Skip to main content
Log in

The lifestyle transition of Arthrobotrys oligospora is mediated by microRNA-like RNAs

  • Research Paper
  • Special Topic: Noncoding RNA: from dark matter to bright star
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

The lifestyle transition of fungi, defined as switching from taking organic material as nutrients to pathogens, is a fundamental phenomenon in nature. However, the mechanisms of such transition remain largely unknown. Here we show microRNA-like RNAs (milRNAs) play a key role in fungal lifestyle transition for the first time. We identified milRNAs by small RNA sequencing in Arthrobotrys oligospora, a known nematode-trapping fungus. Among them, 7 highly expressed milRNAs were confirmed by northern-blot analysis. Knocking out two milRNAs significantly decreased A. oligospora’s ability to switch lifestyles. We further identified that two of these milRNAs were associated with argonaute protein QDE-2 by RNA-immunoprecipitation (RIP) analysis. Three of the predicted target genes of milRNAs were found in immunoprecipitation (IP) products of QDE-2. Disruption of argonaute gene qde-2 also led to serious defects in lifestyle transition. Interestingly, knocking out individual milRNAs or qde-2 lead to diverse responses under different conditions, and qde-2 itself may be targeted by the milRNAs. Collectively, it indicates the lifestyle transition of fungi is mediated by milRNAs through RNA interference (RNAi) machinery, revealing the wide existence of miRNAs in fungi kingdom and providing new insights into understanding the adaptation of fungi from scavengers to predators and the mechanisms underlying fungal infections.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen, E., Xie, Z., Gustafson, A.M., and Carrington, J.C. (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221.

    CAS  PubMed  Google Scholar 

  • Ambros, V. (2004). The functions of animal microRNAs. Nature 431, 350–355.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Betel, D., Koppal, A., Agius, P., Sander, C., and Leslie, C. (2010). Comprehensive modeling of microRNA targets predicts functional nonconserved and non-canonical sites. Genome Biol 11, R90.

    Google Scholar 

  • Boyce, K.J., and Andrianopoulos, A. (2015). Fungal dimorphism: the switch from hyphae to yeast is a specialized morphogenetic adaptation allowing colonization of a host. FEMS Microbiol Rev 39, 797–811.

    Article  CAS  Google Scholar 

  • Colot, H.V., Park, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., Weiss, R.L., Borkovich, K.A., and Dunlap, J.C. (2006). A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103, 10352–10357.

    Article  CAS  Google Scholar 

  • Dang, Y., Yang, Q., Xue, Z., and Liu, Y. (2011). RNA interference in fungi: pathways, functions, and applications. Eukaryotic Cell 10, 1148–1155.

    Article  CAS  Google Scholar 

  • Denman, R.B. (1993). Using RNAFOLD to predict the activity of small catalytic RNAs. Biotechniques 15, 1090–1095.

    CAS  PubMed  Google Scholar 

  • Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L., and Gurr, S.J. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194.

    Article  CAS  Google Scholar 

  • Friedländer, M.R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S., and Rajewsky, N. (2008). Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26, 407–415.

    Article  Google Scholar 

  • Friedman, R.C., Farh, K.K.H., Burge, C.B., and Bartel, D.P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19, 92–105.

    Article  CAS  Google Scholar 

  • Gauthier, G.M. (2015). Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog 11, e1004608.

    Article  Google Scholar 

  • Gursinsky, T., Pirovano, W., Gambino, G., Friedrich, S., Behrens, S.E., and Pantaleo, V. (2015). Homeologs of the Nicotiana benthamiana antiviral ARGONAUTE1 show different susceptibilities to microRNA168-mediated control. Plant Physiol 168, 938–952.

    Article  CAS  Google Scholar 

  • Hendrix, D., Levine, M., and Shi, W. (2010). miRTRAP, a computational method for the systematic identification of miRNAs from high throughput sequencing data. Genome Biol 11, R39.

    Book  Google Scholar 

  • Holbrook, E.D., and Rappleye, C.A. (2008). Histoplasma capsulatum pathogenesis: making a lifestyle switch. Curr Opin Microbiol 11, 318–324.

    Article  CAS  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  Google Scholar 

  • Ji, L., Liu, X., Yan, J., Wang, W., Yumul, R.E., Kim, Y.J., Dinh, T.T., Liu, J., Cui, X., Zheng, B., et al. (2011). ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 7, e1001358.

    Article  CAS  Google Scholar 

  • Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U., and Segal, E. (2007). The role of site accessibility in microRNA target recognition. Nat Genet 39, 1278–1284.

    Article  CAS  Google Scholar 

  • Krüger, J., and Rehmsmeier, M. (2006). RNAhybrid: microRNA target prediction easy, fast and flexible. Nucl Acids Res 34, W451–W454.

    Google Scholar 

  • Lee, H.C., Li, L., Gu, W., Xue, Z., Crosthwaite, S.K., Pertsemlidis, A., Lewis, Z.A., Freitag, M., Selker, E.U., Mello, C.C., et al. (2010). Diverse pathways generate microRNA-like RNAs and Dicerindependent small interfering RNAs in fungi. Mol Cell 38, 803–814.

    Article  CAS  Google Scholar 

  • Li, Y., Zhang, Z., Liu, F., Vongsangnak, W., Jing, Q., and Shen, B. (2012). Performance comparison and evaluation of software tools for microRNA deep-sequencing data analysis. Nucl Acids Res 40, 4298–4305.

    Article  CAS  Google Scholar 

  • Loher, P., and Rigoutsos, I. (2012). Interactive exploration of RNA22 microRNA target predictions. Bioinformatics 28, 3322–3323.

    Article  CAS  Google Scholar 

  • Mallory, A., and Vaucheret, H. (2010). Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22, 3879–3889.

    Article  CAS  Google Scholar 

  • Margolin, B.S., Freitag, M., and Selker, E.U. (1997). Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation. Fungal Genets Rep 44, 34–36.

    Article  Google Scholar 

  • Meerupati, T., Andersson, K.M., Friman, E., Kumar, D., Tunlid, A., and Ahrén, D. (2013). Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genet 9, e1003909.

    Article  Google Scholar 

  • O’Connell, R.J., Thon, M.R., Hacquard, S., Amyotte, S.G., Kleemann, J., Torres, M.F., Damm, U., Buiate, E.A., Epstein, L., Alkan, N., et al. (2012). Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44, 1060–1065.

    Article  Google Scholar 

  • Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. (2002). Prediction of plant microRNA targets. Cell 110, 513–520.

    Article  CAS  Google Scholar 

  • Seitz, H., Tushir, J.S., and Zamore, P.D. (2011). A 5′-uridine amplifies miRNA/miRNA* asymmetry in Drosophila by promoting RNAinduced silencing complex formation. Silence 2, 4.

    Article  CAS  Google Scholar 

  • Várallyay, E., Válóczi, A., Agyi, A., Burgyán, J., and Havelda, Z. (2010). Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J 29, 3507–3519.

    Article  Google Scholar 

  • Wang, X., Li, G., Zou, C., Ji, X., Liu, T., Zhao, P., Liang, L., Xu, J., An, Z., Zheng, X., et al. (2014). Bacteria can mobilize nematode-trapping fungi to kill nematodes. Nat Commun 5, 5776.

    Article  CAS  Google Scholar 

  • Xian, Z., Huang, W., Yang, Y., Tang, N., Zhang, C., Ren, M., and Li, Z. (2014). miR168 influences phase transition, leaf epinasty, and fruit development via SlAGO1s in tomato. J Exp Bot 65, 6655–6666.

    CAS  PubMed  Google Scholar 

  • Yang, J., Wang, L., Ji, X., Feng, Y., Li, X., Zou, C., Xu, J., Ren, Y., Mi, Q., Wu, J., et al. (2011). Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog 7, e1002179.

    Article  CAS  Google Scholar 

  • Zhang, K.Q., and Hyde, K.D. (2014). Nematode-Trapping Fungi (Heidelberg: Springer).

    Book  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Basic Research Program of China (2013CB127500), the National Natural Science Foundation of China (31160021, 31270131 and U1502262) and sponsored by the Nanjing University of Posts and Telecommunications Scientific Foundation (NUPTSF) (NY218140) and a grant (2018KF003) from YNCUB. We thank BGI-Shenzhen who contributed to the small RNA sequencing projects. We thank H. Yin for comments and discussion.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ke-Qin Zhang.

Additional information

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ji, X., Li, H., Zhang, W. et al. The lifestyle transition of Arthrobotrys oligospora is mediated by microRNA-like RNAs. Sci. China Life Sci. 63, 543–551 (2020). https://doi.org/10.1007/s11427-018-9437-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-018-9437-7

Keywords

Navigation