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The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality

Nature Genetics volume 47, pages 949954 (2015) | Download Citation

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Abstract

The deployment of heterosis in the form of hybrid rice varieties has boosted grain yield, but grain quality improvement still remains a challenge. Here we show that a quantitative trait locus for rice grain quality, qGW7, reflects allelic variation of GW7, a gene encoding a TONNEAU1-recruiting motif protein with similarity to C-terminal motifs of the human centrosomal protein CAP350. Upregulation of GW7 expression was correlated with the production of more slender grains, as a result of increased cell division in the longitudinal direction and decreased cell division in the transverse direction. OsSPL16 (GW8), an SBP-domain transcription factor that regulates grain width, bound directly to the GW7 promoter and repressed its expression. The presence of a semidominant GW7TFA allele from tropical japonica rice was associated with higher grain quality without the yield penalty imposed by the Basmati gw8 allele. Manipulation of the OsSPL16-GW7 module thus represents a new strategy to simultaneously improve rice yield and grain quality.

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References

  1. 1.

    et al. A mutant gibberellin-synthesis gene in rice. Nature 416, 701–702 (2002).

  2. 2.

    , & Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc. Natl. Acad. Sci. USA 99, 9043–9048 (2002).

  3. 3.

    Hybrid rice breeding for super high yield. Hybrid Rice 12, 1–6 (1997).

  4. 4.

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

  5. 5.

    et al. Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proc. Natl. Acad. Sci. USA 106, 21760–21765 (2009).

  6. 6.

    , , & RFLP analysis of genomic regions associated with cooked-kernel elongation in rice. Theor. Appl. Genet. 87, 27–32 (1993).

  7. 7.

    et al. QTL mapping of grain quality traits from the interspecific cross Oryza sativa × O. glaberrima. Theor. Appl. Genet. 109, 630–639 (2004).

  8. 8.

    et al. Genetic basis of 17 traits and viscosity parameters characterizing the eating and cooking quality of rice grain. Theor. Appl. Genet. 115, 463–476 (2007).

  9. 9.

    et al. Fine mapping of the grain chalkiness QTL qPGWC-7 in rice (Oryza sativa L.). Theor. Appl. Genet. 118, 581–590 (2009).

  10. 10.

    et al. Mapping QTL main and interaction influences on milling quality in elite US rice germplasm. Theor. Appl. Genet. 122, 291–309 (2011).

  11. 11.

    , , , & Aberrant splicing of intron 1 leads to the heterogeneous 5′ UTR and decreased expression of waxy gene in rice cultivars of intermediate amylose content. Plant J. 14, 459–465 (1998).

  12. 12.

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

  13. 13.

    et al. Chalk5 encodes a vacuolar H+-translocating pyrophosphatase influencing grain chalkiness in rice. Nat. Genet. 46, 398–404 (2014).

  14. 14.

    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).

  15. 15.

    et al. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20, 2146–2159 (2008).

  16. 16.

    et al. The Arabidopsis TRM1-TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell 24, 178–191 (2012).

  17. 17.

    , , & Activity and subcellular compartmentalization of peroxisome proliferator-activated receptor α are altered by the centrosome-associated protein CAP350. J. Cell Sci. 118, 175–186 (2005).

  18. 18.

    et al. Allelic variation for a candidate gene for GS7, responsible for grain shape in rice. Theor. Appl. Genet. 125, 1303–1312 (2012).

  19. 19.

    , , & Mapping and characterization of the major quantitative trait locus qSS7 associated with increased length and decreased width of rice seeds. Theor. Appl. Genet. 125, 1717–1726 (2012).

  20. 20.

    , & TONNEAU2/FASS regulates the geometry of microtubule nucleation and cortical array organization in interphase Arabidopsis cells. Plant Cell 24, 1158–1170 (2012).

  21. 21.

    et al. LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development 133, 4305–4314 (2006).

  22. 22.

    , & A complex of two centrosomal proteins, CAP350 and FOP, cooperates with EB1 in microtubule anchoring. Mol. Biol. Cell 17, 634–644 (2005).

  23. 23.

    et al. A protein phosphatase 2A complex spatially controls plant cell division. Nat. Commun. 4, 1863 (2013).

  24. 24.

    et al. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat. Genet. 46, 652–656 (2014).

  25. 25.

    et al. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture. Plant Cell 25, 3743–3759 (2013).

  26. 26.

    , & Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol. 142, 280–293 (2006).

  27. 27.

    et al. Natural variation in the DEP1 locus enhances grain yield in rice. Nat. Genet. 41, 494–497 (2009).

  28. 28.

    et al. Root architecture and anthocyanin accumulation of phosphate starvation responses are modulated by the GA-DELLA signaling pathway in Arabidopsis. Plant Physiol. 145, 1460–1470 (2007).

  29. 29.

    et al. Profiling histone modification patterns in plants using genomic tiling microarrays. Nat. Methods 2, 213–218 (2005).

  30. 30.

    et al. A rice transient assay system identifies a novel domain in NRR required for interaction with NH1/OsNPR1 and inhibition of NH1-mediated transcriptional activation. Plant Methods 8, 6 (2012).

  31. 31.

    et al. Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40, 419–427 (2004).

  32. 32.

    et al. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat. Cell Biol. 13, 616–622 (2011).

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Acknowledgements

We thank G. Zhang (South China Agricultural University) for providing the single-segment substitution lines (W23-19-6-7-19-3 and W3-20-28-2-8). This work was supported by grants from the National Natural Science Foundation of China (91335207 and 31130070), the Ministry of Science and Technology of China (2012AA10A301) and the National Special Project of China (2014ZX0800935B).

Author information

Affiliations

  1. State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China.

    • Shaokui Wang
    • , Shan Li
    • , Qian Liu
    • , Kun Wu
    • , Jianqing Zhang
    • , Shuansuo Wang
    • , Yi Wang
    • , Xiangbin Chen
    • , Yi Zhang
    • , Caixia Gao
    •  & Xiangdong Fu
  2. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, China.

    • Shaokui Wang
  3. Rice Research Institute of the Guangdong Academy of Agricultural Sciences, Guangzhou, China.

    • Feng Wang
  4. Jiaxing Academy of Agricultural Sciences, Jiaxing, China.

    • Haixiang Huang

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Contributions

Shaokui Wang performed most of the experiments. S.L. and F.W. conducted QTL analysis. K.W. and Y.W. developed the NILs. Y.Z. and C.G. performed rice transformation. S.L. and Q.L. analyzed genetic diversity. K.W. and H.H. analyzed grain quality. Shuansuo Wang and J.Z. performed yeast two-hybrid screening. X.C. and Shaokui Wang performed ChIP and EMSA assays. X.F. designed the experiments and wrote the manuscript. All authors have discussed the results and contributed to the drafting of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Xiangdong Fu.

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DOI

https://doi.org/10.1038/ng.3352

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