Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Suppression of rice miR168 improves yield, flowering time and immunity

Abstract

MicroRNA168 (miR168) is a key miRNA that targets Argonaute1 (AGO1), a major component of the RNA-induced silencing complex1,2. Previously, we reported that miR168 expression was responsive to infection by Magnaporthe oryzae, the causal agent of rice blast disease3. However, how miR168 regulates immunity to rice blast and whether it affects rice development remains unclear. Here, we report our discovery that the suppression of miR168 by a target mimic (MIM168) not only improves grain yield and shortens flowering time in rice but also enhances immunity to M. oryzae. These results were validated through repeated tests in rice fields in the absence and presence of rice blast pressure. We found that the miR168–AGO1 module regulates miR535 to improve yield by increasing panicle number, miR164 to reduce flowering time, and miR1320 and miR164 to enhance immunity. Our discovery demonstrates that changes in a single miRNA enhance the expression of multiple agronomically important traits.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: miR168 regulates rice yield and flowering time.
Fig. 2: miR168 regulates rice immunity against M. oryzae.
Fig. 3: miR1320 contributes to miR168-regulated immunity.
Fig. 4: miR535 and miR164 contribute to miR168-regulated development.

Data availability

All data generated or analysed during this study are included in this Article and in its Supplementary Information files. The data are available upon request. Source data are provided with this paper.

References

  1. 1.

    Li, Y. F. et al. Transcriptome-wide identification of microRNA targets in rice. Plant J. 62, 742–759 (2010).

    CAS  Article  Google Scholar 

  2. 2.

    Peters, L. & Meister, G. Argonaute proteins: mediators of RNA silencing. Mol. Cell 26, 611–623 (2007).

    CAS  Article  Google Scholar 

  3. 3.

    Li, Y. et al. Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiol. 164, 1077–1092 (2014).

    CAS  Article  Google Scholar 

  4. 4.

    Nelson, R., Wiesner-Hanks, T., Wisser, R. & Balint-Kurti, P. Navigating complexity to breed disease-resistant crops. Nat. Rev. Genet. 19, 21–33 (2018).

    CAS  Article  Google Scholar 

  5. 5.

    Bergelson, J. & Purrington, C. B. Surveying patterns in the cost of resistance in plants. Am. Nat. 148, 536–558 (1996).

    Article  Google Scholar 

  6. 6.

    Evans, J. R. Improving photosynthesis. Plant Physiol. 162, 1780–1793 (2013).

    CAS  Article  Google Scholar 

  7. 7.

    Rossi, M., Bermudez, L. & Carrari, F. Crop yield: challenges from a metabolic perspective. Curr. Opin. Plant Biol. 25, 79–89 (2015).

    CAS  Article  Google Scholar 

  8. 8.

    Xu, G. et al. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545, 491–494 (2017).

    CAS  Article  Google Scholar 

  9. 9.

    Wang, J. et al. A single transcription factor promotes both yield and immunity in rice. Science 361, 1026–1028 (2018).

    CAS  Article  Google Scholar 

  10. 10.

    Fang, J. et al. Ef-cd locus shortens rice maturity duration without yield penalty. Proc. Natl Acad. Sci. USA 116, 18717–18722 (2019).

    CAS  Article  Google Scholar 

  11. 11.

    Tang, J. & Chu, C. MicroRNAs in crop improvement: fine-tuners for complex traits. Nat. Plants 3, 17077 (2017).

    Article  Google Scholar 

  12. 12.

    Chandran, V. et al. miR396-OsGRFs module balances growth and rice blast disease-resistance. Front. Plant Sci. 9, 1999 (2019).

    Article  Google Scholar 

  13. 13.

    Mallory, A. C., Elmayan, T. & Vaucheret, H. MicroRNA maturation and action—the expanding roles of ARGONAUTEs. Curr. Opin. Plant Biol. 11, 560–566 (2008).

    CAS  Article  Google Scholar 

  14. 14.

    Li, Y. et al. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol. 152, 2222–2231 (2010).

    CAS  Article  Google Scholar 

  15. 15.

    Sun, M. Z. et al. The multiple roles of OsmiR535 in modulating plant height, panicle branching and grain shape. Plant Sci. 283, 60–69 (2019).

    CAS  Article  Google Scholar 

  16. 16.

    Zhao, Y. F. et al. miR1432-OsACOT (acyl-CoA thioesterase) module determines grain yield via enhancing grain filling rate in rice. Plant Biotechnol. J. 17, 712–723 (2019).

    CAS  Article  Google Scholar 

  17. 17.

    Yang, R. et al. Fine-tuning of MiR528 accumulation modulates flowering time in rice. Mol Plant. 12, 1103–1113 (2019).

    CAS  Article  Google Scholar 

  18. 18.

    Salvador-Guirao, R., Hsing, Y. I. & San Segundo, B. The polycistronic miR166k-166h positively regulates rice immunity via post-transcriptional control of EIN2. Front. Plant Sci. 9, 337 (2018).

    Article  Google Scholar 

  19. 19.

    Zhao, Z. X. et al. Osa-miR167d facilitates infection of Magnaporthe oryzae in rice. J. Integr. Plant Biol. 62, 702–715 (2019).

    Article  Google Scholar 

  20. 20.

    Li, Y. et al. Osa-miR169 negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Front. Plant Sci. 8, 2 (2017).

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Zhang, X. et al. Magnaporthe oryzae induces the expression of a microRNA to suppress the immune response in rice. Plant Physiol. 177, 352–368 (2018).

    CAS  Article  Google Scholar 

  22. 22.

    Li, Y. et al. Osa-miR398b boosts H2O2 production and rice blast disease-resistance via multiple superoxide dismutases. N. Phytol. 222, 1507–1522 (2019).

    CAS  Article  Google Scholar 

  23. 23.

    Xiao, Z. Y. et al. MiR444b.2 regulates resistance to Magnaporthe oryzae and tillering in rice. Acta Phytopathol. Sinica 47, 511–522 (2017).

    Google Scholar 

  24. 24.

    Wang, Z. Y. et al. Osa-miR164a targets OsNAC60 and negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Plant J. 95, 584–597 (2018).

    CAS  Article  Google Scholar 

  25. 25.

    Jiao, Y. et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541–544 (2010).

    CAS  Article  Google Scholar 

  26. 26.

    Wang, L. et al. Coordinated regulation of vegetative and reproductive branching in rice. Proc. Natl Acad. Sci. USA 112, 15504–15509 (2015).

    CAS  Article  Google Scholar 

  27. 27.

    Mannai, Y. E., Akabane, K., Hiratsu, K., Satoh-Nagasawa, N. & Wabiko, W. The NAC transcription factor gene OsY37 (ONAC011) promotes leaf senescence and accelerates heading time in rice. Int. J. Mol. Sci. 18, 2165–2185 (2017).

    Article  Google Scholar 

  28. 28.

    Lin, Z. Z., Jiang, W. W., Wang, J. L. & Lei, C. L. Research and utilization of universally susceptible property of japonica rice variety Lijiangxintuanheigu. Sci. Agricultura Sinica 34, 116–117 (2001).

    Google Scholar 

  29. 29.

    Tsumematsu, H. et al. Development of monogenic lines of rice for blast resistance. Breed. Sci. 50, 229–234 (2000).

    Article  Google Scholar 

  30. 30.

    Kanzaki, H. et al. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J. 72, 894–907 (2012).

    CAS  Article  Google Scholar 

  31. 31.

    Franco-Zorrilla, J. M. et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39, 1033–1037 (2007).

    CAS  Article  Google Scholar 

  32. 32.

    Kankanala, P., Czymmek, K. & Valent, B. Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19, 706–724 (2007).

    CAS  Article  Google Scholar 

  33. 33.

    Kong, L. A. et al. Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 8, e1002526 (2012).

    CAS  Article  Google Scholar 

  34. 34.

    Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).

    Article  Google Scholar 

  35. 35.

    Friedlander, M. R., Mackowiak, S. D., Li, N., Chen, W. & Rajewsky, N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 40, 37–52 (2012).

    Article  Google Scholar 

Download references

Acknowledgements

We thank C.-L. Lei (Institute of Crop Science, Chinese Academy of Agricultural Sciences) for providing IRBLkm-Ts and J.-M. Zhou (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for suggestions on writing the manuscript. This work was supported by grants from the Sichuan Applied Fundamental Research Foundation (no. 2020YJ0332) and National Natural Science Foundation of China (nos. U19A2033, 31672090 and 31430072) to W.-M.W. and by grants from the National Institutes of Health (no. GM59962), USDA NIFA (no. 2017-67013-26590) and the Joint BioEnergy Institute funded by the US DOE (no. DE-AC02-05CH11231) to P.C.R. and M.C.

Author information

Affiliations

Authors

Contributions

Yan Li and W.-M.W. conceived the project. H.W., Y.Z., L.-L.Z., J.-H.L., W.-Q.D., Z.-R.Y., S.-Z.Y. and Z.-X.Z. carried out the experiments. X.-P.L. and X.-C.M. performed the transgenic plant generation and analysis. J.-W.Z. and M.P. conducted the field trials. M.C., J.F. and X.-J.W. analysed the data. Yan Li, M.C., P.C.R. and W.-M.W. wrote the paper. X.-W.C., W.-T.L., J.W., M.H., Y.-Y.H., S.-G.L., P.L. and Yi Li discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Wen-Ming Wang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Yong-Hwan Lee, Shaoqing Li and Guo-Liang Wang for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary figures and methods.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–5.

Supplementary Data 1

Statistical source data.

Supplementary Data 2

Statistical source data.

Supplementary Data 3

Statistical source data.

Supplementary Data 4

Statistical source data.

Supplementary Data 5

Statistical source data.

Supplementary Data 6

Statistical source data.

Supplementary Data 7

Statistical source data.

Supplementary Data 8

Statistical source data.

Supplementary Data 9

Unprocessed western blots.

Supplementary Data 10

Unprocessed western blots.

Supplementary Data 11

Unprocessed northern blots.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Statistical source data.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, H., Li, Y., Chern, M. et al. Suppression of rice miR168 improves yield, flowering time and immunity. Nat. Plants 7, 129–136 (2021). https://doi.org/10.1038/s41477-021-00852-x

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing