A functional allele of CsFUL1 regulates fruit length through inhibiting CsSUP and auxin transport in cucumber

Fruit length is a prominent agricultural trait during cucumber domestication and diversifying selection; however, the regulatory mechanisms of fruit elongation remain elusive. We found two alleles of the FRUITFULL-like MADS-box gene CsFUL1 with 3393C-A SNP variation among 150 cucumber lines, in which CsFUL1A was specifically enriched in the long-fruited East Asian type cucumbers (China and Japan), whereas the CsFUL1C allele was randomly distributed in natural cucumber populations including wild and semi-wild cucumbers. CsFUL1A knockdown led to further fruit elongation in cucumber, whereas elevated expression of CsFUL1A resulted in significantly shorter fruits. No effect on fruit elongation was detected upon modulation of CsFUL1C expression, suggesting that CsFUL1A is a gain-of-function allele in long-fruited cucumber that acts as a repressor during diversifying selection of East Asian cucumbers. Furthermore, CsFUL1A binds to the CArG box in the promoter region of the SUPERMAN (CsSUP) gene to repress its expression in regulating cell division and expansion. Additionally, CsFUL1A inhibits the expression of auxin transporters PIN-FORMED 1 and 7, resulting in decreases in auxin accumulation in fruits. Together, our work provides an agriculturally important allele with practical application for manipulation of fruit length via modulating CsFUL1A expression levels in cucumber breeding.