Skip to main content
Log in

Analysis of genetic architecture and favorable allele usage of agronomic traits in a large collection of Chinese rice accessions

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Genotyping and phenotyping large natural populations provide opportunities for population genomic analysis and genome-wide association studies (GWAS). Several rice populations have been re-sequenced in the past decade; however, many major Chinese rice cultivars were not included in these studies. Here, we report large-scale genomic and phenotypic datasets for a collection mainly comprised of 1,275 rice accessions of widely planted cultivars and parental hybrid rice lines from China. The population was divided into three indica/Xian and three japonica/Geng phylogenetic subgroups that correlate strongly with their geographic or breeding origins. We acquired a total of 146 phenotypic datasets for 29 agronomic traits under multi-environments for different subpopulations. With GWAS, we identified a total of 143 significant association loci, including three newly identified candidate genes or alleles that control heading date or amylose content. Our genotypic analysis of agronomically important genes in the population revealed that many favorable alleles are underused in elite accessions, suggesting they may be used to provide improvements in future breeding efforts. Our study provides useful resources for rice genetics research and breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alexander, D.H., Novembre, J., and Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19, 1655–1664.

    CAS  Google Scholar 

  • Bai, W., Zhang, H., Zhang, Z., Teng, F., Wang, L., Tao, Y., and Zheng, Y. (2010). The evidence for non-additive effect as the main genetic component of plant height and ear height in maize using introgression line populations. Plant Breed 129, 376–384.

    Google Scholar 

  • Chen, W., Gao, Y., Xie, W., Gong, L., Lu, K., Wang, W., Li, Y., Liu, X., Zhang, H., Dong, H., et al. (2014). Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat Genet 46, 714–721.

    CAS  Google Scholar 

  • Crowell, S., Korniliev, P., Falcão, A., Ismail, A., Gregorio, G., Mezey, J., and McCouch, S. (2016). Genome-wide association and high-resolution phenotyping link Oryza sativa panicle traits to numerous trait-specific QTL clusters. Nat Commun 7, 10527.

    CAS  Google Scholar 

  • Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., Yano, M., and Yoshimura, A. (2004). Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18, 926–936.

    CAS  Google Scholar 

  • Dong, H., Zhao, H., Li, S., Han, Z., Hu, G., Liu, C., Yang, G., Wang, G., Xie, W., and Xing, Y. (2018). Genome-wide association studies reveal that members of bHLH subfamily 16 share a conserved function in regulating flag leaf angle in rice (Oryza sativa). PLoS Genet 14, e1007323.

    Google Scholar 

  • Du, H., Yu, Y., Ma, Y., Gao, Q., Cao, Y., Chen, Z., Ma, B., Qi, M., Li, Y., Zhao, X., et al. (2017). Sequencing and de novo assembly of a near complete indica rice genome. Nat Commun 8, 15324.

    Google Scholar 

  • Duan, P., Xu, J., Zeng, D., Zhang, B., Geng, M., Zhang, G., Huang, K., Huang, L., Xu, R., Ge, S., et al. (2017). Natural variation in the promoter of GSE5 contributes to grain size diversity in rice. Mol Plant 10, 685–694.

    CAS  Google Scholar 

  • Fang, J., Zhang, F., Wang, H., Wang, W., Zhao, F., Li, Z., Sun, C., Chen, F., Xu, F., Chang, S., et al. (2019). Ef-cd locus shortens rice maturity duration without yield penalty. Proc Natl Acad Sci USA 116, 18717–18722.

    CAS  Google Scholar 

  • Feng, X., Lin, K., Zhang, W., Nan, J., Zhang, X., Wang, C., Wang, R., Jiang, G., Yuan, Q., and Lin, S. (2019). Improving the blast resistance of the elite rice variety Kongyu-131 by updating the pi21 locus. BMC Plant Biol 19, 249.

    CAS  Google Scholar 

  • Feng, X., Wang, C., Nan, J., Zhang, X., Wang, R., Jiang, G., Yuan, Q., and Lin, S. (2017). Updating the elite rice variety Kongyu 131 by improving the Gn1a locus. Rice 10, 35.

    Google Scholar 

  • Gao, H., Jin, M., Zheng, X.M., Chen, J., Yuan, D., Xin, Y., Wang, M., Huang, D., Zhang, Z., Zhou, K., et al. (2014). Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci USA 111, 16337–16342.

    CAS  Google Scholar 

  • Guo, J., Wang, F., Song, J., Sun, W., and Zhang, X.S. (2010). The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice. Planta 231, 293–303.

    CAS  Google Scholar 

  • Guo, T., Yu, H., Qiu, J., Li, J., Han, B., and Lin, H. (2019). Advances in rice genetics and breeding by molecular design in China (in Chinese). Sci Sin Vitae 49, 1185–1212.

    Google Scholar 

  • Guo, Z., Yang, W., Chang, Y., Ma, X., Tu, H., Xiong, F., Jiang, N., Feng, H., Huang, C., Yang, P., et al. (2018). Genome-wide association studies of image traits reveal genetic architecture of drought resistance in rice. Mol Plant 11, 789–805.

    CAS  Google Scholar 

  • Huang, X., Kurata, N., Wei, X., Wang, Z.X., Wang, A., Zhao, Q., Zhao, Y., Liu, K., Lu, H., Li, W., et al. (2012). A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501.

    CAS  Google Scholar 

  • Huang, X., Wei, X., Sang, T., Zhao, Q., Feng, Q., Zhao, Y., Li, C., Zhu, C., Lu, T., Zhang, Z., et al. (2010). Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42, 961–967.

    CAS  Google Scholar 

  • Huang, X., Yang, S., Gong, J., Zhao, Q., Feng, Q., Zhan, Q., Zhao, Y., Li, W., Cheng, B., Xia, J., et al. (2016). Genomic architecture of heterosis for yield traits in rice. Nature 537, 629–633.

    CAS  Google Scholar 

  • Huang, X., Yang, S., Gong, J., Zhao, Y., Feng, Q., Gong, H., Li, W., Zhan, Q., Cheng, B., Xia, J., et al. (2015). Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. Nat Commun 6, 6258.

    CAS  Google Scholar 

  • Huang, X., Zhao, Y., Wei, X., Li, C., Wang, A., Zhao, Q., Li, W., Guo, Y., Deng, L., Zhu, C., et al. (2011). Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44, 32–39.

    CAS  Google Scholar 

  • Kaneko, M., Inukai, Y., Ueguchi-Tanaka, M., Itoh, H., Izawa, T., Kobayashi, Y., Hattori, T., Miyao, A., Hirochika, H., Ashikari, M., et al. (2004). Loss-of-function mutations of the rice GAMYB gene impair α-amylase expression in aleurone and flower development. Plant Cell 16, 33–44.

    CAS  Google Scholar 

  • Kang, H.M., Sul, J.H., Service, S.K., Zaitlen, N.A., Kong, S.Y., Freimer, N. B., Sabatti, C., and Eskin, E. (2010). Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42, 348–354.

    CAS  Google Scholar 

  • Kovi, M.R., Sablok, G., Bai, X.F., Wendell, M., Rognli, O.A., Yu, H.H., and Xing, Y.Z. (2013). Expression patterns of photoperiod and temperature regulated heading date genes in Oryza sativa. Comput Biol Chem 45, 36–41.

    CAS  Google Scholar 

  • Li, D., Huang, Z., Song, S., Xin, Y., Mao, D., Lv, Q., Zhou, M., Tian, D., Tang, M., Wu, Q., et al. (2016). Integrated analysis of phenome, genome, and transcriptome of hybrid rice uncovered multiple heterosis-related loci for yield increase. Proc Natl Acad Sci USA 113, E6026–E6035.

    CAS  Google Scholar 

  • Li, G., Jin, J., Zhou, Y., Bai, X., Mao, D., Tan, C., Wang, G., and Ouyang, Y. (2019). Genome-wide dissection of segregation distortion using multiple inter-subspecific crosses in rice. Sci China Life Sci 62, 507–516.

    Google Scholar 

  • Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993.

    CAS  Google Scholar 

  • Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760.

    CAS  Google Scholar 

  • Liu, T., Liu, H., Zhang, H., and Xing, Y. (2013). Validation and characterization of Ghd7.1, a major quantitative trait locus with pleiotropic effects on spikelets per panicle, plant height, and heading date in rice (Oryza sativa L.). J Integr Plant Biol 55, 917–927.

    CAS  Google Scholar 

  • McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20, 1297–1303.

    CAS  Google Scholar 

  • Miyoshi, K., Ito, Y., Serizawa, A., and Kurata, N. (2003). OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36, 532–540.

    CAS  Google Scholar 

  • Nan, J., Feng, X., Wang, C., Zhang, X., Wang, R., Liu, J., Yuan, Q., Jiang, G., and Lin, S. (2018). Improving rice grain length through updating the GS3 locus of an elite variety Kongyu 131. Rice 11, 21.

    Google Scholar 

  • Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A., and Reich, D. (2006). Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38, 904–909.

    CAS  Google Scholar 

  • Song, Y.L., Gao, Z.C., and Luan, W.J. (2012). Interaction between temperature and photoperiod in regulation of flowering time in rice. Sci China Life Sci 55, 241–249.

    CAS  Google Scholar 

  • Takahashi, Y., Teshima, K.M., Yokoi, S., Innan, H., and Shimamoto, K. (2009). Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci USA 106, 4555–4560.

    CAS  Google Scholar 

  • Wang, J., Xu, H., Li, N., Fan, F., Wang, L., Zhu, Y., and Li, S. (2015a). Artificial selection of Gn1a plays an important role in improving rice yields across different ecological regions. Rice 8, 37.

    Google Scholar 

  • Wang, Q., Xie, W., Xing, H., Yan, J., Meng, X., Li, X., Fu, X., Xu, J., Lian, X., Yu, S., et al. (2015b). Genetic architecture of natural variation in rice chlorophyll content revealed by a genome-wide association study. Mol Plant 8, 946–957.

    CAS  Google Scholar 

  • Wang, R., Jiang, G., Feng, X., Nan, J., Zhang, X., Yuan, Q., and Lin, S. (2019). Updating the genome of the elite rice variety Kongyu131 to expand its ecological adaptation region. Front Plant Sci 10, 288.

    Google Scholar 

  • Wang, S., Ma, B., Gao, Q., Jiang, G., Zhou, L., Tu, B., Qin, P., Tan, X., Liu, P., Kang, Y., et al. (2018a). Dissecting the genetic basis of heavy panicle hybrid rice uncovered Gn1a and GS3 as key genes. Theor Appl Genet 131, 1391–1403.

    CAS  Google Scholar 

  • Wang, W., Mauleon, R., Hu, Z., Chebotarov, D., Tai, S., Wu, Z., Li, M., Zheng, T., Fuentes, R.R., Zhang, F., et al. (2018b). Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557, 43–49.

    CAS  Google Scholar 

  • Xie, W., Wang, G., Yuan, M., Yao, W., Lyu, K., Zhao, H., Yang, M., Li, P., Zhang, X., Yuan, J., et al. (2015). Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection. Proc Natl Acad Sci USA 112, E5411–E5419.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Xu, H., Zhao, M., Zhang, Q., Xu, Z., and Xu, Q. (2016). The DENSE AND ERECT PANICLE 1 (DEP1) gene offering the potential in the breeding of high-yielding rice. Breed Sci 66, 659–667.

    CAS  Google Scholar 

  • Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C., Li, X., et al. (2008). Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40, 761–767.

    CAS  Google Scholar 

  • Yang, W., Guo, Z., Huang, C., Duan, L., Chen, G., Jiang, N., Fang, W., Feng, H., Xie, W., Lian, X., et al. (2014). Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 5, 5087.

    CAS  Google Scholar 

  • Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba, T., Yamamoto, K., Umehara, Y., Nagamura, Y., et al. (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473–2483.

    CAS  Google Scholar 

  • Ye, J., Niu, X., Yang, Y., Wang, S., Xu, Q., Yuan, X., Yu, H., Wang, Y., Wang, S., Feng, Y., et al. (2018). Divergent Hd1, Ghd7, and DTH7 alleles control heading date and yield potential of Japonica rice in Northeast China. Front Plant Sci 9, 35.

    Google Scholar 

  • Yu, B., Lin, Z., Li, H., Li, X., Li, J., Wang, Y., Zhang, X., Zhu, Z., Zhai, W., Wang, X., et al. (2001). TAC1, a major quantitative trait locus controlling tiller angle in rice. Plant J 52, 891–898.

    Google Scholar 

  • Zeng, D., Tian, Z., Rao, Y., Dong, G., Yang, Y., Huang, L., Leng, Y., Xu, J., Sun, C., Zhang, G., et al. (2017). Rational design of high-yield and superior-quality rice. Nat Plants 3, 17031.

    Google Scholar 

  • Zhang, J., Zhou, X., Yan, W., Zhang, Z., Lu, L., Han, Z., Zhao, H., Liu, H., Song, P., Hu, Y., et al. (2015). Combinations of the Ghd7, Ghd8 and Hd1 genes largely define the ecogeographical adaptation and yield potential of cultivated rice. New Phytol 208, 1056–1066.

    CAS  Google Scholar 

  • Zhang, Y., Li, Y., Wang, Y., Liu, Z., Liu, C., Peng, B., Tan, W., Wang, D., Shi, Y., Sun, B., et al. (2010). Stability of QTL across environments and QTL-by-environment interactions for plant and ear height in maize. Agric Sci China 9, 1400–1412.

    CAS  Google Scholar 

  • Zhao, K., Tung, C.W., Eizenga, G.C., Wright, M.H., Ali, M.L., Price, A.H., Norton, G.J., Islam, M.R., Reynolds, A., Mezey, J., et al. (2011). Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2, 461.

    Google Scholar 

  • Zhao, Q., Feng, Q., Lu, H., Li, Y., Wang, A., Tian, Q., Zhan, Q., Lu, Y., Zhang, L., Huang, T., et al. (2018). Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet 50, 278–284.

    CAS  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the Chinese Academy of Sciences “Strategic Priority Research Program” fund (XDA08020302) and grants from State Key Laboratory of Plant Genomics.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Aihong Li, Shigui Li or Chengzhi Liang.

Additional information

Accession numbers

All raw reads generated for rice accessions used in this study have been deposited in the National Genomics Data Center with BioProject PRJCA000322 and GSA accession CRA000167.

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Supporting Information

Figure S1 SNP density and distribution across the genome.

Figure S2 Linkage disequilibrium differentiation in different rice varietal groups.

Figure S3 GWAS of heading date for NE-GJ and CN-Mix GWAS panels.

Figure S4 GWAS of grain length for NE-GJ and CN-Mix GWAS panels.

Figure S5 GWAS of grain width for NE-GJ and CN-Mix GWAS panels.

Figure S6 The phenotype values were correlated well with genotypes of agronomically important functional genes.

Figure S7 Signals associated with multiple traits.

Figure S8 Local Manhattan plots for amylase content and grain length.

Figure S9 Association signals for heading date with OsMADS51 as a candidate gene.

Figure S10 The allele types of 63 genes containing functionally verified natural variants in all 1,275 rice accessions.

Table S1 The list of collected 1,275 rice accessions as well as their subpopulation classification and sequence information

Table S2 List of phenotypes used for GWAS

Table S3 The agro-ecologically diverse locations of multiple agronomic traits collected for NE-GJ and CN-Mix population panels

Table S4 The agronomic traits and multi-environmental phenotypes used in three NE-GJ-related GWAS panels

Table S5 The agronomic traits and multi-environmental phenotypes used in three CN-Mix-related GWAS panels

Table S6 The Pearson’s correlation between different locations in pair for all measured traits in multi-environments

Table S7 The associated loci and known genes located closely of all GWAS panels

Table S8 The allele types of 63 genes containing functionally verified natural variations in all 1,275 rice accessions

Table S9 The multiple comparisons (LSD) were evaluated for all known alleles of 27 agronomically important genes

The supporting information is available online at http://life.scichina.com and https://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.

Supporting Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., Chen, Z., Zhang, G. et al. Analysis of genetic architecture and favorable allele usage of agronomic traits in a large collection of Chinese rice accessions. Sci. China Life Sci. 63, 1688–1702 (2020). https://doi.org/10.1007/s11427-019-1682-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-019-1682-6

Navigation