Multi-omics responses of red algae Pyropia haitanensis to intertidal desiccation during low tides

Abstract

Since the blades of upper intertidal red algae Pyropia haitanensis can lose 90% cellular water during low tides, it is the desired material to explore complex mechanisms underlying the tolerance to intertidal desiccation, which may also be accompanied by other abiotic stresses. In the present study, multi-omics responses of the blades to single stress (SS) of desiccation, and triple stresses (TS) of desiccation, high-temperature, and high-light were determined using transcriptome, proteome, and metabolome analyses. Differentially expressed genes (DEGs), differentially expressed proteins (DEPs), and differentially accumulated metabolites (DAMs) were identified and further analyzed in pairs. The results showed that several pairs of DEGs/DEPs, DEGs/DAMs, and DEPs/DAMs participated in glyoxylate and dicarboxylate metabolism (ko00630), and carbon fixation in photosynthetic organisms (ko00710). Moreover, several pairs of DEGs/DAMs were significantly enriched in ether lipid metabolism (ko00565). Correlated DEGs/DAMs of glyoxylate and dicarboxylate metabolism were significantly enriched under both stressful conditions, and correlated DEGs/DAMs and DEPs/DAMs of carbon fixation in photosynthetic organisms were significantly enriched under SS and TS conditions, respectively. Therefore, we speculated that plasma membrane responded first to intertidal desiccation and activated stress signal transduction by degradation of phospholipid. Organic acids (malate and succinate) and amino acids (glutamate, aspartate, and alanine) involved in osmoregulation were then synthesized and accumulated to scavenge reactive oxygen species (ROS). Energy metabolism was reduced to prevent the accumulation of ROS and cellular damage by down-regulating most genes and their proteins involved in the pathway. Photosynthesis - antenna proteins (Lhca1) were up-regulated to prevent or lower light stress-induced damage. We considered that these pathways worked together to protect blades of P. haitanensis from intertidal desiccation and other accompanied stresses during low tides in high-temperature weather. Correctively, our current findings provided valuable insights into the breeding strategies of cultivars with improved resistance to abiotic stress caused by global warming.