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High-density NGS-based map construction and genetic dissection of fruit shape and rind netting in Cucumis melo

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Abstract

Melon is an important crop that exhibits broad variation for fruit morphology traits that are the substrate for genetic mapping efforts. In the post-genomic era, the link between genetic maps and physical genome assemblies is key for leveraging QTL mapping results for gene cloning and breeding purposes. Here, using a population of 164 melon recombinant inbred lines (RILs) that were subjected to genotyping-by-sequencing, we constructed and compared high-density sequence- and linkage-based recombination maps that were aligned to the reference melon genome. These analyses reveal the genome-wide variation in recombination frequency and highlight regions of disrupted collinearity between our population and the reference genome. The population was phenotyped over 3 years for fruit size and shape as well as rind netting. Four QTLs were detected for fruit size, and they act in an additive manner, while significant epistatic interaction was found between two neutral loci for this trait. Fruit shape displayed transgressive segregation that was explained by the action of four QTLs, contributed by alleles from both parents. The complexity of rind netting was demonstrated on a collection of 177 diverse accessions. Further dissection of netting in our RILs population, which is derived from a cross of smooth and densely netted parents, confirmed the intricacy of this trait and the involvement of major locus and several other interacting QTLs. A major netting QTL on chromosome 2 co-localized with results from two additional populations, paving the way for future study toward identification of a causative gene for this trait.

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Acknowledgements

We wish to thank Uzi Sa’ar and Fabian Baumkoler for technical assistance in setting the field trials and for plant maintenance, and Tamar Lahav for R and python scripts. Funding for this research was provided by the Israeli Ministry of Agriculture Chief Scientist Grants Nos. 20-01-0141 and 20-10-0071 and by the United States-Israel Binational Agricultural Research and Development Fund (BARD) Grant No. US-5009-17.

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Authors and Affiliations

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

    Elad Oren, Galil Tzuri, Asaf Dafna, Ayala Meir, Ravindra Kumar, Nurit Katzir, Shiri Freilich, Yaakov Tadmor, Joseph Burger & Amit Gur

  2. Plant Science Institute, Agricultural Research Organization, The Volcani Center, P.O. Box 15159, 7507101, Rishon LeZiyyon, Israel

    Arthur A. Schaffer

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

    Elad Oren & Yonatan Elkind

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  1. Elad Oren
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  2. Galil Tzuri
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  12. Amit Gur
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Contributions

AG and EO conceived and designed the study. EO, AD, GT, AM and AG performed field experiments and phenotyping. NK, YE, SF, AAS, YT and JB provided genomic and statistical experimental support. EO and RK analyzed the data. EO and AG wrote the paper. All authors discussed the results and approved the manuscript.

Corresponding author

Correspondence to Amit Gur.

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Communicated by Sanwen Huang.

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 1: Number of double recombinations analysis across the 164 RILs (x axis) in three representative chromosomes, generated by ASMap (Taylor and Butler 2017. The plot annotates the genotypes that have double recombination rates significantly above the expected rate. Figure 2: Genetic map of TAD × DUL RILs. Each horizontal line represents a marker on a recombination point (bin). Blue segments are small linkage groups that were manually merged to their chromosome. Figure 3: Segregation and allele frequencies across lines and markers. a) Distribution of genome-wide allele frequencies across the 164 TAD × DUL RILs. For each line, the proportion of TAD alleles across all markers was calculated. Population average is not different than the expected 0.5 ratio, and distribution is normal. b) genome-wide marker segregation within chromosomes. Blue curves are sliding window representation of TAD allele frequencies across markers. Dashed horizontal lines represent significance threshold. Figure 4: Properties of linkage and sequence-based genetic maps along the 12 melon chromosomes. a) Recombination rates along the chromosomes of both genetic maps. Black solid—sequence-based genetic map. Blue dashed line—linkage-based genetic map. b) Correlation between sequence and linkage-based maps—recombination bins were aligned according to their GBS marker identity. Each dot represents a bin on its respective genetic coordinates (X-sequence-based, Y-linkage-based). The white dashed line marks the diagonal (x = y). Apart from inherent genetic length differences between the two approaches (linkage-based analysis yielded shorter maps), inconsistencies between maps are also visible (e.g., large inversion on chromosome 1 marked by red dashed circle). c) Bin size distributions in the sequence (upper graph) and linkage-based (lower graph) maps. Arrows mark the mean bin size in each map. Figure 5: Evaluation of the quality of the recombination maps through mapping of traits associated with known genes. Associations were tested using a generalized linear model to the physical map and Haley Knott regression interval mapping to the sequence-based genetic map. a) Flesh color locus presented on a Marey map of chromosome 9 on a 240 Kb–23 cM interval. b) Manhattan plot of the flesh color locus and zoom in on chromosome 9 peak, where the causative gene CmOr (MELO3C005449) is shown. c) Rind color locus presented on a Marey map of chromosome 4 on a 420 Kb–4 cM interval. d) Manhattan plot of the rind color locus and zoom in on chromosome 4 peak, where the causative gene CmAPRR2 (MELO3C003775) is shown. Figure 6: Correlation matrix between measured traits in TAD × DUL RILs across three experiments. Figure 7: Fruit weight (FW) QTL mapping results. a) Genome-wide LOD scores by standard interval mapping using Haley Knott regression method. Line color designates year, and the dotted line represents the LOD permutation threshold. b) LOD scores for chromosomes 4 and 8 by composite interval mapping. Figure 8: Fruit area (FAr) QTL mapping. a) Genome-wide LOD scores by standard interval mapping using Haley Knott regression method. Line color designates year, and the dotted line represents the LOD permutation threshold. b) LOD scores for chromosomes 4 and 8 by composite interval mapping. c) LOD profiles generated by the stepwise procedure for significant QTLs in each experiment. The genetic positions of loci are annotated above each peak. Figure 9: Fruit length (FLn) QTL mapping. a) Genome-wide LOD scores by standard interval mapping using Haley Knott regression method. Line color designates year, and the dotted line represents the LOD permutation threshold. b) LOD scores for chromosomes 4, 8 and 9 by composite interval mapping. c) LOD profiles generated by the stepwise procedure for significant QTLs in each experiment. The genetic positions of loci are annotated above each peak. Figure 10: Fruit width (FWd) QTL mapping. a) Genome-wide LOD scores by standard interval mapping using Haley Knott regression method. Line color designates year, and the dotted line represents the LOD permutation threshold. b) LOD scores for chromosomes 3, 4, 8 and 12 by composite interval mapping. c) LOD profiles generated by the stepwise procedure for significant QTLs in each experiment. The genetic positions of loci are annotated above each peak. Figure 11: Fruit shape index QTL mapping. a) LOD profiles generated by the stepwise procedure for significant QTLs in each experiment. The genetic positions of loci are annotated above each peak. b) Transgressive segregation for fruit shape. Lines are ranked based from low to high based on their FSI. All the RILs above or below the dashed lines are significantly more elongated or flat than both parents, based on Student’s t test (P < 0.05). Figure 12: Fruit shape index epistatic interaction between FSI1.1 and FSI12.1, across 3 years. Haplotype means not connected by the same letter are significantly different at P < 0.05. Figure 13: Netting density QTL mapping. a) Genome-wide LOD scores by standard interval mapping using Haley Knott regression method. Line color designates year, and the dotted line represents the LOD permutation threshold. b) LOD scores for the two QTLs on chromosome 2 by composite interval mapping. c) LOD profiles generated by the stepwise procedure for significant QTLs in each experiment. The genetic positions of loci are annotated above each peak. Figure 14: Netting density two-way LS means plot of NDEN2.2 and NDEN9.1 across 3 years. Haplotype means not connected by the same letter are significantly different at P < 0.05. (PDF 335 kb)

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Oren, E., Tzuri, G., Dafna, A. et al. High-density NGS-based map construction and genetic dissection of fruit shape and rind netting in Cucumis melo. Theor Appl Genet 133, 1927–1945 (2020). https://doi.org/10.1007/s00122-020-03567-3

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