Fruit length is a prominent agricultural trait during cucumber (Cucumis sativus) domestication and diversifying selection; however, the regulatory mechanisms of fruit elongation remain elusive. We identified two alleles of the FRUITFULL (FUL)–like MADS-box gene CsFUL1 with 3393^C/A Single Nucleotide Polymorphism variation among 150 cucumber lines. Whereas CsFUL1^A was specifically enriched in the long-fruited East Asian type cucumbers (China and Japan), the CsFUL1^C allele was randomly distributed in cucumber populations, including wild and semiwild cucumbers. CsFUL1^A knockdown led to further fruit elongation in cucumber, whereas elevated expression of CsFUL1^A resulted in significantly shorter fruits. No effect on fruit elongation was detected when CsFUL1^C expression was modulated, suggesting that CsFUL1^A is a gain-of-function allele in long-fruited cucumber that acts as a repressor during diversifying selection of East Asian cucumbers. Furthermore, CsFUL1^A binds to the CArG-box in the promoter region of SUPERMAN, a regulator of cell division and expansion, to repress its expression. Additionally, CsFUL1^A inhibits the expression of auxin transporters PIN-FORMED1 (PIN1) and PIN7, resulting in decreases in auxin accumulation in fruits. Together, our work identifies an agriculturally important allele and suggests a strategy for manipulating fruit length in cucumber breeding that involves modulation of CsFUL1^A expression.

Cucumber, Cucumis sativus L. (2n = 2x = 14), is an important vegetable crop worldwide. It was the first specialty crop with a publicly available draft genome. Its relatively small, diploid genome, short life cycle, and self-compatible mating system offers advantages for genetic studies. In recent years, significant progress has been made in molecular mapping, and identification of genes and QTL responsible for key phenotypic traits, but a systematic review of the work is lacking. Here, we conducted an extensive literature review on mutants, genes and QTL that have been molecularly mapped or characterized in cucumber. We documented 81 simply inherited trait genes or major-effect QTL that have been cloned or fine mapped. For each gene, detailed information was compiled including chromosome locations, allelic variants and associated polymorphisms, predicted functions, and diagnostic markers that could be used for marker-assisted selection in cucumber breeding. We also documented 322 QTL for 42 quantitative traits, including 109 for disease resistances against seven pathogens. By alignment of these QTL on the latest version of cucumber draft genomes, consensus QTL across multiple studies were inferred, which provided insights into heritable correlations among different traits. Through collaborative efforts among public and private cucumber researchers, we identified 130 quantitative traits and developed a set of recommendations for QTL nomenclature in cucumber. This is the first attempt to systematically summarize, analyze and inventory cucumber mutants, cloned or mapped genes and QTL, which should be a useful resource for the cucurbit research community.