SPL转录因子的研究进展
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摘要
SPL(squamosa promoter-binding protein like)基因家族是植物特有的一类转录因子,主要通过结合下游基因启动子区的顺式作用元件GTAC基序,从而参与调控下游基因的表达。SPLs转录因子在植物的生长发育、信号传导、应答环境胁迫等方面有着重要的作用。目前研究表明,大豆SPL转录因子在参与调控大豆植株分枝数,产量和生育期等方面扮演重要作用。文章首先从该家族转录因子的克隆入手,回顾该基因家族的由来历史,然后介绍其结构上的保守性和独特性,最后重点综述SPL转录因子在植物中的调控网络,及其生物学功能,并对其在大豆及其它农作物生产上的应用前景及其调控植物性状的具体机制进行展望。
SPL(squamosa promoter-binding protein like)genes which encoded plant-specific transcription factors, can regulate the expression of target genes by binding to the GTAC cis-element. SPLs transcription factor play an important role in plant growth and development, signaling and response environment stress. Recent research showed that soybean SPL transcription factors play an important role in regulating the number of branches, yield and maturity. This review summarizes the emerging of research work on the function of the SPL transcription factors, introduces the cloning of the SPL genes and regulation network, etc., and describes in detail on the function of the SPL genes of higher plants. This review provides a brief survey about the regulatory network and biological function of SPLs, and a discussion of their potential applications in the agronomic production and the mechanism of regulating plant traits.
SPL(squamosa promoter-binding protein like)genes which encoded plant-specific transcription factors, can regulate the expression of target genes by binding to the GTAC cis-element. SPLs transcription factor play an important role in plant growth and development, signaling and response environment stress. Recent research showed that soybean SPL transcription factors play an important role in regulating the number of branches, yield and maturity. This review summarizes the emerging of research work on the function of the SPL transcription factors, introduces the cloning of the SPL genes and regulation network, etc., and describes in detail on the function of the SPL genes of higher plants. This review provides a brief survey about the regulatory network and biological function of SPLs, and a discussion of their potential applications in the agronomic production and the mechanism of regulating plant traits.
引文
[1]Peter H,Joachim K,Wolf-Ekkehard L,et al.Bracteomania an inflorescence amomaly,is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus[J].The European Molecular Biology Organization Journal,1992,11(4):1239-1249.
[2]Klein J,Saedler H,Huijser P.A new family of proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA[J].Molecular&General Genetics,1996,250(1):7-16.
[3]Guillermo H,Susanne H,Klaus N,et al.Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3:A novel gene involved in the transition[J].The Plant Journal,1997,12(2):367-377.
[4]Xu M L,Hu T Q,Zhao J F,et al.Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE(SPL)Genes in Arabidopsis thaliana[J].PLo S Genetic,2016,12(8):e1006263.
[5]Yu Z X,Wang L J,Zhao B,et al.Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and patchouli(Pogostemon cablin)by the miR156-targeted SPL transcription factors[J].Molecular Plant,2015,8(1):98-110.
[6]Guillermo C,Susanne H,Joachin K,et al.Molecular characterization of the Arabidopsis SBP-box genes[J].Gene,1999,237(1):91-104.
[7]Eriksson M,Moseley J L,Tottey S,et al.Genetic dissection of nutritional copper signaling in chlamydomonas distinguishes regulatory and target genes[J].Genetics,2004,168(2):795-807.
[8]Guo A Y,Zhu Q H,Gu X C,et al.Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family[J].Gene,2008,418(1-2):1-8.
[9]Wu Y W,Ke Y Z,Wen J,et al.Evolution and expression analyses of the MADS-box gene family in Brassica napus[J].Public Library of Science One,2018,13(7):e0200762.
[10]Matthew W R,Brenda J R,Lee P L,et al.Prediction of plant microRNA targets[J].Cell,2002,110:513-520.
[11]Wang S K,Li S,Liu Q,et al.The Os SPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quanlity[J].Nature Genetics,2015,47(8):1-6.
[12]Sun Z,Su C,Yun J,et al.Genetic improvement of the shoot architecture and yeild in soybean plants via the manipulation of GmmiR156[J].Plant Biotechnol Journal,2018,10:1-13.
[13]Wu G,Park M Y,Conway S R,et al.The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis[J].Cell,2009,138(4):750-759.
[14]Ayako Y,Wu M F,Li Y,et al.The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY,FRUITFULL,and APETALA1[J].Developmental Cell,2009,17(2):268-278.
[15]Xie K B,Wu C Q,Xiong L Z.Genomic organization,differential expression,and interaction of SQUAMOSA promoter-binding-like transcription factors and micro-RNA156 in rice[J].Plant Physiology,2006,142(1):280-293.
[16]Rajiv K T,Ridhi G,Sweta K,et al.Genomic organization phylogenetic comparison,and expression profiles of the SPL family genes and their regulation in soybean[J].Development Genes and Evolution,2017,227(2):101-119.
[17]Cao D,Li Y,Wang J,et al.GmmiR156 overexpression delay flowering time in soybean[J].Plant Molecular Biology,2015,89(4-5):353-363.
[18]Lu M C,Liu Y Q,Chen D Y,et al.Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage[J].Molecular Plant,2017,10(5):735-748.
[19]Xu M L,Hu T Q,Zhao J F,et al.Developmental functions miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE(SPL)genes in Arabidopsis thaliana[J].Public Library of Science Genetics,2016,12(8):e4006263.
[20]Meenu S P,Ma S S,Tessa M B,et al.Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity[J].Public Library of Science,2013,9(3):e1003235.
[21]Yamasaki H,Hayashi M,Fukazawa M,et al.SQUAMOSA promoter binding protein like-7 is a central regulator for copper homeostasis in Arabidopsis[J].The Plant Cell,2009,21(1):347-361.
[22]Cui L G,Shan J X,Shi M,et al.The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plant[J].The Plant Journal,2014,80(6):1108-1117.
[23]Gao R M,Wang Y,Gruber M Y,et al.MiR156/SPL10 modulate lateral root development,branching and leaf morphology in Arabidopsis by silencing AGAMOUS 79[J].Frontier in Plant Science,2018,8:2226.
[24]Yue E K,Li C,Li Y,et al.MiR529a modulates panicle architeeture through regulating SQUAMOSA PROMOTER BINDING-LIKEgenes in rice(Oryza sativa)[J].Plant Molecular Biology,2017,94(4-5):469-480.
[25]Liu Q,Shen G Z,Peng K Q,et al.The alteration in the architecture of a T-DNA insertion rice mutant osmtd1 is caused by up-regulation of MicroRNA156f[J].Journal of Integrative Plant Biology,2015,57(10):819-829.
[26]Tang M,Zhou C,Meng L,et al.Overexpression of Os SPL9 enhances accumulation of Cu in rice grain and improves its digestibility and metabolism[J].Journal of Genetics and Genomics,2016,43(11):673-676.
[27]Lan T,Zhang S,Liu T T,et al.Fine mapping and candidate identification of SST,a gene controlling seeding salt tolerance in rice(Oryza sativa L.)[J].Euphytica,2015,205(1):269-274.
[28]Si L Z,Chen J Y,Huang X H,et al.Os SPL13 controls grain size in cultivated rice[J].Nature Genetic,2016,48(4):447-456.
[29]Wang L,Zhang Q F.Boosting rice yield by fine-tuning SPL gene expression[J].Cell Press,2017,22(8):643-646.
[30]Wang S K,Li S,Liu Q,et al.The Os SPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality[J].Nature Genetic,2015,47(8):949-954.
[31]Silva J,Silva E,Azevedo M,et al.microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development[J].The Plant Journay,2014,78(4):604-618.
[32]Fang Y,Spector D L.Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants[J].Current Biology,2007,17(9):818-823.
[33]Liu N,Tu L L,Wang L C,et al.MicroRNA157-targeted SPLgenes regulate floral organ size and ovule production in cotton[J].BioMed Central Plant Biology Plant Biology,2017,17:7-21.
[34]Long J M,Liu C Y,Feng M Q,et al.MiR156-SPL modules regulate induction of somatic embryogenesis in citrus callus[J].Journal of Experimental Botany,2018,69(12):2979-2993.
[35]Poethig R S.Vegetative phase change and shoot maturation in plants[J].Current Topics in Developmental Biology,2013,105:125-152.
[36]Wu G,Mee Y P,Susan R C,et al.The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis[J].Cell,2009,138(4):750-759.
[37]Stefan S,Arne V G,Nora B,et al.The microRNA regulated SBP-box gene SPL9 and SPL15 control shoot maturation in Arabidopsis[J].Plant Molecular Biology,2008,67(1-2):183-195.
[38]Burle I,Dean C.The timing of developmental transitions in plants[J].Cell,2006,125(4):655-664.
[39]Wang J W,Czech B,Weigel D.MiR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana[J].Cell,2009,138(4):738-749.
[40]Madhuri G,Rainer P B,Susanne H,et al.The miRNA156/157recognition element in the 3’UTR of the Arabidopsis SBP-box gene SPL3 prevents early flowering by transcriptional inhibition in seedlings[J].The Plant Journal,2007,49(4):683-693.
[41]Jung J H,Lee H J,Ryu J Y,et al.SPL3/4/5 integrate development aging and photoperiod signals into the FT-FD module in Arabidopsis flowering[J].Molecular Plant,2016,9(12):1647-1659.
[42]Jae H J,Ju Y,Pil S,et al.The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis[J].The Plant Journal,2012,69(4):577-588.
[43]Wang J W,Rebecca S,Benjamin C,et al.Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana[J].The Plant Cell,2008,20(5):1231-1243.
[44]Wang L,Sun S,Jin J,et al.Coordinated regulation of vegetative and reproductive branching in rice[J].Proceedings of the National Academy of Sciences,2015,112(50):15504-15509.
[45]Gao R,Gruber M Y,Amyot L,et al.SPL13 regulates shoot branching and flowering time in Medicago sativa[J].Plant Molecular Biology,2018,96(1-2):119-133.
[46]Maria A M,Lisa C H,Rogar W K,et al.Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis[J].Genes&Development,2018,11(5):616-829.
[47]Wang S,Wu K,Yuan Q B,et al.Control of grain size,shape and quality by Os SPL16 in rice[J].Nature Genetic,2012,44(8):950-954.
[48]Briggs W R,Huala E.Blue-light photoreceptors in higher plants[J].Annual Review of Cell and Developmental Biology,1999,15:33-62.
[49]Maike R,Oliver Z,Heinz S,et al.SBP-domain transcription factors as possible effectors of cryptochrome mediated blue light signaling in the moss Physcomitrella patens[J].Planta,2008,227(2):505-515.
[50]Evans M M,Poethiq R S.Gibberellins promote vegetative phase change and reproductive maturity in rice[J].Plant Physiology,1995,108(2):475-487.
[51]Murase K,Hirano Y,Sun T P,et al.Gibberellin-induced DEL-LA recognition by the gibberellin receptor GID1[J].Nature,2008,456(7221):459-463.
[52]Zhang Y,Stefan S,Heinz S.SPL8,a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis[J].Plant Molecular Biology,2007,63(3):429-439.
[53]Jae J K,Jeong H L,Kim W H,et al.The microRNA156-SQUA-MOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LO-CUS T in Arabidopsis1[J].Plant Physiology,2012,159(1):461-478.
[54]Chao L M,Liu Y Q,Chen D Y,et al.Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage[J].Molecular Plant,2017,10(5):735-748.
[55]Stief A,Altmann S,Hoffmann K,et al.Arabidopsis miR156 regulated tolerance to recurring enviromental stress through SPL transcription factors[J].Plant Cell,2014,26(4):1792-1807.
[56]Hou H,Li J,Gao M,et al.Genomic organization,phylogenetic comparison and differential expression of the SBP-box family genes in grape[J].Public Library of Science One,2013,8(3):e59358.
[57]Sunkar R,Zhu J K.Novel and stress-regulated microRNA and other small RNA from Arabidopsis[J].The Plant Cell,2004,16(8):2001-2019.
[58]Cui L G,Shan J X,Shi M,et al.The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plant[J].The Plant Journal,2014,80(6):1108-1117.
[59]Ning K,Chen S,Huang H J,et al.Molecular characterization and expression analysis of the SPL gene family with BpSPL9 transgenic lines found to confer tolerance to abiotic stress in Betula platyphylla Suk[J].Plant Cell Tissue and Organ Culture,2017,130(3):469-481.
[60]Kropat J,Tottey S,Birkenbihl R P,et al.A regulator of nutritional copper signaling in Chlamydomonasis is an SBP domain protein that recognize the GTAC core of copper response element[J].Proceedings of the National Academy of Sciences of the United States of America,2005,102(51):18730-18735.
[61]Sommer F,Kropat J,Malasarn D.The CRR1 nutritional copper sensor in Chlamydomonas contains two distinct metal-responsive domains[J].Plant Cell,2010,22(12):4098-4113.
[62]Desai K,Sullards M C,Allegood J,et al.Fumonisins and fumonisin analogs as inhibitors of ceramide synthase and inducers of apoptosis[J].Biochimica et Biophysica Acta,2002,1585(2):188-192.
[63]Wang J,Zhou L,Shi H,et al.A single transcription factor promotes both yield and immunity in rice[J].Science,2018,361(6406):1026-1028.
[64]Hou H M,Ya Q,Wang X P,et al.A SBP-box gene Vp SBP5 from Chinese wild Vitis species responds to Erysiphe necator and defense signaling molecules[J].Plant Molecular Biology Reporter,2013,31(6):1261-1270.
[65]Hou H,Li J,Gao M,et al.Genomic organization,phylogenetic comparison and differential expression of the SBP-box family genes in grape[J].Public Library of Science One,2013,8(3):e59358.
[66]Stacy A J,Jill C P.Differential SPL gene expression patterns reveal candidate genes underlying flowering time and architectural differences in Mimulus and Arabidopsis[J].Molecular Phylogenetical and Evolution,2014,73(1):129-139.
[67]Shikata M,Koyama T,Misuda N M,et al.Arabidopsis SBP-box genes SPL10,SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase[J].Plant Cell Physiology,2009,50(12):2133-2145.
[2]Klein J,Saedler H,Huijser P.A new family of proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA[J].Molecular&General Genetics,1996,250(1):7-16.
[3]Guillermo H,Susanne H,Klaus N,et al.Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3:A novel gene involved in the transition[J].The Plant Journal,1997,12(2):367-377.
[4]Xu M L,Hu T Q,Zhao J F,et al.Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE(SPL)Genes in Arabidopsis thaliana[J].PLo S Genetic,2016,12(8):e1006263.
[5]Yu Z X,Wang L J,Zhao B,et al.Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and patchouli(Pogostemon cablin)by the miR156-targeted SPL transcription factors[J].Molecular Plant,2015,8(1):98-110.
[6]Guillermo C,Susanne H,Joachin K,et al.Molecular characterization of the Arabidopsis SBP-box genes[J].Gene,1999,237(1):91-104.
[7]Eriksson M,Moseley J L,Tottey S,et al.Genetic dissection of nutritional copper signaling in chlamydomonas distinguishes regulatory and target genes[J].Genetics,2004,168(2):795-807.
[8]Guo A Y,Zhu Q H,Gu X C,et al.Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family[J].Gene,2008,418(1-2):1-8.
[9]Wu Y W,Ke Y Z,Wen J,et al.Evolution and expression analyses of the MADS-box gene family in Brassica napus[J].Public Library of Science One,2018,13(7):e0200762.
[10]Matthew W R,Brenda J R,Lee P L,et al.Prediction of plant microRNA targets[J].Cell,2002,110:513-520.
[11]Wang S K,Li S,Liu Q,et al.The Os SPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quanlity[J].Nature Genetics,2015,47(8):1-6.
[12]Sun Z,Su C,Yun J,et al.Genetic improvement of the shoot architecture and yeild in soybean plants via the manipulation of GmmiR156[J].Plant Biotechnol Journal,2018,10:1-13.
[13]Wu G,Park M Y,Conway S R,et al.The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis[J].Cell,2009,138(4):750-759.
[14]Ayako Y,Wu M F,Li Y,et al.The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY,FRUITFULL,and APETALA1[J].Developmental Cell,2009,17(2):268-278.
[15]Xie K B,Wu C Q,Xiong L Z.Genomic organization,differential expression,and interaction of SQUAMOSA promoter-binding-like transcription factors and micro-RNA156 in rice[J].Plant Physiology,2006,142(1):280-293.
[16]Rajiv K T,Ridhi G,Sweta K,et al.Genomic organization phylogenetic comparison,and expression profiles of the SPL family genes and their regulation in soybean[J].Development Genes and Evolution,2017,227(2):101-119.
[17]Cao D,Li Y,Wang J,et al.GmmiR156 overexpression delay flowering time in soybean[J].Plant Molecular Biology,2015,89(4-5):353-363.
[18]Lu M C,Liu Y Q,Chen D Y,et al.Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage[J].Molecular Plant,2017,10(5):735-748.
[19]Xu M L,Hu T Q,Zhao J F,et al.Developmental functions miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE(SPL)genes in Arabidopsis thaliana[J].Public Library of Science Genetics,2016,12(8):e4006263.
[20]Meenu S P,Ma S S,Tessa M B,et al.Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity[J].Public Library of Science,2013,9(3):e1003235.
[21]Yamasaki H,Hayashi M,Fukazawa M,et al.SQUAMOSA promoter binding protein like-7 is a central regulator for copper homeostasis in Arabidopsis[J].The Plant Cell,2009,21(1):347-361.
[22]Cui L G,Shan J X,Shi M,et al.The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plant[J].The Plant Journal,2014,80(6):1108-1117.
[23]Gao R M,Wang Y,Gruber M Y,et al.MiR156/SPL10 modulate lateral root development,branching and leaf morphology in Arabidopsis by silencing AGAMOUS 79[J].Frontier in Plant Science,2018,8:2226.
[24]Yue E K,Li C,Li Y,et al.MiR529a modulates panicle architeeture through regulating SQUAMOSA PROMOTER BINDING-LIKEgenes in rice(Oryza sativa)[J].Plant Molecular Biology,2017,94(4-5):469-480.
[25]Liu Q,Shen G Z,Peng K Q,et al.The alteration in the architecture of a T-DNA insertion rice mutant osmtd1 is caused by up-regulation of MicroRNA156f[J].Journal of Integrative Plant Biology,2015,57(10):819-829.
[26]Tang M,Zhou C,Meng L,et al.Overexpression of Os SPL9 enhances accumulation of Cu in rice grain and improves its digestibility and metabolism[J].Journal of Genetics and Genomics,2016,43(11):673-676.
[27]Lan T,Zhang S,Liu T T,et al.Fine mapping and candidate identification of SST,a gene controlling seeding salt tolerance in rice(Oryza sativa L.)[J].Euphytica,2015,205(1):269-274.
[28]Si L Z,Chen J Y,Huang X H,et al.Os SPL13 controls grain size in cultivated rice[J].Nature Genetic,2016,48(4):447-456.
[29]Wang L,Zhang Q F.Boosting rice yield by fine-tuning SPL gene expression[J].Cell Press,2017,22(8):643-646.
[30]Wang S K,Li S,Liu Q,et al.The Os SPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality[J].Nature Genetic,2015,47(8):949-954.
[31]Silva J,Silva E,Azevedo M,et al.microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development[J].The Plant Journay,2014,78(4):604-618.
[32]Fang Y,Spector D L.Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants[J].Current Biology,2007,17(9):818-823.
[33]Liu N,Tu L L,Wang L C,et al.MicroRNA157-targeted SPLgenes regulate floral organ size and ovule production in cotton[J].BioMed Central Plant Biology Plant Biology,2017,17:7-21.
[34]Long J M,Liu C Y,Feng M Q,et al.MiR156-SPL modules regulate induction of somatic embryogenesis in citrus callus[J].Journal of Experimental Botany,2018,69(12):2979-2993.
[35]Poethig R S.Vegetative phase change and shoot maturation in plants[J].Current Topics in Developmental Biology,2013,105:125-152.
[36]Wu G,Mee Y P,Susan R C,et al.The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis[J].Cell,2009,138(4):750-759.
[37]Stefan S,Arne V G,Nora B,et al.The microRNA regulated SBP-box gene SPL9 and SPL15 control shoot maturation in Arabidopsis[J].Plant Molecular Biology,2008,67(1-2):183-195.
[38]Burle I,Dean C.The timing of developmental transitions in plants[J].Cell,2006,125(4):655-664.
[39]Wang J W,Czech B,Weigel D.MiR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana[J].Cell,2009,138(4):738-749.
[40]Madhuri G,Rainer P B,Susanne H,et al.The miRNA156/157recognition element in the 3’UTR of the Arabidopsis SBP-box gene SPL3 prevents early flowering by transcriptional inhibition in seedlings[J].The Plant Journal,2007,49(4):683-693.
[41]Jung J H,Lee H J,Ryu J Y,et al.SPL3/4/5 integrate development aging and photoperiod signals into the FT-FD module in Arabidopsis flowering[J].Molecular Plant,2016,9(12):1647-1659.
[42]Jae H J,Ju Y,Pil S,et al.The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis[J].The Plant Journal,2012,69(4):577-588.
[43]Wang J W,Rebecca S,Benjamin C,et al.Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana[J].The Plant Cell,2008,20(5):1231-1243.
[44]Wang L,Sun S,Jin J,et al.Coordinated regulation of vegetative and reproductive branching in rice[J].Proceedings of the National Academy of Sciences,2015,112(50):15504-15509.
[45]Gao R,Gruber M Y,Amyot L,et al.SPL13 regulates shoot branching and flowering time in Medicago sativa[J].Plant Molecular Biology,2018,96(1-2):119-133.
[46]Maria A M,Lisa C H,Rogar W K,et al.Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis[J].Genes&Development,2018,11(5):616-829.
[47]Wang S,Wu K,Yuan Q B,et al.Control of grain size,shape and quality by Os SPL16 in rice[J].Nature Genetic,2012,44(8):950-954.
[48]Briggs W R,Huala E.Blue-light photoreceptors in higher plants[J].Annual Review of Cell and Developmental Biology,1999,15:33-62.
[49]Maike R,Oliver Z,Heinz S,et al.SBP-domain transcription factors as possible effectors of cryptochrome mediated blue light signaling in the moss Physcomitrella patens[J].Planta,2008,227(2):505-515.
[50]Evans M M,Poethiq R S.Gibberellins promote vegetative phase change and reproductive maturity in rice[J].Plant Physiology,1995,108(2):475-487.
[51]Murase K,Hirano Y,Sun T P,et al.Gibberellin-induced DEL-LA recognition by the gibberellin receptor GID1[J].Nature,2008,456(7221):459-463.
[52]Zhang Y,Stefan S,Heinz S.SPL8,a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis[J].Plant Molecular Biology,2007,63(3):429-439.
[53]Jae J K,Jeong H L,Kim W H,et al.The microRNA156-SQUA-MOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LO-CUS T in Arabidopsis1[J].Plant Physiology,2012,159(1):461-478.
[54]Chao L M,Liu Y Q,Chen D Y,et al.Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage[J].Molecular Plant,2017,10(5):735-748.
[55]Stief A,Altmann S,Hoffmann K,et al.Arabidopsis miR156 regulated tolerance to recurring enviromental stress through SPL transcription factors[J].Plant Cell,2014,26(4):1792-1807.
[56]Hou H,Li J,Gao M,et al.Genomic organization,phylogenetic comparison and differential expression of the SBP-box family genes in grape[J].Public Library of Science One,2013,8(3):e59358.
[57]Sunkar R,Zhu J K.Novel and stress-regulated microRNA and other small RNA from Arabidopsis[J].The Plant Cell,2004,16(8):2001-2019.
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