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The near-complete genome assembly of hexaploid wild oat reveals its genome evolution and divergence with cultivated oats

Nature Plants volume 10, pages 2062–2078 (2024)Cite this article

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Abstract

Avena sterilis, the ancestral species of cultivated oats, is a valuable genetic resource for oat improvement. Here we generated a near-complete 10.99 Gb A. sterilis genome and a high-quality 10.89 Gb cultivated oat genome. Genome evolution analysis revealed the centromeres dynamic and structural variations landscape associated with domestication between wild and cultivated oats. Population genetic analysis of 117 wild and cultivated oat accessions worldwide detected many candidate genes associated with important agronomic traits for oat domestication and improvement. Remarkably, a large fragment duplication from chromosomes 4A to 4D harbouring many agronomically important genes was detected during oat domestication and was fixed in almost all cultivated oats from around the world. The genes in the duplication region from 4A showed significantly higher expression levels and lower methylation levels than the orthologous genes located on 4D in A. sterilis. This study provides valuable resources for evolutionary and functional genomics and genetic improvement of oat.

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Fig. 1: Phenotype, assembly pipeline and genomic landscape of A. sterilis.
Fig. 2: Characteristics of the centromeric regions in the oat genome.
Fig. 3: Phylogenetic variations and SVs in wild and cultivated oat.
Fig. 4: Population structure and selective sweep analyses of wild and cultivated oats.
Fig. 5: Large-fragment duplication from chromosome 4A to 4D.
Fig. 6: Gene function, expression and methylation in the duplication region.

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Data availability

All PacBio sequence data, ONT ultra-long sequence data, transcriptome data, resequencing data and Hi-C data in this study have been deposited in the Chinese National Genomics Data Center (https://bigd.big.ac.cn/) under the BioProject accession number PRJCA023350. The final genome assemblies were also submitted to the Chinese National Genomics Data Center under the accession number GWHERDU00000000. Source data are presented within this article in supplementary table.

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Acknowledgements

We sincerely thank Y. Fan at the School of Food and Biological Engineering, Chengdu University, for sharing with us wild oat accessions. We also thank F. Han, Y. Liu and Q. Liu at the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, for kindly providing CENH3 antibody and helping to perform the ChIP experiments. This work was supported by the Young Elite Scientists Sponsorship Program by Chinese Association for Science and Technology (grant number YESS20210080 to H.D.), the National Natural Science Foundation of China (grant number 32100500 to H.D.), the Natural Science Foundation of Hebei Province (grant numbers C2021201048 and C2023201074 to H.D.), the Interdisciplinary Research Program of Natural Science of Hebei University (grant number 513201422004 to H.D.) and The Excellent Youth Research Innovation Team of Hebei University (QNTD202401 to Q.H.) and was funded by Science and Technology Project of Hebei Education Department (QN2024271 to Q.H.).

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  1. These authors contributed equally: Qiang He, Wei Li, Yuqing Miao, Yu Wang.

Authors and Affiliations

  1. College of Life Sciences, Institute of Life Science and Green Development, Hebei University, Baoding, China

    Qiang He, Wei Li, Yuqing Miao, Yu Wang, Ningkun Liu, Jianan Liu, Tao Li, Yao Xiao, Hongyu Zhang, Yaru Wang, Hanfei Liang, Yange Yun, Shuhui Wang, Qingbin Sun, Zhizhong Gong & Huilong Du

  2. Hebei Basic Science Center for Biotic Interaction, Hebei University, Baoding, China

    Qiang He, Wei Li, Ningkun Liu, Shuhui Wang, Qingbin Sun, Zhizhong Gong & Huilong Du

  3. Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Hongru Wang

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Contributions

H.D. conceived and supervised the project; Q.H. and H.D. wrote the paper; Y.M. sequenced and processed the raw data; Q.H., Yu Wang and Y.M. assembled and annotated the genome; Q.H. and Yu Wang performed the centromere analysis. Q.H., Y.M., W.L. and Y.X. performed the phylogenetic and genome evolution analysis; Q.H. and H.Z. conducted the transcriptome analysis; Q.H., Y.M. and Yaru Wang conducted pan-genome analyses. Q.H., J.L., H.D., W.L., H.L. and Yu Wang performed population analyses. T.L., N.L., S.W. and Q.S. conceived of and designed the experiments. N.L. and Y.Y. conducted the FISH validation of chromosomal segment duplication. H.W. revised the manuscript. Z.G. offered invaluable guidance.

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Correspondence to Huilong Du.

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Nature Plants thanks Jeff Maughan, Klaus Mayer and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Genome assembly for Avena sterilis.

a, Hi-C chromatin interaction map of A. sterilis assembly. b, Principal component analysis (PCA) of differential k-mers from the 21 chromosomes in A. sterilis. Points indicate chromosomes. c, Sequencing coverage and assembly validation of the A. sterilis genome. Uniform whole-genome coverage of mapped HiFi, ONT, Hi-C, and Illumina reads is shown. Black triangle represents the position of gap in the genome. d, BUSCO completeness assessment for genomics data of A. sterilis, Marvellous and Sanfensan. e, LTR Assembly Index (LAI) score for each chromosome of A. sterilis (Aste), Marvellous and Sanfensan. A, C and D subgenome was colored in blue, green and purple, respectively. f, The quality value (QV) score of published T2T genomes. The number on histograms represent genome size.

Extended Data Fig. 2 Identification of A. sterilis centromere.

The centromere region was determined based on Chip-seq peak, gene density, LTR density, and k-mer frequency with 10 Mb window.

Extended Data Fig. 3 Analysis of centromere composition.

a, Comparison of the proportion of LTR‐RT family for the centromeres and non‐centromeres region in OT3098 and Sang genomes. b, Comparison of the insertion time of LTR‐RT family for the centromeres and non‐centromeres region in OT3098 and Sang genomes. Significance levels are computed from two-sided Wilcoxon tests. c, Proportion of LTR-RT family in centromere regions of different subgenome in OT3098 and Sang. d, Proportion of LTR-RT family in centromere regions of different subgenome in Avena eriantha (CC) and Avena insularis (CCDD) oats. e, Copy of Cen46 and Cen55 repeats units in C subgenome of A. eriantha and A. insularis oats.

Extended Data Fig. 4 Gene family and subgenome differentiation.

a, Venn diagram showing the numbers of common and unique gene families identified in the subgenomes of three oat genomes. Aste: A. sterilis. b-c, KEGG enrichment analysis of specific genes in three subgenomes and the expanded genes in the A. sterilis genome. d, Venn diagram showing the numbers of common and unique gene families identified in Pan-A, Pan-C and Pan-D of hexaploid oat. e, GO term enrichment analysis for specific genes in Pan-A, Pan-C, and Pan-D of hexaploid oat. f, Comparison of Ks values between subgenomes in A. sterilis genome. Significance levels are computed from two-sided Wilcoxon tests. g, Gene expression pattern in the A, C, and D subgenome across three tissues in A. sterilis genome. h, Gene expression pattern across different subgenomes in three tissues, using a window of 10 collinear genes in A. sterilis genome. The horizontal axis represents the number of windows based on the A subgenome as a reference.

Extended Data Fig. 5 Identification and verification of structural variation.

a, Synteny and rearrangement plot for six oat species, including three hexaploid cultivated oat, A. sterilis, A. longiglumis (AA) and A. insularis (CCDD). b, Verification of SVs. The short-read data were used to validate the borders of deletions randomly selected between Marvellous and A. sterilis genome. c, Schematic diagrams of the distribution of inversion between Marvellous and A. sterilis geome (x-axis: A. sterilis, y-axis: Marvellous). Red box represented the inverted segments relative to A. sterilis. d, Illustration of inversion identified between Marvellous and A. sterilis genome by Hi-C contact map. Chromatin interaction heatmap revealed inversion signals appearing after manual flipping. These maps supported the inversions in chromosome 1C, 2C, 3A, 3C and 4C. e, The validation of inversion borders by PCR amplification. This experiment was repeated independently at least three times with similar results.

Extended Data Fig. 6 Analysis of specific LTR-RTs families.

a, Cluster analysis of transposable element (TE) families in three oat genomes. The pie chart represents the proportion of PAVs overlapped with repeat and non-repeat regions. b, The number and insertion time of specific LTR-RTs families in three oat genomes. c, GO term enrichment analysis of genes affected by specific TEs in the A. sterilis genome. d, Gene structures and expression of homologous SAM-MT genes (AVESA.00702a.r1.1Ag0146002, AVESA.00401a.r1.1Ag0188833, AVESA.00022a.r1.1A0151681, and AVESA.00010b.r1.1Ag1357780) in four oat genomes, comprising A. sterilis, Marvellous, Sanfensan, and Sang.

Extended Data Fig. 7 Genetic diversity of wild and cultivated oats.

a, Principal component analysis (PCA) for 117 oat accessions. b, Nucleotide diversity (π) and population divergence (FST) of G1, G2 and G3 groups. The value in each circle represents an estimation of nucleotide diversity for each group, and values on each line indicate pairwise population divergence. c, The linkage disequilibrium (LD) decay analysis for G1, G2 and G3 groups. d-e, GO and KEGG enrichment analysis of genes in selective sweeps region between wild and cultivated group. f, Signals of artificial selection in the OsCLP1 gene related to shattering. Scale bar, 10 cm. Black dashed line is the threshold of the top 5% π ratio and Fst between wild and cultivated oat. g, Gene structure, haplotype, selective signature and expression of OsCLP1 gene between wild and cultivated oat. qRT-PCR was repeated independently at least three times with similar results. Significance levels are computed from two-sided Wilcoxon tests. h, Signals of artificial selection in the An1 gene related to awn length. Scale bar, 1 cm. Black dashed line is the threshold of the top 5% π ratio and Fst between wild and cultivated oat. i, Gene structure, haplotype, selective signature and expression for An1 gene between wild and cultivated oat. qRT-PCR was repeated independently at least three times with similar results. Significance levels are computed from two-sided Wilcoxon tests.

Extended Data Fig. 8 Identification of a candidate locus associated with oat improvement.

a, Manhattan plots showing selective sweep regions based on FST values (G2 vs G3). Candidate locus was marker with gray. b, Different genotypes in candidate locus are represented by different colors. c, Pairwise linkage disequilibrium heatmap (top) of the candidate locus. This locus exhibits high degree of synteny with a previously reported NOH1 locus on rice chromosome 1. d, Top is haplotype frequency of AsTRP1 (AVESA.00022a.r1.4Dg0170063) in Marvellous between G2 and G3 group. Down is reads depth distributions of an SV region in AsTRP1 gene.

Extended Data Fig. 9 The large fragment duplication from 4A to 4D.

a, The Illumina read coverage of the chromosome 4D. Ains: A. insularis. b, The gene collinear between the start of chromosome 4A and 4D. c, Hi-C contact map showing a translocation event occurred from 4A to 4D and this fragment exist two copies. d, FISH confirms the duplication segment in cultivated oat, as observed in cells at the metaphase of mitosis. This experiment was repeated independently at least three times with similar results. e, Differential transcript expression patterns of genes located on start (1–28 Mb) of chromosome 4A and 4D in A. sterilis. f, Expression of genes in chromosome 4A and 4D in A. sterilis.

Extended Data Table 1 Genome assembly and annotation statistics
Full size table

Supplementary information

Supplementary Information

Supplementary Figs. 1–7 and Tables 1–17.

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He, Q., Li, W., Miao, Y. et al. The near-complete genome assembly of hexaploid wild oat reveals its genome evolution and divergence with cultivated oats. Nat. Plants 10, 2062–2078 (2024). https://doi.org/10.1038/s41477-024-01866-x

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