Regulation of the growth-to-ripening transition in tomato fruits by energy charge involving SlATP-PRT and SlAPRT1

The lifecycle of tomato fruit mainly comprises two distinct phases: the initial growth and development phase, followed by the ripening and senescence phase. However, the mechanism initially triggering the transition from an energy-intensive growth phase to the ripening phase remains unclear. First, we found that the fruit energy charge was significantly reduced before this transition, which might be caused by elevated levels of adenosine monophosphate (AMP) and histidine (His). Second, we constructed transgenic tomato plants for the key enzymes in the AMP salvage pathway (SlAPRT1) and His biosynthesis pathway (SlATP-PRT) via genome editing and overexpression. All transgenic plants caused a severe inhibition of fruit ripening, which was consistent with exogenous AMP treatment on wild-type plants, primarily due to the increased energy charge. Particularly, Slatp-prt mutant fruits could hardly produce ethylene or initiate ripening, but exogenous His treatment could restore their energy charge and ripening initiation. Finally, reducing the energy charge via exogenous His treatment also effectively accelerated the growth-to-ripening transition of wild-type fruits both on the plant and post-harvest. In conclusion, this study reveals that low energy charge and high His levels co-trigger the growth-to-ripening transition of tomato fruits, providing novel and valuable insights into the mechanisms underlying ripening initiation.