Skip to main content

Genomewide analysis of intronic microRNAs in rice and Arabidopsis

Journal of Genetics volume 91, pages 313–324 (2012)Cite this article

Abstract

MicroRNAs (miRNAs) are potent regulators of gene transcription and posttranscriptional processes. The majority of miRNAs are localized within intronic regions of protein-coding genes (host genes) and have diverse functions in regulating important cellular processes in animals. To date, few plant intronic miRNAs have been studied functionally. Here we report a comprehensive computational analysis to characterize intronic miRNAs in rice and Arabidopsis. RT-PCR analysis confirmed that the identified intronic miRNAs were derived from the real introns of host genes. Interestingly, 13 intronic miRNAs in rice and two in Arabidopsis were located within seven clusters, of which four polycistronic clusters contain miRNAs derived from different families, suggesting that these clustered intronic miRNAs might be involved in extremely complex regulation in rice. Length analysis of miRNA-carrying introns, promoter prediction and qRT-PCR analysis results indicated that intronic miRNAs are coexpressed with their host genes. Expression pattern analysis demonstrated that host genes had a very broad expression spectrum in different stages of development, suggesting the intronic miRNAs might play an important role in plant development. This comparative genomics analysis of intronic miRNAs in rice and Arabidopsis provides new insight into the functions and regulatory mechanisms of intronic miRNAs in monocots and dicots.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

References

  • 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, 221.

    PubMed  Article  CAS  Google Scholar 

  • Bari R., Datt Pant B., Stitt M. and Scheible W. R. 2006 PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988–999.

    PubMed  Article  CAS  Google Scholar 

  • Barik S. 2008 An intronic microRNA silences genes that are functionally antagonistic to its host gene. Nucleic Acids Res. 36, 5232–5241.

    PubMed  Article  CAS  Google Scholar 

  • Barrett T., Troup D. B., Wilhite S. E., Ledoux P., Evangelista C., Kim I. F. et al. 2011 NCBI GEO: archive for functional genomics data sets–10 years on. Nucleic Acids Res. 39, 1005–1010.

    Article  Google Scholar 

  • Baskerville S. and Bartel D. P. 2005 Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11, 241–247.

    PubMed  Article  CAS  Google Scholar 

  • Bentwich I., Avniel A., Karov Y., Aharonov R., Gilad S., Barad O. et al. 2005 Identification of hundreds of conserved and nonconserved human microRNAs. Nat. Genet. 37, 766–770.

    PubMed  Article  CAS  Google Scholar 

  • Brown J. W., Marshall D. F. and Echeverria M. 2008 Intronic noncoding RNAs and splicing. Trends Plant Sci. 13, 335–342.

    PubMed  Article  CAS  Google Scholar 

  • Chapman E. J. and Carrington J. C. 2007 Specialization and evolution of endogenous small RNA pathways. Nat. Rev. Genet. 8, 884–896.

    PubMed  Article  CAS  Google Scholar 

  • Chen D., Meng Y., Yuan C., Bai L., Huang D., Lv S. et al. 2011 Plant siRNAs from introns mediate DNA methylation of host genes. RNA 17, 1012–1024.

    PubMed  Article  CAS  Google Scholar 

  • Ghildiyal M. and Zamore P. D. 2009 Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94–108.

    PubMed  Article  CAS  Google Scholar 

  • Griffiths-Jones S., Saini H. K., van Dongen S. and Enright A. J. 2008 miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, 154–158.

    Article  Google Scholar 

  • Hertel J., Lindemeyer M., Missal K., Fried C., Tanzer A., Flamm C. et al. 2006 The expansion of the metazoan microRNA repertoire. BMC Genomics 7, 25.

    PubMed  Article  Google Scholar 

  • Itoh T., Tanaka T., Barrero R. A., Yamasaki C., Fujii Y., Hilton P. B. et al. 2007 Curated genome annotation of Oryza sativa ssp. japonica and comparative genome analysis with Arabidopsis thaliana. Genome Res. 17, 175–183.

    PubMed  Article  Google Scholar 

  • Kim V. N. 2005 MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 6, 376–385.

    PubMed  Article  CAS  Google Scholar 

  • Kim Y. K. and Kim V. N. 2007 Processing of intronic microRNAs. EMBO J. 26, 775–783.

    PubMed  Article  CAS  Google Scholar 

  • Kozomara A. and Griffiths-Jones S. 2011 miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, 152–157.

    Article  Google Scholar 

  • Kurihara Y. and Watanabe Y. 2004 Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl. Acad. Sci. USA 101, 12753–12758.

    PubMed  Article  CAS  Google Scholar 

  • Lagos-Quintana M., Rauhut R., Lendeckel W. and Tuschl T. 2001 Identification of novel genes coding for small expressed RNAs. Science 294, 853–858.

    PubMed  Article  CAS  Google Scholar 

  • Lagos-Quintana M., Rauhut R., Meyer J., Borkhardt A. and Tuschl T. 2003 New microRNAs from mouse and human. RNA 9, 175–179.

    PubMed  Article  CAS  Google Scholar 

  • Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J. et al. 2003 The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.

    PubMed  Article  CAS  Google Scholar 

  • Li S. C., Tang P. and Lin W. C. 2007 Intronic microRNA: discovery and biological implications. DNA Cell Biol. 26, 195–207.

    PubMed  Article  Google Scholar 

  • Lund E., Guttinger S., Calado A., Dahlberg J. E. and Kutay U. 2004 Nuclear export of microRNA precursors. Science 303, 95–98.

    PubMed  Article  CAS  Google Scholar 

  • Lynch M. and Conery J. S. 2000 The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155.

    PubMed  Article  CAS  Google Scholar 

  • Maher C., Stein L. and Ware D. 2006 Evolution of Arabidopsis microRNA families through duplication events. Genome Res. 16, 510–519.

    PubMed  Article  CAS  Google Scholar 

  • Meng Y. and Shao C. 2012 Large-scale identification of mirtrons in Arabidopsis and rice. PLoS One 7, e31163.

    Article  Google Scholar 

  • Meyers B. C., Haudenschild C. D. and Vemaraju K. 2007 Use of massively parallel signature sequencing to study genes expressed during the plant defense response. Methods Mol. Biol. 354, 105–119.

    PubMed  CAS  Google Scholar 

  • Najafi-Shoushtari S. H., Kristo F., Li Y., Shioda T., Cohen D. E., Gerszten R. E. et al. 2010 MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328, 1566–1569.

    PubMed  Article  CAS  Google Scholar 

  • Okamura K., Hagen J. W., Duan H., Tyler D. M. and Lai E. C. 2007 The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89–100.

    PubMed  Article  CAS  Google Scholar 

  • Olena A. F. and Patton J. G. 2010 Genomic organization of microRNAs. J. Cell Physiol. 222, 540–545.

    PubMed  CAS  Google Scholar 

  • Ouyang S., Zhu W., Hamilton J., Lin H., Campbell M., Childs K. et al. 2007 The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 35, 883–887.

    Article  Google Scholar 

  • Rajagopalan R., Vaucheret H., Trejo J. and Bartel D. P. 2006 A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407–3425.

    PubMed  Article  CAS  Google Scholar 

  • Rayner K. J., Suarez Y., Davalos A., Parathath S., Fitzgerald M. L., Tamehiro N. et al. 2010 MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328, 1570–1573.

    PubMed  Article  CAS  Google Scholar 

  • Rodriguez A., Griffiths-Jones S., Ashurst J. L. and Bradley A. 2004 Identification of mammalian microRNA host genes and transcription units. Genome Res. 14, 1902–1910.

    PubMed  Article  CAS  Google Scholar 

  • Shan D. P., Huang J. G., Yang Y. T., Guo Y. H., Wu C. A., Yang G. D. et al. 2007 Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytol. 176, 70–81.

    PubMed  Article  CAS  Google Scholar 

  • Shomron N., Golan D. and Hornstein E. 2009 An evolutionary perspective of animal microRNAs and their targets. J. Biomed. Biotechnol. 2009, 594738.

    PubMed  Google Scholar 

  • Thatcher E. J., Bond J., Paydar I. and Patton J. G. 2008 Genomic organization of zebrafish microRNAs. BMC Genomics 9, 253.

    PubMed  Article  Google Scholar 

  • van Rooij E., Sutherland L. B., Qi X., Richardson J. A., Hill J. and Olson E. N. 2007 Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575–579.

    PubMed  Article  Google Scholar 

  • Wang D., Lu M., Miao J., Li T., Wang E. and Cui Q. 2009a Cepred: predicting the co-expression patterns of the human intronic microRNAs with their host genes. PLoS One 4, e4421.

    Article  Google Scholar 

  • Wang J. W., Czech B. and Weigel D. 2009b miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738–749.

    PubMed  Article  CAS  Google Scholar 

  • Weber M. J. 2005 New human and mouse microRNA genes found by homology search. FEBS J. 272, 59–73.

    PubMed  Article  CAS  Google Scholar 

  • Wei L. Q., Yan L. F. and Wang T. 2011 Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol. 12, 53.

    Article  Google Scholar 

  • Xie Z., Kasschau K. D. and Carrington J. C. 2003 Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol. 13, 784–789.

    PubMed  Article  CAS  Google Scholar 

  • Xie Z., Allen E., Fahlgren N., Calamar A., Givan S. A. and Carrington J. C. 2005 Expression of Arabidopsis MIRNA genes. Plant Physiol. 138, 2145–2154.

    PubMed  Article  CAS  Google Scholar 

  • Yu J., Wang J., Lin W., Li S., Li H., Zhou J. et al. 2005 The Genomes of Oryza sativa: a history of duplications. PLoS Biol. 3, e38.

    Article  Google Scholar 

  • Zhang Z., Yu J., Li D., Liu F., Zhou X., Wang T. et al. 2010 PMRD: plant microRNA database. Nucleic Acids Res. 38, 806–813.

    Article  Google Scholar 

  • Zhou X., Ruan J., Wang G. and Zhang W. 2007 Characterization and identification of microRNA core promoters in four model species. PLoS Comput. Biol. 3, e37.

    Article  Google Scholar 

  • Zhu Q. H., Spriggs A., Matthew L., Fan L., Kennedy G., Gubler F. et al. 2008 A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res. 18, 1456–1465.

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation (grant no. 31070240) and the Genetically Modified Organisms Breeding Major Projects (grant no. 2008ZX08009-003-002) in China.

Author information

Affiliations

  1. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an, Shandong, 271018, People’s Republic of China

    G. D. YANG, K. YAN, B. J. WU, Y. H. WANG, Y. X. GAO & C. C. ZHENG

Authors
  1. G. D. YANG
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. YAN
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. J. WU
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Y. H. WANG
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Y. X. GAO
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. C. ZHENG
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. C. ZHENG.

Additional information

[Yang G. D., Yan K., Wu B. J., Wang Y. H., Gao Y. X. and Zheng C. C. 2012 Genomewide analysis of intronic microRNAs in rice and Arabidopsis. J. Genet. 91, xx–xx]

Electronic Supplementary Material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

YANG, G.D., YAN, K., WU, B.J. et al. Genomewide analysis of intronic microRNAs in rice and Arabidopsis . J Genet 91, 313–324 (2012). https://doi.org/10.1007/s12041-012-0199-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-012-0199-6

Keywords

  • rice
  • Arabidopsis
  • intronic miRNA
  • host gene
  • bioinformatics
  • function