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Article|15 Mar 2020|OPEN
Gynoecy instability in cucumber (Cucumis sativus L.) is due to unequal crossover at the copy number variation-dependent Femaleness (F) locus 
Zheng Li;;Yonghua Han;;Yuhui Wang;;Biao Jiang;; Yiqun Weng1, Zheng Li ;; Huanhuan Niu2, Yonghua Han3, Biao Jiang4 & Yiqun Weng5
1Horticulture Department, University of Wisconsin, Madison, WI, 53706, USA
2College of Horticulture, Northwest A&F University, Yangling, Shaanxi, 712100, China
3Institute of Integrative Plant Biology, School of Life Sciences, Jiangsu Normal University, Xuzhou, 221116, China
4Vegetable Research Institute, Guangdong Academy of Agricultural Science, Guangzhou, Guangdong, 510640, China
5USDA-ARS, Vegetable Crops Research Unit, Madison, WI, 53706, USA

Horticulture Research 7,
Article number: 20032 (2020)
doi: 10.1038/hortres.2020.32
Views: 310

Received: 28 Oct 2019
Revised: 06 Jan 2020
Accepted: 15 Jan 2020
Published online: 15 Mar 2020

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.