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Topological characteristics of target genes regulated by abiotic-stress-responsible miRNAs in a rice interactome network

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Abstract

A great number of microRNAs (miRNAs) have been identified in responding and acting in gene regulatory networks associated with plant tolerance to abiotic stress conditions, such as drought, salinity, and high temperature. The topological exploration of target genes regulated by abiotic-stress-responsible miRNAs (ASRmiRs) in a network facilitates to discover the molecular basis of plant abiotic stress response. This study was based on the staple food rice (Oryza sativa) in which ASRmiRs were manually curated. After having compared the topological properties of target genes (stress-miR-targets) with those (non-stress-miR-targets) not regulated by ASRmiRs in a rice interactome network, we found that stress-miR-targets exhibited distinguishable topological properties. The interaction probability analysis and k-core decomposition showed that stress-miR-targets preferentially interacted with non-stress-miR-targets and located at the peripheral positions in the network. Our results indicated an obvious topological distinction between the two types of genes, reflecting the specific mechanisms of action of stress-miR-targets in rice abiotic stress response. Also, the results may provide valuable clues to elucidate molecular mechanisms of crop response to abiotic stress.

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References

  • Akpinar BA, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genomics 15(5):587–598

    Article  CAS  PubMed  Google Scholar 

  • Aranda B et al (2010) The IntAct molecular interaction database in 2010. Nucleic Acids Res 38(suppl 1):D525–D531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Assenov Y et al (2008) Computing topological parameters of biological networks. Bioinformatics 24(2):282–284

    Article  CAS  PubMed  Google Scholar 

  • Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinforma 4(1):2

    Article  Google Scholar 

  • Barabasi A-L, Oltvai ZN (2004) Network biology: understanding the cell’s functional organization. Nat Rev Genet 5(2):101–113

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    Article  CAS  PubMed  Google Scholar 

  • Bartel PL, Fields S (1997) The yeast two-hybrid system. Oxford University Press

  • Brandao MM, Dantas LL, Silva-Filho MC (2009) AtPIN: Arabidopsis thaliana protein interaction network. BMC Bioinforma 10:454

    Article  Google Scholar 

  • Brown KR, Jurisica I (2005) Online predicted human interaction database. Bioinformatics 21(9):2076–2082

    Article  CAS  PubMed  Google Scholar 

  • Bu D et al (2003) Topological structure analysis of the protein–protein interaction network in budding yeast. Nucleic Acids Res 31(9):2443–2450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budak H et al (2015a) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13

    Article  CAS  PubMed  Google Scholar 

  • Budak H, Khan Z, Kantar M (2015b) History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief Funct Genomics 14(3):189–198

    Article  PubMed  Google Scholar 

  • Burnham JF (2006) Scopus database: a review. Biomed Digit Libr 3(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  • Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70

    Article  CAS  PubMed  Google Scholar 

  • Chatr-Aryamontri A et al (2007) MINT: the Molecular INTeraction database. Nucleic Acids Res 35(suppl 1):D572–D574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Perocchi F (2015) ProtPhylo: identification of protein–phenotype and protein–protein functional associations via phylogenetic profiling. Nucleic Acids Res:gkv455

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39(suppl 2):W155–W159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Bodt S et al (2009) Predicting protein-protein interactions in Arabidopsis thaliana through integration of orthology, gene ontology and co-expression. BMC Genomics 10(1):288

    Article  PubMed  PubMed Central  Google Scholar 

  • Ge Y et al (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10(1):153

    Article  PubMed  PubMed Central  Google Scholar 

  • Giot L et al (2003) A protein interaction map of Drosophila melanogaster. Science 302(5651):1727–1736

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S et al (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(Database issue):D140–D144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henderson J (2005) Google scholar: a source for clinicians? Can Med Assoc J 172(12):1549–1550

    Article  Google Scholar 

  • Jeong H et al (2001) Lethality and centrality in protein networks. Nature 411(6833):41–42

    Article  CAS  PubMed  Google Scholar 

  • Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics 10(4):493–507

    Article  CAS  PubMed  Google Scholar 

  • Kawahara Y et al (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6(1):4

    Article  PubMed  Google Scholar 

  • Kuchaiev O et al (2010) Topological network alignment uncovers biological function and phylogeny. J R Soc Interface 7(50):1341–1354

    Article  PubMed  PubMed Central  Google Scholar 

  • Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38:S31–S36

    Article  CAS  PubMed  Google Scholar 

  • Matthews LR et al (2001) Identification of potential interaction networks using sequence-based searches for conserved protein-protein interactions or “interologs”. Genome Res 11(12):2120–2126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morsy M et al (2008) Charting plant interactomes: possibilities and challenges. Trends Plant Sci 13(4):183–191

    Article  CAS  PubMed  Google Scholar 

  • Pawson T (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116(2):191–203

    Article  CAS  PubMed  Google Scholar 

  • Pazos F et al (1997) Correlated mutations contain information about protein-protein interaction. J Mol Biol 271(4):511–523

    Article  CAS  PubMed  Google Scholar 

  • Ren Y et al (2012) Identification of novel and conserved Populus tomentosa microRNA as components of a response to water stress. Funct Integr Genomics 12(2):327–339

    Article  CAS  PubMed  Google Scholar 

  • Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25(7):2383–2399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salwinski L et al (2004) The database of interacting proteins: 2004 update. Nucleic Acids Res 32(suppl 1):D449–D451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez B, Rasmussen A, Porter JR (2014) Temperatures and the growth and development of maize and rice: a review. Glob Chang Biol 20(2):408–417

    Article  PubMed  Google Scholar 

  • Shah NR, Chen H (2014) MicroRNAs in pathogenesis of breast cancer: implications in diagnosis and treatment. World J Clin Oncol 5(2):48–60

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen J et al (2007) Predicting protein–protein interactions based only on sequences information. Proc Natl Acad Sci 104(11):4337–4341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smoot ME et al (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27(3):431–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stark C et al (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34(suppl 1):D535–D539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R (2015) Role of microRNAs in plant abiotic stress responses. In: Plant and Animal Genome XXIII Conference. Plant and Animal Genome

  • Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17(4):196–203

    Article  CAS  PubMed  Google Scholar 

  • Uetz P et al (2000) A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae. Nature 403(6770):623–627

    Article  CAS  PubMed  Google Scholar 

  • Urano K et al (2010) ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13(2):132–138

    Article  CAS  PubMed  Google Scholar 

  • Wang P et al (2013) The MPK6-ERF6-ROS-responsive cis-acting Element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol 161(3):1392–1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wheeler DL et al (2007) Database resources of the national center for biotechnology information. Nucleic Acids Res 35(suppl 1):D5–D12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong KA, O’Bryan JP (2011) Bimolecular fluorescence complementation. J Vis Exp (50)

  • Wuchty S, Almaas E (2005) Peeling the yeast protein network. Proteomics 5(2):444–449

    Article  CAS  PubMed  Google Scholar 

  • Xie M, Zhang S, Yu B (2015) microRNA biogenesis, degradation and activity in plants. Cell Mol Life Sci 72(1):87–99

    Article  CAS  PubMed  Google Scholar 

  • Yin F et al (2014) Genome-wide analysis of Water-stress-responsive microRNA expression profile in tobacco roots. Funct Integr Genomics 14(2):319–332

    Article  CAS  PubMed  Google Scholar 

  • Yu H et al (2007) The importance of bottlenecks in protein networks: correlation with gene essentiality and expression dynamics. PLoS Comput Biol 3(4):e59

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang S et al (2013) PASmiR: a literature-curated database for miRNA molecular regulation in plant response to abiotic stress. BMC Plant Biol 13:33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong W, Sternberg PW (2006) Genome-wide prediction of C. elegans genetic interactions. Science 311(5766):1481–1484

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The research was supported by the National Natural Science Foundation of China (grant no. 31301248) and the Science Research Foundation of Anhui Provincial Colleges (grant no. KJ2013Z075).

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Correspondence to Shihua Zhang.

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Linzhong Zhang and Hongdong Xuan contributed equally to this work.

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Zhang, L., Xuan, H., Zuo, Y. et al. Topological characteristics of target genes regulated by abiotic-stress-responsible miRNAs in a rice interactome network. Funct Integr Genomics 16, 243–251 (2016). https://doi.org/10.1007/s10142-016-0481-4

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  • DOI: https://doi.org/10.1007/s10142-016-0481-4

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