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Genetic mapping of a major codominant QTL associated with β-carotene accumulation in watermelon

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Abstract

The common flesh color of commercially grown watermelon is red due to the accumulation of lycopene. However, natural variation in carotenoid composition that exists among heirloom and exotic accessions results in a wide spectrum of flesh colors. We previously identified a unique orange flesh watermelon accession (NY0016) that accumulates mainly β-carotene and no lycopene. We hypothesized this unique accession could serve as a viable source for increasing provitamin A content in watermelon. Here we characterize the mode of inheritance and genetic architecture of this trait. Analysis of testcrosses of NY0016 with yellow and red fruited lines indicated a codominant mode of action as F1 fruits exhibited a combination of carotenoid profiles from both parents. We combined visual color phenotyping with genotyping-by-sequencing of an F2:3 population from a cross of NY0016 by a yellow fruited line, to map a major locus on chromosome 1, associated with β-carotene accumulation in watermelon fruit. The QTL interval is approximately 20 cM on the genetic map and 2.4 Mb on the watermelon genome. Trait-linked marker was developed and used for validation of the QTL effect in segregating populations across different genetic backgrounds. This study is a step toward identification of a major gene involved in carotenoid biosynthesis and accumulation in watermelon. The codominant inheritance of β-carotene provides opportunities to develop, through marker-assisted breeding, β-carotene-enriched red watermelon hybrids.

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Acknowledgements

We gratefully acknowledge support from the “Center for the Improvement of Cucurbit Fruit Quality,” ARO, Israel. We also acknowledge partial support by US-Israel Binational Agricultural Research & Development (BARD) Senior Research Fellowship Program (USDA-BARD Agreement Number 58-6080-5-011F), and by USDA-National Institute of Food and Agriculture (NIFA), Specialty Crop Research Initiative (SCRI) grant number 2015-51181-24285. We also thank the USA National Watermelon Research and Promotion Board for their continual support; publication no. 211/2017 of the Agricultural Research Organization, Bet Dagan, Israel.

Funding

Funding for this research was provided by the Israeli Ministry of Agriculture Chief Scientist grant no. 20-01-0135.

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Author notes

  1. Sandra Branham, Lea Vexler and Ayala Meir contributed equally to this work.

Authors and Affiliations

  1. USDA, ARS, US Vegetable Laboratory, 2700 Savannah, Highway, Charleston, SC, 29414, USA

    Sandra Branham, Amnon Levi & William P. Wechter

  2. Plant Science Institute, Agricultural Research Organization, Newe Ya’ar Research Center, P.O. Box 1021, 3009500, Ramat Yishay, Israel

    Lea Vexler, Ayala Meir, Galil Tzuri, Zohar Frieman, Yaakov Tadmor & Amit Gur

  3. The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel

    Lea Vexler

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  1. Sandra Branham
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Contributions

AG, AL, AM, and YT conceived and designed the study. LV, AM, and GT performed field experiments, phenotyping, and genotyping. AG, ZF, and SB analyzed the data. AG, SB, AL, WW, and YT wrote the paper. All authors discussed the results and approved the manuscript.

Corresponding author

Correspondence to Amit Gur.

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The authors declare that they have no conflict of interest.

Additional information

Key message

Major QTL regulating the accumulation of β-carotene in the fruit flesh was mapped to  2 Mbp intervals on chromosome 1 in watermelon.

Electronic supplementary material

ESM 1

Figure S1. Photographs of longitudinal cross-sections of representative individuals for each flesh color category and a pie chart of segregation ratios for the (a) F2 population and (b) F2:3 families. Figures S2-S3. Genetic linkage map of Citrullus lanatus with 1078 binned SNPs produced from an F2:3 population derived from experimental line NY0016 crossed with cultivar EMB. Linkage groups 1 through 6 are displayed in Figure S1 and linkage groups 7–11 in Figure S2. SNP positions (cM) are labelled to the left of each linkage group (labelled at the top of the figure) and the chromosome and physical position (bp) are to the right. The 1.5-LOD interval of qFlesh-1 is indicated with a pink vertical bar to the right of linkage group 1. Fig. S4. Plots of genetic (cM) versus physical distance (bp) of each SNP across the 11 watermelon chromosomes. Fig. S5. Gel electrophoresis of PCR with CAPS marker for the parents (EMB and NY0016), F1, and representative F2 individuals. Letters above the gel bands represent the translated genotype: E = Homozygote EMB, N = Homozygote NY0016, H = Heterozygote. (PDF 1735 kb)

Table S1

Variation in color and carotenoid concentrations in four testcrosses with NY0016 (XLSX 10 kb)

Table S2

Flesh color data for the F2:3 families in categorical and continuous scales (separated tabs), including pedigree, family ID (family); the family flesh color categories used for QTL mapping (flesh0–1), family categorical flesh ratings (seg) and the individual fruit colors (fruit1-fruit10). (XLSX 23 kb)

Table S3

1078 Binned SNPs information, including: SNP name (SNP), genetic position (cM) on each linkage group (LG), physical position (bp) on each chromosome (CS), results of a chi test for segregation distortion (P, neglog10P, and FDR), and the proportions of individuals with each genotype at that locus (AA, AB, BB, or missing). AA indicates individuals homozygous for NY0016 alleles, BB homozygous for EMB alleles or heterozygous individuals AB. (XLSX 111 kb)

Table S4

Annotated genes list within the 1.5-LOD interval (8.00 to 10.50 Mb on chromosome 1) for flesh color QTL (qFC.1). Gene information includes: identifier for watermelon gene (geneID), chromosome (CG_Chr), start position (bp), stop position (bp), and the functional annotation. Annotated candidates are highlighted. (XLSX 18 kb)

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Branham, S., Vexler, L., Meir, A. et al. Genetic mapping of a major codominant QTL associated with β-carotene accumulation in watermelon. Mol Breeding 37, 146 (2017). https://doi.org/10.1007/s11032-017-0747-0

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