Regulatory mechanisms underlying the maintenance of homeostasis in Pyropia haitanensis under hypersaline stress conditions.

Intertidal macroalgae are highly resistant to hypersaline stress conditions. However, the underlying mechanism remains unknown. In the present study, the mechanism behind Pyropia haitanensis responses to two hypersaline stress conditions [100‰ (HSS_100) and 110‰ (HSS_110)] was investigated via analyses of physiological and transcriptomic changes. We observed that the differences between the responses of Py. haitanensis to HSS_100 and HSS_110 conditions involved the following three aspects: osmotic regulation, ionic homeostasis, and adjustment to secondary stresses. First, the water retention of Py. haitanensis was maintained through increased expansin production under HSS_100 conditions, while cell wall pectin needed to be protected from hydrolysis via the increased abundance of a pectin methylesterase inhibitor under HSS_110 conditions. Meanwhile, Py. haitanensis achieved stable and rapid osmotic adjustments because of the coordinated accumulation of inorganic ions (K, Na, and Cl) and organic osmolytes (glycine betaine and trehalose) under HSS_100 conditions, but not under HSS_110 conditions. Second, Py. haitanensis maintained a higher K/Na ratio under HSS_100 conditions than under HSS_110 conditions, mainly via the export of Na into the apoplast rather than compartmentalizing it into the vacuoles, and the enhanced uptake and retention of K. However, K/Na homeostasis was not completely disrupted during a short-term exposure to HSS_110 conditions. Finally, the Py. haitanensis antioxidant system scavenged more ROS and synthesized more heat shock proteins under HSS_100 conditions than under HSS_110 conditions, although thalli may have been able to maintain a certain redox balance during a short-term exposure to HSS_110 conditions. These differences may explain why Py. haitanensis can adapt to HSS_100 conditions rather than HSS_110 conditions, and also why the thalli exposed to HSS_110 conditions can recover after being transferred to normal seawater. Thus, the data presented herein may elucidate the mechanisms enabling Pyropia species to tolerate the sudden and periodic changes in salinity typical of intertidal systems.