The Chlamydomonas bZIP transcription factor BLZ8 confers oxidative stress tolerance by inducing the carbon-concentrating mechanism

Abstract

Photosynthetic organisms are exposed to various environmental sources of oxidative stress. Land plants have diverse mechanisms to withstand oxidative stress, but how microalgae do so remains unclear. Here, we characterized the Chlamydomonas reinhardtii bZIP transcription factor BLZ8, which is highly induced by oxidative stress. Oxidative stress tolerance increased with increasing BLZ8 expression levels. BLZ8 regulated the expression of genes likely involved in the carbon-concentrating mechanism (CCM): HIGH-LIGHT ACTIVATED 3 (HLA3), CARBONIC ANHYDRASE 7 (CAH7), and CARBONIC ANHYDRASE 8 (CAH8). BLZ8 expression increased the photosynthetic affinity for inorganic carbon under alkaline stress conditions, suggesting that BLZ8 induces the CCM. BLZ8 expression also increased the photosynthetic linear electron transfer rate, reducing the excitation pressure of the photosynthetic electron transport chain and in turn suppressing reactive oxygen species (ROS) production under oxidative stress conditions. A carbonic anhydrase inhibitor, ethoxzolamide, abolished the enhanced tolerance to alkaline stress conferred by BLZ8 overexpression. BLZ8 directly regulated the expression of the three target genes and required bZIP2 as a dimerization partner in activating CAH8 and HLA3. Our results suggest that a CCM-mediated increase in the CO2 supply for photosynthesis is critical to minimize oxidative damage in microalgae, since slow gas diffusion in aqueous environments limits CO2 availability for photosynthesis, which can trigger ROS formation.

Uncovering the “ZIP code” for bZIP dimers reveals novel motifs, regulatory rules and one billion years of cis-element evolution

“…Our results suggest that the important role of C/S1 bZIPs in seed development 30,51 may be mediated by hypoxia-related target genes. In fact, the functions of bZIPs in tolerance to oxidative stress can be traced back as early as algae 52 . Since hypoxia responses are also relevant in the context of plant response to submergence 53,54 , we compared the S1 and S1:C targets to genes that are differentially expressed following submergence treatment 55 and observed a much higher level of enrichment of S1 and S1:C targets in submergence-induced genes compared to submergence-repressed genes (Fig.…”

Widening the landscape of transcriptional regulation of green algal photoprotection

“…Therefore, acclimation to low-CO 2 availability needs to include not only activation of CCM to elevate CO 2 levels at the site of fixation, but also of protection against photooxidative damage. It was recently shown that overexpression of the bZIP transcription factor BLZ8, resulting in enhanced CCM via overexpression of HLA3, CAH7, and CAH8, conferred enhanced oxidative tolerance triggered by alkaline stress 57 . Although the qE capacity of the BLZ8 overexpressing lines was not assessed, this work suggests that CCM and protection from oxidative stress are physiologically interconnected.…”

Widening the landscape of transcriptional regulation of green algal photoprotection

“…Therefore, acclimation to low-CO 2 availability needs to include not only activation of CCM to elevate CO 2 levels at the site of fixation, but also of protection against photooxidative damage. It was recently shown that overexpression of the bZIP transcription factor BLZ8, resulting in enhanced CCM via overexpression of HLA3, CAH7 and CAH8, conferred enhanced oxidative tolerance triggered by alkaline stress 59 . Although the qE capacity of the BZL8 overexpressing lines was not assessed, this work suggests that CCM and protection from oxidative stress are physiologically interconnected.…”