植物重金属胁迫相关miRNA的研究进展
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摘要
重金属胁迫是植物面临的一种重要的非生物胁迫。重金属会破坏细胞中的蛋白质结构,它产生的活性氧等有害物质也会对植物的生长发育造成危害。植物在进化过程中形成了多种应对重金属胁迫的分子机制,而miRNA在其中发挥了重要的调控作用。本综述概括总结了重金属对植物的危害作用、植物解除重金属胁迫的机制、miRNA的形成过程和作用机理,具体分析了在铜、镉、砷、汞等不同重金属胁迫条件下miRNA及其靶基因的应答情况,并对国内外相关研究内容和研究重点进行了总结和展望。本综述内容为更深入地研究植物应答重金属胁迫的调控机制及植物的抗性育种提供一定的参考。
Heavy metal stress is an important abiotic stress that plants face. Heavy mental can damage the structure of the protein in cells, and produce harmful substances such as reactive oxygen species, which will damage the growth and development of plants. Plants have formed a variety of molecular mechanisms that respond to heavy metal stress in the evolutionary process, and miRNAs play an important regulatory role. The review outlined the harmful effects of heavy metals in plants, the mechanism of plants relieving heavy metal stress, as well as the formation process and action mechanism of miRNA. It specifically analyzed the response of miRNA and its target genes under different heavy metal stresses such as copper, cadmium, arsenic and mercury. It also summarized and forecast the relevant research contents and emphasis at home and abroad. The review would be valuable for further research on the regulation mechanism of plants under heavy metal stress as well as the resistance breeding of plants.
Heavy metal stress is an important abiotic stress that plants face. Heavy mental can damage the structure of the protein in cells, and produce harmful substances such as reactive oxygen species, which will damage the growth and development of plants. Plants have formed a variety of molecular mechanisms that respond to heavy metal stress in the evolutionary process, and miRNAs play an important regulatory role. The review outlined the harmful effects of heavy metals in plants, the mechanism of plants relieving heavy metal stress, as well as the formation process and action mechanism of miRNA. It specifically analyzed the response of miRNA and its target genes under different heavy metal stresses such as copper, cadmium, arsenic and mercury. It also summarized and forecast the relevant research contents and emphasis at home and abroad. The review would be valuable for further research on the regulation mechanism of plants under heavy metal stress as well as the resistance breeding of plants.
引文
Abdel-Ghany S.E.,and Pilon M.,2008,MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis,J.Biol.Chem.,283(23):15932-15945
Axtell M.J.,Westholm J.O.,and Lai E.C.,2011,Vive la difference:biogenesis and evolution of microRNAs in plants and animals,Genome Biol.,12(4):221
Bartel D.P.,2004,MicroRNAs:genomics,biogenesis,mechanism,and function,Cell,116(2):281-297
Baumberger N.,and Baulcombe D.C.,2005,Arabidopsis ARGO-NAUTE1 is an RNA Slicer that selectively recruits micro R-NAs and short interfering RNAs,Proc.Natl.Acad.Sci.USA,102(33):11928-11933
Beauclair L.,Yu A.,and Bouche N.,2010,microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase m RNA in Arabidopsis,Plant J.,62(3):454-462
Chen X.B.,Zhang Z.L.,Liu D.M.,Zhang K.,Li A.L.,and Mao L.,2010,SQUAMOSA promoter-binding protein-like transcription factors:star players for plant growth and development,J.Integr.Plant Biol.,52(11):946-951
DalCorso G.,Manara A.,and Furini A.,2013,An overview of heavy metal challenge in plants:from roots to shoots,Metallomics,5(9):1117-1132
Ding D.,Zhang L.F.,Wang H.,Liu Z.J.,Zhang Z.X.,and Zheng Y.L.,2009,Differential expression of mi RNAs in response to salt stress in maize roots,Ann.Bot.,103(1):29-38
Ding Y.F.,Chen Z.,and Zhu C.,2011,Microarray-based analysis of cadmium-responsive microRNAs in rice(Oryza sativa),J.Exp.Bot.,62(10):3563-3573
Emamverdian A.,Ding Y.L.,Mokhberdoran F.,and Xie Y.F.,2015,Heavy metal stress and some mechanisms of plant defense response,Scientific World Journal,2015:756120
Fang X.L.,Zhao Y.Y.,Ma Q.B.,Huang Y.,Wang P.,Zhang J.,Nian H.,and Yang C.Y.,2013,Identification and comparative analysis of cadmium tolerance-associated mi RNAs and their targets in two soybean genotypes,PLoS One,8(12):e81471
Feng X.,Lai Z.X.,Lin Y.L.,Lai G.T.,and Lian C.L.,2015,Genome-wide identification and characterization of the superoxide dismutase gene family in Musa acuminata cv.Tianbaojiao(AAA group),BMC Genomics,16:823
Garcia-Molina A.,Xing S.,and Huijser P.,2014,Functional characterisation of Arabidopsis SPL7 conserved protein domains suggests novel regulatory mechanisms in the Cu deficiency response,BMC Plant Biol.,14:231
Ge C.L.,Ding Y.,Wang Z.G.,Wan D.Z.,Wang Y.L.,Shang Q.,and Luo S.S.,2009,Responses of wheat seedlings to cadmium,mercury and trichlorobenzene stresses,J.Environ.Sci.,21(16):806-813
Gielen H.D.,Remans T.,Vangronsveld J.,and Cuypers A.,2016,Toxicity responses of Cu and Cd:the involvement of mi R-NAs and the transcription factor SPL7,BMC Plant Biol.,16(1):145
He L.,and Hannon G.J.,2004,MicroRNAs:small RNAs with a big role in gene regulation,Nat.Rev.Genet.,5(7):522-531
He X.Y.,Zheng W.T.,Cao F.B.,and Wu F.B.,2016,Identification and comparative analysis of the microRNA transcriptome in roots of two contrasting tobacco genotypes in response to cadmium stress,Sci.Rep.,6:32805
Huang S.Q.,Xiang A.L.,Che L.L.,Chen S.,Li H.,Song J.B.,and Yang Z.M.,2010,A set of mi RNAs from Brassica napus in response to sulphate deficiency and cadmium stress,Plant Biotechnol.J.,8(8):887-899
Jones-Rhoades M.W.,and Bartel D.P.,2004,Computational identification of plant microRNAs and their targets,including a stress-induced mi RNA,Mol.Cell,14(6):787-799
Kurihara Y.,and Watanabe Y.,2004,Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions,Proc.Natl.Acad.Sci.USA,101(34):12753-12758
Liu Q.P.,Hu H.C.,Zhu L.Y.,Li R.C.,Feng Y.,Zhang L.Q.,Yang Y.Y.,Liu X.Q.,and Zhang H.M.,2015a,Involvement of mi R528 in the regulation of arsenite tolerance in rice(Oryza sativa L.),J.Agric.Food Chem.,63(40):8849-8861
Liu W.,Xu L.,Wang Y.,Shen H.,Zhu X.W.,Zhang K.Y.,Chen Y.L.,Yu RG.,Limera C.,and Liu L.W.,2015b,Transcriptome-wide analysis of chromium-stress responsive microR-NAs to explore mi RNA-mediated regulatory networks in radish(Raphanus sativus L.),Sci.Rep.,5:14024
Liu Q.,and Zhang H.,2012,Molecular identification and analysis of arsenite stress-responsive mi RNAs in rice,J.Agric.Food Chem.,60(26):6524-6536
Lu S.,Sun Y.H.,and Chiang V.L.,2008,Stress-responsive microRNAs in Populus,Plant J.,55(1):131-151
Lu S.,Yang C.,and Chiang V.L.,2011,Conservation and diversity of microRNA-associated copper-regulatory networks in Populus trichocarpa,J.Integr.Plant Biol.,53(11):879-891
Noman A.,and Aqeel M.,2017,mi RNA-based heavy metal homeostasis and plant growth,Environ.Sci.Pollut.Res.,24(11):10068-10082
Qiu Z.,Hai B.,Guo J.,Li Y.,and Zhang L.,2016,Characterization of wheat mi RNAs and their target genes responsive to cadmium stress,Plant Physiol.Biochem.,101:60-67
Rizwan M.,Ali S.,Adrees M.,Rizvi H.,Zia-Ur-Rehman M.,Hannan F.,Qayyum M.F.,Hafeez F.,and Ok Y.S.,2016,Cadmium stress in rice:toxic effects,tolerance mechanisms,and management:a critical review,Environ.Sci.Pollut.Res.Int.,23(18):17859-17879
Sharma D.,Tiwari M.,Lakhwani D.,Tripathi R.D.,and Trivedi P.K.,2015,Differential expression of microRNAs by arsenate and arsenite stress in natural accessions of rice,Metallomics,7(1):174-187
Sharma S.S.,and Dietz K.J.,2009,The relationship between metal toxicity and cellular redox imbalance,Trends Plant Sci.,14(1):43-50
Singh S.,Parihar P.,Singh R.,Singh V.P.,and Prasad S.M.,2015,Heavy metal tolerance in plants:role of transcriptomics,proteomics,metabolomics,and lonomics,Front.Plant Sci.,6:1143
Srivastava S.,Srivastava A.K.,Suprasanna P.,and D'Souza S.F.,2009,Comparative biochemical and transcriptional profiling of two contrasting varities of Brassica juncea L.in response to arsenic exposure reveals mechanisms of stress perception and tolerance,J.Exp.Bot.,60(12):3419-3431
Srivastava S.,Srivastava A.K.,Suprasanna P.,and D'Souza S.F.,2013,Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea,J.Exp.Bot.,64(1):303-315
Srivastava S.,Suprasanna P.,and D'Souza S.F.,2012,Mechanisms of arsenic tolerance and detoxification in plants and their application in transgenic technology:a critical appraisal,Int.J.Phytoremediation,14(5):506-517
Sterjiades R.,Dean J.F.,and Eriksson K.E.,1992,Laccase from SYCAMORE maple(Acer pseudoplatanus)polymerizes monolignols,Plant Physiol.,99(3):1162-1168
Sunkar R.,2010,MicroRNAs with macro-effects on plant stress responses,Semin.Cell Dev.Biol.,21(8):805-811
Sunkar R.,Kapoor A.,and Zhu J.K.,2006,Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of mi R398 and im portant for oxidative stress tolerance,Plant Cell,18(8):2051-2065
Valdes-Lopez O.,Yang S.S.,Aparicio-Fabre R.,Graham P.H.,Reyes J.L.,Vance C.P.,and Hernandez G.,2010,MicroR-NA expression profile in common bean(Phaseolus vulgaris)under nutrient deficiency stresses and manganese toxicity,New Phytol.,187(3):805-818
Voinnet O.,2009,Origin,biogenesis,and activity of plant microRNAs,Cell,136(4):669-687
Wang C.Y.,Zhang S.,Yu Y.,Luo Y.C.,Liu Q.,Ju C.,Zhang Y.C.,Qu L.H.,Lucas W.J.,Wang X.,and Chen Y.Q.,2014,Mi R397b regulates both lignin content and seed number in Arabidopsis via modulating a laccase involved in lignin biosynthesis,Plant Biotechnol.J.,12(8):1132-1142
Wang Y.L.,Zhao Z.L.,Deng M.J.,Liu R.N.,Niu S.Y.,and Fan G.Q.,2015,Identification and functional analysis of microRNAs and their targets in Platanus acerifolia under lead(Pb)stress,Int.J.Mol.Sci.,16(4):7098-7111
Xiao M.M.,and Chen X.B.,2018,Research progress of microR-NA response to plant abiotic stress,Fenzi Zhiwu Yuzhong(Molecular Plant Breeding),16(10):3154-3159(肖敏敏,陈信波,2018,microRNA响应植物非生物胁迫的研究进展,分子植物育种,16(10):3154-3159)
Yamasaki H.,Hayashi M.,Fukazawa M.,Kobayashi Y.,and Shikanai T.,2009,SQUAMOSA promoter binding protein-like7is a central regulator for copper homeostasis in Arabidopsis,Plant Cell,21(1):347-361
Yu L.J.,Luo Y.F.,Liao B.,Xie L.J.,Chen L.,Xiao S.,Li J.T.,Hu S.N.,and Shu W.S.,2012,Comparative transcriptome analysis of transporters,phytohormone and lipid metabolism pathways in response to arsenic stress in rice(Oryza sativa),New Phytol.,195(1):97-112
Zhang H.,and Li L.,2013,SQUAMOSA promoter binding proteinlike7 regulated microRNA408 is required for vegetative development in Arabidopsis,Plant J.,74(1):98-109
Zhang L.W.,Song J.B.,Shu X.X.,Zhang Y.,and Yang Z.M.,2013a,mi R395 is involved in detoxification of cadmium in Brassica napus,J.Hazard.Mater.,250-251:204-211
Zhang Y.C.,Yu Y.,Wang C.Y.,Li Z.Y.,Liu Q.,Xu J.,Liao J.Y.,Wang X.J.,Qu L.H.,Chen F.,Xin P.,Yan C.,Chu J.,Li H.Q.,and Chen Y.Q.,2013b,Overexpression of microRNAOsmi R397 improves rice yield by increasing grain size and promoting panicle branching,Nat.Biotechnol.,31(9):848-852
Zhou Z.S.,Huang S.Q.,and Yang Z.M.,2008,Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula,Biochem.Biophys.Res.Commun.,374(3):538-542
Zhou Z.S.,Zeng H.Q.,Liu Z.P.,and Yang Z.M.,2012,Genomewide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal,Plant Cell Environ.,35(1):86-99
Axtell M.J.,Westholm J.O.,and Lai E.C.,2011,Vive la difference:biogenesis and evolution of microRNAs in plants and animals,Genome Biol.,12(4):221
Bartel D.P.,2004,MicroRNAs:genomics,biogenesis,mechanism,and function,Cell,116(2):281-297
Baumberger N.,and Baulcombe D.C.,2005,Arabidopsis ARGO-NAUTE1 is an RNA Slicer that selectively recruits micro R-NAs and short interfering RNAs,Proc.Natl.Acad.Sci.USA,102(33):11928-11933
Beauclair L.,Yu A.,and Bouche N.,2010,microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase m RNA in Arabidopsis,Plant J.,62(3):454-462
Chen X.B.,Zhang Z.L.,Liu D.M.,Zhang K.,Li A.L.,and Mao L.,2010,SQUAMOSA promoter-binding protein-like transcription factors:star players for plant growth and development,J.Integr.Plant Biol.,52(11):946-951
DalCorso G.,Manara A.,and Furini A.,2013,An overview of heavy metal challenge in plants:from roots to shoots,Metallomics,5(9):1117-1132
Ding D.,Zhang L.F.,Wang H.,Liu Z.J.,Zhang Z.X.,and Zheng Y.L.,2009,Differential expression of mi RNAs in response to salt stress in maize roots,Ann.Bot.,103(1):29-38
Ding Y.F.,Chen Z.,and Zhu C.,2011,Microarray-based analysis of cadmium-responsive microRNAs in rice(Oryza sativa),J.Exp.Bot.,62(10):3563-3573
Emamverdian A.,Ding Y.L.,Mokhberdoran F.,and Xie Y.F.,2015,Heavy metal stress and some mechanisms of plant defense response,Scientific World Journal,2015:756120
Fang X.L.,Zhao Y.Y.,Ma Q.B.,Huang Y.,Wang P.,Zhang J.,Nian H.,and Yang C.Y.,2013,Identification and comparative analysis of cadmium tolerance-associated mi RNAs and their targets in two soybean genotypes,PLoS One,8(12):e81471
Feng X.,Lai Z.X.,Lin Y.L.,Lai G.T.,and Lian C.L.,2015,Genome-wide identification and characterization of the superoxide dismutase gene family in Musa acuminata cv.Tianbaojiao(AAA group),BMC Genomics,16:823
Garcia-Molina A.,Xing S.,and Huijser P.,2014,Functional characterisation of Arabidopsis SPL7 conserved protein domains suggests novel regulatory mechanisms in the Cu deficiency response,BMC Plant Biol.,14:231
Ge C.L.,Ding Y.,Wang Z.G.,Wan D.Z.,Wang Y.L.,Shang Q.,and Luo S.S.,2009,Responses of wheat seedlings to cadmium,mercury and trichlorobenzene stresses,J.Environ.Sci.,21(16):806-813
Gielen H.D.,Remans T.,Vangronsveld J.,and Cuypers A.,2016,Toxicity responses of Cu and Cd:the involvement of mi R-NAs and the transcription factor SPL7,BMC Plant Biol.,16(1):145
He L.,and Hannon G.J.,2004,MicroRNAs:small RNAs with a big role in gene regulation,Nat.Rev.Genet.,5(7):522-531
He X.Y.,Zheng W.T.,Cao F.B.,and Wu F.B.,2016,Identification and comparative analysis of the microRNA transcriptome in roots of two contrasting tobacco genotypes in response to cadmium stress,Sci.Rep.,6:32805
Huang S.Q.,Xiang A.L.,Che L.L.,Chen S.,Li H.,Song J.B.,and Yang Z.M.,2010,A set of mi RNAs from Brassica napus in response to sulphate deficiency and cadmium stress,Plant Biotechnol.J.,8(8):887-899
Jones-Rhoades M.W.,and Bartel D.P.,2004,Computational identification of plant microRNAs and their targets,including a stress-induced mi RNA,Mol.Cell,14(6):787-799
Kurihara Y.,and Watanabe Y.,2004,Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions,Proc.Natl.Acad.Sci.USA,101(34):12753-12758
Liu Q.P.,Hu H.C.,Zhu L.Y.,Li R.C.,Feng Y.,Zhang L.Q.,Yang Y.Y.,Liu X.Q.,and Zhang H.M.,2015a,Involvement of mi R528 in the regulation of arsenite tolerance in rice(Oryza sativa L.),J.Agric.Food Chem.,63(40):8849-8861
Liu W.,Xu L.,Wang Y.,Shen H.,Zhu X.W.,Zhang K.Y.,Chen Y.L.,Yu RG.,Limera C.,and Liu L.W.,2015b,Transcriptome-wide analysis of chromium-stress responsive microR-NAs to explore mi RNA-mediated regulatory networks in radish(Raphanus sativus L.),Sci.Rep.,5:14024
Liu Q.,and Zhang H.,2012,Molecular identification and analysis of arsenite stress-responsive mi RNAs in rice,J.Agric.Food Chem.,60(26):6524-6536
Lu S.,Sun Y.H.,and Chiang V.L.,2008,Stress-responsive microRNAs in Populus,Plant J.,55(1):131-151
Lu S.,Yang C.,and Chiang V.L.,2011,Conservation and diversity of microRNA-associated copper-regulatory networks in Populus trichocarpa,J.Integr.Plant Biol.,53(11):879-891
Noman A.,and Aqeel M.,2017,mi RNA-based heavy metal homeostasis and plant growth,Environ.Sci.Pollut.Res.,24(11):10068-10082
Qiu Z.,Hai B.,Guo J.,Li Y.,and Zhang L.,2016,Characterization of wheat mi RNAs and their target genes responsive to cadmium stress,Plant Physiol.Biochem.,101:60-67
Rizwan M.,Ali S.,Adrees M.,Rizvi H.,Zia-Ur-Rehman M.,Hannan F.,Qayyum M.F.,Hafeez F.,and Ok Y.S.,2016,Cadmium stress in rice:toxic effects,tolerance mechanisms,and management:a critical review,Environ.Sci.Pollut.Res.Int.,23(18):17859-17879
Sharma D.,Tiwari M.,Lakhwani D.,Tripathi R.D.,and Trivedi P.K.,2015,Differential expression of microRNAs by arsenate and arsenite stress in natural accessions of rice,Metallomics,7(1):174-187
Sharma S.S.,and Dietz K.J.,2009,The relationship between metal toxicity and cellular redox imbalance,Trends Plant Sci.,14(1):43-50
Singh S.,Parihar P.,Singh R.,Singh V.P.,and Prasad S.M.,2015,Heavy metal tolerance in plants:role of transcriptomics,proteomics,metabolomics,and lonomics,Front.Plant Sci.,6:1143
Srivastava S.,Srivastava A.K.,Suprasanna P.,and D'Souza S.F.,2009,Comparative biochemical and transcriptional profiling of two contrasting varities of Brassica juncea L.in response to arsenic exposure reveals mechanisms of stress perception and tolerance,J.Exp.Bot.,60(12):3419-3431
Srivastava S.,Srivastava A.K.,Suprasanna P.,and D'Souza S.F.,2013,Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea,J.Exp.Bot.,64(1):303-315
Srivastava S.,Suprasanna P.,and D'Souza S.F.,2012,Mechanisms of arsenic tolerance and detoxification in plants and their application in transgenic technology:a critical appraisal,Int.J.Phytoremediation,14(5):506-517
Sterjiades R.,Dean J.F.,and Eriksson K.E.,1992,Laccase from SYCAMORE maple(Acer pseudoplatanus)polymerizes monolignols,Plant Physiol.,99(3):1162-1168
Sunkar R.,2010,MicroRNAs with macro-effects on plant stress responses,Semin.Cell Dev.Biol.,21(8):805-811
Sunkar R.,Kapoor A.,and Zhu J.K.,2006,Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of mi R398 and im portant for oxidative stress tolerance,Plant Cell,18(8):2051-2065
Valdes-Lopez O.,Yang S.S.,Aparicio-Fabre R.,Graham P.H.,Reyes J.L.,Vance C.P.,and Hernandez G.,2010,MicroR-NA expression profile in common bean(Phaseolus vulgaris)under nutrient deficiency stresses and manganese toxicity,New Phytol.,187(3):805-818
Voinnet O.,2009,Origin,biogenesis,and activity of plant microRNAs,Cell,136(4):669-687
Wang C.Y.,Zhang S.,Yu Y.,Luo Y.C.,Liu Q.,Ju C.,Zhang Y.C.,Qu L.H.,Lucas W.J.,Wang X.,and Chen Y.Q.,2014,Mi R397b regulates both lignin content and seed number in Arabidopsis via modulating a laccase involved in lignin biosynthesis,Plant Biotechnol.J.,12(8):1132-1142
Wang Y.L.,Zhao Z.L.,Deng M.J.,Liu R.N.,Niu S.Y.,and Fan G.Q.,2015,Identification and functional analysis of microRNAs and their targets in Platanus acerifolia under lead(Pb)stress,Int.J.Mol.Sci.,16(4):7098-7111
Xiao M.M.,and Chen X.B.,2018,Research progress of microR-NA response to plant abiotic stress,Fenzi Zhiwu Yuzhong(Molecular Plant Breeding),16(10):3154-3159(肖敏敏,陈信波,2018,microRNA响应植物非生物胁迫的研究进展,分子植物育种,16(10):3154-3159)
Yamasaki H.,Hayashi M.,Fukazawa M.,Kobayashi Y.,and Shikanai T.,2009,SQUAMOSA promoter binding protein-like7is a central regulator for copper homeostasis in Arabidopsis,Plant Cell,21(1):347-361
Yu L.J.,Luo Y.F.,Liao B.,Xie L.J.,Chen L.,Xiao S.,Li J.T.,Hu S.N.,and Shu W.S.,2012,Comparative transcriptome analysis of transporters,phytohormone and lipid metabolism pathways in response to arsenic stress in rice(Oryza sativa),New Phytol.,195(1):97-112
Zhang H.,and Li L.,2013,SQUAMOSA promoter binding proteinlike7 regulated microRNA408 is required for vegetative development in Arabidopsis,Plant J.,74(1):98-109
Zhang L.W.,Song J.B.,Shu X.X.,Zhang Y.,and Yang Z.M.,2013a,mi R395 is involved in detoxification of cadmium in Brassica napus,J.Hazard.Mater.,250-251:204-211
Zhang Y.C.,Yu Y.,Wang C.Y.,Li Z.Y.,Liu Q.,Xu J.,Liao J.Y.,Wang X.J.,Qu L.H.,Chen F.,Xin P.,Yan C.,Chu J.,Li H.Q.,and Chen Y.Q.,2013b,Overexpression of microRNAOsmi R397 improves rice yield by increasing grain size and promoting panicle branching,Nat.Biotechnol.,31(9):848-852
Zhou Z.S.,Huang S.Q.,and Yang Z.M.,2008,Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula,Biochem.Biophys.Res.Commun.,374(3):538-542
Zhou Z.S.,Zeng H.Q.,Liu Z.P.,and Yang Z.M.,2012,Genomewide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal,Plant Cell Environ.,35(1):86-99