Gynoecy instability in cucumber (Cucumis sativus L.) is due to unequal crossover at the copy number variation-dependent femaleness (F) locus

Authors: LI, ZHENG - University Of Wisconsin; HAN, YONGHUA - University Of Wisconsin; NIU, HUANHUAN - Northwest Agricultural & Forestry University; WANG, YUHUI - University Of Wisconsin; JIANG, BIAO - University Of Wisconsin; Weng, Yiqun

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/20/2020
Publication Date: 3/15/2020
Citation: Li, Z., Han, Y., Niu, H., Wang, Y., Jiang, B., Weng, Y. 2020. Gynoecy instability in cucumber (Cucumis sativus L.) is due to unequal crossover at the copy number variation-dependent femaleness (F) locus. Horticulture Research. 7:32. https://doi.org/10.1038/s41438-020-0251-2.
DOI: https://doi.org/10.1038/s41438-020-0251-2

Interpretive Summary: Background information Cucumber 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, gynoecy expression seems unstable since monoecious plants could often be found in F-dependent gynoecious cucumber inbreds. Findings: We hypothesized that gynoecy instability (gynoecy loss) may be due to unequal crossover (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, and 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, ‘gynoecious loss’ mutants were identified with similar mutation rates (~0.12%). We show that these monoecious 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. Who cares? 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.

Technical 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, gynoecy expression seems unstable since monoecious plants could often be found in F-dependent gynoecious cucumber inbreds. We hypothesized that gynoecy instability (gynoecy loss) may be due to unequal crossover (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, ‘gynoecious loss’ mutants were identified with similar mutation rates (~0.12%). We show that these monoecious 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.