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.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
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 (SAMN12791768–SAMN12792667, SAMN12791484–SAMN12791767). 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.
References
Pitrat, M., Hanelt, P. & Hammer, K. Some comments on infraspecific classification of melon. Acta Hortic. 510, 29–36 (2000).
Luan, F., Delannay, I. & Staub, J. E. Chinese melon (Cucumis melo L.) diversity analyses provide strategies for germplasm curation, genetic improvement, and evidentiary support of domestication patterns. Euphytica 164, 445–461 (2008).
Kerje, T. & Grum, M. The origin of melon, Cucumis melo: a review of the literature. Acta Hortic. 510, 37–44 (2000).
Sebastian, P., Schaefer, H., Telford, I. R. & Renner, S. S. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc. Natl Acad. Sci. USA 107, 14269–14273 (2010).
Endl, J. et al. Repeated domestication of melon (Cucumis melo) in Africa and Asia and a new close relative from India. Am. J. Bot. 105, 1662–1671 (2018).
Jeffrey, C. A review of the Cucurbitaceae. Bot. J. Linn. Soc. 81, 233–247 (1980).
Serres-Giardi, L. & Dogimont, C. How microsatellite diversity helps to understand the domestication. In Proc. Xth EUCARPIA Meeting on Genetics and Breeding of Cucurbitaceae (eds Sari, N. et al.) 254–263 (Antalya, 2012).
Staub, J. E., Lopez-Sese, A. I. & Fanourakis, N. Diversity among melon landraces (Cucumis melo L.) from Greece and their genetic relationships with other melon germplasm of diverse origins. Euphytica 136, 151–166 (2004).
Tanaka, K. et al. Seed size and chloroplast DNA of modern and ancient seeds explain the establishment of Japanese cultivated melon (Cucumis melo L.) by introduction and selection. Genet. Resour. Crop Evol. 63, 1237–1254 (2016).
Paris, H. S., Amar, Z. & Lev, E. Medieval emergence of sweet melons, Cucumis melo (Cucurbitaceae). Ann. Bot. 110, 23–33 (2012).
Garcia-Mas, J. et al. The genome of melon (Cucumis melo L.). Proc. Natl Acad. Sci. USA 109, 11872–11877 (2012).
Boualem, A. et al. A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321, 836–838 (2008).
Tzuri, G. et al. A ‘golden’ SNP in CmOr governs the fruit flesh color of melon (Cucumis melo). Plant J. 82, 267–279 (2015).
Feder, A. et al. A kelch domain-containing F-box coding gene negatively regulates flavonoid accumulation in muskmelon. Plant Physiol. 169, 1714–1726 (2015).
Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961–967 (2010).
Tian, F. et al. Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat. Genet. 43, 159–162 (2011).
Jia, G. et al. A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat. Genet. 45, 957–961 (2013).
Zhou, Z. et al. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat. Biotechnol. 33, 408–414 (2015).
Du, X. et al. Resequencing of 243 diploid cotton accessions based on an updated A genome identifies the genetic basis of key agronomic traits. Nat. Genet. 50, 796–802 (2018).
Shang, Y. et al. Biosynthesis, regulation, and domestication of bitterness in cucumber. Science 346, 1084–1088 (2014).
Tieman, D. et al. A chemical genetic roadmap to improved tomato flavor. Science 355, 391–394 (2017).
Zhu, G. et al. Rewiring of the fruit metabolome in tomato breeding. Cell 172, 249–261 (2018).
Argyris, J. M. et al. Use of targeted SNP selection for an improved anchoring of the melon (Cucumis melo L.) scaffold genome assembly. BMC Genomics 16, 4 (2015).
Qi, J. et al. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat. Genet. 45, 1510–1515 (2013).
Dhillon, N. P. S. et al. Diversity among landraces of Indian snapmelon (Cucumis melo var. momordica). Genet. Resour. Crop Evol. 54, 1267–1283 (2007).
Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983).
Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).
Diaz, A. et al. Quantitative trait loci analysis of melon (Cucumis melo L.) domestication-related traits. Theor. Appl. Genet. 130, 1837–1856 (2017).
Kuang, J. F. et al. Two GH3 genes from longan are differentially regulated during fruit growth and development. Gene 485, 1–6 (2011).
Lin, T. et al. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46, 1220–1226 (2014).
Kato-Emori, S., Higashi, K., Hosoya, K., Kobayashi, T. & Ezura, H. Cloning and characterization of the gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase in melon (Cucumis melo L. reticulatus). Mol. Genet. Genomics 265, 135–142 (2001).
Zhou, Y. et al. Convergence and divergence of bitterness biosynthesis and regulation in Cucurbitaceae. Nat. Plants 2, 16183 (2016).
Ma, D., Sun, L., Gao, S., Hu, R. & Liu, M. Studies on the genetic pattern of bitter taste in yong fruit of melon (Cucumis melo L.) [in Chinese]. Acta Hortic. Sin. 23, 255–258 (1996).
Fujishita, N., Furukawa, H. & Morii, S. Distribution of three genotypes for bitterness of F1 immature fruit in Cucumis melo [in Japanese]. Jpn. J. Breed. 43 (Suppl. 2), 206 (1993).
Cohen, S. et al. The PH gene determines fruit acidity and contributes to the evolution of sweet melons. Nat. Commun. 5, 4026 (2014).
Nardi, C. F. et al. Expression of FaXTH1 and FaXTH2 genes in strawberry fruit. Cloning of promoter regions and effect of plant growth regulators. Sci. Hortic. 165, 111–122 (2014).
Dogra, V., Sharma, R. & Yelam, S. Xyloglucan endo-transglycosylase/hydrolase (XET/H) gene is expressed during the seed germination in Podophyllum hexandrum: a high altitude Himalayan plant. Planta 244, 505–515 (2016).
Périn, C. et al. A reference map of Cucumis melo based on two recombinant inbred line populations. Theor. Appl. Genet. 104, 1017–1034 (2002).
Pereira, L. et al. QTL mapping of melon fruit quality traits using a high-density GBS-based genetic map. BMC Plant Biol. 18, 324 (2018).
Liljegren, S. J. et al. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766–770 (2000).
Vrebalov, J. et al. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21, 3041–3062 (2009).
Tadmor, Y. et al. Genetics of flavonoid, carotenoid, and chlorophyll pigments in melon fruit rinds. J. Agric. Food Chem. 58, 10722–10728 (2010).
Abe, A. et al. Genome sequencing reveals agronomically important loci in rice using MutMap. Nat. Biotechnol. 30, 174–178 (2012).
Liu, H. et al. Map-based cloning, identification and characterization of the w gene controlling white immature fruit color in cucumber (Cucumis sativus L.). Theor. Appl. Genet. 129, 1247–1256 (2016).
Oren, E. et al. The multi-allelic APRR2 gene is associated with fruit pigment accumulation in melon and watermelon. J. Exp. Bot. 70, 3781–3794 (2019).
Pan, Y. et al. Network inference analysis identifies an APRR2-like gene linked to pigment accumulation in tomato and pepper fruits. Plant Physiol. 161, 1476–1485 (2013).
Hu, Z. et al. The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis. J. Exp. Bot. 65, 1111–1123 (2014).
Galpaz, N. et al. Deciphering genetic factors that determine melon fruit-quality traits using RNA-Seq-based high-resolution QTL and eQTL mapping. Plant J. 94, 169–191 (2018).
Gawel, N. J. & Jarret, R. L. A modified CTAB DNA extraction procedure for Musa and Ipomoea. Plant Mol. Biol. 9, 262–266 (1991).
Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967 (2009).
Li, R. et al. SNP detection for massively parallel whole-genome resequencing. Genome Res. 19, 1124–1132 (2009).
He, W. et al. ReSeqTools: an integrated toolkit for large-scale next-generation sequencing based resequencing analysis. Genet. Mol. Res. 12, 6275–6283 (2013).
Harel-Beja, R. et al. A genetic map of melon highly enriched with fruit quality QTLs and EST markers, including sugar and carotenoid metabolism genes. Theor. Appl. Genet. 121, 511–533 (2010).
Gur, A. et al. Genome-wide linkage-disequilibrium mapping to the candidate gene level in melon (Cucumis melo). Sci. Rep. 7, 9770 (2017).
Brewer, M. T. et al. Development of a controlled vocabulary and software application to analyze fruit shape variation in tomato and other plant species. Plant Physiol. 141, 15–25 (2006).
Darrigues, A., Hall, J., Knaap, E. & Francis, D. M. Tomato analyzer-color test: a new tool for efficient digital phenotyping. J. Am. Soc. Hort. Sci. 133, 579–586 (2008).
Ma, S. et al. Descriptors and Data Standard for Melon (Cucumis melo L.) (China Agriculture Press, 2006).
Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003).
Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).
Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).
Goudet, J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186 (2005).
Hutter, S., Vilella, A. J. & Rozas, J. Genome-wide DNA polymorphism analysesusing VariScan. BMC Bioinformatics 7, 409 (2006).
Barrett, J. C., Fry, B., Maller, J. & Daly, M. J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265 (2005).
Kang, H. M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348–354 (2010).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
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
Authors and Affiliations
Contributions
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.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
Supplementary information
Supplementary Information
Supplementary Figs. 1–11, Tables 2–4, 10, 11, 14–18 and Note
Supplementary Tables
Supplementary Tables 1, 5–9, 12, 13
Supplementary Dataset 1
Supplementary Dataset 1
Rights and permissions
About this article
Cite this article
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). https://doi.org/10.1038/s41588-019-0522-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41588-019-0522-8
This article is cited by
-
Whole-genome sequencing of tetraploid potato varieties reveals different strategies for drought tolerance
Scientific Reports (2024)
-
Genomic variation and candidate genes dissect quality and yield traits in Boehmeria nivea (L.) Gaudich
Cellulose (2024)
-
Comparative network analysis reveals the dynamics of organic acid diversity during fruit ripening in peach (Prunus persica L. Batsch)
BMC Plant Biology (2023)
-
Genetic diversity analysis and variety identification using SSR and SNP markers in melon
BMC Plant Biology (2023)
-
Resequencing of global Lotus corniculatus accessions reveals population distribution and genetic loci, associated with cyanogenic glycosides accumulation and growth traits
BMC Biology (2023)