Abstract
The sexual expression of watermelon plants is the result of the distribution and occurrence of male, female, bisexual and hermaphrodite flowers on the main and secondary stems. Plants can be monoecious (producing male and female flowers), andromonoecious (producing male and hermaphrodite flowers), or partially andromonoecious (producing male, female, bisexual, and hermaphrodite flowers) within the same plant. Sex determination of individual floral buds and the distribution of the different flower types on the plant, are both controlled by ethylene. A single missense mutation in the ethylene biosynthesis gene CitACS4, is able to promote the conversion of female into hermaphrodite flowers, and therefore of monoecy (genotype MM) into partial andromonoecy (genotype Mm) or andromonoecy (genotype mm). We phenotyped and genotyped, for the M/m locus, a panel of 207 C. lanatus accessions, including five inbreds and hybrids, and found several accessions that were repeatedly phenotyped as PA (partially andromonoecious) in several locations and different years, despite being MM. A cosegregation analysis between a SNV in CitACS4 and the PA phenotype, demonstrated that the occurrence of bisexual and hermaphrodite flowers in a PA line is not dependent on CitACS4, but conferred by an unlinked recessive gene which we called pa. Two different approaches were performed to map the pa gene in the genome of C. lanatus: bulk segregant analysis sequencing (BSA-seq) and genome wide association analysis studies (GWAS). The BSA-seq study was performed using two contrasting bulks, the monoecious M-bulk and the partially andromonoecious PA-bulk, each one generated by pooling DNA from 20 F2 plants. For GWAS, 122 accessions from USDA gene bank, already re-sequenced by genotyping by sequencing (GBS), were used. The combination of the two approaches indicates that pa maps onto a genomic region expanding across 32.24–36.44 Mb in chromosome 1 of watermelon. Fine mapping narrowed down the pa locus to a 867 Kb genomic region containing 101 genes. A number of candidate genes were selected, not only for their function in ethylene biosynthesis and signalling as well as their role in flower development and sex determination, but also by the impact of the SNPs and indels differentially detected in the two sequenced bulks.
Highlights
Watermelons, genus Citrullus (2n=2x=22) Schrad. ex Eckl. et Zeyh., are among the most grown vegetable fruit crops worldwide (Levi et al, 2017), representing a planted area of more than 3 million hectares, and production exceeding 100 million tons annually
Thereafter, we mapped the trait by using bulk segregant analysis combined with new generation sequencing (BSA-seq), and by genome-wide association analysis (GWAS). These two methods allow the identifications of DNA markers closely linked to the causal gene for a given phenotype (Giovannoni et al, 1991; Michelmore et al, 1991; Mansfeld and Grumet, 2018). By combining these two approaches, we identified a genomic region on chromosome 1 that regulates the partial andromonoecy trait in watermelon
We studied the diversity of sex morphotypes among a large germplasm panel of watermelon, comprising 207 watermelon accessions: 155 from USDA-National Plant Germplasm System (NPGS) gene bank, 47 from the Spanish gene banks COMAV and BGHCITA, plus two commercial cultivars and three inbred lines (Supplementary Table 1)
Summary
Watermelons, genus Citrullus (2n=2x=22) Schrad. ex Eckl. et Zeyh., are among the most grown vegetable fruit crops worldwide (Levi et al, 2017), representing a planted area of more than 3 million hectares, and production exceeding 100 million tons annually (http://faostat.fao.org/). The cultivated citron, egusi, and dessert watermelons have been treated as subspecies of the single species Citrullus lanatus (Fursa, 1972). Andromonoecy and PA are undesirable traits in watermelon, since bisexual and hermaphrodite flowers need to be emasculated when acting as female parents in the production of hybrid seed (Prothro et al, 2013). They are undesirable because these traits are usually associated with a reduction in fruit set and fruit quality (Aguado et al, 2018)
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