Discovery of MicroRNAs Associated with the S Type Cytoplasmic Male Sterility in Maize

doi:10.1016/S2095-3119(13)60222-1

Journal of Integrative Agriculture ›› 2013, Vol. 12 ›› Issue (2): 229-238.DOI: 10.1016/S2095-3119(13)60222-1

Discovery of MicroRNAs Associated with the S Type Cytoplasmic Male Sterility in Maize

YU Jiang-hua, ZHAO Yan-xin, QIN Ya-ting, YUE Bing, ZHENG Yong-lian , XIAO Hai-lin

National Key Laboratory of Crop Genetic Improvement/Huazhong Agricultural University, Wuhan 430070, P.R.China

收稿日期:2012-04-19 出版日期:2013-02-01 发布日期:2013-02-06
通讯作者: Correspondence XIAO Hai-lin, Mobile: 18627050215, E-mail: hailinxiao@gmail.com
作者简介:YU Jiang-hua, Tel: +86-27-87282689, E-mail: jianghuayu@gmail.com
基金资助:
This study was financially supported by the National Natural Science Foundation of China (31171565).

Discovery of MicroRNAs Associated with the S Type Cytoplasmic Male Sterility in Maize

YU Jiang-hua, ZHAO Yan-xin, QIN Ya-ting, YUE Bing, ZHENG Yong-lian , XIAO Hai-lin

National Key Laboratory of Crop Genetic Improvement/Huazhong Agricultural University, Wuhan 430070, P.R.China

Received:2012-04-19 Online:2013-02-01 Published:2013-02-06
Contact: Correspondence XIAO Hai-lin, Mobile: 18627050215, E-mail: hailinxiao@gmail.com
About author:YU Jiang-hua, Tel: +86-27-87282689, E-mail: jianghuayu@gmail.com
Supported by:
This study was financially supported by the National Natural Science Foundation of China (31171565).

摘要/Abstract

摘要： MicroRNAs (miRNAs) are endogenous small RNAs that play important regulatory roles in the growth and development processes of plants and animals. In this study, we examined the expression profiles of pollen miRNAs from a maize S type cytoplasmic male sterile line and its fertility restored line. In total, 100 known miRNAs belonging to 20 families and 81 novel miRNAs belonging to 44 families were identified. Two and seven known miRNAs had significant expression difference between the two lines at the level of P-value<0.01 and 0.011.5 fold expression difference were verified by stem-loop RT-qPCR. Gene Ontology analysis of miRNA target genes revealed that these genes mainly participated in the transcriptional regulation processes.

关键词: CMS-S , microRNAs , real-time PCR , Solexa sequencing , target gene , maize

Abstract: MicroRNAs (miRNAs) are endogenous small RNAs that play important regulatory roles in the growth and development processes of plants and animals. In this study, we examined the expression profiles of pollen miRNAs from a maize S type cytoplasmic male sterile line and its fertility restored line. In total, 100 known miRNAs belonging to 20 families and 81 novel miRNAs belonging to 44 families were identified. Two and seven known miRNAs had significant expression difference between the two lines at the level of P-value<0.01 and 0.011.5 fold expression difference were verified by stem-loop RT-qPCR. Gene Ontology analysis of miRNA target genes revealed that these genes mainly participated in the transcriptional regulation processes.

Key words: CMS-S , microRNAs , real-time PCR , Solexa sequencing , target gene , maize

YU Jiang-hua, ZHAO Yan-xin, QIN Ya-ting, YUE Bing, ZHENG Yong-lian , XIAO Hai-lin. Discovery of MicroRNAs Associated with the S Type Cytoplasmic Male Sterility in Maize[J]. Journal of Integrative Agriculture, 2013, 12(2): 229-238.

参考文献

[1]Achard P, Herr A, Baulcombe D C, Harberd N P. 2004.Modulation of floral development by a gibberellinregulatedmicroRNA. Development, 131, 3357-3365

[2]Allen E, Xie Z, Gustafson A M, Carrington J C. 2005.MicroRNA-directed phasing during trans-acting siRNAbiogenesis in plants. Cell, 121, 207-221

[3]Allen R S, Li J Y, Stahle M I, Dubroue A, Gubler F, Millar A A.2007. Genetic analysis reveals functional redundancy andthe major target genes of the Arabidopsis miR159 family.Proceedings of the National Academy of Sciences ofthe United States of America, 104, 16371-16376

[4]Audic S, Claverie J M. 1997. The significance of digitalgene expression profiles. Genome Research, 7, 986-995

[5]Bedinger P A, Edgerton M D. 1990. Developmental stagingof maize microspores reveals a transition in developing microspore proteins. Plant Physiology, 92, 474-479

[6]Benson D A, Karsch-Mizrachi I, Lipman D J, Ostell J,Wheeler D L. 2006. GenBank. Nucleic Acids Research,34, D16-D20.Bonnet E, Wuyts J, Rouzé P, van de Peer Y. 2004. Evidencethat microRNA precursors, unlike other non-codingRNAs, have lower folding free energies than randomsequences. Bioinformatics, 20, 2911-2917

[7]Cai X, Ballif J, Endo S, Davis E, Liang M, Chen D, DeWaldD, Kreps J, Zhu T, Wu Y. 2007. A putative CCAATbindingtranscription factor is a regulator of floweringtiming in Arabidopsis. Plant Physiology, 145, 98-105

[8]Chen C F, Ridzon D A, Broomer A J, Zhou Z H, Lee D H,Nguyen J T, Barbisin M, Xu N L, Mahuvakar V R,Andersen M R, et al. 2005. Real-time quantification ofmicroRNAs by stem-loop RT-PCR. Nucleic AcidsResearch, 33, e179.

[9]Chen X B, Zhang Z L, Liu D M, Zhang K, Li A L, Mao L.2010. SQUAMOSA promoter-binding protein-liketranscription factors: star players for plant growth anddevelopment. Journal of Integrative Plant Biology,52, 946-951

[10]Chuck G, Meeley R B, Hake S. 1998. The control of maizespikelet meristem fate by the APETALA2-like geneindeterminate spikelet1. Genes Development, 12, 1145-1154

[11]Chuck G, Whipple C, Jackson D, Hake S. 2010. The maizeSBP-box transcription factor encoded by tasselsheath4regulates bract development and the establishment ofmeristem boundaries. Development, 137, 1243-1250

[12]Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y. 2009.Differential expression of miRNAs in response to saltstress in maize roots. Annals of Botany, 109, 29-38

[13]Gardner P P, Daub J, Tate J G, Nawrocki E P, Kolbe D L,Lindgreen S, Wilkinson A C, Finn R D, Griffiths-Jones S,Eddy S R, et al. 2009. Rfam: updates to the RNA familiesdatabase. Nucleic Acids Research, 37, D136-D140.

[14]Griffiths-Jones S, Saini H K, Dongen S, Enright A J. 2008.miRBase: tools for microRNA genomics. Nucleic AcidsResearch, 36, D154-D158.

[15]Hanson M R, Bentolila S. 2004. Interactions of mitochondrialand nuclear genes that affect male gametophytedevelopment. The Plant Cell, 16, S154-S169.Hodgins K A, Rieseberg L, Otto S P. 2009. Genetic controlof invasive plants species using selfish geneticelements. Evolutionary Applications, 2, 555-569

[16]Howad W, Kempken F. 1997. Cell type-specific loss of atp6RNA editing in cytoplasmic male sterile Sorghumbicolor. Proceedings of the National Academy of Sciencesof the United States of America, 94, 11090-11095

[17]Kurek I, Ezra D, Begu D, Erel N, Litvak S, Breiman A. 1997.Studies on the effects of nuclear background and tissuespecificity on RNA editing of the mitochondrial ATPsynthase subunits a, 6 and 9 in fertile and cytoplasmicmale-sterile CMS wheat. Theoretical and AppliedGenetics, 95, 1305-1311

[18]Lee R C, Feinbaum R L, Ambros V. 1993. The C. elegansheterochronic gene lin-4 encodes small RNAs withantisense complementarity to lin-14 Cell, 75, 843-854

[19]Leyser O. 2006. Dynamic integration of auxin transport andsignaling. Current Biology, 6, R424-R433.Li R Q, Li Y R, Kristiansen K, Wang J. 2008. SOAP: shortoligonucleotide alignment program. Bioinformatics, 24,713-714

[20]Li X G, Su Y H, Zhao X Y, Li W, Gao X Q, Zhang X S. 2010.Cytokinin overproduction-caused alteration of flowerdevelopment is partially mediated by CUC2 and CUC3in Arabidopsis. Gene, 450, 109-120

[21]Maere S, Heymans K, Kuiper M. 2005. BiNGO: a Cytoscapeplugin to assess overrepresentation of gene ontologycategories in biological networks. Bioinformatics, 21,3448-3449

[22]Mallory A C, Vaucheret H. 2006. Functions of microRNAsand related small RNAs in plants. Nature Genetics, 38,S31-S36.Marin E, Jouannet V, Herz A, Lokerse A S, Weijers D,Vaucheret H, Nussaume L, Crespi M D, Maizel A. 2010.miR390, Arabidopsis TAS3 tasiRNAs, and their AUXINRESPONSE FACTOR targets define an autoregulatorynetwork quantitatively regulating lateral root growth.The Plant Cell, 22, 1104-1117

[23]Meyers B C, Axtell M J, Bartel B, Bartel D P, Baulcombe D,Bowman J L, Cao X F, Carrington J C, Chen X M, GreenP J, et al. 2008. Criteria for annotation of plantmicroRNAs. The Plant Cell, 20, 3186-3190

[24]Mi S J, Cai T, Hu Y G, Chen Y M, Hodges E, Ni F R, Wu L,Li S, Zhou H Y, Long C Z, et al. 2008. Sorting of smallRNAs into Arabidopsis argonaute complexes is directedby the 5´ terminal nucleotide. Cell, 133, 116-127

[25]Millar A A, Gubler F. 2005. The Arabidopsis GAMYB-likegenes, MYB33 and MYB65, are microRNA-regulatedgenes that redundantly facilitate anther development.The Plant Cell, 17, 705-721

[26]Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G,Nakazono M, Hiral A, Kadowaki K. 2002. The completesequence of the rice (Oryza sativa L.) mitochondrialgenome: frequent DNA sequence acquisition and lossduring the evolution of flowering plants. MolecularGenetics and Genomics, 268, 434-445

[27]Rajagopalan R, Vaucheret H, Trejo J, Bartel D P. 2006. Adiverse and evolutionarily fluid set of microRNAs inArabidopsis thaliana. Genes Development, 20, 3407-3425

[28]Rhoades M W, Reinhart B J, Lim L P, Burge C B, Bartel B,Bartel D P. 2002. Prediction of plant microRNA targets.Cell, 110, 513-520

[29]Riechmann J L, Heard J, Martin G, Reuber L, Jiang C Z,Keddie J, Adam L, Pineda O, Ratcliffe O J, Samaha R R,e al. 2000. Arabidopsis transcription factors: genomewidecomparative analysis among eukaryotes. Science,290, 2105-2110

[30]Ru P, Xu L, Ma H, Huang H. 2006. Plant fertility defectsinduced by the enhanced expression of microRNA167. Cell Research, 16, 457-465

[31]Saha S, Bridges S, Magbanua Z V, Peterson D G. 2008.Empirical comparison of ab initio repeat findingprograms. Nucleic Acids Research, 36, 2284-2294

[32]Shen Y, Zhang Z, Lin H, Liu H, Chen J, Peng H, Cao M J,Rong T Z, Pan G T. 2011. Cytoplasmic male sterilityregulatednovel microRNAs from maize. Functional andIntegrative Genomics, 11, 179-191

[33]Sunkar R, Zhou X F, Zheng Y, Zhang W X, Zhu J K. 2008.Identification of novel and candidate miRNAs in riceby high throughput sequencing. BMC Plant Biology,8, 25.Tan Q K G, Irish V F. 2006. The Arabidopsis zinc fingerhomeodomaingenes encode proteins with uniquebiochemical properties that are coordinately expressedduring floral development. Plant Physiology, 140, 1095-1108

[34]Tanaka H, Dhonukshe P, Brewer P B, Friml J. 2006.Spatiotemporal asymmetric auxin distribution: a meansto coordinate plant development. Cellular andMolecular Life Science, 63, 2738-2754

[35]Valoczi A, Varallyay E, Kauppinen S, Burgyan J, Havelda Z.2006. Spatio-temporal accumulation of microRNAs ishighly coordinated in developing plant tissues. ThePlant Journal, 47, 140-151

[36]Varkonyi-Gasic E, Wu R M, Wood M, Walton E F, HellensR P. 2007. Protocol: a highly sensitive RT-PCR methodfor detection and quantification of microRNAs. PlantMethods, 3, 12.Vaucheret H, Vazquez F, Crete P, Bartel D P. 2004. Theaction of ARGONAUTE1 in the miRNA pathway andits regulation by the miRNA pathway are crucial forplant development. Genes and Development, 18, 1187-1197

[37]Wang L, Liu H, Li D, Chen H. 2011. Identification andcharacterization of maize microRNAs involved in thevery early stage of seed germination. BMC Genomics,12, 154.Williams L, Carles C C, Osmont K S, Fletcher J C. 2005. Adatabase analysis method identifies an endogenoustrans-acting short-interfering RNA that targets theArabidopsis ARF2, ARF3, and ARF4 genes.Proceedings of the National Academy of Sciences ofthe United States of America, 102, 9703-9708

[38]Wise R P, Pring D R. 2002. Nuclear-mediated mitochondrialgene regulation and male fertility in higher plants: lightat the end of the tunnel? Proceedings of the NationalAcademy of Sciences of the United States of America,99, 10240-10242

[39]Wu M F, Tian Q, Reed J W. 2006. Arabidopsis microRNA167controls patterns of ARF6 and ARF8 expression, andregulates both female and male reproduction.Development, 133, 4211-4218

[40]Xiao H L, Zhang F D, Zheng Y L. 2006. The 5´ stem-loopand its role in mRNA stability in maize S cytoplasmicmale sterility. The Plant Journal, 47, 864-872

[41]Xie Z, Kasschau K D, Carrington J C. 2003. Negativefeedback regulation of Dicer-Like1 in Arabidopsis bymicroRNA-guided mRNA degradation. CurrentBiology, 13, 784-789

[42]Xing S P, Salinas M, Hohmann S, Berndtgen R, Huijser P.2010. MiR156-targeted and nontargeted SBP-boxtranscription factors act in concert to secure malefertility in Arabidopsis. The Plant Cell, 22, 3935-3950

[43]Yamaguchi A, Wu M F, Yang L, Wu G, Poethig R S, WagnerD. 2009. The microRNA regulated SBP-box transcriptionfactor SPL3 is a direct upstream activator of LEAFY,FRUITFULL, and APETALA1. Developmental Cell, 17,268-278

[44]Yang J H, Han S J, Yoon E K, Lee W S. 2006. Evidence of anauxin signal pathway, microRNA167-ARF8-GH3, andits response to exogenous auxin in cultured rice cells.Nucleic Acids Research, 34, 1892-1899

[45]Zabala G, Gabay-Laughnan S, Laughnan J R. 1997. Thenuclear gene Rf3 affects the expression of themitochondrial chimeric sequence R implicated in S-typemale sterility in maize. Genetics, 147, 847-850

[46]Zhang B, Pan X, Anderson T A. 2006. Identification of 188conserved microRNAs and their targets. FEBS Letters,580, 3753-3762

[47]Zhang H, Ransom C, Ludwig P, Nocker S. 2003. Geneticanalysis of early flowering mutants in Arabidopsisdefines a class of pleiotropic developmental regulatorrequired for expression of the flowering-time switchFlowering Locus C. Genetics, 164, 347-358

[48]Zhang L, Chia J M, Kumari S, Stein J C, Liu Z, NarechaniaA, Maher CA, Guill K, McMullen M D, Ware D. 2009. Agenome-wide characterization of microRNA genes inmaize. PLoS Genetics, 5, e1000716.Zhao L, Kim Y J, Dinh T T, Chen X M. 2007. miR172regulates stem cell fate and defines the inner boundaryof APETALA3 and PISTILLATA expression domain inArabidopsis floral meristems. The Plant Journal, 51,840-849

[49]Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li W X. 2012. Cloningand characterization of maize miRNAs involved inresponses to nitrogen deficiency. PLoS ONE, 7, e29669.Zuker M. 2003. Mfold web server for nucleic acid foldingand hybridization prediction. Nucleic Acids Research,31, 3406-3415.

Discovery of MicroRNAs Associated with the S Type Cytoplasmic Male Sterility in Maize

Discovery of MicroRNAs Associated with the S Type Cytoplasmic Male Sterility in Maize

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