Unravelling miRNA regulation in yield of rice (Oryza sativa) based on differential network model

Rice (Oryza sativa L.) is one of the essential staple food crops and tillering, panicle branching and grain filling are three important traits determining the grain yield. Although miRNAs have been reported being regulating yield, no study has systematically investigated how miRNAs differentially function in high and low yield rice, in particular at a network level. This abundance of data from high-throughput sequencing provides an effective solution for systematic identification of regulatory miRNAs using developed algorithms in plants. We here present a novel algorithm, Gene Co-expression Network differential edge-like transformation (GRN-DET), which can identify key regulatory miRNAs in plant development. Based on the small RNA and RNA-seq data, miRNA-gene-TF co-regulation networks were constructed for yield of rice. Using GRN-DET, the key regulatory miRNAs for rice yield were characterized by the differential expression variances of miRNAs and co-variances of miRNA-mRNA, including osa-miR171 and osa-miR1432. Phytohormone cross-talks (auxin and brassinosteroid) were also revealed by these co-expression networks for the yield of rice.

[1]  K. Aihara,et al.  Personalized characterization of diseases using sample-specific networks , 2016, bioRxiv.

[2]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[3]  Xiangbin Xu,et al.  Genome-Wide Analysis of MicroRNAs and Their Target Genes Related to Leaf Senescence of Rice , 2014, PloS one.

[4]  Zhou Du,et al.  agriGO: a GO analysis toolkit for the agricultural community , 2010, Nucleic Acids Res..

[5]  Jiawei Wang,et al.  Arabidopsis miR171-Targeted Scarecrow-Like Proteins Bind to GT cis-Elements and Mediate Gibberellin-Regulated Chlorophyll Biosynthesis under Light Conditions , 2014, PLoS genetics.

[6]  Rui Liu,et al.  Edge biomarkers for classification and prediction of phenotypes , 2014, Science China Life Sciences.

[7]  Blake C Meyers,et al.  sPARTA: a parallelized pipeline for integrated analysis of plant miRNA and cleaved mRNA data sets, including new miRNA target-identification software , 2014, Nucleic acids research.

[8]  Jing Zhang,et al.  Characterization and Expression Patterns of microRNAs Involved in Rice Grain Filling , 2013, PloS one.

[9]  H. Vaucheret,et al.  Erratum: Functions of microRNAs and related small RNAs in plants , 2006, Nature Genetics.

[10]  M. Matsuoka,et al.  The SCARECROW gene's role in asymmetric cell divisions in rice plants. , 2003, The Plant journal : for cell and molecular biology.

[11]  J. Duan,et al.  OsTIR1 and OsAFB2 Downregulation via OsmiR393 Overexpression Leads to More Tillers, Early Flowering and Less Tolerance to Salt and Drought in Rice , 2012, PloS one.

[12]  L. Mao,et al.  Identification of novel MiRNAs and MiRNA expression profiling during grain development in indica rice , 2012, BMC Genomics.

[13]  Jugal K. Kalita,et al.  Reconstruction of gene co-expression network from microarray data using local expression patterns , 2014, BMC Bioinformatics.

[14]  Comparative expression profiling of miRNAs between the cytoplasmic male sterile line MeixiangA and its maintainer line MeixiangB during rice anther development , 2014, Planta.

[15]  Xiaofeng Cao,et al.  Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica) , 2010, Frontiers in Biology.

[16]  Yan Ma,et al.  The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14 , 2013, Nature Communications.

[17]  Michael Hecker,et al.  Gene regulatory network inference: Data integration in dynamic models - A review , 2009, Biosyst..

[18]  Ana Kozomara,et al.  miRBase: annotating high confidence microRNAs using deep sequencing data , 2013, Nucleic Acids Res..

[19]  Er-kui Yue,et al.  MiR529a modulates panicle architecture through regulating SQUAMOSA PROMOTER BINDING-LIKE genes in rice (Oryza sativa) , 2017, Plant Molecular Biology.

[20]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[21]  Qian Qian,et al.  Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice , 2010, Nature Genetics.

[22]  G. Tang,et al.  Differentially expressed microRNA cohorts in seed development may contribute to poor grain filling of inferior spikelets in rice , 2014, BMC Plant Biology.

[23]  Xia Li,et al.  Comparative Transcriptome Analysis Reveals Heat-Responsive Genes in Chinese Cabbage (Brassica rapa ssp. chinensis) , 2016, Front. Plant Sci..

[24]  V. Ambros,et al.  Role of MicroRNAs in Plant and Animal Development , 2003, Science.

[25]  S. Horvath,et al.  A General Framework for Weighted Gene Co-Expression Network Analysis , 2005, Statistical applications in genetics and molecular biology.

[26]  Jing Zhang,et al.  Dynamic Analysis of Gene Expression in Rice Superior and Inferior Grains by RNA-Seq , 2015, PloS one.

[27]  Liang-Hu Qu,et al.  Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching , 2013, Nature Biotechnology.

[28]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[29]  Yun Zheng,et al.  Transcriptome-wide identification of microRNA targets in rice. , 2010, The Plant journal : for cell and molecular biology.

[30]  Fengxi Yang,et al.  Integrated mRNA and microRNA transcriptome variations in the multi-tepal mutant provide insights into the floral patterning of the orchid Cymbidium goeringii , 2017, BMC Genomics.

[31]  W. Cao,et al.  The high yield of irrigated rice in Yunnan, China 'A cross-location analysis' , 2008 .

[32]  Q. Qian,et al.  Brassinosteroid Regulates Cell Elongation by Modulating Gibberellin Metabolism in Rice[C][W][OPEN] , 2014, Plant Cell.

[33]  Q. Qian,et al.  Small RNA and degradome profiling reveals miRNA regulation in the seed germination of ancient eudicot Nelumbo nucifera , 2016, BMC Genomics.

[34]  Nana Jia,et al.  Small RNA and Transcriptome Sequencing Reveal a Potential miRNA-Mediated Interaction Network That Functions during Somatic Embryogenesis in Lilium pumilum DC. Fisch. , 2017, Front. Plant Sci..

[35]  Lei Zhang,et al.  Small RNAs as important regulators for the hybrid vigour of super-hybrid rice , 2014, Journal of experimental botany.

[36]  Matthew R Willmann,et al.  Conservation and evolution of miRNA regulatory programs in plant development. , 2007, Current opinion in plant biology.

[37]  Liang-Hu Qu,et al.  Expression analysis of phytohormone‐regulated microRNAs in rice, implying their regulation roles in plant hormone signaling , 2009, FEBS letters.

[38]  Qian Qian,et al.  Identification and Expression Analysis of microRNAs at the Grain Filling Stage in Rice(Oryza sativa L.)via Deep Sequencing , 2013, PloS one.

[39]  M. Kojima,et al.  Suppression of α-amylase genes improves quality of rice grain ripened under high temperature. , 2012, Plant biotechnology journal.

[40]  Xiaoping Liu,et al.  Diagnosing phenotypes of single-sample individuals by edge biomarkers. , 2015, Journal of molecular cell biology.

[41]  Robert D. Finn,et al.  Rfam: updates to the RNA families database , 2008, Nucleic Acids Res..

[42]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[43]  Y. Liu,et al.  Blocking miR396 increases rice yield by shaping inflorescence architecture , 2015, Nature Plants.

[44]  Ruiqiang Li,et al.  SOAP: short oligonucleotide alignment program , 2008, Bioinform..

[45]  Xiaoman Li,et al.  Transcriptional regulation of co-expressed microRNA target genes. , 2011, Genomics.

[46]  Bin Hu,et al.  Control of grain size and rice yield by GL2-mediated brassinosteroid responses , 2015, Nature Plants.

[47]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[48]  Byung Ha Lee,et al.  The Arabidopsis GRF-INTERACTING FACTOR Gene Family Performs an Overlapping Function in Determining Organ Size as Well as Multiple Developmental Properties1[C][W][OA] , 2009, Plant Physiology.

[49]  Zhao Zhang,et al.  MTide: an integrated tool for the identification of miRNA-target interaction in plants , 2015, Bioinform..

[50]  D. di Bernardo,et al.  How to infer gene networks from expression profiles , 2007, Molecular systems biology.

[51]  Lili Liu,et al.  An Integrative Bioinformatics Framework for Genome-scale Multiple Level Network Reconstruction of Rice , 2013, J. Integr. Bioinform..

[52]  Makoto Matsuoka,et al.  OsSPL14 promotes panicle branching and higher grain productivity in rice , 2010, Nature Genetics.

[53]  Xia Li,et al.  sPAGM: inferring subpathway activity by integrating gene and miRNA expression-robust functional signature identification for melanoma prognoses , 2017, Scientific Reports.

[54]  Jing Zhang,et al.  Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). , 2011, Journal of experimental botany.

[55]  Dongbo Lin,et al.  Overexpression of a tomato miR171 target gene SlGRAS24 impacts multiple agronomical traits via regulating gibberellin and auxin homeostasis , 2016, Plant biotechnology journal.

[56]  Jianxiong Li,et al.  Spatial and temporal expression modes of MicroRNAs in an elite rice hybrid and its parental lines , 2013, Planta.

[57]  S. Okawa,et al.  Effect of irradiance on the partitioning of assimilated carbon during the early phase of grain filling in rice. , 2003, Annals of botany.

[58]  Jiayang Li,et al.  Activation of Big Grain1 significantly improves grain size by regulating auxin transport in rice , 2015, Proceedings of the National Academy of Sciences.

[59]  E. F. Walton,et al.  Plant Methods Protocol: a Highly Sensitive Rt-pcr Method for Detection and Quantification of Micrornas , 2022 .

[60]  Xu-dong Zhu,et al.  Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice , 2015, Nature Plants.

[61]  Xiangtian Yu,et al.  Unravelling personalized dysfunctional gene network of complex diseases based on differential network model , 2015, Journal of Translational Medicine.

[62]  Chengcai Chu,et al.  MicroRNAs in crop improvement: fine-tuners for complex traits , 2017, Nature Plants.

[63]  Ana Kozomara,et al.  miRBase: integrating microRNA annotation and deep-sequencing data , 2010, Nucleic Acids Res..

[64]  Cai-guo Xu,et al.  Coordinated regulation of vegetative and reproductive branching in rice , 2015, Proceedings of the National Academy of Sciences.

[65]  E. Marcotte,et al.  Genetic dissection of the biotic stress response using a genome-scale gene network for rice , 2011, Proceedings of the National Academy of Sciences.