The WUSCHEL-related homeobox1 gene of cucumber regulates reproductive organ development

The WUSCHEL-related homeobox1 (WOX1) transcription factor plays an important role in lateral growth of plant organs; however, the underlying mechanisms in the regulation of reproductive development are largely unknown. Cucumber (Cucumis sativus) has separate male and female flowers, facilitating the study of the role of WOX1 in stamen and carpel development. Here, we identified a mango fruit (mf) mutant in cucumber, which displayed multiple defects in flower growth as well as male and female sterility. Map-based cloning showed that Mf encodes a WOX1-type transcriptional regulator (CsWOX1), and that the mf mutant encodes a truncated protein lacking the conserved WUS box. Further analysis showed that elevated expression of CsWOX1 was responsible for the mutant phenotype in cucumber and Arabidopsis. Comparative transcriptome profiling revealed certain key players and CsWOX1-associated networks that regulate reproductive development. CsWOX1 directly interacts with cucumber SPOROCYTELESS (CsSPL), and many genes in the CsSPL-mediated pathway were down-regulated in plants with the mutant allele at the Mf locus. In addition, auxin distribution was affected in both male and female flowers of the mutant. Taking together, these data suggest that CsWOX1 may regulate early reproductive organ development and be involved in sporogenesis via the CsSPL-mediated pathway and/or modulate auxin signaling in cucumber.