A unique chromosome translocation disrupting ClWIP1 leads to gynoecy in watermelon

Abstract

Summary To understand sex determination in watermelon (Citrullus lanatus), a spontaneous gynoecious watermelon mutant, XHBGM, was selected from the monoecious wild type XHB. Using map‐based cloning, resequencing and fluorescence in situ hybridization analysis, a unique chromosome translocation between chromosome 2 and chromosome 3 was found in XHBGM. Based on the breakpoint location in chromosome 2, a putative C2H2 zinc finger transcription factor gene, ClWIP1 (gene ID Cla008537), an orthologue of the melon gynoecy gene CmWIP1, was disrupted. Using clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR‐associated system 9 to edit ClWIP1, we obtained gynoecious watermelon lines. Functional studies showed that ClWIP1 is expressed specifically in carpel primordia and is related to the abortion of carpel primordia in early floral development. To identify the cellular and metabolic processes associated with ClWIP1, we compared the shoot apex transcriptomes of two gynoecious mutants and their corresponding wild types. Transcriptome analysis showed that differentially expressed genes related to the ethylene and cytokinin pathways were upregulated in the gynoecious mutants. This study explores the molecular mechanism of sex determination in watermelon and provides a theoretical and technical basis for breeding elite gynoecious watermelon lines.

Comparative transcriptomic analysis of the tea plant (Camellia sinensis) reveals key genes involved in pistil deletion

“…Studies have indicated that CsWIP1 can directly bind to the promoter of CsACO2 and inhibit its expression in cucumber plants, which affects the parthenocarpic composition [35]. Similar mechanisms have been observed in melons [34] and watermelons [36]. In the present study, the WIP transcription factor CSA026801 was also identified in DEGs.…”

“…Furthermore, a loss-of-function mutation in the CmWIP1 gene induces the formation of gynoecious plants [34]. The ortholog CsWIP1 of CmWIP1 can bind to the promoter of CsACO2 and suppress its expression, thereby regulating the development of unisexual flowers in cucumbers [35]; ClWIP1 was determined to be involved in the sex determination of watermelons [36].…”

Gene Interactions Regulating Sex Determination in Cucurbits

“…In gynoecious lines, an insertion of a transposon (1.3 kb downstream of the gene) represses the expression of CmWIP1 via epigenetic changes in its gene promoter. In watermelon, a chromosome translocation produced an insertion mutation in the ClWIP1 gene (the CmWIP1 ortholog), leading to a gynoecious line (Zhang et al, 2019). Natural mutants of CsWIP1 in cucumber varieties are unavailable.…”

“…Therefore, phenotype–genotype relationships are proposed as: monoecious, AAGyGyTmTm ; trimonoecious, AAGyGytmtm ; andromonoecious, aaGyGy ; gynoecious, AAgygyTmTm ; gynomonoecious, AAgygytmtm ; and hermaphroditic, aagygy . Recent gene cloning helped to identify that the a gene is a mutation in ClACS7 / CitACS4 , and the gy gene is mutated in ClWIP1 , which are orthologous genes of CsACS2 / CmACS7 and CsWIP1 / CmWIP1 , respectively (Boualem et al, 2016; Ji et al, 2016; Manzano et al, 2016;Zhang et al, 2019). Therefore, it seems that the WIP1 - CsACS2 / CmACS7 relationship is conserved in all the studied cucurbits.…”

Gynoecy instability in cucumber (Cucumis sativus L.) is due to unequal crossover at the copy number variation-dependent Femaleness (F) locus

“…Cucumber has a unique system for gynoecious sex expression which is based on CNV of a 30.2 kb region containing CsACS1G, a duplicated copy of CsACS1 but with recombinant promoter 38,39 . In melon and watermelon, the gynoecious sex expression is controlled by WIP1 homologs encoding a C2H2 zinc-finger transcription factor, which is a negative regulator of femaleness 66,67 . No gynoecious WIP1 mutant (CsWIP1) have been identified in natural cucumber populations.…”