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.

  • Letter
  • Published:

Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching

Abstract

Increasing grain yields is a major focus of crop breeders around the world. Here we report that overexpression of the rice microRNA (miRNA) OsmiR397, which is naturally highly expressed in young panicles and grains, enlarges grain size and promotes panicle branching, leading to an increase in overall grain yield of up to 25% in a field trial. To our knowledge, no previous report has shown a positive regulatory role of miRNA in the control of plant seed size and grain yield. We determined that OsmiR397 increases grain yield by downregulating its target, OsLAC, whose product is a laccase-like protein that we found to be involved in the sensitivity of plants to brassinosteroids. As miR397 is highly conserved across different species, our results suggest that manipulating miR397 may be useful for increasing grain yield not only in rice but also in other cereal crops.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Phenotypes of OXmiR397 and OXLAC transgenic rice plants.
Figure 2: Confirmation of OsmiR397-mediated downregulation of OsLAC and the expression patterns of OsmiR397 and OsLAC.
Figure 3: Mechanism analysis of OsmiR397-mediated OsLAC silence in increasing grain yield.

Similar content being viewed by others

Accession codes

Primary accessions

Sequence Read Archive

References

  1. Xing, Y. & Zhang, Q. Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 61, 421–442 (2010).

    Article  CAS  Google Scholar 

  2. Song, X.J., Huang, W., Shi, M., Zhu, M.Z. & Lin, H.X.A. QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623–630 (2007).

    Article  CAS  Google Scholar 

  3. Mao, H. et al. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc. Natl. Acad. Sci. USA 107, 19579–19584 (2010).

    Article  CAS  Google Scholar 

  4. Xue, W. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761–767 (2008).

    Article  CAS  Google Scholar 

  5. Sakamoto, T. et al. Genetic manipulation of gibberellin metabolism in transgenic rice. Nat. Biotechnol. 21, 909–913 (2003).

    Article  CAS  Google Scholar 

  6. Hong, Z. et al. A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15, 2900–2910 (2003).

    Article  CAS  Google Scholar 

  7. Tanabe, S. et al. A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17, 776–790 (2005).

    Article  CAS  Google Scholar 

  8. Sakamoto, T. et al. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol. 24, 105–109 (2006).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545–549 (2010).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Zhu, Q.H. et al. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res. 18, 1456–1465 (2008).

    Article  CAS  Google Scholar 

  13. Xue, L.J., Zhang, J.J. & Xue, H.W. Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res. 37, 916–930 (2009).

    Article  CAS  Google Scholar 

  14. Chen, C.J. et al. Genome-wide discovery and analysis of microRNAs and other small RNAs from rice embryogenic callus. RNA Biol. 8, 538–547 (2011).

    Article  CAS  Google Scholar 

  15. Ikeda-Kawakatsu, K. et al. Expression level of ABERRANT PANICLE ORGANIZATION1 determines rice inflorescence form through control of cell proliferation in the meristem. Plant Physiol. 150, 736–747 (2009).

    Article  CAS  Google Scholar 

  16. Terao, T., Nagata, K., Morino, K. & Hirose, T. A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor. Appl. Genet. 120, 875–893 (2010).

    Article  CAS  Google Scholar 

  17. Jones-Rhoades, M.W., Bartel, D.P. & Bartel, B. MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19–53 (2006).

    Article  CAS  Google Scholar 

  18. Jones-Rhoades, M.W. & Bartel, D.P. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787–799 (2004).

    Article  CAS  Google Scholar 

  19. Jeong, D.H. et al. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23, 4185–4207 (2011).

    Article  CAS  Google Scholar 

  20. Riva, S. Laccases: blue enzymes for green chemistry. Trends Biotechnol. 24, 219–226 (2006).

    Article  CAS  Google Scholar 

  21. Berthet, S. et al. Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23, 1124–1137 (2011).

    Article  CAS  Google Scholar 

  22. Yamamuro, C. et al. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12, 1591–1606 (2000).

    Article  CAS  Google Scholar 

  23. Zhang, L.Y. et al. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21, 3767–3780 (2009).

    Article  CAS  Google Scholar 

  24. Nakamura, A. et al. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 140, 580–590 (2006).

    Article  CAS  Google Scholar 

  25. Hu, X. & Liu, Y. The construction of RNAi vectors and the use for gene silencing in rice. Mol. Plant Breed. 4, 621–626 (2006).

    CAS  Google Scholar 

  26. Toki, S. et al. Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J. 47, 969–976 (2006).

    Article  CAS  Google Scholar 

  27. Wang, J.F., Zhou, H., Chen, Y.Q., Luo, Q.J. & Qu, L.H. Identification of 20 microRNAs from Oryza sativa. Nucleic Acids Res. 32, 1688–1695 (2004).

    Article  CAS  Google Scholar 

  28. Kouchi, H. & Hata, S. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol. Gen. Genet. 238, 106–119 (1993).

    CAS  PubMed  Google Scholar 

  29. Suzaki, T. et al. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131, 5649–5657 (2004).

    Article  CAS  Google Scholar 

  30. Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967 (2009).

    Article  CAS  Google Scholar 

  31. Zhang, G. et al. Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res. 20, 646–654 (2010).

    Article  CAS  Google Scholar 

  32. Xin, P., Yan, J., Fan, J., Chu, J. & Yan, C. An improved simplified high-sensitivity quantification method for determining brassinosteroids in different tissues of rice and Arabidopsis. Plant Physiol. doi: http://dx.doi.org/10.1104/pp.113.221952 (25 June 2013).

Download references

Acknowledgements

We thank Q. Qian for helping with the field trial and C.C. Chu for the comments on brassinosteroid analysis. This research was supported by a key project of the National Natural Science Foundation of China (No. U0631001 and 90917011), funds from Ph.D. Programs Foundation of Ministry of Education of China (20120171130003), and from the Natural Science and Technology Department of Guangdong Province (2009A020102001 and S2011020001232).

Author information

Authors and Affiliations

Authors

Contributions

Y.-C.Z. conceived the experiment, and together with Y.Y., C.-Y.W., Z.-Y.L. and Q.L. carried it out; J.X. and J.-Y.L. carried out the transgenic plant generation and analysis; X.-J.W. and L.-H.Q. analyzed the data; F.C. carried out the field trial; P.X., C.Y. and J.C. performed brassinosteroid detection; Y.-C.Z., H.-Q.L. and Y.-Q.C. conceived the experiment and wrote the paper.

Corresponding authors

Correspondence to Hong-Qing Li or Yue-Qin Chen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5 and Supplementary Tables 1–3 (PDF 741 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, YC., Yu, Y., Wang, CY. et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31, 848–852 (2013). https://doi.org/10.1038/nbt.2646

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt.2646

This article is cited by

Search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research