Molecular Mechanisms of LFR-Mediated Resistance to Alternaria alternata Mr1 in Malus

Sorbitol is a major primary metabolite in Malus species, serving as the primary product of photosynthesis and the main form of carbon translocation. It also functions as a signaling molecule that regulates plant growth, development, and stress responses. Fungal foliar diseases are widespread in Malus and can cause substantial economic losses, yet the molecular mechanism underlying sorbitol-mediated disease resistance remains poorly understood. This study focused on Malus resistance to Alternaria alternata Mr1 and found that sorbitol markedly increased the accumulation of flavonoids, including phlorizin, phloretin, and catechin, enhancing disease resistance. Based on our previous transcriptome data, transcriptome analysis identified the chromatin remodeling factor LFR as a susceptibility-associated gene. LFR was transcriptionally downregulated by sorbitol and negatively regulated flavonoid biosynthesis. This study further identified the transcription factor MYBR1 , whose expression showed a negative correlation with that of LFR . MYBR1 was activated by sorbitol and facilitated flavonoid accumulation, and its overexpression restored resistance to Alternaria alternata Mr1 in plants with high LFR expression. Collectively, sorbitol suppresses LFR expression, relieving its inhibitory effect on MYBR1 , which in turn enhances flavonoid accumulation and boosts resistance to Alternaria alternata Mr1 in Malus . • This study unveils a novel signaling role for sorbitol in disease resistance. Beyond its known function as a photosynthetic product, sorbitol acts as an upstream epigenetic signal that inhibits the chromatin remodeler LFR, thereby linking sugar metabolism to chromatin-based immunity in apple. • We demonstrate that sorbitol-mediated suppression of LFR enhances chromatin accessibility, activating downstream defense metabolic pathways and boosting disease resistance in Malus species. • We identify LFR as a direct transcriptional repressor of MYBR1 and elucidate the mechanistic link: reduced LFR expression de-represses MYBR1, leading to the accumulation of flavonoid-based defense metabolites. • Functional validation confirms phlorizin, catechin, and phloretin as core antifungal metabolites within this pathway, providing tangible molecular targets for future disease-resistant apple breeding.