Abstract
Global primary production is driven largely by oxygenic photosynthesis, with algae as major contributors. The green alga Chromochloris zofingiensis reversibly switches off photosynthesis in the presence of glucose in the light and augments production of biofuel precursors (triacylglycerols) and the high-value antioxidant astaxanthin. Here we used forward genetics to reveal that this photosynthetic and metabolic switch is mediated by the glycolytic enzyme hexokinase (CzHXK1). In contrast to wild-type, glucose-treated hxk1 mutants do not shut off photosynthesis or accumulate astaxanthin, triacylglycerols, or cytoplasmic lipid droplets. We show that CzHXK1 is critical for the regulation of genes related to photosynthesis, ketocarotenoid synthesis and fatty acid biosynthesis. Sugars play fundamental regulatory roles in gene expression, physiology, metabolism, and growth in plants and animals, and we introduce a relatively simple, emerging model system to investigate conserved eukaryotic sugar sensing and signaling at the base of the green lineage.
Highlights
Global primary production is driven largely by oxygenic photosynthesis, with algae as major contributors
We investigated the regulation of photosynthesis and metabolism in C. zofingiensis in response to exogenous glucose, building on the foundation provided by the recent highquality, chromosome-level genome and transcriptome of C. zofingiensis[5]
Using UV mutagenesis followed by selection on the glucose analog, 2-deoxy-D-glucose (2-DOG), we generated eight independent mutant strains that did not shut off photosynthesis and grew in the presence of 2-DOG with light. 2DOG is transported into the cell and phosphorylated but cannot be metabolized by glycolysis15–17. 2-DOG has been utilized to investigate sugar sensing in a variety of organisms[15,16]
Summary
Global primary production is driven largely by oxygenic photosynthesis, with algae as major contributors. The green alga Chromochloris zofingiensis reversibly switches off photosynthesis in the presence of glucose in the light and augments production of biofuel precursors (triacylglycerols) and the high-value antioxidant astaxanthin. Sugars play fundamental regulatory roles in gene expression, physiology, metabolism, and growth in plants and animals, and we introduce a relatively simple, emerging model system to investigate conserved eukaryotic sugar sensing and signaling at the base of the green lineage. Chromochloris zofingiensis, a unicellular coccoid green alga that is closely related to C. reinhardtii[5], reversibly turns off photosynthesis, degrades the photosynthetic apparatus, and reduces thylakoid membranes in the presence of glucose in the light[6]. Through a forward genetics screen, we uncovered hexokinase[1] (CzHXK1) as a master regulator of photosynthesis, carbon metabolism, and ketocarotenoid (astaxanthin) biosynthesis in C. zofingiensis. Our work establishes C. zofingiensis as a relatively simple system to investigate conserved mechanisms of sugar sensing and signaling in the green lineage
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