Gametophyte Thermal Priming Modifies the Transcriptomic Heat Stress Response of Sporophyte Progeny in Saccharina...

Saccharina latissima (sugar kelp) is a brown macroalga that forms kelp forests along North Atlantic coasts, playing a key role in coastal ecosystems. It is also of growing economic importance as the dominant species used in European kelp aquaculture. Both wild and cultivated kelps are increasingly threatened by marine heatwaves and elevated sea surface temperatures. Enhancing thermal tolerance could therefore benefit both conservation and production. Thermal priming, a method originating in agriculture where early life stages are exposed to moderate heat stress, can enhance resilience by inducing molecular stress memory. We applied a thermal priming treatment (20°C, 3 weeks) to S. latissima gametophytes before gametogenesis and sporophyte formation to test whether priming alters thermal responses in the derived sporophytes. Young sporophytes, produced by crossing primed or naïve (controls kept at 10°C) gametophytes, were reared at 10°C and then exposed to a heat stress (21.5°C for 48 h) before being allowed to recover at 10°C. Transcriptomic profiles and photophysiological characteristics were assessed before, during and after stress exposure to investigate priming-induced changes in thermal stress resilience. Sporophytes derived from primed gametophytes showed stronger transcriptomic responses under heat stress; for example, upregulation of HSP90B was unique to primed samples. Naïve sporophytes exhibited a delayed response with extensive downregulation during recovery (2027 DEGs). Gene ontology enrichment analysis indicated higher expression of protein phosphorylation, chloroplast-related functions, and post-transcriptional regulation by ncRNA in primed sporophytes, suggesting a priming effect on their transcriptomic thermal response. Primed sporophytes exhibited a delayed reduction in photosynthetic performance compared with naïve throughout the heat stress. These findings suggest that thermal priming induces a transgenerational stress memory. Our results support the view that temperature priming alters the transcriptomic thermal response in kelp through regulatory changes in gene expression, in line with existing literature on priming.