Lipid metabolism-driven regulatory networks involved in cone senescence and seed maturation in pine (Pinus massoniana)

Abstract

Pine cone ripening represents a senescence process during which seed maturity increases. However, the regulatory mechanisms underlying these divergent developmental trajectories are poorly defined. We have integrated physiological, transcriptomic, and lipidomic analyses of Pinus massoniana cones and seeds to construct co-expression networks to elucidate maturation mechanisms. We report seed germination capacity to increased markedly during cone color transition (green to brown) and plateau thereafter, while seed vigor peaked during cone cracking. Transcriptomic analysis indicates that lipid metabolic pathways were enriched during maturation, with α-linolenic, linoleic, and arachidonic acid metabolism enriched in cones, and glycerolipid, fatty acid metabolism, and fatty acid biosynthesis enriched in seeds. Lipidomic profiling reveals dynamic lipid reprogramming: cone senescence was associated with triglyceride accumulation and glycerophospholipid degradation, whereas seed maturation involved a shift in lipid classes, with triglycerides/diglycerides and glycerophospholipids showing distinct associations with germination capacity and vigor, respectively. A time-ordered co-expression network reveals key regulatory modules: senescence-associated factors (e.g., ERF3) are linked to dehydrogenases involved in membrane lipid homeostasis disruption correlated with cone aging. Conversely, core genes involved in lipid metabolism, hormone response factors, and key transcription factors (e.g., bZIP1) formed a central module that is closely associated with lipid fluxes and may contribute to the regulation of seed germination capacity and vigor. These findings inform optimal harvest timing for P. massoniana seeds and elucidate molecular mechanisms driving conifer reproductive development.