A mutation in CsABCB19 encoding an ATP-binding cassette auxin transporter leads to erect and compact leaf architecture in cucumber (Cucumis sativus L.)

Leaf architecture, including leaf position and leaf morphology, is a critical component of plant architecture that directly determines plant appearance, photosynthetic utilization, and ultimate productivity. The mechanisms regulating leaf petiole angle and leaf flatness in cucumber remain unclear. In this study, we identified an erect and compact leaf architecture mutant (ecla) from an EMS (ethyl methanesulfonate) -mutagenized cucumber population, which exhibited erect petioles and crinkled leaves. Histological examination revealed significant phenotypic variation in ecla was associated with asymmetric cell expansion. MutMap sequencing combined with genetic mapping revealed that CsaV3_5G037960 is the causative gene for the ecla mutant phenotype. Through protein sequence alignment and Arabidopsis genetic complementation, we identified this gene as a functional direct homolog encoding the ATP-binding cassette transporter AtABCB19, hence named CsABCB19. A nonsynonymous mutation in the eleventh exon of CsABCB19 leads to premature termination of translation. The expression level of CsABCB19 in the ecla mutant was significantly reduced in all tissues compared to the wild type (WT). Transcriptome analysis revealed that auxin and polarity-related genes were significantly differentially expressed in mutant petioles and leaves, compared with those in WT. Auxin assay and exogenous treatment further demonstrated that CsABCB19 regulates leaf architecture by mediating auxin accumulation and transport. Our research is the first report describing the role of the ABCB19 transporter protein in auxin transport controlling cucumber leaf development. Furthermore, this study provides recent insights into the genetic mechanisms conferring morphological diversity and regulation of petiole angle and leaf flattening. DATA AVAILABILITY: The RNA-seq data in this study have been deposited in the NCBI SRA under BioProject accession number PRJNA874548.