SlATG8f coordinates ethylene signaling and chloroplast turnover to drive tomato fruit ripening.

Abstract

Key message: qRT-PCR and yeast two-hybrid assays revealed that SlATG8f interacts with ethylene signaling to regulate fruit ripening via chloroplast autophagy and other biological pathways. Tomato fruit ripening is a highly coordinated process influenced by both internal and external signals, with ethylene recognized as a central regulator. However, the role of autophagy in ripening remains largely unexplored. Here, we demonstrate that ethylene signaling induces the expression of multiple SlATG8 genes, linking hormonal regulation with autophagic activity. Functional redundancy, compensation, or feedback regulation may exist among ATG8 family members. In particular, SlATG8f appears to mediate the degradation of negative regulators in the ethylene pathway via autophagy, thereby promoting ripening. We show that SlATG8f is essential for ethylene-induced fruit softening and must be maintained at optimal levels to ensure a proper ripening response. Moreover, SlATG8f contributes to sugar and acid accumulation, enhancing fruit quality. Using split-ubiquitin yeast two-hybrid screening, we identified 74 potential SlATG8F-interacting proteins, many of which are associated with chlorophyll degradation, energy metabolism, stress responses, and hormone signaling. These findings suggest that SlATG8F plays a broader role in integrating developmental and environmental cues through selective autophagy. Our study provides the first direct evidence that autophagy, particularly mediated by SlATG8f, fine-tunes tomato fruit ripening. This work offers new insights into the crosstalk between ethylene signaling and autophagy and highlights SlATG8f as a potential molecular hub for improving fruit quality and shelf life.