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Genomic analyses in cotton identify signatures of selection and loci associated with fiber quality and yield traits

Nature Genetics volume 49, pages 1089–1098 (2017)Cite this article

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Abstract

Upland cotton (Gossypium hirsutum) is the most important natural fiber crop in the world. The overall genetic diversity among cultivated species of cotton and the genetic changes that occurred during their improvement are poorly understood. Here we report a comprehensive genomic assessment of modern improved upland cotton based on the genome-wide resequencing of 318 landraces and modern improved cultivars or lines. We detected more associated loci for lint yield than for fiber quality, which suggests that lint yield has stronger selection signatures than other traits. We found that two ethylene-pathway-related genes were associated with increased lint yield in improved cultivars. We evaluated the population frequency of each elite allele in historically released cultivar groups and found that 54.8% of the elite genome-wide association study (GWAS) alleles detected were transferred from three founder landraces: Deltapine 15, Stoneville 2B and Uganda Mian. Our results provide a genomic basis for improving cotton cultivars and for further evolutionary analysis of polyploid crops.

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Figure 1: Formation and improvement of the allotetraploid cottons.
Figure 2: Phylogenetic relationships and genetic diversity of 318 cotton accessions.
Figure 3: GWAS for yield and identification of the candidate gene AIL6 on chromosome A02.
Figure 4: GWAS for yield and identification of the candidate gene EIL.
Figure 5: GWAS for fiber quality and identification of the candidate gene GhXI-K.
Figure 6: Identification of IBD regions in the cotton breeding pedigree.

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Acknowledgements

This work was financially supported in part by the NSFC (grant U1503284 to T.Z.), the National Key R&D Program for Crop Breeding in China (grant 2016YFD0100203 to X.D. and B.Z.), the Distinguished Discipline Support Program of Zhejiang University, the Priority Academic Program Development of Jiangsu Higher Education Institutions, the 111 project (grant B08025 to Nanjing Agricultural University) and the JCIC-MCP project (to Nanjing Agricultural University). We thank the National Medium-term Gene Bank of Cotton in the Institute of Cotton Research of the Chinese Academy of Agricultural Sciences (Henan, China) for providing some of the cotton germplasm resource seeds and permitting us to harvest the leaves of seven G. hirsutum races so we could isolate DNA for the present study.

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Author notes

  1. Lei Fang, Qiong Wang, Yan Hu, Yinhua Jia and Jiedan Chen: These authors contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Cotton Hybrid R&D Engineering Center (the Ministry of Education), Nanjing Agricultural University, Nanjing, China

    Lei Fang, Qiong Wang, Yan Hu, Jiedan Chen, Bingliang Liu, Zhiyuan Zhang, Xueying Guan, Shuqi Chen, Baoliang Zhou, Gaofu Mei, Caiping Cai, Xiefei Zhu, Wangzhen Guo & Tianzhen Zhang

  2. Agronomy Department, College of Agriculture and Biotechnology, Zhejiang University, Zhejiang, China

    Lei Fang, Yan Hu, Jiedan Chen, Zhiyuan Zhang, Xueying Guan & Tianzhen Zhang

  3. Institute of Cotton Research (ICR), Chinese Academy of Agricultural Sciences (CAAS), State Key Laboratory of Cotton Biology, Key Laboratory of Cotton Genetic Improvement, Ministry of Agriculture, Anyang, China

    Yinhua Jia, Junling Sun, Zhaoe Pan, Shoupu He, Wenfang Gong & Xiongming Du

  4. Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, China

    Songhua Xiao & Jianguang Liu

  5. Economic Crop Research Institute, Xinjiang Academy of Agricultural Science, Urumqi, China

    Weijun Shi & Jun Ma

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Contributions

T.Z. conceptualized the research program. T.Z. and X.D. designed the experiments and coordinated the project. T.Z., X.D., B.Z., Y.J., J.S., Z.P., S.H., S.X., W.S., W. Gong, J.L., J.M., X.Z. and W. Guo collected the 318 cotton samples and worked on the phenotype. Y.H., L.F., Q.W., J.C., B.L. and G.M. extracted the high-quality DNA. L.F., Y.H., S.C., C.C. and B.L. constructed DNA-sequencing libraries and carried out genome sequencing. L.F., Q.W., J.C., Y.H., Z.Z. and X.G. performed the genotyping and bioinformatics analyses. T.Z. and L.F. analyzed all of the data and wrote the manuscript. All authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Xiongming Du or Tianzhen Zhang.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 The pedigree information for American upland cotton breeding.

The integrated figure was modified from Fig. 1 to 10 in Calhoun, Bowman & May (1994). The accessions with blue color were collected and analyzed in our study.

Supplementary Figure 2 Phylogenetic tree of all resequenced accessions.

Neighbour-joining tree of all these accessions was constructed using the whole-genome SNPs, including outgroup, landrace and improved modern cultivars marked with light blue, red and dark blue lines, respectively. All these cultivars could be classified into three clades, including a special clade I, Stoneville 2B clade (subclade 1) and Deltapine 15 clade (subclade 2).

Supplementary Figure 3 Phylogenetic relationships of 318 cotton accessions.

(a) Principal component analysis of all cotton accessions using whole-genome SNP data. The outgroups were clustered together. Clade I mainly contained recently domesticated founders and from which developed cultivars such as Acala, Burling’s Mexican and the Maryland Green seed. Clade II included most of Upland cotton cultivars mainly derived from the landraces originated from the same ancestral resource. Subclade #x0049; included the American landraces Stoneville 2B (STV2B), Auburn 56 and Paymaster 54, and those modern cultivars developed from STV2B and were planted mainly in the Yellow river cotton growing area in China. Subclade I#x0049; contained the American landraces such as Deltapine 15 (DPL15), Lankart 57 and Dixie king, and the cultivars developed mainly from DPL15 and were planted in the Yellow river, Yangtze river and Northwest (Xinjiang) cotton growing areas in China. (b) Population structure of cotton accessions determined using STRUCTURE. When K was set to 4, the outgroup component was present. The components of clade #x0049; and clade #x0049;#x0049; including landraces and modern cultivars were difficult to be distinguished from K=2 to K=4.

Supplementary Figure 4 Frequency distribution of phenotypic variation of ten agronomic traits in 258 accessions.

The yield traits included lint percent, seed index, boll weight and boll number. The fiber quality traits included fiber length, fiber elongation, fiber strength, micronaire and fiber uniformity. The Verticillium wilt was for biotic disease resistance.

Supplementary Figure 5 The overlapping regions between selective sweeps and GWAS associated loci.

Four selective sweeps were found located around associated loci for fiber length (FL) (A11:63389724), fiber strength (FS) (A11:68009704) and lint percentage (LP) (D02:5454307 and D03:35858092). The horizontal dashed line indicated the genome-wide threshold (2.5) defining the 1% of πlandrace/πcultivar values. The horizontal line in Manhattan plot indicated the threshold of GWAS (1 × 10-6).

Supplementary Figure 6 The independent assortment between two elite alleles of GhLYI-A02 and GhLYI-D08.

These two alleles segregated independently and randomly united at fertilization. Along with crossing over, they would get together through independent assortment and introduce into some cultivars leading to increased number of bolls per plant and lint percentage. The horizontal box indicated the chromosomes A02 and D08. The vertical line in chromosome indicated two elite alleles.

Supplementary Figure 7 Manhattan plots for lint percentage in nine environments, determined with EMMAx.

Negative log10 (P-value) from a genome-wide scan was plotted against position on each of 26 chromosomes. The horizontal line indicated the threshold (10-6).

Supplementary Figure 8 Two significant associated loci for lint percentage.

(a) Manhattan plot for lint percentage. Negative log10 (P-value) from a genome-wide scan was plotted against position on chromosome D03 and D11. The horizontal line indicated the threshold (10-6). The arrows indicated the associated signal peak D03: 35858092 and D11: 60519747. (b) Local Manhattan plot and LD heatmap. The candidate region was identified between dashed lines. The arrow indicated the SNP in candidate gene.

Supplementary Figure 9 Manhattan plots for seed index in nine environments, generated with EMMAx.

Negative log10 (P-value) from a genome-wide scan was plotted against position on each of 26 chromosomes. The horizontal line indicated the threshold (10-6).

Supplementary Figure 10 The candidate gene AHP5 within the most strongly associated locus for seed index.

(a) Negative log10 P-values for association of seed index (SI) was plotted against SNP positions (X axis). The genome-wide significant P-value threshold (10-6) was indicated by a horizontal blue line. The arrow indicated the signal peak containing the candidate gene (AHP5). (b) Transcription level of the gene AHP5 in different tissues using FPKM with single experiment. (c) Comparison of expression level of AHP5 in ovule development stage from two accessions, TM-1 and ZMS12. The asterisk indicated the significant difference at P < 0.01 (two-side t-test, three independent biological replications).

Supplementary Figure 11 GWAS of Verticillium wilt resistance in nine environments, done with EMMAx.

(a) Manhattan plot for Verticillium wilt-resistance. Negative log10 (P-value) from a genome-wide scan was plotted against position on chromosome D06. The horizontal line indicated the threshold (10-6). The arrows indicated the associated signal peak D06:11815621. (b) Local Manhattan plot and LD heatmap. The candidate region was identified between dashedlines. Red arrow indicated the SNP in candidate gene.

Supplementary Figure 12 The pedigrees of ten deep-sequenced cultivars and landraces extensively planted in China.

The accessions for deep sequencing included three founder landraces, DPL15, STV2B and UGDmian (UDGM). The remaining seven grown cultivars for deep sequencing included SM2, SM3, 86-1, Shiyuan321, ZMS12, Jumian 1 and XLZ42.

Supplementary Figure 13 The detection of in-frame indels in the NAC gene in accessions.

This gene was located in two GWAS associated loci, D02:7014970 and D02:1486735, which were associated with boll weight (BW) and number of bolls per plant (BN), respectively. A 7-bp indel insertion was detected in the founders compared to the reference genome (TM-1).

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–13 and Supplementary Tables 2–5, 7, 8, 12, 13, 15, 17, 20, 22, 23, 27 and 29–32 (PDF 3539 kb)

Supplementary Table 1

Summary of 318 cotton samples and sequencing. (XLS 95 kb)

Supplementary Table 6

Detection of SNP quality by PCR sequencing. (XLSX 15 kb)

Supplementary Table 9

Cotton QTLs overlapping with improvement sweeps. (XLSX 20 kb)

Supplementary Table 10

Genome-wide association signals of yield, fiber quality and disease resistance. (XLS 43 kb)

Supplementary Table 11

The associated loci that overlapped with QTLs. (XLS 40 kb)

Supplementary Table 14

Identification of candidate gene in associated locus A02_79153947 for lint yield. (XLSX 14 kb)

Supplementary Table 16

Identification of candidate gene in associated locus D08_3040023 for lint yield. (XLSX 22 kb)

Supplementary Table 18

The SNP information in associated loci for fiber quality. (XLSX 28 kb)

Supplementary Table 19

Identification of candidate gene in associated loci for fiber quality. (XLSX 28 kb)

Supplementary Table 21

Identification of candidate gene in associated locus D03_35858092 for LP. (XLSX 12 kb)

Supplementary Table 24

The summary of indels identified in ten cultivars by deep sequencing. (XLS 290 kb)

Supplementary Table 25

The indels that overlapped with GWAS loci. (XLSX 23 kb)

Supplementary Table 26

The genes involved in copy-number variation. (XLS 152 kb)

Supplementary Table 28

Identity-by-descent (IBD) regions for Chinese cultivars compared with the traditional landraces. (XLSX 239 kb)

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Fang, L., Wang, Q., Hu, Y. et al. Genomic analyses in cotton identify signatures of selection and loci associated with fiber quality and yield traits. Nat Genet 49, 1089–1098 (2017). https://doi.org/10.1038/ng.3887

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