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Rare genetic variants are abundant in genomes but less tractable in genome wide association study. Here we exploit a strategy of rare variation mapping to discover a gene essential to tendril development in cucumber (Cucumis sativus L.). In a collection of >3,000 lines, we discovered a unique tendril-less line that forms branches instead of tendrils and therefore, loses its climbing ability. We hypothesized that this unusual phenotype was caused by a rare variation and subsequently identified the causative single nucleotide polymorphism (SNP). The affected gene TEN is conserved within the cucurbits and is expressed specially in tendrils, representing a new organ identity gene. The variation occurs within a protein motif unique to the cucurbits and apparently impairs its function as a transcriptional activator. Analyses of transcriptomes from near-isogenic lines identified downstream genes required for tendril’s capability to sense and climb a support. This study provides an example to explore rare functional variants in plant genomes.
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