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Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication

Abstract

Comparative population genomics offers an excellent opportunity for unraveling the genetic history of crop domestication. Upland cotton (Gossypium hirsutum) has long been an important economic crop, but a genome-wide and evolutionary understanding of the effects of human selection is lacking. Here, we describe a variation map for 352 wild and domesticated cotton accessions. We scanned 93 domestication sweeps occupying 74 Mb of the A subgenome and 104 Mb of the D subgenome, and identified 19 candidate loci for fiber-quality-related traits through a genome-wide association study. We provide evidence showing asymmetric subgenome domestication for directional selection of long fibers. Global analyses of DNase I–hypersensitive sites and 3D genome architecture, linking functional variants to gene transcription, demonstrate the effects of domestication on cis-regulatory divergence. This study provides new insights into the evolution of gene organization, regulation and adaptation in a major crop, and should serve as a rich resource for genome-based cotton improvement.

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Figure 1: Geographic distribution and population diversity of Upland cotton accessions.
Figure 2: Genome-wide screening of domestication sweeps and GWAS on fiber-quality-related traits.
Figure 3: Asymmetric selection signals between the A subgenome (At) and the D subgenome (Dt).
Figure 4: Characterization of cotton DNase I–hypersensitive sites (DHSs) and detection of selected DHSs during domestication.
Figure 5: Characterization of the cotton chromatin interactome.

Accession codes

Primary accessions

Sequence Read Archive

Referenced accessions

Sequence Read Archive

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Acknowledgements

We thank T. Zhang (Nanjing Agricultural University) for releasing resequencing data of wild cotton accessions. This work was supported by funding from the National Natural Science Foundation of China (31230056) to X.Z. and the National Natural Science Foundation of China (31201251) to D.Y.

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Authors and Affiliations

Authors

Contributions

X. Zhang, L.T. and M.W. conceived and designed the project. P.W., M.L., Q.Y., Z.Y., X. Zhou, M.W. and X.N. performed the experiments. M.W., P.W. and Q.Z. developed libraries and performed sequencing. M.W., C.S., J.L., L. Zhang, K.G., Y.M., Z. Li, C.H. and D.Y. analyzed the data. Z. Lin, L.T., S.J., L. Zhu, X.Y. and L.M. collected materials and managed sequencing. M.W. wrote the manuscript draft, which was revised by K.L. and X. Zhang.

Corresponding authors

Correspondence to Keith Lindsey or Xianlong Zhang.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Lengths of small insertions and deletions in different genomic regions.

All identified indels are categorized into intergenic, intron and exon regions. For each group, the percentage of insertions or deletions with lengths below 10 bp is compared with the total indels.

Supplementary Figure 2 Population structure analysis with Structure.

Analysis with Structure1. Each color represents one subpopulation. Each vertical bar represents one cotton accession. When K=2, Chinese cottons were separated. When K=3, cottons from America, Brazil, and India were separated from wild cotton accessions.

Supplementary Figure 3 Genetic diversity and population divergence at the subgenomic level among three cotton groups.

(a) Genetic diversity and population divergence in the At subgenome. (b) Genetic diversity and population divergence in the Dt subgenome. For each group, nucleotide diversity (π) is shown inside the circle. Population divergence (FST) between two groups is shown on each line.

Supplementary Figure 4 Decay of linkage disequilibrium (LD) in the At and Dt subgenomes.

(a) Decay of LD for the At subgenome in each group. (b) Decay of LD for the Dt subgenome in each group. LD was calculated in 1 Mb distances. In the Wild group, the LD extent was estimated to be 92 kb (r2 = 0.16) in the At and 64 kb (r2 = 0.15) in the Dt. In the ABI group, the LD extent was estimated to be 214 kb (r2 = 0.21) in the At and 138 kb (r2 = 0.24) in the Dt. In the Chinese group, the LD extent was estimated to be 310 kb (r2 = 0.24) in the At and 270 kb (r2 = 0.25) in the Dt.

Supplementary Figure 5 Heat map showing genes differentially expressed between wild and domesticated cotton accessions.

Expression levels of genes between five cultivated (TM-1, Maxxa, CascotL-7, CRB252 and Coker315) and four wild (TX2090, TX2094, TX2095 and TX665)2 cotton accessions were compared. A total of 30 genes under domestication sweeps are shown, and which are known to be important for fiber development.

Supplementary Figure 6 Asymmetric subgenome selection signals in each ancestral state.

Each ancestral state was reconstructed using homoeologous gene pairs between the At and Dt. The upper track shows selection signals in the At and the lower track shows selection signals in the Dt. Some important genes with selection signals are indicated in red, and the expression levels of these genes are shown in Supplementary Table 14. The horizontal dashed line shows the cutoff of 4.8 (πwc). The ancestral state 3 is shown in Fig. 3c.

Supplementary Figure 7 RNA-seq analysis of 50 cotton accessions.

(a) Clustering of the wild and cultivated cottons. Cotton accessions are represented by dots in four different colors respectively. The wild and cultivated accessions are each grouped with grey circles. (b) Expression breadth of genes. High Jensen–Shannon (JS) scores3 indicate that genes are highly expressed in one or a few accessions, indicating that these genes exhibit wide variation in expression level. This analysis shows that genes in wild cottons exhibit a wider variation in expression than do cultivated cottons. Abbreviations representing cottons from different cultivation regions in China were the same as those in Fig. 1c.

Supplementary Figure 8 DNase I digestion of cotton nuclei.

M, marker. 1, 4°C treatment without digestion. 2, 37°C treatment without digestion. 3-10, DNase I digestion at 37°C with different enzyme dose at 0.5U, 1U, 2U, 3U, 4U, 8U, 10U, 16U, respectively. The digestion time is 10 min.

Supplementary Figure 9 Chromosomal landscape of DNase I–hypersensitive sites (DHSs) and chromatin-modification marks.

(a) TE content. Regions with high TE content are represented by the dark purple bands. (b) Gene density. (c) Enrichment for H3K4me1 modification. (d) Enrichment for H3K4me3 modification. (e) Enrichment for H3K27me3 modification. (f) Enrichment for H3K9me2 modification. (g) Number of DHSs in cotton leaves. (h) Number of DHSs in cotton fibers. For tracks b-h, high column bars show high enrichment of chromatin modification marks or large numbers of DHSs in chromosomal regions. For the circos plot, each chromosome was divided into 1 Mb windows sliding 200 kb.

Supplementary Figure 10 Patterns of chromatin-modification marks in genic and TE regions.

(a) Enrichment of chromatin modification marks in genic regions. (b) Enrichment of chromatin modification marks in short TEs (<500 bp). (c) Enrichment of chromatin modification marks in long TEs (>4 kb). The chromatin modification level was normalized by Input DNA sequencing data. For each analysis, the upstream and downstream 2 kb sequences were divided into 100 bins of 20 bp. Gene and TE bodies were divided into 100 bins of equal lengths.

Supplementary Figure 11 Clustering and ordering contigs of G. hirsutum with LACHESIS.

(a) The results of clustering of simulated contigs in the At subgenome of G. hirsutum. (b) The results of clustering of simulated contigs in the Dt subgenome of G. hirsutum. In this analysis, we split the TM-1 genome into 100 kb simulated contigs and mapped Hi-C clean reads to them. The LACHESIS software4 was used to cluster and order these contigs. The derived contig groups were compared with chromosome assemblies in the reference genome of TM-15. Discrete dots show putative genome assembly errors.

Supplementary Figure 12 Global chromatin interaction in the At and Dt subgenomes.

Chromatin interaction for the At subgenome is indicated in the upper right triangular matrix. Chromatin interaction for the Dt subgenome is indicated in the lower left triangular matrix. The chromatin interaction maps are visualized at a 200-kb resolution. Strong contact is represented in red and weak contact in white.

Supplementary Figure 13 Patterns of chromatin-modification marks in topologically associated domain–like (TAD-like) and boundary-like regions.

(a) Enrichment of chromatin modification marks in TAD-like regions. (b) Enrichment of chromatin modification marks in boundary-like regions. For each modification mark, the enrichment level was normalized by Input DNA sequencing data.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–13 and Supplementary Tables 1–6, 8, 11, 17, 18, 22 and 23 (PDF 3191 kb)

Supplementary Table 7

Identification of domestication sweeps and genes (XLSX 52 kb)

Supplementary Table 9

Summary of genes in QTL hotspot regions with selection signals (XLSX 41 kb)

Supplementary Table 10

Fiber quality-related traits used for GWAS (XLSX 75 kb)

Supplementary Table 12

Expression and annotation of candidate genes identified by GWAS (XLSX 18 kb)

Supplementary Table 13

Summary of homoeologous gene pairs with selection signals in at least one subgenome (XLSX 48 kb)

Supplementary Table 14

Summary of genes and expression with asymmetric subgenome selection signals (XLSX 22 kb)

Supplementary Table 15

Summary of promoter DHSs with domestication signals (XLSX 77 kb)

Supplementary Table 16

Summary of transcription factor binding motifs identified in TM-1 genome (XLSX 10608 kb)

Supplementary Table 19

Identification of topological domain-like and boundary-like regions in TM-1 genome (XLSX 99 kb)

Supplementary Table 20

Summary of promoter-centered chromatin interactions in TM-1 accession (XLSX 8214 kb)

Supplementary Table 21

Summary of enhancers under domestication selection (XLSX 98 kb)

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Wang, M., Tu, L., Lin, M. et al. Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat Genet 49, 579–587 (2017). https://doi.org/10.1038/ng.3807

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