Abstract
Cucumber, Cucumis sativus is an important vegetable crop, and gynoecy has played a critical role in yield increase of hybrid cucumber production. Cucumber has a unique genetic system for gynoecious sex expression, which is determined by the copy number variation (CNV)-based, dominant, and dosage-dependent femaleness (F) locus. However, this gynoecy expression system seems unstable since monecious plants could often be found in F-dependent gynoecious cucumber inbreds. We hypothesized that gynoecy instability (gynoecy loss) may be due to unequal crossing over (UCO) during meiosis among repeat units of the CNV. In this study, using high throughput genome resequencing, fiber-FISH and genomic qPCR analyses, we first confirmed and refined the structure of the F locus, which was a CNV of a 30.2-kb tandem repeat. Gynoecious plants contained three genes: CsACS1, CsACS1G, and CsMYB, of which CsACS1G is a duplication of CsACS1 but with a recombinant distal promoter that may contribute to gynoecy sex expression. In two large populations from self-pollinated gynoecious inbred lines, ‘gynoecy loss’ mutants were identified with similar mutation rates (~0.12%). We show that these monecious mutants have lost CsACS1G. In addition, we identified gynoecious lines in natural populations that carry two copies of CSACS1G. We proposed a model to explain gynoecy instability in F-dependent cucumbers, which is caused by UCO among CSACS1/G units during meiosis. The findings present a convincing case that the phenotypic variation of an economically important trait is associated with the dynamic changes of copy numbers at the F locus. This work also has important implications in cucumber breeding.
Highlights
The common ancestor of all angiosperms was likely hermaphroditic with perfect flowers that have both stamens and pistils[1]
In large populations of two gynoecious inbred lines (Gy14 and G06), we identified monecious ‘gynoecy loss’ mutants and confirmed the gynoecy instability was due to elimination of the CsACS1G copy through unequal crossing over (UCO) during meiosis
Structure and function of the F locus in cucumber Cucumber has a unique system for gynoecious sex expression which is based on copy number variation (CNV) of a 30.2 kb region containing CsACS1G, a duplicated copy of CsACS1 but with recombinant promoter[38,39]
Summary
The common ancestor of all angiosperms was likely hermaphroditic with perfect flowers that have both stamens and pistils[1]. During the evolution of flowering plants, sex determination is an important mechanism to increase genetic fitness by promoting outcrossing, and decreasing inbreeding[2]. One such strategy taken by species in the Cucurbitaceae family is monoecy in which plants produce unisexual flowers on the same individual. Among the ~950 species in this family, ~50% are monecious[3,4] including the economically important vegetable crop cucumber, Cucumis sativus L. that has long been a favorite model for study of sex determination in plants. Three types of flowers can be present in a cucumber plant: staminate (male), pistillate (female) and hermaphrodite (bisexual/perfect).
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