Homeodomain-leucine zipper (HD-Zip) transcription factors are only present in higher plants and are involved in plant development and stress responses. However, our understanding of their participation in the fruit ripening of economical plants, such as tomato (Solanum lycopersicum), remains largely unclear. Here, we report that VAHOX1, a member of the tomato HD-Zip I subfamily, was expressed in all tissues, was highly expressed in breaker+4 fruits, and could be induced by ethylene. RNAi repression of VAHOX1 (VAHOX1-RNAi) resulted in accelerated fruit ripening, enhanced sensitivity to ethylene, and increased total carotenoid content and ethylene production. Conversely, VAHOX1 overexpression (VAHOX1-OE) in tomato had the opposite effect. RNA-Seq results showed that altering VAHOX1 expression affected the transcript accumulation of a series of genes involved in ethylene biosynthesis and signal transduction and cell wall modification. Additionally, a dual-luciferase reporter assay, histochemical analysis of GUS activity and a yeast one-hybrid (Y1H) assay revealed that VAHOX1 could activate the expression of AP2a. Our findings may expand our knowledge about the physiological functions of HD-Zip transcription factors in tomato and highlight the diversities of transcriptional regulation during the fruit ripening process.
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