The bZIP1 Transcription Factor Regulates Lipid Remodeling and Contributes to ER Stress Management in <i>Chlamydomonas reinhardtii</i>

Abstract

Endoplasmic reticulum (ER) stress is caused by the stress-induced accumulation of unfolded proteins in the ER. Here, we identified proteins and lipids that function downstream of the ER stress sensor INOSITOL-REQUIRING ENZYME1 (CrIRE1) that contributes to ER stress tolerance in Chlamydomonas (<i>Chlamydomonas reinhardtii</i>). Treatment with the ER stress inducer tunicamycin resulted in the splicing of a 32-nucleotide fragment of a basic leucine zipper 1 (bZIP1) transcription factor (<i>CrbZIP1</i>) mRNA by CrIRE1 that, in turn, resulted in the loss of the transmembrane domain in CrbZIP1, and the translocation of CrbZIP1 from the ER to the nucleus. Mutants deficient in <i>CrbZIP1</i> failed to induce the expression of the unfolded protein response genes and grew poorly under ER stress. Levels of diacylglyceryltrimethylhomoserine (DGTS) and pinolenic acid (18:3Δ5,9,12) increased in the parental strains but decreased in the <i>crbzip1</i> mutants under ER stress. A yeast one-hybrid assay revealed that CrbZIP1 activated the expression of enzymes catalyzing the biosynthesis of DGTS and pinolenic acid. Moreover, two lines harboring independent mutant alleles of <i>Chlamydomonas desaturase</i> (<i>CrDES</i>) failed to synthesize pinolenic acid and were more sensitive to ER stress than were their parental lines. Together, these results indicate that <i>CrbZIP1</i> is a critical component of the ER stress response mediated by CrIRE1 in Chlamydomonas that acts via lipid remodeling.