoreceptor regulation of CONSTANSprotein in photoperiodic flowering.Science,303,1003-1006.
Wang C L,Cheng F F,Sun Z H,Tang J H,Wu L C,Ku LX,Chen Y H.2008.Genetic analysis of photoperiod sensitivity in a tropical by temperate maize recombinant inbred population using molecular markers.Theoretical and Applied Genetics,117,1129-1139.
Wang H,Pan J,Li Y,Lou D,Hu Y,Yu D.2016.The DELLA-CONSTANS transcription factor cascade integrates gibberellic acid and photoperiod signaling to regulate flowering.Plant Physiology,172,479-488.
Wang X,Wu L,Zhang S,Wu L,Ku L,Wei X,Xie L,Chen Y.2011.Robust expression and association of ZmCCA1with circadian rhythms in maize.Plant Cell Reports,30,1261-1272.
Wu L,Lei T,Wang S,Zhang J,Ping L,Tian Z,Zhang H,Liu H,Chen Y.2016a.Comparative proteomic analysis of the response of maize(Zea mays L.)leaves to long photoperiod condition.Frontiers in Plant Science,7,752.
Wu L,Liu D,Wu J,Zhang R,Qin Z,Liu D,Li A,Fu D,Zhai W,Mao L.2013.Regulation of FLOWERING LOCUS T by a micro RNA in Brachypodium distachyon.The Plant Cell,25,4363-4377.
Wu L,Wang X,Wang S,Wu L,Tian L,Tian Z,Liu P,Chen Y.2016b.Comparative proteomic analysis of the shoot apical meristem in maize between a ZmCCT-associated nearisogenic line and its recurrent parent.Scientific Reports,6,30641.
Xue W,Xing Y,Weng X,Zhao Y,Tang W,Wang L,Zhou H,Yu S,Xu C,Li X,Zhang Q.2008.Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice.Nature Genetics,40,761.
Yang Q,Li Z,Li W,Ku L,Wang C,Ye J,Li K,Yang N,Li Y,Zhong T.2013.CACTA-like transposable element in Zm CCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize.Proceedings of the National Academy of Sciences of the United States of America,110,16969-16974.
Zhang B,Wang L,Zeng L,Zhang C,Ma H.2015.Arabidopsis TOE proteins convey a photoperiodic signal to antagonize CONSTANS and regulate flowering time.Genes&Development,29,975-987.
An H,Roussot C,Suárez-López P,Corbesier L,Vincent C,Pi?eiro M,Hepworth S,Mouradov A,Justin S,Turnbull C.2004.CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis.Development,131,3615.
Bindea G,Galon J,Mlecnik B.2013.CluePedia Cytoscape plugin:pathway insights using integrated experimental and in silico data.Bioinformatics,29,661.
Bindea G,Mlecnik B,Hackl H,Charoentong P,Tosolini M,Kirilovsky A,Fridman W H,Pagès F,Trajanoski Z,Galon J.2009.ClueGO:A Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks.Bioinformatics,25,1091-1093.
Brambilla V,Fornara F.2016.Y flowering regulation and activity of CONSTANS and CCT-domain proteins in Arabidopsis and crop species.Biochimica et Biophysica Acta-Gene Regulatory Mechanisms,5,655-660.
Buckler E S,Holland J B,Bradbury P J,Acharya C B,Brown P J,Browne C,Ersoz E,Flintgarcia S,Garcia A,Glaubitz J C.2009.The genetic architecture of maize flowering time.Science,325,714-718.
Choudhary M K,Nomura Y,Shi H,Nakagami H,Somers D E.2016.Circadian profiling of the Arabidopsis proteome using2D-DIGE.Frontiers in Plant Science,7,1007.
Colasanti J,Yuan Z,Sundaresan V.1998.The indeterminate gene encodes a zinc finger protein and regulates a leafgenerated signal required for the transition to flowering in maize.Cell,93,593-603.
Coles N D,Mcmullen M D,Balint P J,Pratt R C,Holland J B.2010.Genetic control of photoperiod sensitivity in maize revealed by joint multiple population analysis.Genetics,184,799-812.
Corbesier L,Vincent C,Jang S,Fornara F,Fan Q,Searle I,Giakountis A,Farrona S,Gissot L,Turnbull C.2007.FTprotein movement contributes to long-distance signaling in floral induction of Arabidopsis.Science,316,1030.
David K M,Armbruster U,Tama N,Putterill J.2006.Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark.FEBS Letters,580,1193-1197.
Ding Y,Liu N,Virlouvet L,Riethoven J J,Fromm M,Avramova Z.2013.Four distinct types of dehydration stress memory genes in Arabidopsis thaliana.BMC Plant Biology,13,229.
Ding Y,Virlouvet L,Liu N,Riethoven J J,Fromm M,Avramova Z.2014.Dehydration stress memory genes of Zea mays;comparison with Arabidopsis thaliana.BMC Plant Biology,14,141.
Fernández V,Takahashi Y,Legourrierec J,Coupland G.2016.Photoperiodic and thermosensory pathways interact through CONSTANS to promote flowering at high temperature under short days.The Plant Journal,86,426.
Fornara F,Panigrahi K C,Gissot L,Sauerbrunn N,Rühl M,Jarillo J A,Coupland G.2009.Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response.Developmental Cell,17,75.
Fournier M L,Paulson A,Pavelka N,Mosley A L,Gaudenz K,Bradford W D,Glynn E,Li H,Sardiu M E,Fleharty B.2010.Delayed correlation of mRNA and protein expression in rapamycin-treated cells and a role for Ggc1 in cellular sensitivity to rapamycin.Molecular&Cellular Proteomics,9,271.
Ghatak A,Chaturvedi P,Weckwerth W.2017.Cereal crop proteomics:Systemic analysis of crop drought stress responses towards marker-assisted selection breeding.Frontiers in Plant Science,8,757.
Gil K E,Park M J,Lee H J,Park Y J,Han S H,Kwon Y J,Seo PJ,Jung J H,Park C M.2016.Alternative splicing provides a proactive mechanism for the diurnal CONSTANS dynamics in Arabidopsis photoperiodic flowering.The Plant Journal,89,128-140.
Gnanasekaran T,Karcher D,Nielsen A Z,Martens H J,Ruf S,Kroop X,Olsen C E,Motawie M S,Pribil M,Moller BL,Bock R,Jensen P E.2016.Transfer of the cytochrome P450-dependent dhurrin pathway from Sorghum bicolor into Nicotiana tabacum chloroplasts for light-driven synthesis.Journal of Experimental Botany,67,2495-2506.
Graf A,Coman D,Uhrig R G,Walsh S,Flis A,Stitt M,Gruissem W.2017.Parallel analysis of Arabidopsis circadian clock mutants reveals different scales of transcriptome and proteome regulation.Open Biology,7,160333.
Greenup A,Peacock W J,Dennis E S,Trevaskis B.2009.The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals.Annals of Botany,103,1165-1172.
van Heerwaarden J,Doebley J,Briggs W H,Glaubitz J C,Goodman M M,Gonzalez J,Ross J.2011.Genetic signals of origin,spread,and introgression in a large sample of maize landraces.Proceedings of the National Academy of Sciences of the United States of America,108,1088-1092.
Hoenicka H,Lautner S,Klingberg A,Koch G,El-Sherif F,Lehnhardt D,Zhang B,Burgert I,Odermatt J,Melzer S,Fromm J,Fladung M.2012.Influence of over-expression of the flowering promoting factor 1 gene(FPF1)from arabidopsis on wood formation in hybrid poplar(Populus tremula L.×P.tremuloides Michx.).Planta,235,359-373.
Ito S,Song Y H,Josephson-Day A R,Miller R J,Breton G,Olmstead R G,Imaizumi T.2012.FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis.Proceedings of the National Academy of Sciences of the United States of America,109,3582.
Itoh H,Izawa T.2013.The coincidence of critical day length recognition for florigen gene expression and floral transition under long-day conditions in rice.Molecular Plant,6,635-649.
Jackson S D.2009.Plant responses to photoperiod.New Phytologist,181,517-531.
Kim S J,Hong S M,Yoo S J,Moon S,Jung H S,Ahn J H.2016.Post-translational regulation of FLOWERING LOCUS Tprotein in Arabidopsis.Molecular Plant,9,308-311.
Ku L,Tian L,Su H,Wang C,Wang X,Wu L,Shi Y,Li G,Wang Z,Wang H.2016.Dual functions of the ZmCCT-associated quantitative trait locus in flowering and stress responses under long-day conditions.BMC Plant Biology,16,239.
Kumimoto R W,Zhang Y,Siefers N,Holt B F.2010.NF-YC3,NF-YC4 and NF-YC9 are required for CONSTANS-mediated,photoperiod-dependent flowering in Arabidopsis thaliana.The Plant Journal,63,379-391.
Langmead B,Trapnell C,Pop M,Salzberg S L.2009.Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.Genome Biology,10,R25.
Liron S.2015.Post-translational Regulation of CONSTANSProtein in the Photoperiod Pathway of Arabidopsis thaliana.[2018-01-06].http://kups.ub.uni-koeln.de/6204/
Liu L,Adrian J,Pankin A,Hu J,Dong X,von Korff M,Turck F.2014.Induced and natural variation of promoter length modulates the photoperiodic response of FLOWERINGLOCUS T.Nature Communications,5,4558.
Ma Q,Wu M,Pei W,Li H,Li X,Zhang J,Yu J,Yu S.2014.Quantitative phosphoproteomic profiling of fiber differentiation and initiation in a fiberless mutant of cotton.BMC Genomics,15,466.
Mathieu J,Warthmann N,Küttner F,Schmid M.2007.Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis.Current Biology,17,1055-1060.
Matsuoka Y,Vigouroux Y,Goodman M M,Sanchez G J,Buckler E,Doebley J.2002.A single domestication for maize shown by multilocus microsatellite genotyping.Proceedings of the National Academy of Sciences of the United States of America,99,6080-6084.
Michael T P,Mockler T C,Ghislain B,Connor M E,Amanda B,Trout J D,Hazen S P,Shen R,Priest H D,Sullivan C M.2008.Network discovery pipeline elucidates conserved time-ofday-specific cis-regulatory modules.PLo S Genetics,4,e14.
Noh Y S,Bizzell C M,Noh B,Schomburg F M,Amasino R M.2004.EARLY FLOWERING 5 acts as a floral repressor in Arabidopsis.The Plant Journal,38,664-672.
Ponnala L,Wang Y,Sun Q,Wijk K J.2014.Correlation of mRNAand protein abundance in the developing maize leaf.The Plant Journal,78,424-440.
Putterill J,Robson F,Lee K,Simon R,Coupland G.1995.The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors.Cell,80,847-857.
Seo E,Yu J,Ryu K H,Lee M M,Lee I.2011.WEREWOLF,a regulator of root hair pattern formation,controls flowering time through the regulation of FT mRNA stability.Plant Physiology,156,1867-1877.
Song Y H,Estrada D A,Johnson R S,Kim S K,Lee S Y,Maccoss M J,Imaizumi T.2014.Distinct roles of FKF1,GIGANTEA,and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering.Proceedings of the National Academy of Sciences of the United States of America,111,17672.
Tian L,Wang S,Song X,Zhang J,Liu P,Chen Z,Chen Y,Wu L.2018.Long photoperiod affects the maize transition from vegetative to reproductive stages:A proteomic comparison between photoperiod-sensitive inbred line and its recurrent parent.Amino Acids,50,149-161.
Valverde F,Mouradov A,Soppe W,Ravenscroft D,Samach A,Coupland G.2004.Photoreceptor regulation of CONSTANSprotein in photoperiodic flowering.Science,303,1003-1006.
Wang C L,Cheng F F,Sun Z H,Tang J H,Wu L C,Ku LX,Chen Y H.2008.Genetic analysis of photoperiod sensitivity in a tropical by temperate maize recombinant inbred population using molecular markers.Theoretical and Applied Genetics,117,1129-1139.
Wang H,Pan J,Li Y,Lou D,Hu Y,Yu D.2016.The DELLA-CONSTANS transcription factor cascade integrates gibberellic acid and photoperiod signaling to regulate flowering.Plant Physiology,172,479-488.
Wang X,Wu L,Zhang S,Wu L,Ku L,Wei X,Xie L,Chen Y.2011.Robust expression and association of ZmCCA1with circadian rhythms in maize.Plant Cell Reports,30,1261-1272.
Wu L,Lei T,Wang S,Zhang J,Ping L,Tian Z,Zhang H,Liu H,Chen Y.2016a.Comparative proteomic analysis of the response of maize(Zea mays L.)leaves to long photoperiod condition.Frontiers in Plant Science,7,752.
Wu L,Liu D,Wu J,Zhang R,Qin Z,Liu D,Li A,Fu D,Zhai W,Mao L.2013.Regulation of FLOWERING LOCUS T by a micro RNA in Brachypodium distachyon.The Plant Cell,25,4363-4377.
Wu L,Wang X,Wang S,Wu L,Tian L,Tian Z,Liu P,Chen Y.2016b.Comparative proteomic analysis of the shoot apical meristem in maize between a ZmCCT-associated nearisogenic line and its recurrent parent.Scientific Reports,6,30641.
Xue W,Xing Y,Weng X,Zhao Y,Tang W,Wang L,Zhou H,Yu S,Xu C,Li X,Zhang Q.2008.Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice.Nature Genetics,40,761.
Yang Q,Li Z,Li W,Ku L,Wang C,Ye J,Li K,Yang N,Li Y,Zhong T.2013.CACTA-like transposable element in Zm CCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize.Proceedings of the National Academy of Sciences of the United States of America,110,16969-16974.
Zhang B,Wang L,Zeng L,Zhang C,Ma H.2015.Arabidopsis TOE proteins convey a photoperiodic signal to antagonize CONSTANS and regulate flowering time.Genes&Development,29,975-987.