Early signaling events in the heat stress response of Pyropia haitanensis revealed by phosphoproteomic and lipidomic analyses

Abstract

Deciphering the heat stress signaling pathway will increase our ability to improve the thermotolerance of the economically important seaweed species Pyropia haitanensis, as one component of sustainable development against a background of ongoing climate change. Protein phosphorylation has several functions, including the integration of various signals, gene expression, and metabolic activities, in plant responses to abiotic stresses. In this study, we used quantitative phosphoproteomics and lipidomics techniques to identify the putative signal and downstream responses involved in P. haitanensis thermotolerance. The results revealed a broad network of highly dynamic changes in the phosphoprotein profile of thalli exposed to heat stress. The functional annotation of differentially phosphorylated proteins indicated that many of them are involved in calcium signaling, target of rapamycin (TOR) signaling, and mitogen-activated protein kinase (MAPK) signaling pathways at 30 min and 6 h under heat stress. Differentially phosphorylated proteins involved in phosphatidylinositol signaling, energy metabolism, and endocytosis as well as heat shock proteins were enriched at 12, 18, and 24 h after the heat treatment was initiated. Further analyses suggested that Ca2+ signaling and MAPK signaling may regulate the early response of thalli to heat stress by activating heat shock proteins. TOR signaling may lead to the rapid phosphorylation of the translation initiation factor to promote protein synthesis and trigger glycolysis to provide the energy and intermediate metabolites needed for thalli to resist the adverse effects of heat stress. Additionally, PI signaling was activated later to regulate the removal of polyunsaturated monogalactosyldiacylglycerol, increase saturated triacylglycerol contents, and increase endocytosis to maintain thalli membrane integrity in response to sustained heat stress. The present data provide insights into the signaling networks involved in the P. haitanensis response to heat stress.