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Control of rice grain-filling and yield by a gene with a potential signature of domestication

Nature Genetics volume 40, pages 1370–1374 (2008)Cite this article

Abstract

Grain-filling, an important trait that contributes greatly to grain weight, is regulated by quantitative trait loci and is associated with crop domestication syndrome1,2,3,4. However, the genes and underlying molecular mechanisms controlling crop grain-filling remain elusive. Here we report the isolation and functional analysis of the rice GIF1 (GRAIN INCOMPLETE FILLING 1) gene that encodes a cell-wall invertase required for carbon partitioning during early grain-filling. The cultivated GIF1 gene shows a restricted expression pattern during grain-filling compared to the wild rice allele, probably a result of accumulated mutations in the gene's regulatory sequence through domestication. Fine mapping with introgression lines revealed that the wild rice GIF1 is responsible for grain weight reduction. Ectopic expression of the cultivated GIF1 gene with the 35S or rice Waxy promoter resulted in smaller grains, whereas overexpression of GIF1 driven by its native promoter increased grain production. These findings, together with the domestication signature that we identified by comparing nucleotide diversity of the GIF1 loci between cultivated and wild rice, strongly suggest that GIF1 is a potential domestication gene and that such a domestication-selected gene can be used for further crop improvement.

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Figure 1: Grain-filling and sugar content of gif1 mutant and wild-type rice.
Figure 2: Expression pattern and localization of GIF1.
Figure 3: Molecular domestication and grain-filling of introgression lines.
Figure 4: Increased grain size and weight in transgenic rice overexpressing GIF1.

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Acknowledgements

We thank J.Y. Li, T. Sang and J.M. Li for critical reading of the manuscript and helpful suggestions; B. Han for the rice BAC clone; Z.Y. Wang for the Waxy promoter; D. Luo for help with in situ hybridization; X.Y. Gao and X.S. Gao for assistance with scanning electron microscopy and confocal laser microscopy; X.M. Zhang, L.J. Zeng and S.H. Ye for rice growth; and H.Q. Zheng for assistance with sugar measurement. This work was supported by grants from the Ministry of Science and Technology of China (2007AA02Z162, 2006AA10A102 and 2007AA10Z187), grants from the National Natural Science Foundation of China (30721061 and 30623006) and the Reproductive Development Project of the Shanghai Institutes for Biological Sciences.

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Authors and Affiliations

  1. Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China

    Ertao Wang, Wei Hao, Qun Li, Wei He, Hongxuan Lin & Zuhua He

  2. China National Rice Research Institute, 359 TiyuChang Road, Hangzhou, 31006, China

    Ertao Wang & Xudong Zhu

  3. Zhejiang Academy of Agricultural Sciences, 198 Shiqiao Road, Hangzhou, 310021, China

    Jianjun Wang, Linyou Wang & Lixia Zhang

  4. School of Life Sciences, Fudan University, 220 Handan Road, Shanghai, 200433, China

    Baorong Lu

  5. Department of Biology and the Huck Institutes of Life Sciences, Pennsylvania State University, University Park, 16802, Pennsylvania, USA

    Hong Ma

  6. College of Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Guiquan Zhang

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  1. Ertao Wang
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Contributions

E.W. and Z.H. conceived the research project, designed experiments and analyzed the data. E.W. carried out field phenotyping, genetics, gene cloning and functional and molecular evolution experiments. X.Z. screened the mutant. J.W. and L.W. conducted the genetic and field phenotype analyses. W. Hao, H.L. and G.Z. developed the introgression lines. Q.L. helped with the microarray assay. L.Z. helped with field testing. W. He helped with in situ hybridization. H.M. contributed to the funding and discussed the experiments. B.L. helped with wild rice analysis. Z.H. oversaw the entire study.

Corresponding author

Correspondence to Zuhua He.

Supplementary information

Supplementary Text and Figures

Supplementary Methods, Supplementary Figures 1–12, Supplementary Tables 1, 4 and 6 (PDF 999 kb)

Supplementary Table 2 (Excel)

Summary of 341 reproducibly differentially regulated genes of the gif1 mutant versus wild-type Zhonghua11 at 7 DAF (XLS 185 kb)

Supplementary Table 3 (Excel)

Summary of 44 carbohydrate metabolism-related genes reproducibly differentially regulated in the gif1 mutant versus wild-type Zhonghua11 at 7 DAF (XLS 61 kb)

Supplementary Table 5 (Excel)

Analysis of recombinant plants in fine-mapping of the IL locus (XLS 25 kb)

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Wang, E., Wang, J., Zhu, X. et al. Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40, 1370–1374 (2008). https://doi.org/10.1038/ng.220

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