Ubiquitination-dependent protein homeostasis is critical for the thermotolerance of the economically valuable seaweed Pyropia haitanensis

Abstract

Enhancing protein ubiquitination modifications via genetic manipulation may improve plant tolerance to various stresses. To identify ubiquitinated proteins and the related pathways influencing the thermotolerance of the seaweed Pyropia haitanensis, quantitative ubiquitome and proteome analyses of a thermotolerant strain (WO72–4) exposed to heat stress were performed. A total of 3,694 ubiquitinated sites in 1,285 proteins were identified after 0, 1, 3 and 120 h of a high-temperature treatment. In general, the ubiquitination modifications were negatively correlated with the protein expression patterns, but there were exceptions. The ubiquitin-modified proteins were divided into four clusters. The proteins that underwent changes in ubiquitination in response to heat stress were mainly related to protein processing in the endoplasmic reticulum, endocytosis, and ribosomes. Further analyses suggested that P. haitanensis can activate the ubiquitin–proteasome system through ubiquitination modifications and endocytosis to quickly remove incorrectly folded proteins and damaged organelles. Furthermore, the ubiquitination of HSP70 and HSP90 may modify their activities to ensure proteins are properly folded or they may lead to auxiliary ubiquitinations that result in the degradation of substrates, ultimately minimizing the detrimental effects of endoplasmic reticulum stress. The study findings have increased our understanding of how ubiquitination participates in the seaweed response to excessive heat (e.g., global warming).