Physiological and transcriptome analysis of γ-aminobutyric acid (GABA) in improving Gracilariopsis lemaneiformis stress tolerance at high temperatures

Gracilariopsis lemaneiformis, an economically important red seaweed in China, is currently undergoing high-temperature (HT) stress due to global warming. To alleviate summertime HT stress, algae can acquire resistance through metabolism reprogramming and modulation of stress-related gene expression. gamma-Aminobutyric acid (GABA), a non-protein four-carbon amino acid, plays an important role in regulating various abiotic stresses. In the present study, GABA was applied to examine the effect on the tolerance of G. lemaneiformis against HT stress. It turned out that exogenous 100 mg/L GABA remarkably improved the algal relative growth rate (RGR) and phycobilipmtein (PBP) contents compared to those in the no-GABA treatment group under HT conditions. In addition, GABA significantly elevated the activities of antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) to efficiently scavenge ROS, thereby reducing oxidative damage to the membranes of HT-stressed algae. Subsequently, a de novo transcriptomic assembly of G. lemaneiformis thalli was performed to analyze transcriptional responses to HT stress. GABA significantly upregulated the expression of genes encoding antioxidant enzymes (SOD, CAT, POD, PRXR and APX), triggered calmodulin (CaM) and calcium-dependent protein kinase (CDPK) signaling, and improved the expression of genes encoding heat shock proteins (HSP70s and HSP90s) during HT stress. Moreover, GABA enhanced the expression of genes involved in proline and polyamine (PA) synthesis, TCA cycle, amino acid metabolism and alpha-linolenic acid metabolism in G. lemaneiformis, which helped to maintain better energy supply and metabolic homeostasis under HT stress. Collectively, these data reveals the critical roles of GABA in antioxidant activation, molecular signaling and energy metabolism that coordinately contribute to the improvement of HT stress tolerance in G. lemaneiformis. These data will also be useful for breeding heat-tolerant G. lemaneiformis genotypes in the future.