Environmentally Associated Developmental Reprogramming from Mycelial Growth to Fruiting Body Formation in Morchella eximia Under Off-Season Industrial Cultivation

Abstract

Morels (Morchella spp.) are highly valued edible fungi, but their cultivation remains largely dependent on seasonal field conditions. In this study, we established a stable off-season industrial cultivation system for Morchella eximia G10 through precise environmental regulation, including substrate and ambient temperature, humidity, and irrigation management. Based on this controllable cultivation platform, integrated transcriptomic and metabolomic analyses were conducted to explore developmental reprogramming from vegetative growth to fruiting body maturation. Metabolomic profiling was performed only at the reproductive stages, whereas transcriptomic analysis covered both vegetative and reproductive stages. Low-temperature stimulation was associated with marked increases in the expression of genes involved in cell wall remodeling, carbohydrate metabolism and stress responses, together with downregulation of genes annotated with oxidoreductase- and hydrolase-related functions. The transition to the primordium stage represented the most dynamic developmental transition and was associated with transcriptional regulation, cytoskeletal organization, and signal transduction pathways. Subsequently, distinct developmental trajectories were observed between pileus and stipe tissues, suggesting tissue-specific regulatory programs during fruiting body maturation. In the pileus, early amino acid- and nitrogen-related metabolism was coordinated with transcriptional changes, followed by a shift toward carbon and lipid metabolism. In the stipe, early development featured elevated aminoacyl-tRNA biosynthesis and translational capacity, followed by later adjustments in carbon, sulfur and lipid metabolism. These results provide a tissue-resolved multi-omics view of developmental reprogramming during the cold-treatment-associated transition from vegetative growth to fruiting in Morchella under controlled off-season cultivation. By linking environmental cues with stage- and tissue-specific transcriptional and metabolic programs, this work provides additional insights into reproductive development and extends previous descriptive omics studies, while offering a molecular basis for optimizing environmental regulation and improving the stability of industrial morel production.