Genome-wide selection and genetic improvement during modern maize breeding

Abstract

Since the development of single-hybrid maize breeding programs in the first half of the twentieth century1, maize yields have increased over sevenfold, and much of that increase can be attributed to tolerance of increased planting density2,3,4. To explore the genomic basis underlying the dramatic yield increase in maize, we conducted a comprehensive analysis of the genomic and phenotypic changes associated with modern maize breeding through chronological sampling of 350 elite inbred lines representing multiple eras of germplasm from both China and the United States. We document several convergent phenotypic changes in both countries. Using genome-wide association and selection scan methods, we identify 160 loci underlying adaptive agronomic phenotypes and more than 1,800 genomic regions representing the targets of selection during modern breeding. This work demonstrates the use of the breeding-era approach for identifying breeding signatures and lays the foundation for future genomics-enabled maize breeding.

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Fig. 1: Morphological trait improvement during modern maize breeding in the United States and China.
Fig. 2: Nucleotide diversity, LD decay and population structure of 350 maize inbred lines.
Fig. 3: GWAS identification of candidate genes for variation of LA, DTA and TBN.
Fig. 4: Profiling of the selective sweeps during modern maize breeding.
Fig. 5: Validation of two candidate genes associated with EH and TBN.

Data availability

DNA-sequencing reads for all maize lines were deposited in the NCBI with the accession code of PRJNA609577 and BIGD (BIG Data Center in Beijing institute of Genomics) with the accession code of CRA002372. All phenotype data of 350 inbred maize lines are included in Supplementary Table 1. Source data for Figs. 1–3 and 5 and Extended Data Figs. 1, 2 and 8–10 are presented with the paper. All other reasonable requests for data and research materials are available via contacting the corresponding authors.

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Acknowledgements

The work was supported by National Key R&D Program of China (grant no. 2016YFD0101001), the Major Program of Guangdong Basic and Applied Research (grant no. 2019B030302006), National Transgenic Science and Technology Program (grant no. 2019ZX08010003-002-004), National Natural Science Foundation of China (grant nos. 31801377, 31430008 and 31921004), the Agricultural Science and Technology Innovation Program, and Jilin Provincial Science and Technology Key Project (grant no. 20170204007NY).

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Authors

Contributions

B.W. and Haiyang Wang conceived and designed the research. B.W., J.L., Z.M., T.W., Y.L., Xinhai Li, Y.C., Y.X. and Hai Wang participated in germplasm collection. B.W., B.Z., G.S., X.M., Q.L., Z.Z., D.K., H. Wei and C.C. performed phenotypic measurement. Z.L., B.W., Xin Li, M.H., J.R.-I. and H.H. analyzed the data. Y.Z. performed plasmid construction and genetic transformation. B.W., G.W., H. Wu and R.S. characterized the CRISPR–Cas9 mutants. B.W. conducted gene expression analysis. B.W., Z.L., Xin Li, M.H., J.R.-I. and H.H. wrote the manuscript. Haiyang Wang, M.H. and J.R.-I. revised the manuscript.

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Correspondence to Hang He or Haiyang Wang.

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Extended data

Extended Data Fig. 1 Changes in morphological traits during maize breeding in the United States and China.

a, Changes of 12 morphological traits during modern maize breeding in the United States and China. Different letters above the boxes indicate significant difference (p < 0.05, Bonferroni correction) in pairwise comparison. Note that days to anthesis (DTA, p = 0.015) and ear height (EH, p = 0.007) are significantly different between Public-US and Ex-PVP inbred lines as revealed by two-tailed t-test. b, Changes of four morphological traits in four subgroups (SS, NSS, HZS and Mixed) during modern maize breeding in the United States and China. Subgroups with at least 10 inbred lines in each US or Chinese era were used in the analysis. The x-axis represents the eras with prefixed sub-group names. The * or ** above the SS sub-group indicate the t-test results at significant level of 0.05 and 0.01, respectively. Source data

Extended Data Fig. 2 GWAS identification of the candidate genes for Cob Color, Kernel Color, and days to anthesis (DTA).

ac, Manhattan plot for Cob Color (a), Kernel Color (b) and DTA (c). d, Pericarp color1 (P1) is associated with cob color. The peak SNP is located in the tandem repeat region of P1. e, f, Yellow endosperm1 (Y1) and White Cap1 (WC1) are associated with kernel color. The peak SNP of GWAS signal on chromosome 6 is located in the genic region of Y1. The second top SNP of GWAS signal on chromosome 9 is located in the genic region of WC1. g,Vegetative to Generative Transition1 (VGT1) is associated with DTA. The second top SNP of GWAS signal is located within the VGT1 region. Source data

Extended Data Fig. 3 Accumulation of favorable alleles contributes to improvement of four selected morphological traits for adaptation to high-density planting.

ad, Favorable allele frequency changing profiles of relative ear height (EP, a), upper leaf angle (LAU, b), tassel branch number (TBN, c) and days to silking (DTS, d) at QTN loci from GWAS loci during the US and Chinese inbred lines breeding process. Red indicates an increase, whereas blue indicates a decrease in the frequency of a favorable allele during breeding. Each row represents a GWAS locus, with cyan and gray colors (in the first column) mark rows representing GWAS loci obtained by the cutoff of p < 1e-6 and 1e-5, respectively. Later breeding stages in United States and China were compared to Public-US and CN1960&70s respectively. eh, Pie plot for the numbers of GWAS loci with favorable allele frequency increased during the US and Chinese inbred lines breeding process. GWAS loci with favorable allele frequency increased during both CN1960&70s-CN1980&90s and CN1960&70s-CN2000&10s comparisons were included. The trait name and corresponding total GWAS loci number (p < 1e-5) are shown below the pie plot.

Extended Data Fig. 4 Representative selected genes related to biotic stress responses.

Each plot group represents the results for a selected representative candidate gene, which includes XP-CLR plot (left), gene annotation (above the pie plot), nonsynonymous SNP frequency changes during the corresponding breeding process (pie plot) and nonsynonymous SNP information (below the pie plot). For XP-CLR plots, the XP-CLR scores for whole data panel and subgroups are plotted above and under the zero, respectively. Red arrows along the x-axis indicate the position of the candidate genes. The blue and red horizontal dashed lines above the zero represent the 80th quantile and genome-wide significant cutoff, respectively, for XP-CLR scores in whole data panel. The horizontal dashed lines under the zero represent the 80th quantile for XP-CLR scores in subgroups. Arabidopsis homologs were used for annotation of the candidate genes. The p-value of fisher’s exact test for allele frequency changes are shown above the pie plot. The nonsynonymous SNP information includes SNP location, variation from alleles in B73 to others, and corresponding amino acid changes (separated by comma).

Extended Data Fig. 5 Representative selected genes related to abiotic stress responses.

Each plot group represents the results for a selected representative candidate gene, which includes XP-CLR plot (left), gene annotation (above the pie plot), nonsynonymous SNP frequency changes during the corresponding breeding process (pie plot) and nonsynonymous SNP information (below the pie plot). For XP-CLR plots, the XP-CLR scores for whole data panel and subgroups are plotted above and under the zero, respectively. Red arrows along the x-axis indicate the position of the candidate genes. The blue and red horizontal dashed lines above the zero represent the 80th quantile and genome-wide significant cutoff, respectively, for XP-CLR scores in whole data panel. The horizontal dashed lines under the zero represent the 80th quantile for XP-CLR scores in subgroups. Arabidopsis homologs were used for annotation of the candidate genes. The p-value of fisher’s exact test for allele frequency changes are shown above the pie plot. The nonsynonymous SNP information includes SNP location, variation from alleles in B73 to others, and corresponding amino acid changes (separated by comma).

Extended Data Fig. 6 Representative selected genes related to light signaling, flowering time regulation, biosynthesis or signaling of auxin.

Each plot group represents the results for a selected representative candidate gene, which includes XP-CLR plot (left), gene annotation (above the pie plot), nonsynonymous SNP frequency changes during the corresponding breeding process (pie plot) and nonsynonymous SNP information (below the pie plot). For XP-CLR plots, the XP-CLR scores for whole data panel and subgroups are plotted above and under the zero, respectively. Red arrows along the x-axis indicate the position of the candidate genes. The blue and red horizontal dashed lines above the zero represent the 80th quantile and genome-wide significant cutoff, respectively, for XP-CLR scores in whole data panel. The horizontal dashed lines under the zero represent the 80th quantile for XP-CLR scores in subgroups. Arabidopsis homologs were used for annotation of the candidate genes. The p-value of fisher’s exact test for allele frequency changes are shown above the pie plot. The nonsynonymous SNP information includes SNP location, variation from alleles in B73 to others and corresponding amino acid changes (separated by comma).

Extended Data Fig. 7 Representative selected genes related to biosynthesis or signaling of other phytohormones.

Each plot group represents the results for a selected representative candidate gene, which includes XP-CLR plot (left), gene annotation (above the pie plot), nonsynonymous SNP frequency changes during the corresponding breeding process (pie plot) and nonsynonymous SNP information (below the pie plot). For XP-CLR plots, the XP-CLR scores for whole data panel and subgroups are plotted above and under the zero, respectively. Red arrows along the x-axis indicate the position of the candidate genes. The blue and red horizontal dashed lines above the zero represent the 80th quantile and genome-wide significant cutoff, respectively, for XP-CLR scores in whole data panel. The horizontal dashed lines under the zero represent the 80th quantile for XP-CLR scores in subgroups. Arabidopsis homologs were used for annotation of the candidate genes. The p-value of fisher’s exact test for allele frequency changes are shown above the pie plot. The nonsynonymous SNP information includes SNP location, variation from alleles in B73 to others and corresponding amino acid changes (separated by comma).

Extended Data Fig. 8 Two detected GWAS loci for relative ear height (EP).

a, b, XP-CLR (upper), Manhattan plot (middle) and LD heat map (lower) for the detected EP loci on 7.07 Mb of chromosome 7 (a), and 25.43 Mb of chromosome 1 (b). The candidate genes GRMZM2G398996 (a) is marked with red arrows. The structure and top SNP information of the candidate gene are shown below the LD heat map plots. To verify that the selection region on chromosome 1 might be resulted from the extended haplotype of the locus, the XP-EHH score was also investigated and shown as red curve in the Manhattan plot. Source data

Extended Data Fig. 9 Phenotype analyses of CRISPR/Cas9 mutations for ZmPIF3.3 and TSH4.

a, Sequences of ZmPIF3.3 target regions in wild type, Zmpif3.3-2 and Zmpif3.3-3 CRISPR/Cas9 knockout mutants. The target sites and protospacer-adjacent motifs (PAM) are shown as underscored letters and blue letters respectively. The gap lengths of sequences are shown above the wild type sequences. b, Height profile of wild type, Zmpif3.3-2 and Zmpif3.3-3 mutant plants. Bar, 15 cm. c, d, Statistics of plant height (c) and ear height (d) of wild type, Zmpif3.3-2 and Zmpif3.3-3 mutant plants. e, Sequences of TSH4 target regions in wild type and tsh4 CRISPR/Cas9 knockout mutants. f, g, Tassel profile (f) and TBN statistics (g) of wild type and tsh4-1 CRISPR-knockout mutants. Bar, 5 cm. h, i, Tassel profile (h) and TBN statistics (i) of wild type and tsh4-2 CRISPR-knockout mutants. Bar, 5 cm. The p-values of two-tailed t-tests are shown above the plots. Error bars indicate ±s.d. Source data

Extended Data Fig. 10 GWAS identification of TSH4 as a candidate gene for tassel branch number (TBN) variation.

a, Manhattan plot (upper left) and LD heat map (lower left) for GWAS signal TBN_7_133305039. SNP and indel based association analysis results are shown as blue and orange dots in the Manhattan plot, respectively. Peak markers and putative causal polymorphisms are circled and their positions in LD heat map are indicated by red lines. The candidate gene position in Manhattan plot is showed as red arrows. The significantly associated SNP (chr7_133305039, P = 6.83 × 10–8) and indel (chr7_133209283_C/CT, 1-bp deletion, P = 1.86 × 10–5) were strongly correlated (r2 = 0.53). b, Candidate gene structure and polymorphisms of chr7_133209283_C/CT. c, d, Phenotype of different haplotypes (c, box plot) and haplotype frequency changes during breeding (d, bar plot), for the association signal of chr7_133209283_C/CT. Source data

Supplementary information

Supplementary Information

Supplementary Note, Figs. 1 and 2, and Tables 2–5, 10, 12, 18 and 19

Reporting Summary

Supplementary Tables

Supplementary Tables 1, 6, 7, 8, 9, 11 and 13–17

Source data

Source Data Fig. 1

Phenotype data of LAU_BLUP, TBN_BLUP and EP_BLUP for 350 Inbred Lines.

Source Data Fig. 2

Source Data for Fig. 2 individual items.

Source Data Fig. 3

Source Data for Fig. 3 individual items.

Source Data Fig. 5

Source Data for Fig. 5 individual items.

Source Data Extended Data Fig. 1

Phenotype data of 12 traits for 350 Inbred Lines.

Source Data Extended Data Fig. 2

Phenotype data and GWAS results for traits of DTA_LF2016, Cob_color and Kernel_color.

Source Data Extended Data Fig. 8

Source data for Extended Data Fig. 8 individual items.

Source Data Extended Data Fig. 9

Phenotype data for WT and CRISPR mutants.

Source Data Extended Data Fig. 10

GWAS results and haplotype profile around TSH4.

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Wang, B., Lin, Z., Li, X. et al. Genome-wide selection and genetic improvement during modern maize breeding. Nat Genet (2020). https://doi.org/10.1038/s41588-020-0616-3

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