TAF1 and GCN5-mediated histone acetylation of regulatory cascade AHL14/17-A/NINV7 promotes sucrose catabolism and sugar accumulation for cold tolerance in Citrus.

Sugar metabolism plays a vital role in plant cold tolerance. Histone acetyltransferases (HATs) act as key epigenetic regulators of stress-responsive genes, yet the function and mechanism underlying HAT-mediated histone acetylation (HA) in regulation of sugar metabolism under cold stress remain largely unclear. In this study, we demonstrate that PtrAHL14 and PtrAHL17, two cold-induced AT-hook motif-containing nuclear-localized proteins (AHLs) from Poncirus trifoliata, interact with TATA-binding protein (TBP)-Associated Factor 1 (PtrTAF1) and General Control Nonrepressed protein 5 (PtrGCN5), forming a functional quaternary complex at the nuclear matrix. The AHLs recruit PtrTAF1 and PtrGCN5 to the matrix-associated region of PtrA/NINV7, an alkaline/neutral invertase gene, leading to acetylation of H3K9, H3K14, H3K27, and H4K8 under cold stress. Furthermore, both HATs were found to modulate cold tolerance by cooperatively regulating PtrA/NINV7-mediated accumulation of reducing sugars. PtrAHL14 and PtrAHL17 directly interact with H3 and H4 and enhance HA, while PtrTAF1 and PtrGCN5 exhibit accumulative effects on triggering HA, thereby amplifying AHL-mediated regulation of PtrA/NINV7. Taken together, our findings unveil a novel HATs-AHLs-A/NINV7 regulatory module that epigenetically controls sucrose catabolism in response to cold stress, providing valuable insights into understanding the molecular regulation of sugar accumulation for improved cold tolerance.