RiLinc6978-encoded P6978 interacts with ASR1 to regulate ROS homeostasis

Tomato (Solanum lycopersicum) fruit ripening is tightly associated with dynamic changes in reactive oxygen species (ROS) homeostasis, yet the underlying regulatory mechanisms remain incompletely understood. Here, we identify a functional protein, P6978, encoded by the long non-coding RNA RiLinc6978, which contains a conserved 333-nucleotides short open reading frame (sORF) with high translational potential. Structural and physicochemical analyses revealed that P6978 is a stable, hydrophilic 110-amino acid basic polypeptide. P6978 predominantly localizes to the nucleus and directly interacts with the abscisic acid/stress-ripening transcription factor ABA stress-ripening 1 (ASR1). Multi-modal interaction assays (in vitro and in vivo) demonstrated that P6978 binding modulates ASR1’s transcriptional repression of antioxidant-related genes, thereby coordinately enhancing both enzymatic (such as superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; and glutathione reductase, GR) and non-enzymatic (ascorbate, glutathione, carotenoids, polyamines) ROS-scavenging systems during fruit maturation. Integrated transcriptomic and alternative splicing analyses revealed that loss of P6978 perturbs metabolic pathways linked to ROS metabolism, pigment biosynthesis, and stress responses. Our findings establish a previously unrecognized regulatory module in which a lncRNA-derived protein fine-tunes transcription factor output to optimize ROS homeostasis, accelerate tomato fruit ripening, and potentially improve postharvest stress resilience. This work expands the functional scope of plant lncRNAs and provides promising targets for horticultural crop improvement.