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Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield

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Abstract

Increases in the yield of rice, a staple crop for more than half of the global population, are imperative to support rapid population growth. Grain weight is a major determining factor of yield. Here, we report the cloning and functional analysis of THOUSAND-GRAIN WEIGHT 6 (TGW6), a gene from the Indian landrace rice Kasalath. TGW6 encodes a novel protein with indole-3-acetic acid (IAA)-glucose hydrolase activity. In sink organs, the Nipponbare tgw6 allele affects the timing of the transition from the syncytial to the cellular phase by controlling IAA supply and limiting cell number and grain length. Most notably, loss of function of the Kasalath allele enhances grain weight through pleiotropic effects on source organs and leads to significant yield increases. Our findings suggest that TGW6 may be useful for further improvements in yield characteristics in most cultivars.

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Figure 1: Positional cloning and expression pattern of TGW6.
Figure 2: Effect of TGW6 on sink development.
Figure 3: Haplotype network of the TGW6 gene and its effects on yield characteristics across cultivars.

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Gene Expression Omnibus

NCBI Reference Sequence

Referenced accessions

Protein Data Bank

References

  1. Sweeney, M. & McCouch, S. The complex history of the domestication of rice. Ann. Bot. (Lond.) 100, 951–957 (2007).

    Article  Google Scholar 

  2. Harlan, J. Crops and Man (American Society of Agronomy, Crop Science Society of America, Madison, Wisconsin, 1992).

  3. 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 

  4. Takano-Kai, N. et al. Evolutionary history of GS3, a gene conferring grain length in rice. Genetics 182, 1323–1334 (2009).

    CAS  Article  Google Scholar 

  5. Shomura, A. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat. Genet. 40, 1023–1028 (2008).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  7. Nagata, K., Yoshinaga, S., Takanashi, J. & Terao, T. Effects of dry matter production, translocation of nonstructural carbohydrates and nitrogen application on grain filling in rice cultivar Takanari, a cultivar bearing a large number of spikelets. Plant Prod. Sci. 4, 173–183 (2001).

    Article  Google Scholar 

  8. Yang, J. et al. Grain and dry matter yields and partitioning of assimilates in japonica/indica hybrid rice. Crop Sci. 42, 766–772 (2002).

    Article  Google Scholar 

  9. Peng, S., Khush, G.S., Virk, P., Tang, Q. & Zoh, Y. Progress in ideotype breeding to increase rice yield potential. Field Crops Res. 108, 32–38 (2008).

    Article  Google Scholar 

  10. Dingkuhn, M., Penning de Vries, F.M.T., de Datta, S.K. & van Laar, H.H. Concepts for a New Plant Type for Direct Seeded Flooded Tropical Rice (International Rice Research Institute, Los Baños, Philippines, 1991).

  11. Ishimaru, K., Kashiwagi, T., Hirotsu, N. & Madoka, Y. Identification and physiological analyses of a locus for rice yield potential across the genetic background. J. Exp. Bot. 56, 2745–2753 (2005).

    CAS  Article  Google Scholar 

  12. Ishimaru, K., Kosone, M., Sasaki, H. & Kashiwagi, T. Leaf contents differ depending on the position in a rice leaf sheath during sink-source transition. Plant Physiol. Biochem. 42, 855–860 (2004).

    CAS  Article  Google Scholar 

  13. Ishimaru, K. Identification of a locus increasing rice yield and physiological analysis of its function. Plant Physiol. 133, 1083–1090 (2003).

    CAS  Article  Google Scholar 

  14. Hoshikawa, K. The Growing Rice Plant: an Anatomical Monograph (Nosan Gyoson Bunka Kyokai, Tokyo, 1989).

  15. Hoshikawa, K. Studies on the development in rice. Process of endosperm tissue formation. Jpn. J. Crop. Sci. 36, 151–161 (1967).

    Article  Google Scholar 

  16. Brown, R.C., Lemmon, B.E. & Olsen, O.-D. Development of the endosperm in rice (Oryza sativa L.): cellularization. J. Plant Res. 109, 301–313 (1996).

    Article  Google Scholar 

  17. Mizutani, M., Naganuma, T., Tsutsumi, K. & Saitoh, Y. The syncytium-specific expression of the Orysa;KRP3 CDK inhibitor: implication of its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm. J. Exp. Bot. 61, 791–798 (2010).

    CAS  Article  Google Scholar 

  18. Jawad, Z. & Paoli, M. Novel sequences propel familiar folds. Structure 10, 447–454 (2002).

    CAS  Article  Google Scholar 

  19. Marchler-Bauer, A. et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225–D229 (2011).

    CAS  Article  Google Scholar 

  20. Scharff, E.I., Koepke, J., Fritzsch, G., Lucke, C. & Ruterjans, H. Crystal structure of diisopropylfluorophosphatase from Loligo vulgaris. Structure 9, 493–502 (2001).

    CAS  Article  Google Scholar 

  21. Lur, H.S. & Setter, T.L. Role of auxin in maize endosperm development (timing of nuclear DNA endoreduplication, zein expression, and cytokinin). Plant Physiol. 103, 273–280 (1993).

    CAS  Article  Google Scholar 

  22. Ludwig-Müller, J. Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757–1773 (2011).

    Article  Google Scholar 

  23. Jakubowska, A. & Kowalczyk, S. A specific enzyme hydrolyzing 6-O(4-O)-indole-3-ylacetyl-β-D-glucose in immature kernels of Zea mays. J. Plant Physiol. 162, 207–213 (2005).

    CAS  Article  Google Scholar 

  24. Song, X.-J. et al. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623–630 (2007).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  26. Wang, E. et al. Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 40, 1370–1374 (2008).

    CAS  Article  Google Scholar 

  27. Kurata, N. & Yamazaki, Y. Oryzabase. an integrated biological and genome information database for rice. Plant Physiol. 140, 12–17 (2006).

    CAS  Article  Google Scholar 

  28. Kojima, Y., Ebana, K., Fukuoka, S., Nagamine, T. & Kawase, M. Development of an RFLP-based rice diversity research set of germplasm. Breed. Sci. 55, 431–440 (2005).

    CAS  Article  Google Scholar 

  29. Tanksley, S.D. & McCouch, S.R. Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277, 1063–1066 (1997).

    CAS  Article  Google Scholar 

  30. Yamakawa, H., Hirose, T., Kuroda, M. & Yamaguchi, T. Comprehensive expression profiling of rice grain filling–related genes under high temperature using DNA microarray. Plant Physiol. 144, 258–277 (2007).

    CAS  Article  Google Scholar 

  31. Peng, S. et al. Rice yields decline with higher night temperature from global warming. Proc. Natl. Acad. Sci. USA 101, 9971–9975 (2004).

    CAS  Article  Google Scholar 

  32. Miki, D. & Shimamoto, K. Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 45, 490–495 (2004).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  34. Ma, X., Panjikar, S., Koepke, J., Loris, E. & Stöckigt, J. The sturucture of Rauvolfia serpentina strictosidine synthase is novel six-bladed β-propeller fold in plant proteins. Plant Cell 18, 907–920 (2006).

    CAS  Article  Google Scholar 

  35. Stöckigt, J., Barleben, L., Panjikar, S. & Loris, E.A. 3D-structure and function of strictosidine synthase—the key enzyme of monoterpenoid indole alkaloid biosynthesis. Plant Physiol. Biochem. 46, 340–355 (2008).

    Article  Google Scholar 

  36. Shi, J., Blundell, T.L. & Mizuguchi, K. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243–257 (2001).

    CAS  Article  Google Scholar 

  37. Dolan, M.A., Keil, M. & Baker, D.S. Comparison of composer and ORCHESTRAR. Proteins 72, 1243–1258 (2008).

    CAS  Article  Google Scholar 

  38. Clark, M., Cramer, R.D. & van den Opdenbosch, N. III. Validation of the general purpose tripose 5.2 force field. J. Comput. Chem. 10, 982–1012 (1989).

    CAS  Article  Google Scholar 

  39. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283–291 (1993).

    CAS  Article  Google Scholar 

  40. Tsunoda, Y. et al. Improving expression and solubility of rice proteins produced as fusion proteins in Escherichia coli. Protein Expr. Purif. 42, 268–277 (2005).

    CAS  Article  Google Scholar 

  41. Ishimaru, K., Hirotsu, N., Madoka, Y. & Kashiwagi, T. Quantitative trait loci for sucrose, starch, and hexose accumulation before heading in rice. Plant Physiol. Biochem. 45, 799–804 (2007).

    CAS  Article  Google Scholar 

  42. Matsuda, F., Miyazawa, H., Wakasa, K. & Miyagawa, H. Quantification of indole-3-acetic acid and amino acid conjugates in rice by liquid chromatography–electrospray ionization–tandem mass spectrometry. Biosci. Biotechnol. Biochem. 69, 778–783 (2005).

    CAS  Article  Google Scholar 

  43. Hirose, T. et al. Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period. Physiol. Plant. 128, 425–435 (2006).

    CAS  Article  Google Scholar 

  44. Komatsuda, T. et al. Six-rowed barley originated from a mutation in a homeodomain–leucine zipper I–class homeobox gene. Proc. Natl. Acad. Sci. USA 104, 1424–1429 (2007).

    CAS  Article  Google Scholar 

  45. Clement, M., Posada, D. & Crandall, K. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1659 (2000).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank T. Meshi for helpful and important suggestions, Y. Shimoda and A. Miyamoto for help with experiments, T. Yanai and S. Yoshimizu for rice growth, K. Shimamoto (Nara Institute of Science and Technology) for providing the pANDA vector, K. Toshimitsu (Japan International Cooperation Agency) for providing seeds of NERICA and T. Kobayakawa for helpful discussions. The wild rice accessions used in this study were distributed from the National Institute of Genetics supported by the National Bioresource Project, Ministry of Education, Culture, Sports, Science and Technology, Japan. This work was supported by grants from the Bio Cosmos Program and Genomics for Agricultural Innovation (QTL-4007), Ministry of Agriculture, Forestry and Fisheries of Japan.

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Authors

Contributions

K.I. conceived the research project, designed experiments and wrote the manuscript with help from N. Hirotsu, Y.M. and E.K. K.I., N. Hirotsu and Y.M. carried out field phenotyping, genetics, gene cloning and functional and molecular evolution experiments and analyzed the data. N. Hara helped with in situ hybridization, and H.O. assisted in transformation. N.M. helped with phenotyping, genotyping and gene cloning. T.K. and K.U. helped with field work, and B.S., A.O. and H.M. quantified IAA content. E.K. performed structure analysis.

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Correspondence to Ken Ishimaru.

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The authors declare no competing financial interests.

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Supplementary Figures 1–21 and Supplementary Tables 1–5 (PDF 2839 kb)

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Ishimaru, K., Hirotsu, N., Madoka, Y. et al. Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45, 707–711 (2013). https://doi.org/10.1038/ng.2612

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