Integrated Transcriptomic and Metabolomic Analysis of Cold Stress Network in Interspecific Hybrids Between Chrysanthemum lavandulifolium (Fisch. ex Trautv.) Makino and × morifolium Ramat., cv. ‘Yannong Qiujin’

Groundcover chrysanthemums exhibit inherently poor low-temperature adaptability, making them highly vulnerable to cold stress and thereby constraining their large-scale regional cultivation. Interspecific hybridization was conducted between diploid Chrysanthemum lavandulifolium (Fisch. ex Trautv.) Makino (pollen donor) and hexaploid cultivar Chrysanthemum × morifolium Ramat., cv. ‘Yannong Qiujin’ (seed parent) to generate cold-tolerant groundcover chrysanthemum germplasm. Comprehensive physiological profiling and integrated multi-omics analyses were performed on both parental plants and their hybrid progeny to identify candidate molecular pathways associated with cold adaptation in ploidy-divergent Chrysanthemum hybrids. Hybrid progeny exhibited significantly lower semi-lethal temperature (LT50), malondialdehyde (MDA) content, and relative electrical conductivity compared with the female parent, indicating heterosis-mediated enhancement of cellular membrane integrity. Integrated transcriptomic and metabolomic profiling identified significant enrichment of glycerophospholipid metabolism in the hybrid progeny. Upregulated expression of glycerol-3-phosphate acyltransferase (GPAT) and lysophosphatidic acid acyltransferase (LPAAT) genes promoted substantial accumulation of lysophosphatidic acid (LPA) and phosphatidic acid (PA). We found that higher expression levels of GPAT and LPAAT were positively associated with increased accumulation of LPA and PA. PA further contributes to phosphatidylcholine (PC) synthesis, potentially improving plasma-membrane permeability and sustaining plasma membrane integrity under chilling stress. Meanwhile, transcript abundance of the inducer of CBF expression (ICE), cold-regulated (COR) genes were markedly elevated. This study identifies candidate molecular pathways underlying cold adaptation in hybrid progeny derived from ploidy-divergent Chrysanthemum, thereby providing a robust theoretical foundation for breeding novel cold-tolerant chrysanthemum cultivars.