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De novo genome assembly and analyses of 12 founder inbred lines provide insights into maize heterosis

Nature Genetics volume 55, pages 312–323 (2023)Cite this article

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An Author Correction to this article was published on 02 February 2023

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Abstract

Hybrid maize displays superior heterosis and contributes over 30% of total worldwide cereal production. However, the molecular mechanisms of heterosis remain obscure. Here we show that structural variants (SVs) between the parental lines have a predominant role underpinning maize heterosis. De novo assembly and analyses of 12 maize founder inbred lines (FILs) reveal abundant genetic variations among these FILs and, through expression quantitative trait loci and association analyses, we identify several SVs contributing to genomic and phenotypic differentiations of various heterotic groups. Using a set of 91 diallel-cross F1 hybrids, we found strong positive correlations between better-parent heterosis of the F1 hybrids and the numbers of SVs between the parental lines, providing concrete genomic support for a prevalent role of genetic complementation underlying heterosis. Further, we document evidence that SVs in both ZAR1 and ZmACO2 contribute to yield heterosis in an overdominance fashion. Our results should promote genomics-based breeding of hybrid maize.

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Fig. 1: Phylogenetic analysis of representative maize ILs used in modern maize breeding.
Fig. 2: Pan- and core-genome analyses of the 14 maize FILs.
Fig. 3: Global comparison of the 14 FIL genomes.
Fig. 4: Functional verification of Zm00001d006055.
Fig. 5: Functional verification of Zm00001d011140.
Fig. 6: Correlation analysis between better-parent heterosis (BPH) and different types of genetic variants between the parents of 91 diallel-cross F1s.
Fig. 7: Natural variations in ZmACO2 and ZAR1 contribute to heterosis.

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Data availability

All data sets reported in this study have been deposited in NCBI. The raw reads of 150-bp pair-end Illumina sequencing, PacBio SMRT sequencing, and RNA-seq (for gene annotation), sequences of genome assemblies have been deposited in the NCBI database under the BioProject accession PRJNA755430. The RNA-seq data of 131 inbred lines have been deposited in the NCBI database under the BioProject accession PRJNA783356. Source data are provided with this paper.

Code availability

The code for construction pseudomolecules is available at GitHub (https://github.com/JunpengShi/Maize_pseudomolecule_construction) and Zenodo (https://doi.org/10.5281/zenodo.7407607) (ref. 87).

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Acknowledgements

This work is supported by National Key R&D Program of China (grant 2021YFF1000301 to Haiyang Wang), National Natural Science Foundation of China (32022065 to B.W., 32130077 to Haiyang Wang, 31871639 to Y.C.), the Major Program of Guangdong Basic and Applied Research (2019B030302006 to Haiyang Wang), the Beijing Scholars Program (BSP041 to J.Z.) and the Agricultural Science and Technology Innovation Program of CAAS to B.W.

Author information

Author notes

  1. These authors contributed equally: Baobao Wang, Mei Hou, Junpeng Shi, Lixia Ku, Wei Song, Chunhui Li.

Authors and Affiliations

  1. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, China

    Baobao Wang, Mei Hou, Xin Li, Changyu Li, Binbin Zhao, Hua Xu, Zhijing Bai, Zhanchao Xia & Hai Wang

  2. Key Laboratory of Herbage and Endemic Crop Biology, Ministry of Education, Inner Mongolia University, Hohhot, China

    Mei Hou & Zhi Qi

  3. State Key Laboratory of Plant Physiology and Biochemistry & National Maize Improvement Center, Department of Plant Genetics and Breeding, China Agricultural University, Beijing, China

    Junpeng Shi & Jinsheng Lai

  4. College of Agronomy and National Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, China

    Lixia Ku, Wen Yao, Gege Hou & Yanhui Chen

  5. Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Maize Research Center, Beijing Academy of Agriculture & Forestry Sciences, Beijing, China

    Wei Song, Ruyang Zhang, Chunhui Li, Xuan Sun, Shuaishuai Wang & Jiuran Zhao

  6. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China

    Chunhui Li, Yu Li & Tianyu Wang

  7. National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, China

    Qiang Ning & Zuxin Zhang

  8. Guangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, China

    Dexin Kong, Hongbin Wei, Yifeng Jing, Zhouyan Dai, Hu Hailing Wang, Xinyu Zhu & Haiyang Wang

  9. Biomarker Technologies Corporation, Beijing, China

    He Dai, Xuming Li & Hongkun Zheng

  10. Institute of Systems Medicine, Chinese Academy of Medical Sciences & Peking Union Medical College, Suzhou, China

    Taijiao Jiang & Zhaoman Wan

  11. Guangzhou Laboratory, Guangzhou, China

    Taijiao Jiang

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  1. Baobao Wang
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Haiyang Wang, J.L., J.Z., Y.C. and B.W. conceived and designed the project. B.W., Haiyang Wang, J.L., J.Z. and Y.C. participated in FILs collection. W.S., X.S., S.W. and C.L. (BAAFS) performed the identity verification for the 12 FILs. L.K., W.S. and B.W. analyzed the pedigree of 14 FILs. Xin Li and J.S. constructed the pseudomolecules for 12 FILs. Xuming Li, H.D., H.Z. and M.H. conducted genome assembly and gene annotation for the 12 FILs. J.S. performed TE annotation. M.H., Xin Li and Changyu Li conducted genome quality assessments, synteny analysis, SNP, InDel, SV and PAV identification. B.W., B.Z., Hai Wang and Hongbin Wei collected samples for RNA-seq. Changyu Li conducted RNA-seq analysis. B.Z. conducted gene expression analysis of ZmLOX3. B.W., B.Z., H.X., Z.B. and Z.X. performed PCR genotyping of 350 temperate inbred lines. B.W. and B.Z. made the diallel-cross for the 14 FILs. B.W., R.Z., L.K., B.Z., D.K., Y.J., Z.D., H.H.W., X.Z., Z.Q., W.Y. and G.H. performed phenotypic measurement for the diallel-cross F1s. C.L. (CAAS), Y.L. and T.W. conducted molecular and phenotypic analyses of the Zm00001d006055 and Zm00001d011140 mutants. Q.N. and Z.Z. conducted heterotic analysis of ZmACO2 using the NILs. T.J. and Z.W. performed some of the statistical analyses. We thank Professor William Terzaghi (Wilkes University) for proofing the manuscript. Haiyang Wang, B.W. and M.H. wrote the manuscript.

Corresponding authors

Correspondence to Yanhui Chen, Jiuran Zhao, Jinsheng Lai or Haiyang Wang.

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The authors declare no competing interests.

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Nature Genetics thanks Georg Haberer and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer review reports are available.

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Extended data

Extended Data Fig. 1 Distribution profile of genes and three types of most abundant transposable elements (Gypsy, Copia and Helitron superfamilies) in the 14 FIL genomes.

The purple rectangles below each chromosome indicate positions of the centromeres.

Source data

Extended Data Fig. 2 Pan-gene distribution and global comparison profile of the syntenic blocks between B73 genome with the genomes of other 13 FILs.

a, Distribution profile of the Core- and Pan-genes in the B73_v4 genome. b, Profile of whole-genome alignment (WGA) of 13 FIL genomes against the B73_v4 genome. The purple rectangles below each plot of B73 chromosomes indicate positions of the centromeres. c, d, Length (c) and ratio (d) of syntenic sequences occupied the B73 genome for pan-WGA map.

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Extended Data Fig. 3 Profile of 12 high-confident mega-base SVs between B73 and the other 13 FILs.

a-l, Profile of synteny relationship for 12 high-confident mega-base SVs between B73 and the other 13 FILs. m-o, Synteny relationship of the 8 cross-validated mega-base SVs among the 14 FILs. The yellow segments represent sequence of Ns among the Contigs (gaps estimated based on the BioNano physical map), while the green segments (very rare here) represent sequence of Ns among the Scaffolds. The red segments represent the putative SVs between the paired FILs.

Extended Data Fig. 4 Structural variations of ZmCCT9, VGT1, ZCN8, KRN4, KNR6 and ZmGDIα in the 14 maize FIL genomes.

a, The 57 kb upstream region of ZmCCT9. b, The 2 kb conserved noncoding region of Vegetative to generative transition 1 (Vgt1). c, The promoter region of ZCN8. d, The ~60 kb downstream region of UNBRANCHED3 (UB3). e, The genomic region of KNR6. The trait value of kernel row number (KRN) or ear length (EL) are shown on the right. f, The resistance performance of maize rough dwarf disease (MRDD) for Xu178 and HuangC in normal or MRDD epidemic environments. Scale bar, 15 cm. g, QTL mapping for MRDD resistance using a recombinant inbred lines (RILs) population derived from Xu178 and HuangC. h, The genomic region of ZmGDIα. Each horizontal long bar represents genomic sequence of the FILs. The blank regions represent no difference among the FILs. The green, red, black, blue and orange vertical segments represent the A, T, G, C and missing type, respectively. The red box indicates position of the reported causal variant.

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Extended Data Fig. 5 Haplotype frequency profile of the known functional variations for ZmCCT9, VGT1, ZCN8, KRN4, KNR6, ZmGDIα and ZmTrxh in different heterotic groups.

These analyses were based on PCR-genotyping of 350 temperate inbred lines. Sample numbers are shown in brackets neighboring names of heterotic groups.

Source data

Extended Data Fig. 6 Phenotype variation profile among different heterotic groups.

For each box, the upper and lower boundaries represent the 25th and 75th percentile, respectively. The middle horizontal lines represent the median. The whiskers represent 1.5× the interquartile range. The dots beyond the whiskers represent outliers. The “compact letter display (CLD)” method is used to determine the multiple comparison results (conducted by the least significant difference method). Different letters above the boxes indicate significant differences (P < 0.05, Bonferroni correction) in a pairwise comparison. Sample numbers are shown in brackets on x axis. DTA: days to anthesis; KRN: kernel row number; EL: ear length; TBN: tassel branch number; EH: ear height; EP: relative ear height (ear height/plant height).

Source data

Extended Data Fig. 7 Two SVs in the promoter region and second intron regulate expression variation in ZmLOX3.

a, Association mapping identifies SV151 and SV363 as the SVs affecting ZmLOX3 expression level. The upper panel is the Manhattan plot; the lower panel is the LD heatmap. The y axis of Manhatten plot represents the −log10 p-value for candidate association analysis using the MLM method. b, Four haplotypes formed by SV151 and SV363 in 131 inbred lines. Hap-151/363 was excluded for further analysis due to its small sample size (n < 10). c, The relative expression level (qRT-PCR) of ZmLOX3 in ovules (prior to pollination) or kernels (5 days after pollination) of 12 FILs. Values shown are mean ± SD. d, Violin plot for ZmLOX3 expression levels (RNA-Seq) in inbred lines of Hap-0/363, Hap-0/0 and Hap-151/0 (n = number of inbred lines, which is shown in the parenthesis). For the violin plot, the white dot represents the median, the black box limits indicate the 25th and 75th percentiles, and the whiskers represent 1.5× the interquartile range. p-values for two-sided t-tests are shown. e, Frequency changes of Hap-0/363, Hap-0/0 and Hap-151/0 in 350 inbred lines of different breeding eras in the US and China. f, Frequency profile of Hap-0/363, Hap-0/0 and Hap-151/0 in different heterotic groups.

Source data

Extended Data Fig. 8 Correlation analysis between BPH performance and different kinds of SVs between the parents of 91 diallel-cross F1s.

(a-f) Correlation analysis between over parent heterosis of grain yield per plant (GYPP) and different kinds of SVs between the parents of 91 diallel-cross F1s. The p-values (p) and Spearman rank-based correlation coefficients (r) are shown on the top of each plot. The 7 registered varieties in China or the US are shown as colored points with corresponding names shown at the bottom.

Source data

Extended Data Fig. 9 Relationship between genetic variations and GYPP_BPH performance in 7 historically released varieties.

a, Comparison of the genetic variations between 7 historically released varieties and other F1s. The p-values (p) for two-sided t-test results are shown on the top of each plot. For each box plot, the upper and lower boundaries represent the 25th and 75th percentile, respectively. The middle horizontal lines represent the median. The whiskers represent 1.5× the interquartile range. The dots beyond the whiskers represent outliers. b, Correlation analysis between GYPP_BPH performance and different types of genetic variants between the parents of the seven registered varieties. The p-values (p) and Spearman rank-based correlation coefficients (r) are shown on the top of each plot.

Source data

Supplementary information

Supplementary Information

Supplementary Note and Fig. 1.

Reporting Summary

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Supplementary Tables

Supplementary Tables 1–21.

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Source Data Extended Data Fig. 1

Distribution profile of genes and three types of most abundant transposable elements (Gypsy, Copia and Helitron superfamilies) in the 14 FIL genomes.

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PCR-genotyping of 229 of the 350 temperate inbred lines.

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Phenotyping profile of the 350 inbred lines.

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GYPP_BPH performance and different kinds of SVs between the parents of the 91 diallel-cross F1s.

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Wang, B., Hou, M., Shi, J. et al. De novo genome assembly and analyses of 12 founder inbred lines provide insights into maize heterosis. Nat Genet 55, 312–323 (2023). https://doi.org/10.1038/s41588-022-01283-w

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