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

Abstract

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