Gain-of-function of the 1-aminocyclopropane-1-carboxylate synthase geneACS1Ginduces female flower development in cucumber gynoecy

Abstract

Unisexual flowers provide a useful system for studying plant sex determination. In cucumber (Cucumis sativus L.), three major Mendelian loci control unisexual flower development, Female (F), androecious [a; 1-aminocyclopropane-1-carboxylate {ACC} synthase 11, acs11], and Monoecious (M; ACS2), referred to here as the Female, Androecious, Monoecious (FAM) model, in combination with two genes, gynoecious (g, the WIP family C2H2 zinc finger transcription factor gene WIP1) and the ethylene biosynthetic gene ACC oxidase 2 (ACO2). The F locus, conferring gynoecy and the potential for increasing fruit yield, is defined by a 30.2-kb tandem duplication containing three genes. However, the gene that determines the Female phenotype, and its mechanism, remains unknown. Here, we created a set of mutants and revealed that ACS1G is responsible for gynoecy conferred by the F locus. The duplication resulted in ACS1G acquiring a new promoter and expression pattern; in plants carrying the F locus duplication, ACS1G is expressed early in floral bud development, where it functions with ACO2 to generate an ethylene burst. The resulting ethylene represses WIP1 and activates ACS2 to initiate gynoecy. This early ACS1G expression bypasses the need for ACS11 to produce ethylene, thereby establishing a dominant pathway for female floral development. Based on these findings, we propose a model for how these ethylene biosynthesis genes cooperate to control unisexual flower development in cucumber.

Graph-based pan-genome reveals structural and sequence variations related to agronomic traits and domestication in cucumber

“…We next performed genome-wide association studies (GWAS) using these genotyped SVs for three traits: female flower rate on a primary branch, fruit spine/wart density, and branch number. Two reported genes involved in cucumber sex determination ( m 30 and F 31 , 32 ) were detected in our association signals (Supplementary Fig. 7a ), and the highest peak of fruit spine/wart density on chromosome 6 directly pinpointed the reported causative SV (SV_COMINS_6G012210) upstream of CsGL3 (ref.…”

Exogenous auxin-induced ENHANCER OF SHOOT REGENERATION 2 (ESR2) enhances femaleness of cucumber by activating theCsACS2gene

“…These results indicated that the antagonistic relationship between CsWIP1 expression and ethylene synthesis was still present in exogenous auxin-induced cucumber sex determination. Because the mutation in CsACO2 (in the 406a line) results in the inhibition of ethylene synthesis in sex determination [ 12 , 15 ], the 406a line was used to determine the direct effect of exogenous IAA on sex-controlling genes. At 1 h of IAA treatment, CsACS2 and CsACS11 were upregulated, and the upregulation of CsACS2 was greater than that of CsACS11 .…”

“…In cucumber, CsACS2 and CsACS11 encode ACC synthases with different functions in sex determination. The ethylene synthesized jointly by CsACS11 and CsACO2 can promote the expression of CsACS2 , which then inhibits stamen development [ 12 , 17 ]. Mutations in CsACS2 and CsACS11 lead to the emergence of andromonoecious and androecious plants, respectively [ 14 , 29 ].…”

“…Three major loci ( F / f , M / m , and A / a ) have been proposed to determine the sex phenotype of cucumber, and all of them encode ACC synthases, the rate-limiting enzymes in ethylene synthesis [ 11 ]. Among them, CsACS1G is responsible for gynoecy conferred by the F locus [ 12 ]. The M gene encodes CsACS2, which is expressed in the carpel region of the female flower; its inactive form ( m ) results in the formation of bisexual flowers [ 13 ].…”

“…An additional androecious mutant was identified from a mutation of the CsACO2 gene [ 15 ]. The expression of CsACO2 has no sex specificity, but it initiates carpel development by promoting ethylene synthesis synergistically with CsACS1G and CsACS11 , both of which are expressed specifically in female flowers [ 12 , 15 ]. CsWIP1 encodes a C2H2 family transcription factor, and its mutation results in a plant with a few bisexual flowers at the lower nodes and continuous female flowers at the upper nodes [ 16 ].…”