The basic helix-loop-helix transcription factor PpeUNE12 regulates peach ripening by promoting polyamine catabolism and anthocyanin synthesis.

Abstract

The basic helix-loop-helix (bHLH) transcription factors (TFs) play important roles in various plant developmental and biological processes. However, the precise mechanisms by which bHLH TFs regulate fruit ripening warrant further investigation. Polyamine oxidase (PAO) is crucial for polyamine (PA) catabolism and plays crucial roles in fruit ripening. However, the regulatory mechanism of PAO gene expression during fruit ripening remains largely unexplored. In this study, we identified a peach bHLH TF, PpeUNE12, which directly binds to and activates the promoter of PpePAO1. Silencing PpeUNE12 substantially increased PA accumulation and delayed peach fruit ripening, while overexpressing PpeUNE12 decreased PA accumulation and accelerated peach fruit ripening. Additionally, anthocyanin content decreased in PpeUNE12-silenced fruits but increased in PpeUNE12-overexpressing peach fruits compared to the control. RNA-seq and RT-qPCR analyses revealed that the majority of genes involved in anthocyanin biosynthesis, including PpeF3H, PpeCHS, PpeDFR, PpeUFGT and PpeMYB10.1 exhibited down-regulation in fruits with silenced PpeUNE12, while these genes were up-regulated in fruits overexpressing PpeUNE12. Although PpeUNE12 exhibited no direct binding to the promoters of PpeUFGT and PpeMYB10.1, it substantially activated their activity. This investigation is the first to provide evidence that bHLH regulates fruit maturation via promoting both PA catabolism and anthocyanin synthesis. It reveals a novel mechanism of bHLH in regulating fruit ripening and enhances our comprehension of the regulatory mechanism of PA catabolism and anthocyanin synthesis during fruit maturation.