A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits

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Abstract

Melon is an economically important fruit crop that has been cultivated for thousands of years; however, the genetic basis and history of its domestication still remain largely unknown. Here we report a comprehensive map of the genomic variation in melon derived from the resequencing of 1,175 accessions, which represent the global diversity of the species. Our results suggest that three independent domestication events occurred in melon, two in India and one in Africa. We detected two independent sets of domestication sweeps, resulting in diverse characteristics of the two subspecies melo and agrestis during melon breeding. Genome-wide association studies for 16 agronomic traits identified 208 loci significantly associated with fruit mass, quality and morphological characters. This study sheds light on the domestication history of melon and provides a valuable resource for genomics-assisted breeding of this important crop.

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Fig. 1: Geographic distribution and population structure of melon accessions.
Fig. 2: Independent selection in domesticated traits between C. melo. ssp. melo and agrestis.
Fig. 3: Identification of a candidate gene for the melon sutures trait.
Fig. 4: GWAS, bulked segregation analysis and QTL analysis identified the same region as being potentially important for peel color.

Data availability

The raw sequencing data reported in this paper have been deposited in the Sequence Read Archive (SRA) under a NCBI BioProject accession (PRJNA565104) and NCBI BioSample accessions (SAMN12791768SAMN12792667, SAMN12791484SAMN12791767). The sequencing data are also accessible from the BIG Data Center (http://bigd.big.ac.cn/gsa) under the accession number CRA001513. In addition, the data are also available from the corresponding authors on reasonable request.

Code availability

All codes are available from the corresponding authors upon request.

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Acknowledgements

We thank B. S. Gaut (Department of Ecology and Evolutionary Biology, University of California Irvine), W. Lucas (University of California, Davis), J. Ruan (Agricultural Genome Institute at Shenzhen, Chinese Academy of Agricultural Sciences) and D. Wu (Kunming Institute of Zoology, Chinese Academy of Sciences) for critical comments. This work was supported by funding from the Agricultural Science and Technology Innovation Program (to Yongyang Xu, S.H., Z.Z. and H.W.), the China Agriculture Research System (CARS-25 to Yongyang Xu and H.W.), the Leading Talents of Guangdong Province Program (00201515 to S.H.), the Shenzhen Municipal (The Peacock Plan KQTD2016113010482651 to S.H.), the Dapeng district government, National Natural Science Foundation of China (31772304 to Z.Z.), the Science and Technology Program of Guangdong (2018B020202007 to S.H.), the National Natural Science Foundation of China (31530066 to S.H.), the National Key R&D Program of China (2016YFD0101007 to S.H.), USDA National Institute of Food and Agriculture Specialty Crop Research Initiative (2015-51181-24285 to Z.F.), the European Research Council (ERC-SEXYPARTH to A.B.), the Spanish Ministry of Economy and Competitiveness (AGL2015–64625-C2-1-R to J.G.-M.), Severo Ochoa Programme for Centres of Excellence in R&D 2016–2010 (SEV-2015–0533 to J.G.-M.), the CERCA Programme/Generalitat de Catalunya to J.G.-M. and the German Science Foundation (SPP1991 Taxon-OMICS to H.S.).

Author information

S.H., Yongyang Xu and J.G.-M. designed studies and contributed to the original concept of the project, S.H., G.Z., T.L., Z.Z. and Q.F. managed the project, T.G., I.J., R.W., V.R. and W.F. performed the bioinformatics, S.M., J.S., Yongyang Xu, M. Pitrat, C.D., J.W., J.L. and A.J.M. contributed to the collection of the melon accessions, Y.H., G.Z., W.K., H.W., J.Z., Z.X., A.G., N.K., E.O., D.S., S.Z., Y.Z. and N.L. planted accessions, prepared the samples and performed phenotyping, P.W., Y.H., Y.Z., J.A., C.M., L.P., M. Pujol and D.O. designed and performed the molecular experiments, G.Z., Q.L. and T.L. prepared the figures and tables, S.H., T.L., J.G.-M., Z.F., T.G., A.J.M., V.R., A.G., Yong Xu, A.B., H.S. and J.J. revised the manuscript, G.Z., Q.L. T.L., Z.Z. and Q.F. analyzed data and wrote the paper.

Correspondence to Jordi Garcia-Mas or Yongyang Xu or Sanwen Huang.

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Extended data

Extended Data Fig. 1 Distribution of small indels.

Distribution of small indels ( ≤ 5 bp) in different genomic regions. Indels in all regions were shown in blue. Those in intergenic regions were shown in purple. Indels in introns (green) are predominantly short (1 or 2 bp), whereas those in exons (orange) are often 3-bp long as this length does not cause a frame shift.

Extended Data Fig. 2 Chloroplast Phylogenetic tree.

Phylogenetic tree constructed with the chloroplast SNPs for 977 melon accessions.

Extended Data Fig. 3 The result of DAPC.

Population structure analysis of melon accessions with DAPC. a, Cumulated variance explained by the eigenvalues of the PCA. b, Variation curve of BIC value. c, Model-based clustering analysis with different numbers of clusters (K = 2, 3 and 4).

Extended Data Fig. 4 Principal component analysis (PCA).

Principal component analysis (PCA) of 968 melon accessions. SNPs with missing data rate ≤ 40% were used for PCA. Two-dimension coordinates were plotted for the 968 melon accessions. The African group (green) and melo group (blue) have a discrete distribution; the agrestis group (red) has an obviously centralized distribution.

Extended Data Fig. 5 The differentiation of Heterozygosity.

The heterozygosity of different groups. Each box represents the mean and interquartile range. The top whisker denotes the maximum value and the bottom whisker denotes the minimum value. The significance was determined by two-tailed Student’s t tests.

Extended Data Fig. 6 The analysis of introgression.

Treemix analysis of the main genetic clusters. Arrows represent the direction of migrations.

Extended Data Fig. 7 Expression of CmBi and CmBt.

RT–qPCR of CmBi (a) and CmBt (b) in young fruits of WM, CM, WA and CA accessions. Data are presented as mean ± s.d.(n = 3 independent measurements).

Extended Data Fig. 8 Population differentiation in cultivated melon.

Population differentiation between CM (cultivated melo) and CA (cultivated agrestis) groups. a, Distribution of FST across the melon genome. Highly divergent genomic regions overlapping previously reported QTL signals are indicated. The horizontal dashed line indicates the top 10% threshold. b,c, QTLs for flesh thickness identified from an F2 population from the cross of a cultivated melo accession and a cultivated agrestis accession. Both QTLs are located in regions with higher divergence levels (FST = 0.69) and (FST = 0.48), respectively. The black horizontal dashed lines indicate the threshold (LOD > 3.0) of QTL-mapping. d, Association signals identified by GWAS on ovary pubescence using the whole population. The significant threshold of -log10P value was set at 5.6.

Extended Data Fig. 9 The verification of known genes in GWAS analysis.

Previously reported genes identified in the GWAS analysis. a-c, Manhattan plots (left) and quantile-quantile plots (right) of GWAS for sex determination (a), orange flesh color (b) and yellow and white peel color (c) using the MLM model. The significant threshold of -log10P value was set at 5.6. Genes CmACS-7 (ref. 1), CmOr2 and CmKFB3 are marked by red arrows.

Extended Data Fig. 10 GWAS analysis of flesh aroma.

GWAS analysis of flesh aroma in three different populations. a-c, Manhattan plots (left) and quantile-quantile plots (right) for GWAS on flesh aroma in the melo population (a), in the agrestis population (b), and in the whole population (c). The significant threshold of -log10P value was set at 5.6.

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Supplementary Figs. 1–11, Tables 2–4, 10, 11, 14–18 and Note

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Supplementary Dataset 1

Supplementary Dataset 1

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Zhao, G., Lian, Q., Zhang, Z. et al. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet 51, 1607–1615 (2019) doi:10.1038/s41588-019-0522-8

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