Lipid remodeling associated with chitooligosaccharides-induced heat tolerance of marine macroalgae Gracilariopsis lemaneiformis

Heat stress is a detrimental environmental factor limiting the growth and productivity of Gracilariopsis lemaneiformis, one of the most important economic marine red algae, and its adverse effects are expected to increase in the near future due to global warming. Thus, understanding the heat stress response of G. lemaneiformis and enhancing its ability to adapt to high temperatures have become of critical importance to aquaculture development. Previous study found that chitooligosaccharides (COS) can effectively alleviate the adverse effects of heat stress and enhance the heat tolerance of G. lemaneiformis. Although membrane lipids are of fundamental importance to the survival of plants under abiotic stress, whether membrane lipid adjustment is associated with COS-induced thermotolerance of G. lemaneiformis and possible related mechanism are still unclear. In this work, the variations of the lipid metabolic pathways of G. lemaneiformis in response to COS and subsequent heat stress are investigated. As manifested by transcriptomic profiles, the expression of genes involved in glycerolipid metabolism, glycerophospholipid metabolism, fatty acid metabolism, and alpha-linolenic acid metabolism were significantly enhanced in COS-induced thermotolerant G. lemaneiformis. Consistently, lipidomics analysis further revealed that glycerolipids of G. lemaneiformis, such as monogalactosyldiacylglycerol, digalactosyldiacylglycerol, sulfoquinovosyldiacylglycerol, phosphatidylglycerol, phosphatidylcholine, phosphatidylethanolamine and phosphatidic acid were significantly accumulated in response to COS and subsequent heat stress. Elevated unsaturation levels of lipid classes and free fatty acids might also be an effective strategy for improving thermotolerance in COS-induced G. lemaneiformis. Notably, jasmonic acid and ethylene have potential roles in the regulation of the COS-induced heat resistance of G. lemaneiformis. These results not only advance our understanding of the molecular mechanisms underlying the survival strategy of G. lemaneiformis under heat stress but also pave the way for the molecular breeding of the thermotolerant G. lemaneiformis.