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Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice

A Corrigendum to this article was published on 05 January 2016

Abstract

An increase in grain yield is crucial for modern agriculture1. Grain size is one of the key components of grain yield in rice and is regulated by quantitative trait loci (QTLs)2,3. Exploring new QTLs for grain size will help breeders develop elite rice varieties with higher yields3,4. Here, we report a new semi-dominant QTL for grain size and weight (GS2) in rice, which encodes the transcription factor OsGRF4 (GROWTH-REGULATING FACTOR 4) and is regulated by OsmiR396. We demonstrate that a 2 bp substitution mutation in GS2 perturbs OsmiR396-directed regulation of GS2, resulting in large and heavy grains and increased grain yield. Further results reveal that GS2 interacts with the transcription coactivitors OsGIF1/2/3, and overexpression of OsGIF1 increases grain size and weight. Thus, our findings define the regulatory mechanism of GS2, OsGIFs and OsmiR396 in grain size and weight control, suggesting this pathway could be used to increase yields in crops.

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Figure 1: Map-based cloning of the GS2 QTL.
Figure 2: GS2 interacts with OsGIF1/2/3, and overexpression of OsGIF1 increases grain size and weight.
Figure 3: The GS2AA allele affects OsmiR396-directed regulation on GS2.
Figure 4: Yield traits of NIL-GS2 and NIL-GS2AA plants.

References

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

    CAS  Article  Google Scholar 

  2. Fan, C. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164–1171 (2006).

    CAS  Article  Google Scholar 

  3. 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. Nature Genet. 39, 623–630 (2007).

    CAS  Article  Google Scholar 

  4. Zuo, J. & Li, J. Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu. Rev. Genet. 48, 99–118 (2014).

    CAS  Article  Google Scholar 

  5. Zhang, X. et al. Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proc. Natl Acad. Sci. USA 109, 21534–21539 (2012).

    CAS  Article  Google Scholar 

  6. Duan, P. et al. SMALL GRAIN 1, which encodes a mitogen-activated protein kinase 4, influences grain size in rice. Plant J. 77, 547–557 (2014).

    CAS  Article  Google Scholar 

  7. Weng, J. et al. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res. 18, 1199–1209 (2008).

    CAS  Article  Google Scholar 

  8. 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).

    CAS  Article  Google Scholar 

  9. Li, Y. et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nature Genet. 43, 1266–1269 (2011).

    CAS  Article  Google Scholar 

  10. Qi, P. et al. The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res. 22, 1666–1680 (2012).

    CAS  Article  Google Scholar 

  11. Wang, S. et al. Control of grain size, shape and quality by OsSPL16 in rice. Nature Genet. 44, 950–954 (2012).

    CAS  Article  Google Scholar 

  12. Ishimaru, K. et al. Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nature Genet. 45, 707–711 (2013).

    CAS  Article  Google Scholar 

  13. Song, X. J. et al. Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc. Natl Acad. Sci. USA 112, 76–81 (2015).

    CAS  Article  Google Scholar 

  14. Hong, Z. et al. The rice brassinosteroid-deficient dwarf2 mutant, defective in the rice homolog of Arabidopsis DIMINUTO/DWARF1, is rescued by the endogenously accumulated alternative bioactive brassinosteroid, dolichosterone. Plant Cell 17, 2243–2254 (2005).

    CAS  Article  Google Scholar 

  15. Heang, D. & Sassa, H. An atypical bHLH protein encoded by POSITIVE REGULATOR OF GRAIN LENGTH 2 is involved in controlling grain length and weight of rice through interaction with a typical bHLH protein APG. Breed. Sci. 62, 133–141 (2012).

    CAS  Article  Google Scholar 

  16. Xu, F. et al. Variations in CYP78A13 coding region influence grain size and yield in rice. Plant Cell Environ. 38, 800–811 (2015).

    CAS  Article  Google Scholar 

  17. van der Knaap, E., Kim, J. H. & Kende, H. A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol. 122, 695–704 (2000).

    CAS  Article  Google Scholar 

  18. Kuijt, S. J. et al. Interaction between the GROWTH-REGULATING FACTOR and KNOTTED1-LIKE HOMEOBOX families of transcription factors. Plant Physiol. 164, 1952–1966 (2014).

    CAS  Article  Google Scholar 

  19. Liu, H. et al. OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol. 165, 160–174 (2014).

    CAS  Article  Google Scholar 

  20. Kim, J. H., Choi, D. & Kende, H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J. 36, 94–104 (2003).

    CAS  Article  Google Scholar 

  21. Horiguchi, G., Kim, G. T. & Tsukaya, H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J. 43, 68–78 (2005).

    CAS  Article  Google Scholar 

  22. Hoe Kim, J. & Tsukaya, H. Regulation of plant growth and development by the GROWTH-REGULATING FACTOR and GRF-INTERACTING FACTOR duo. J Exp. Bot. 66, 6093–6107 (2015).

    Article  Google Scholar 

  23. Kanei, M., Horiguchi, G. & Tsukaya, H. Stable establishment of cotyledon identity during embryogenesis in Arabidopsis by ANGUSTIFOLIA3 and HANABA TARANU. Development 139, 2436–2446 (2012).

    CAS  Article  Google Scholar 

  24. Rodriguez, R. E. et al. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137, 103–112 (2009).

    Article  Google Scholar 

  25. Debernardi, J. M. et al. Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J. 79, 413–426 (2014).

    CAS  Article  Google Scholar 

  26. Vercruyssen, L. et al. GROWTH REGULATING FACTOR5 stimulates Arabidopsis chloroplast division, photosynthesis, and leaf longevity. Plant Physiol. 167, 817–832 (2015).

    CAS  Article  Google Scholar 

  27. Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271–282 (1994).

    CAS  Article  Google Scholar 

  28. Llave, C., Xie, Z., Kasschau, K. D. & Carrington, J. C. Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053–2056 (2002).

    CAS  Article  Google Scholar 

  29. Chen, C. et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179 (2005).

    Article  Google Scholar 

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Acknowledgements

We would like to thank Q. Qian, D. Zeng and G. Dong for their helps in field experiments. This work was supported by the grants from the National Basic Research Program of China (2013CBA01401), the National Natural Science Foundation of China (grants 91535203, 31425004 and 91417304), the Ministry of Agriculture of China (2014ZX08009-003) and Chinese Academy of Sciences (XDA08020108).

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P.D., X.Z. and Y.L designed the research. Y.L. and X.Z supervised the project. P.D., S.N., J.W. and B.Z. performed most of experiments. P.D. did molecular and biochemical experiments. S.N. and Y.W. performed yield analysis. B.Z. conducted rice transformation. R. X., J.W. and H.C. performed QTL mapping. P.D., X.Z. and Y.L. analysed data. Y.L. and P.D. wrote the paper.

Corresponding authors

Correspondence to Xudong Zhu or Yunhai Li.

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The authors declare no competing financial interests.

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Duan, P., Ni, S., Wang, J. et al. Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nature Plants 2, 15203 (2016). https://doi.org/10.1038/nplants.2015.203

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