Integrated transcriptomics and metabolomics analyses reveal key genes and essential metabolic pathways for the acquisition of cold tolerance during dormancy in apple

Low temperature is a primary abiotic stress that significantly affects plant growth and development in the cool regions of Northeast China. It is the primary limiting factor in the development of the global apple industry. Numerous studies have investigated the alterations in transcriptional metabolism under low-temperature stress in various plants. However, research on the role of dormancy in regulating differences in cold tolerance among apple varieties is limited. Therefore, this study conducted a comprehensive analysis of the physiological and biochemical indices, transcriptome, and metabolome of the cold-tolerant variety ‘Hanfu’ (HF) and cold-sensitive variety ‘Naganofuji 2′ (CF) during endodormancy and ecodormancy. Under the low-temperature treatment, the cross-section of a 1-year-old branch of CF exhibited more severe browning than HF did, and the relative electrolyte leakage value of CF was higher than that of HF. Transcriptomics and metabolomics analysis revealed the key pathways of apples in response to low-temperature stress. Functional enrichment analysis showed that hormone signal transduction pathways and amino acid metabolism-related pathways were significantly enriched during endodormancy and ecodormancy, and these pathways were considered an important way for apples to respond to low-temperature freezing injury. The galactose metabolism pathway was significantly enriched only during endodormancy, while the membrane lipid metabolism pathway was significantly enriched only during ecodormancy. A gene co-expression network was constructed using weighted gene correlation network analysis, and six modules with biological significance were selected from the network. Among them, genes encoding transcription factors such as DREB1C/CBF2, JUB1, CCCH, and VIP1 are hub genes in different modules, which can be used as candidate genes to explore the network regulation pathway of apple response to low-temperature stress. Overall, these findings help to elucidate the molecular mechanism underlying freeze-tolerance in apples and provide novel insights into the regulatory network involved in the response of apples to low-temperature stress during dormancy.