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The unique flavonoids, quinochalcones, such as hydroxysafflor yellow A (HSYA) and carthamin, in the floret of safflower showed an excellent pharmacological effect in treating cardiocerebral vascular disease, yet the regulating mechanisms governing the flavonoid biosynthesis are largely unknown. In this study,  CtACO3 , the key enzyme genes required for the ethylene signaling pathway, were found positively related to the flavonoid biosynthesis at different floret development periods in safflower and has two  CtACO3  transcripts,  CtACO3-1  and  CtACO3-2 , and the latter was a splice variant of  CtACO3  that lacked 5’ coding sequences. The functions and underlying probable mechanisms of the two transcripts have been explored. The quantitative PCR data showed that  CtACO3-1  and  CtACO3-2  were predominantly expressed in the floret and increased with floret development. Subcellular localization results indicated that  Ct ACO3-1 was localized in the cytoplasm, whereas  Ct ACO3-2 was localized in the cytoplasm and nucleus. Furthermore, the overexpression of  Ct ACO3-1 or  Ct ACO3-2 in transgenic safflower lines significantly increased the accumulation of quinochalcones and flavonols. The expression of the flavonoid pathway genes showed an upward trend, with  CtCHS1 ,  CtF3H1 ,  CtFLS1 , and  CtDFR1  was considerably induced in the overexpression of  CtACO3-1  or  CtACO3-2  lines. An interesting phenomenon for  Ct ACO3-2 protein suppressing the transcription of  CtACO3-1  might be related to the nucleus location of  Ct ACO3-2. Yeast two-hybrid (Y2H), glutathione  S -transferase (GST) pull-down, and BiFC experiments revealed that  Ct ACO3-2 interacted with  Ct CSN5a. In addition, the interactions between  Ct CSN5a and  Ct COI1,  Ct COI1 and  Ct JAZ1,  Ct JAZ1 and  Ct bHLH3 were observed by Y2H and GST pull-down methods, respectively. The above results suggested that the  Ct ACO3-2 promoting flavonoid accumulation might be attributed to the transcriptional activation of flavonoid biosynthesis genes by  Ct bHLH3, whereas the  Ct bHLH3 might be regulated through  Ct CSN5- Ct COI1- Ct JAZ1 signal molecules. Our study provided a novel insight of  Ct ACO3 affected the flavonoid biosynthesis in safflower.

Both Two CtACO3 Transcripts Promoting the Accumulation of the Flavonoid Profiles in Overexpressed Transgenic Safflower