Skip to main content
SpringerLink
Log in

Expression analysis of argonaute, Dicer-like, and RNA-dependent RNA polymerase genes in cucumber (Cucumis sativus L.) in response to abiotic stress

  • RESEARCH ARTICLE
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Posttranscriptional control of gene expression can be achieved through RNA interference when the activities of Dicer-like (DCL), argonaute (AGO) and RNA-dependent RNA polymerase (RDR) proteins are significant. In this study, we analysed the expression of seven AGO, five DCL and eight RDR genes in cucumber under cold, heat, hormone, salinity and dehydration treatments using quantitative reverse-transcription PCR (qRT-PCR). All CsAGO, CsDCL and CsRDR genes were differentially expressed under abiotic stress treatment. In response to abiotic stress treatment, most genes were expressed at higher levels in flowers or stems than in other organs, whereas some CsAGOs (CsAGO1c, CsAGO6 and CsAGO7) and CsRDRs (CsRDR1d and CsRDR2) were highly expressed in roots during dehydration treatment. The expression patterns indicate that most CsDCLs, CsAGOs and CsRDRs respond to abiotic stress, and stems or flowers are the most sensitive organs, followed by roots. This is the first report of expression analysis of all CsDCL, CsAGO and CsRDR family genes in cucumber under abiotic stress, which provides basic information and insights into the putative roles of these genes in abiotic stress. The results of this study should serve as a basis for further functional characterization of these gene families in cucumber and related Cucurbitaceae species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Bai M., Yang G. S., Chen W. T., Mao Z. C., Kang H. X., Chen G. H. et al. 2012 Genome-wide identification of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analyses in response to viral infection and abiotic stresses in Solanum lycopersicum. Gene 501, 52–62.

    Article  CAS  PubMed  Google Scholar 

  • Bartel D. P. 2004 MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.

    Article  CAS  PubMed  Google Scholar 

  • Bartel D. P. 2009 MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baulcombe D. 2004 RNA silencing in plants. Nature 431, 356–363.

    Article  CAS  PubMed  Google Scholar 

  • Bouche N., Lauressergues D., Gasciolli V. and Vaucheret H. 2006 An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25, 3347–3356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodersen P. and Voinnet O. 2009 Revisiting the principles of microRNA target recognition and mode of action. Nat. Rev. Mol. Cell Biol. 10, 141–148.

    Article  CAS  PubMed  Google Scholar 

  • Carmell M. A., Xuan Z., Zhang M. Q. and Hannon G. J. 2002 The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733–2742.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Curtin S. J., Kantar M. B., Yoon H. W., Whaley A. M., Schlueter J. A. and Stupar R. M. 2012 Co-expression of soybean Dicer-like genes in response to stress and development. Funct. Integr. Genomics 12, 671–682.

    Article  CAS  PubMed  Google Scholar 

  • Dalmay T., Hamilton A., Rudd S., Angell S. and Baulcombe D. C. 2000 An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101, 543–553.

    Article  CAS  PubMed  Google Scholar 

  • Ding S. W. 2010 RNA-based antiviral immunity. Nat. Rev. Immunol. 9, 632–644.

    Article  Google Scholar 

  • Dunoyer P., Himber C. and Voinnet O. 2005 DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37, 1356–1360.

    Article  CAS  PubMed  Google Scholar 

  • Fabian M. R., Sonenberg N. and Filipowicz W. 2010 Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351–379.

    Article  CAS  PubMed  Google Scholar 

  • Fagard M., Boutet S., Morel J. B., Bellini C. and Vaucheret H. 2000 AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl. Acad. Sci. USA 97, 11650–11654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finnegan E. J., Margis R. and Waterhouse P. M. 2003 Posttranscriptional gene silencing is not compromised in the Arabidopsis CARPEL FACTORY (DICER-LIKE1) mutant, a homolog of Dicer-1 from Drosophila. Curr. Biol. 13, 236–240.

    Article  CAS  PubMed  Google Scholar 

  • Gan D. F., Liang D. D., Wu J., Zhan M. D., Yang F., Xu W. J. et al. 2016 Genome-wide identification of the Dicer-Like, Argonaute, and RNA-dependent RNA polymerase gene families in cucumber (Cucumis sativus L.). J. Plant Growth Regul. 35, 135–150.

    Article  CAS  Google Scholar 

  • Gasciolli V., Mallory A. C., Bartel D. P. and Vaucheret H. 2005 Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing transacting siRNAs. Curr. Biol. 15, 1494–1500.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havecker E. R., Wallbridge L. M., Hardcastle T. J., Bush M. S., Kelly K. A., Dunn R. M. et al. 2010 The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22, 321–334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herr A. J., Jensen M. B., Dalmay T. and Baulcombe D. C. 2005 RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118–120.

    Article  CAS  PubMed  Google Scholar 

  • Hu L. F. and Liu S. Q. 2012 Genome-wide analysis of the MADS-box gene family in cucumber. Genome 55, 245–256.

    Article  CAS  PubMed  Google Scholar 

  • Hunter C., Sun H. and Poethig R. S. 2003 The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr. Biol. 13, 1734–1739.

    Article  CAS  PubMed  Google Scholar 

  • Hutvagner G. and Simard M. J. 2008 Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9, 22–32.

    Article  CAS  PubMed  Google Scholar 

  • Kapoor M., Arora R., Lama T., Nijhawan A., Khurana J. P., Tyagi A. K. and Kapoor S. 2008 Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA Polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics 9, 451.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khraiwesh B., Zhu J. K. and Zhu J. 2012 Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta 1819, 137–148.

    Article  CAS  PubMed  Google Scholar 

  • Liu X., Lu T., Dou Y. C., Yu B. and Zhang C. 2014 Identification of RNA silencing components in soybean and sorghum. BMC Bioinform. 15, 4.

    Article  CAS  Google Scholar 

  • Margis R., Fusaro A. F., Smith N. A., Curtin S. J., Watson J. M., Finnegan E. J. and Waterhouse P. M. 2006 The evolution and diversification of Dicers in plants. FEBS Lett. 580, 2442–2450.

    Article  CAS  PubMed  Google Scholar 

  • Martínez de Alba A. E., Parent J. S. and Vaucheret H. 2013 Small RNA-mediated control of development in plants. In Epigenetic memory and control in plants, signaling and communication in plants (ed. G. Grafi and N. Ohand), pp. 177–199. Springer Berlin Heidelberg, Germany.

  • McFarlane L., Svingen T., Braasch I., Koopman P., Schartl M. and Wilhelm D. 2011 Expansion of the Ago gene family in the teleost clade. Dev. Genes Evol. 221, 95–104.

    Article  CAS  PubMed  Google Scholar 

  • Migocka M. and Papierniak A. 2011 Identification of suitable reference genes for studying gene expression in cucumber plants subjected to abiotic stress and growth regulators. Mol. Breed. 28, 343–357.

    Article  Google Scholar 

  • Mlotshwa S., Schauer S. E., Smith T. H., Mallory A. C., Herr J. M., Roth B. et al. 2005 Ectopic DICER-LIKE1 expression in P1/HC-Pro Arabidopsis rescues phenotypic anomalies but not defects in microRNA and silencing pathways. Plant Cell 17, 2873–2885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mourrain P., Beclin C., Elmayan T., Feuerbach F., Godon C., Morel J. B. et al. 2000 Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533–542.

    Article  CAS  PubMed  Google Scholar 

  • Qian Y. X., Cheng Y., Cheng X., Jiang H. Y., Zhu S. W. and Cheng B. J. 2011 Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep. 30, 1347–1363.

    Article  CAS  PubMed  Google Scholar 

  • Sahu P. P., Rai N. K., Chakraborty S., Singh M., Chandrappa P. H., Ramesh B. et al. 2010 Tomato cultivar tolerant to tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defence-associated host gene expression. Mol. Plant Pathol. 11, 531–544.

    Article  CAS  PubMed  Google Scholar 

  • Sahu P. P., Pandey G., Sharma N., Puranik S., Muthamilarasan M. and Prasad M. 2013 Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep. 32, 1151–1159.

    Article  CAS  PubMed  Google Scholar 

  • Seo J. K., Wu J., Lii Y., Li Y. and Jin H. 2013 Contribution of small RNA pathway components in plant immunity. Mol. Plant Microbe Interact. 26, 617–625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao F. and Lu S. F. 2014 Identification, molecular cloning and expression analysis of five RNA-dependent RNA polymerase genes in Salvia miltiorrhiza. PLoS One 9, e95117.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tolia N. H. and Joshua-Tor L. 2007 Slicer and the argonautes. Nat. Chem. Biol. 3, 36–43.

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H. 2008 Plant ARGONAUTES. Trends Plant Sci. 13, 350–358.

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O. 2009 Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669–687.

    Article  CAS  PubMed  Google Scholar 

  • Wheeler B. S. 2013 Small RNAs, big impact: small RNA pathways in transposon control and their effect on the host stress response. Chromosom Res. 21, 587–600.

    Article  CAS  Google Scholar 

  • Xie Z., Johansen L. K., Gustafson A. M., Kasschau K. D., Lellis A. D., Zilberman D., Jacobsen S. E. and Carrington J. C. 2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, e104.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie Z., Allen E., Wilken A. and Carrington J. C. 2005 DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102, 12984–12989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav C. B., Muthamilarasan M., Pandey G. and Prasad M. 2015 Identification, characterization and expression profiling of Dicer-Like, Argonaute and RNA-dependent RNA polymerase gene families in foxtail millet. Plant Mol. Biol. Rep. 33, 43–55.

    Article  CAS  Google Scholar 

  • Yang Y., Zhong J., Ouyang Y. D. and Yao J. 2013 The integrative expression and co-expression analysis of the AGO gene family in rice. Gene 528, 221–235.

    Article  CAS  PubMed  Google Scholar 

  • Yu B. and Wang H. 2010 Translational inhibition by microRNAs in plants. Prog. Mol. Subcell. Biol. 50, 41–57.

    Article  CAS  PubMed  Google Scholar 

  • Yu D. Q., Fan B. F., MacFarlane S. A. and Chen Z. X. 2003 Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol. Plant Microbe. Interact. 16, 206–216.

    Article  CAS  PubMed  Google Scholar 

  • Zhao H. L., Zhao K., Wang J., Chen X., Chen Z., Cai R. H. and Xiang Y. 2015 Comprehensive analysis of Dicer-like, Argonaute, and RNA-dependent RNA polymerase gene families in grapevine (Vitis vinifera). J. Plant Growth Regul. 34, 108–121.

    Article  Google Scholar 

  • Zilberman D., Cao X. and Jacobsen S. E. 2003 ARGONAUTE 4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716–719.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research is supported by grants from the Natural Science Research Project of Anhui Province (KJ2015A025), the Higher Education Revitalization Project of Anhui Province (2013zdjy057), Academic Backbone Cultivation Project of Anhui Agricultural University (2014XKPY-12), and the Innovation Fund of Master Degree Candidate (2015-07). We thank members of the Key Laboratory of Crop Biology of Anhui Province for their assistance in this study.

Author information

Author notes

  1. Defang Gan and Mengdan Zhan contributed equally to this work.

Authors and Affiliations

  1. School of Horticulture, Anhui Agricultural University, Hefei, 230036, People’s Republic of China

    DEFANG GAN, MENGDAN ZHAN, FENG YANG, QIQI ZHANG, KELING HU, WENJUAN XU, LING ZHANG & DANDI LIANG

  2. Modern Agricultural Science and Technology Cooperative Extension Service Center of Mingguang City, Mingguang, 239400, People’s Republic of China

    QINGHUI LU

Authors
  1. DEFANG GAN
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. MENGDAN ZHAN
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. FENG YANG
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. QIQI ZHANG
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. KELING HU
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. WENJUAN XU
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. QINGHUI LU
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. LING ZHANG
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. DANDI LIANG
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to DEFANG GAN.

Additional information

Corresponding editor: Rajiva Raman

[Gan D., Zhan M., Yang F., Zhang Q., Hu K., Xu W., Lu Q., Zhang L. and Liang D. 2017 Expression analysis of argonaute, Dicer-like, and RNA-dependent RNA polymerase genes in cucumber (Cucumis sativus L.) in response to abiotic stress. J. Genet. 96, xx–xx]

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 281 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

GAN, D., ZHAN, M., YANG, F. et al. Expression analysis of argonaute, Dicer-like, and RNA-dependent RNA polymerase genes in cucumber (Cucumis sativus L.) in response to abiotic stress. J Genet 96, 235–249 (2017). https://doi.org/10.1007/s12041-017-0758-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-017-0758-y

Keywords

Search

Navigation