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Genomic selection and genetic architecture of agronomic traits during modern rapeseed breeding

Nature Genetics volume 54, pages 694–704 (2022)Cite this article

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Abstract

Rapeseed (Brassica napus L.) is an important oil-producing crop for the world. Its adaptation, yield and quality have been considerably improved in recent decades, but the genomic basis underlying successful breeding selection remains unclear. Hence, we conducted a comprehensive genomic assessment of rapeseed in the breeding process based on the whole-genome resequencing of 418 diverse rapeseed accessions. We unraveled the genomic basis for the selection of adaptation and agronomic traits. Genome-wide association studies identified 628 associated loci-related causative candidate genes for 56 agronomically important traits, including plant architecture and yield traits. Furthermore, we uncovered nonsynonymous mutations in plausible candidate genes for agronomic traits with significant differences in allele frequency distributions across the improvement process, including the ribosome recycling factor (BnRRF) gene for seed weight. This study provides insights into the genomic basis for improving rapeseed varieties and a valuable genomic resource for genome-assisted rapeseed breeding.

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Fig. 1: Geographic distribution and population diversity of 418 rapeseed accessions.
Fig. 2: Genome-wide analysis of selective sweeps during modern rapeseed breeding.
Fig. 3: Features of rapeseed genome with integration of GWAS results.
Fig. 4: GWAS for leaf angle and identification of the candidate gene BnPIN2.
Fig. 5: GWAS for seed weight and identification of the causal gene BnRRF.
Fig. 6: GWAS for GSL content and identification of the candidate gene BnLSG.

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Data availability

The raw resequencing data of 418 rapeseed accessions are available in the NCBI Sequence Read Archive under accessions PRJNA416679 and Genome Sequence Archive (GSA) database in BIG Data Center (http://bigd.big.ac.cn/gsa) under accession number CRA005979. The high-coverage resequencing data of 135 rapeseed accessions and Hi-C data were deposited in GSA under accession number CRA005980. The public RNA-seq data used was downloaded from NCBI and the accession numbers are summarized in Supplementary Table 22. The relevant data of genotype and phenotype are available at the website http://brassicanapusdata.cn/DOWNLOAD. All the data and research materials in this study are available upon reasonable request.

Code availability

All the analysis tools used in this study have been published before as described in the Methods and Reporting Summary.

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Acknowledgements

We thank G. Cai (Oil Crops Research Institute, CAAS) for help with technical analysis. This work was supported by the National Key Research and Development Program of China (2016YFD0100202), Germplasm Resources Protection Project in China (2016NWB040) and Agricultural Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences (CAAS-ASTIP- 2015-OCRI) to X.W. and National Natural Science Foundation of China to J.H. (31901426) and to G.Y. (32072106) and the Young Elite Scientists Sponsorship Program by China Association for Science and Technology (2019QNRC001) to T.X.

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Author notes

  1. The authors contributed equally: Jihong Hu, Biyun Chen, Jing Zhao, Fugui Zhang, Ting Xie, Kun Xu.

Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan, China

    Jihong Hu, Biyun Chen, Fugui Zhang, Ting Xie, Kun Xu, Guizhen Gao, Guixin Yan, Hongge Li, Lixia Li, Gaoxiang Ji, Hao Li, Qian Huang, Meili Zhang, Jinfeng Wu, Weilin Song, Xiaojun Zhang, Yujie Luo & Xiaoming Wu

  2. Novogene Bioinformatics Institute, Beijing, China

    Jing Zhao & Shilin Tian

  3. Division of Biological Sciences, Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

    Hong An & J. Chris Pires

  4. School of Biological Science and Institute of Agriculture, The University of Western Australia, Crawley, Western Australia, Australia

    Jacqueline Batley

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  1. Jihong Hu
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Contributions

X.W., S.T. and J.H. conceived and designed the research. X.W., B.C., K.X. and H.L. participated in germplasm collection. B.C., J.H., H.L., K.X., F.Z., G.G., L.L., H.G.L., Q.H., J.W., W.S. and Y.L. performed field experiments and phenotyping. J.H., J.Z., X.W., S.T., T.X. and G.J. performed sequencing, genomic variant and analyzed the data. T.X. and F.Z. performed Hi-C experiments and data analysis. G.Y., M.Z., F.Z. and J.H. performed plasmid construction and genetic transformation. F.Z., J.H. and X.Z. conducted gene expression analysis. J.H., J.Z. and T.X. wrote the manuscript. X.W., J.C.P, H.A., S.T. and J.B. revised the manuscript.

Corresponding authors

Correspondence to Shilin Tian or Xiaoming Wu.

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Extended data

Extended Data Fig. 1 Changes in agronomic traits during rapeseed breeding in Europe and China.

PH, plant height; BH, branch height; BA, branch angle; BN, primary branch number; DM, diameter of main stem; YP, yield per plant; SW, 1,000-seed weight; SP, seeds per pod; SN, silique number per plant; HI, harvest index; FT, flowering time; SOC, seed oil content; GSL, glucosinolate. Different letters above the boxes indicate significant differences (P < 0.05, two-tailed t-test). The center lines indicate the median, box limits represent the upper and lower quartiles, whiskers extend to 1.5× the interquartile range, and dots represent outliers. EU, Europe; CN, China. EU1950&70 s (n = 93); EU1980&90 s (n = 35); CN1950&70 s (n = 73); CN1980&90 s (n = 67); CN00, CN2000&10 s (n = 35) (See Supplementary Fig. 6).

Extended Data Fig. 2 GWAS identification of the candidate genes for flowering time.

a, Manhattan plots of SNP-GWAS for flowering time in Wuhan 2015. The red arrowheads indicate the FT genes (BnaA02g12130D and BnaC06g27090D). b,c, Boxplots for flowering time based on the haplotypes (Hap) of BnaA02g12130D (b) and BnaC06g27090D (c). Center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. Significant differences between the haplotypes were evaluated by two-tailed t-test and shown by P value or different letters (P < 0.01). d, Haplotype frequency changes of BnaA02g12130D and BnaC06g27090D in different ecotypes and breeding eras. e, Local Manhattan plot (top) and LD heatmap (bottom) surrounding the peak for flowering time on chromosome C06 (BnaC06g27090D). The red arrowheads indicate the SNP in candidate gene (BnaC06g27090D). The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). f, XP-CLR plot of BnaC06g27090D. The red horizontal dashed line represents the genome-wide cutoff with the highest being 1%. g, The spectrum of allele frequencies at the causal polymorphisms of BnaC06g27090D. EU, Europe; CN, China. EU50, EU1950&70 s; EU80, EU1980&90 s; CN50, CN1950&70 s; CN80, CN1980&90 s; CN00, CN2000&10 s.

Extended Data Fig. 3 GWAS identification of candidate genes for plant height and branch height.

a, b, Manhattan plots of SNP-GWAS and InDel-GWAS for plant height (a) and branch height (b) in Yangluo 2013. The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). c, Local Manhattan plot (top) and LD heatmap (bottom) surrounding the peak for plant height and branch height on chromosome C07 using SNPs (blue dots) and InDels (red triangles). The candidate region lies between red dashed lines. The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). d, XP-CLR plot of BnaC07g34270D. The red horizontal dashed line represents the genome-wide cutoff with the highest being 1%. e, Boxplot of plant height and branch height for the haplotypes (Hap) of BnaC07g34270D using both SNPs and InDels. Center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. Different letters above the boxes indicate significant differences (P < 0.01, two-tailed t-test) in a pairwise comparison. f, Haplotype frequency changes of BnaC07g34270D in different ecotypes and breeding eras.

Extended Data Fig. 4 GWAS for seed weight and identification of the candidate gene on chromosome A09 and C08.

a, Manhattan plots of SNP-GWAS (blue dots) and InDel-GWAS (red dots) for 1000-seed weight on chromosome A09_random. The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). b, Boxplots for silique length and 1000-seed weight based on the haplotypes of BnaA09g55580D (ARF18). Center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. The P values based on two-tailed t-test are shown. c, Phenotypes of silique length (left) and seed size (right) between 2AF456 (small seed) and 2AF410 (large seed). Scale bar, 1 cm and 0.3 cm. d, Boxplots for 1000-seed weight based on the haplotypes of BnaC08g31420D and frequency changes of BnaC08g31420D in different ecotypes and breeding eras. Center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. Different letters above the boxes indicate significant differences (P < 0.01, two-tailed t-test) in a pairwise comparison. e, XP-CLR plot of BnaC08g32730D (BnRRF). The red horizontal dashed line represents the genome-wide cutoff with the highest being 1%. f, Phenotypes of seeds in WT (Col -0) and Arabidopsis overexpression (OE) lines. Scale bar, 0.5 mm. g, Overexpression (OE) of BnRRF in Arabidopsis increases the seed weight with the expression levels. Error bars, data were presented as the mean ± SD, n = 6 and 3, respectively. Significant differences were evaluated by two-tailed Student’s t-test (** P < 0.01).

Extended Data Fig. 5 GWAS for yield and identification of the candidate genes associated with 1,000-seed weight (SW) and silique length (SL).

a, b, Manhattan plots of SNP-GWAS and InDel-GWAS for SW (a) and SL(b) in Wuhan 2016. The red arrowheads indicate the previous reported genes (ARF18 and CYP78A9). The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). c,d, Boxplot for SW and SL based on the haplotypes of BnaA09g40330D (c) and BnaC08g32200D (d) using SNPs. e, qRT–PCR analysis of the expression of BnaA09g40330D in large seed and small seed accessions. Error bars, data were presented as the mean ± SD, n = 3 biological replicates. f, Gene structure and DNA polymorphism of BnaA09g40330D and BnaC08g32200D. Two nonsynonymous SNPs were found to be associated with the GWAS signals for SW and SL on chromosomes A09 (A09DFG and A09DCG) and C08 (C08LAL and C08LVL), respectively. g, Boxplot for SW and SL based on the haplotypes of the recombination of two alleles on A09 and C08. In c, d and g, center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. The P values based on two-tailed t-test are shown. h, qRT–PCR analysis of the expression of BnaC08g32200D in large seed and small seed accessions. Error bars, data were presented as the mean ± SD, n = 3 biological replicates.

Extended Data Fig. 6 GWAS identification of the candidate genes for glucosinolate (GSL) content.

a, Manhattan plots of InDel-GWAS for GSL content. The red arrowheads indicate the previous reported genes (GTR2 and HAG1). The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). b, Selective sweeps of BnaA02g33270D based on π-ratio and FST between oil- and vegetable-use rapeseeds. c, Local Manhattan plot (top) and LD heatmap (bottom) surrounding the peak for GSLs on chromosome C09 based on SNPs (blue dots) and InDels (red triangles). The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). d, Boxplots for GSLs based on the haplotypes (Hap) of BnaC09g05240D using both SNPs and InDels. e, Haplotype frequency changes of BnaC09g05240D in different ecotypes and breeding eras. f, XP-CLR plot of BnaC09g04850D. The red horizontal dashed line represents the genome-wide cutoff with the highest being 1%. g, Boxplots for GSL based on the haplotypes (Hap) of BnaC09g04850D using both SNPs and InDels. In d and g, center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. Different letters above the boxes indicate significant differences (P < 0.01, two-tailed t-test) in a pairwise comparison. h, Haplotype frequency changes of BnaC09g04850D in different ecotypes and breeding eras.

Extended Data Fig. 7 GWAS identification of candidate genes for erucic acid (C22:1) content.

a, Local Manhattan plot (top) and LD heatmap (bottom) surrounding the peak for C22:1 on chromosome A08 using SNPs. The red dashed line indicates the previous reported genes (FAE1). The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction). b, XP-CLR plot of BnaA08g11130D (FAE1) and BnaA08g11140D (KCS17). The red horizontal dashed line represents the genome-wide cutoff with the highest being 1%. c, Selective sweeps of BnaA08g11130D and BnaA08g11140D based on π-ratio and FST betweenoil- and vegetable-use rapeseeds. d, Exon–intron structure and DNA polymorphism of BnaA08g11140D. e, Boxplots for C22:1 based on the haplotypes (Hap) of BnaA08g11020D and BnaA08g11140D. f, qRT–PCR analysis of the expression of BnaA08g11140D in large seed and small seed accessions. In e and f, center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. Significant differences between the haplotypes or pairwise comparison were evaluated by two-tailed t-test and shown by P values or different letters (P < 0.01). g, Haplotype frequency changes of BnaA08g11140D in different ecotypes and breeding eras.

Extended Data Fig. 8 GWAS analysis and identification of the candidate genes for clubroot resistance.

a, Manhattan plots for disease index of clubroot on chromosome C04 using SNPs. Arrowhead indicates the position of strong associated peak with the SNP (C04:32815573). The horizontal dashed line represents the significance threshold (P < 1 × 10−6, Bonferroni correction).b, Heatmap showing the differentially expressed genes during four stages after infecting clubroot in resistant and sensitive rapeseeds (Li et al., 2020). c, Phenotypic features clubroot tolerant (2AF430 and 2AF451) and sensitive (2AF459 and 2AF478) accessions. Scale bar, 5 cm. d, Exon–intron structure and DNA polymorphism of BnaC04g30930D. e, Boxplots for disease index of clubroot based on the haplotypes (Hap) of BnaC04g30930D. Center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range, and dots represent outliers. Different letters above the boxes indicate significant differences (P < 0.01, two-tailed t-test) in a pairwise comparison. f, Local Manhattan plot (top) and LD heatmap (bottom) surrounding the peak for disease index of clubroot on chromosome C04 (BnaC04g30930D). g, Expression levels of the clubroot resistance candidate gene BnaC04g30930D in different rapeseed accessions by qRT–PCR. Error bars, data were presented as the mean ± SD, n = 3 biological replicates. Different letters above the boxes indicate significant differences (P < 0.05, two-tailed t-test).

Extended Data Fig. 9 Association networks across different traits in rapeseed and the chromatin interactions (Hi-C) for plant architecture (PA) and yield (PY) traits.

a, Network for 17 traits based on the link powers between loci. The nodes represent traits and their corresponding loci (see Supplementary Table 19). The edges between the loci from different traits are linked by LD. Only the edges with an average LD ≥ 0.4 are shown. BH, branch height; BA, branch angle; BN, primary branch number; DM, diameter of main stem; FT, flowering time; PH, plant height; SI, Silique number of main inflorenscence; SL, silique length; SN, silique number per plant; SP, seeds per pod; SS, Stem strength; SW, 1,000-seed weight; YP, yield per plant. The octagon represents traits and circle indicates different loci. Blue, flowering time; skyblue, PA; purple, PY; yellow, fatty acid components. b, High chromatin interactions (top 5%) between the loci of PA and PY. c, Collinearity analysis of the causal genes for PA and PY with the high chromatin interactions.

Extended Data Fig. 10 Stepwise selection for agronomic traits during rapeseed breeding.

a, Allelic distributions of genes for plant growth and circadian rhythm. b, Allelic distributions of genes involved in plant architecture and yield. c, The spectrum of allele frequencies at the causal polymorphisms in genes involved in seed quality. EU50, EU1950&70 s; EU80, EU1980&90 s; CN50, CN1950&70 s; CN80, CN1980&90 s; CN00, CN2000&10 s. PH, plant height; BH, branch height; YP, yield per plant; SP, seeds per pod. GSL, glucosinolate; SOC, seed oil content.

Supplementary information

Supplementary Information

Supplementary Figs. 1–44, Tables 2–4, 8, 13–15, 18, 22 and 24 and captions for Tables 1, 5–7, 9–12, 16, 17, 19–21 and 23.

Reporting Summary

Supplementary Tables

Supplementary Tables: 1, Summary of 418 accessions for genome resequencing in this study; 5, Selective sweeps among the three ecotypes of semiwinter versus winter and spring versus winter; 6, Selective sweeps among different breeding eras in Europe and China; 7, Summary of QTL and genes for PA, FT and PY that overlap with selective sweeps; 9, Different environments for the 56 traits of rapeseed phenotyping in this study; 10, Summary of quantitative traits phenotyped in six environments; 11, Genome-wide association signals of agronomics traits by SNP-GWAS; 12, Genome-wide association signals of agronomics traits by InDel-GWAS; 16, Summary of the InDels from exons overlapped with GWAS loci identified in this study; 17, Summary of the haplotypes of candidate genes identified by SNP-GWAS for different agronomic traits; 19, Link loci across 17 traits based on the pairwise LD value in rapeseed; 20, Characterization of large interchromosomal translocations between 418 B. napus and ‘Darmor-bzh' reference genomes; 21, The common loci between PA and PY-related traits identified in rapeseed; 23, Summary of rapeseed accessions used for qRT–PCR of different traits in this study

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Hu, J., Chen, B., Zhao, J. et al. Genomic selection and genetic architecture of agronomic traits during modern rapeseed breeding. Nat Genet 54, 694–704 (2022). https://doi.org/10.1038/s41588-022-01055-6

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