A Functional Allele of CsFUL1 Regulates Fruit Length through Repressing CsSUP and Inhibiting Auxin Transport in Cucumber

Abstract

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.