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Genomic architecture of heterosis for yield traits in rice

Nature volume 537, pages 629–633 (2016)Cite this article

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Abstract

Increasing grain yield is a long-term goal in crop breeding to meet the demand for global food security. Heterosis, when a hybrid shows higher performance for a trait than both parents, offers an important strategy for crop breeding. To examine the genetic basis of heterosis for yield in rice, here we generate, sequence and record the phenotypes of 10,074 F2 lines from 17 representative hybrid rice crosses. We classify modern hybrid rice varieties into three groups, representing different hybrid breeding systems. Although we do not find any heterosis-associated loci shared across all lines, within each group, a small number of genomic loci from female parents explain a large proportion of the yield advantage of hybrids over their male parents. For some of these loci, we find support for partial dominance of heterozygous locus for yield-related traits and better-parent heterosis for overall performance when all of the grain-yield traits are considered together. These results inform on the genomic architecture of heterosis and rice hybrid breeding.

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Figure 1: Large-scale sequencing, genotyping and genetic mapping in 10,074 F2 lines.
Figure 2: Evaluation of dominance effects for all yield-related QTLs.
Figure 3: Two candidate genes hd3a and tac1 for heterosis for yield traits in type-A hybrids.
Figure 4: Combination of multiple beneficial alleles in type-C hybrids.

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European Nucleotide Archive

Data deposits

DNA sequencing data are deposited in the European Nucleotide Archive under the accession number PRJEB13735.

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Acknowledgements

This work was supported by the Chinese Academy of Sciences (XDA08020101) and the National Natural Science Foundation of China (31322028, 91535202, 31421093 and 31301302).

Author information

Author notes

  1. Xuehui Huang, Shihua Yang and Junyi Gong: These authors contributed equally to this work.

Authors and Affiliations

  1. National Center for Gene Research, CAS Center for Excellence of Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, 200233, China

    Xuehui Huang, Qiang Zhao, Qi Feng, Qilin Zhan, Yan Zhao, Wenjun Li, Tao Huang, Lei Zhang, Danlin Fan, Jiaying Chen, Congcong Zhou, Yiqi Lu, Qijun Weng & Bin Han

  2. State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310006, China

    Shihua Yang, Junyi Gong, Benyi Cheng, Junhui Xia & Neng Chen

Authors
  1. Xuehui Huang
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Contributions

B.H. conceived the project and its components. X.H. and B.H. designed studies and contributed to the original concept of the project. S.Y. and J.G. contributed the generation of the genetic populations. J.G., Qil.Z., B.C., J.X., N.C. and S.Y. contributed in phenotyping for grain yield traits. W.L., Y.L. J.C., C.Z., D.F., Q.W. and Q.F. performed the genome sequencing. X.H., Qia.Z., Y.Z., L.Z. and T.H. performed genome data analysis and genetic analysis. X.H. and B.H. analysed whole data and wrote the paper.

Corresponding authors

Correspondence to Xuehui Huang or Bin Han.

Additional information

Reviewer Information

Nature thanks J. Ross-Ibarra, D. Weigel and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Figure 1 The experimental design and analysis procedure used in the study.

Extended Data Figure 2 Selection of 17 representative hybrid combinations from 1,495 hybrids.

a, Plots of the first two principal components of 1,495 hybrids. The 17 representative hybrids are coloured in red. b, Plots of the principal component 3 and the principal component 4 of 1,495 hybrids. c, Plots of heading date and plant height of 1,495 hybrids. d, Plots of grain number and seed-setting rate of 1,495 hybrids.

Extended Data Figure 3 High-resolution genotyping of F2 lines by whole-genome sequencing.

a, Aligned recombination maps of 1,105 lines from a cross between Fuhui676 and Guangzhan63-4S. Three genotypes were indicated by blue, red and yellow, respectively (blue, Fuhui676/Fuhui676; red, Guangzhan63-4S/Guangzhan63-4S; yellow, Fuhui676/Guangzhan63-4S). b, The recombination map of a single F2 line from a cross between Fuhui676 × Guangzhan63-4S. The genomic DNA of the line was sequenced in the HiSeq2500 system, and genotyped through the SEG-Map computational algorithm. Detected SNP genotypes in this line were indicated along chromosomes according to their physical locations. A sliding window approach was used for genotype calling, recombination breakpoint determination and map construction. There were several IBS (identity by state) segments shared by both parents (for example, the regions on the chromosomes 10 and 11), which are indicated by the grey boxes.

Extended Data Figure 4 Analysis of flowering time in type-A hybrids.

a, Flowering-time modelling using the genotypes of four genes (Hd3a, Ghd7, Hd2 and Ehd1) known to regulate flowering time. We used the data in one type-A population (Guanghui998 × Tianfeng) for experimentation, and evaluated the accuracy of the modelling in the other eight populations. b, The estimates of the genetic effects of three genotypes of the four genes, in which the flowering time of the homozygous genotypes of male parents was set to be 90 days according to the average performance of restorer lines. The arrows indicated the flowering time for the genotypes Hd3a/hd3a and hd3a/hd3a.

Extended Data Figure 5 The linkage drag around the hd3a locus.

The allelic combinations of six candidate genes on the short arm of chromosome 6 and their frequencies in 1,063 indica CMS lines.

Extended Data Figure 6 QTL for heterosis for yield traits in type-B hybrids.

a, Plots of the dominance effects of three traits at the Tms5 locus in the four type-B hybrids. b, Plots of the dominance effects of three traits at the Ghd8 locus in the four type-B hybrids. c, The yield advantages in the hybrid LYP9 by two QTLs LAX1 and SS3p10 from PA64S (**P < 0.001, two-tailed t-test). The male (M) and heterozygous (H) genotypes are indicated. d, The yield advantages in the hybrid Liangyou676 by two QTLs at the ‘ghd8’ locus and PN3q23 from Guangzhan63-4S (**P < 0.001, two-tailed t-test).

Extended Data Figure 7 Support for pseudo-overdominance at the Tms5 locus.

a, The linkage mapping of fertility in one population of type B. LOD values are plotted against the physical positions, and the threshold (3.5) is indicated by a horizontal dashed line. b, The linkage mapping of panicle number in one population of type A. c, The linkage mapping of yield per plant in the population of type A. d, Gene structure and causal variation site between Tms5 and tms5 alleles in the hybrids of type B. e, No mutations are detected at the Tms5 gene between both parents (Fuhui838 and II32A) of the type-A population.

Extended Data Figure 8 Performances of two QTLs LAX1 and SS3p10 in type-B hybrid LYP9.

a, The linkage mapping of seed-setting rate in the population of type-B hybrid LYP9. LOD values are plotted against the physical positions, and the threshold (3.5) is indicated by a horizontal dashed line. b, The performances of seed-setting rate for three genotypes of the SS3p10 locus in the population of type-B hybrid LYP9. c, The linkage mapping of grain weight in the population of type-B hybrid LYP9. d, The performances of grain weight for three genotypes of the LAX1 locus in the population of type-B hybrid LYP9.

Extended Data Figure 9 Performances of two QTLs, GW3p6 and PN3q23, in type-B hybrid Liangyou676.

a, The linkage mapping of grain weight in the population of type-B hybrid Liangyou676. b, The performances of grain weight for three genotypes of the GW3p6 locus in the population of type-B hybrid Liangyou676. c, The linkage mapping of panicle number in the population of type-B hybrid Liangyou676. d, The performances of panicle number for three genotypes of the PN3q23 locus in the population of type-B hybrid Liangyou676.

Extended Data Figure 10 Partial positive dominance effect of IPA1 for the yield components.

a, The performances of grain number per panicle for three genotypes of the IPA1 gene. b, The performances of panicle number for three genotypes of the IPA1 gene. c, The performances of seed-setting rate for three genotypes of the IPA1 gene.

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Huang, X., Yang, S., Gong, J. et al. Genomic architecture of heterosis for yield traits in rice. Nature 537, 629–633 (2016). https://doi.org/10.1038/nature19760

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