A CIPTL-CIDW1 module controls dwarfism and organ size through auxin transport-mediated cell elongation in watermelon

Dwarfism offers agronomic advantages in watermelon for high-density cultivation especially for protected cultivation, yet the genetic mechanisms underlying compact architecture in watermelon remain poorly understood. In this study, we demonstrate that CIDW1, a previously fine-mapped gene encoding an auxin transporter of the ABCB family, positively regulates plant height and fruit size in watermelon. CRISPR/Cas9-mediated knockout of CIDW1 resulted in dwarf plants with shorter stems and smaller fruits due to impaired cell elongation. This was further validated by knockout its cucumber homolog CsABCB19, suggesting their conserved function in regulating plant height and fruit size in cucurbit crops. Multi-omics analyses revealed that CIDW1 dysfunction disrupts auxin-response pathways and reduces basipetal auxin efflux, leading to auxin accumulation in stems. We further identified the trihelix transcription factor CIPTL as a direct transcriptional activator of CIDW1, binding to a light-responsive GT3-bx motif in its promoter independently of light signaling. Mutants of CIPTL recapitulated the dwarf and small-fruit phenotypes, confirming the CIPTL-CIDW1 module as a key regulator of auxin-mediated growth. Utilizing a 5K liquid-phase chip for marker-assisted selection, we developed six elite dwarf germplasms carrying the Cldw1 allele, which exhibit significantly reduced plant height and fruit size without affecting fruit quality. Our study elucidates a conserved regulatory pathway governing plant architecture and organ size in cucurbits, and provides functional germplasm for breeding compact watermelon varieties suited to mechanized and high-density production systems.