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Title: Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga

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.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
  1. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Biological Systems Science Division
OSTI Identifier:
1580873
Alternate Identifier(s):
OSTI ID: 1562686
Grant/Contract Number:  
AC02-05CH11231; SC0018301
Resource Type:
Accepted Manuscript
Journal Name:
Communications Biology
Additional Journal Information:
Journal Volume: 2; Journal Issue: 1; Journal ID: ISSN 2399-3642
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Roth, Melissa S., Westcott, Daniel J., Iwai, Masakazu, and Niyogi, Krishna K. Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga. United States: N. p., 2019. Web. doi:10.1038/s42003-019-0577-1.
Roth, Melissa S., Westcott, Daniel J., Iwai, Masakazu, & Niyogi, Krishna K. Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga. United States. doi:10.1038/s42003-019-0577-1.
Roth, Melissa S., Westcott, Daniel J., Iwai, Masakazu, and Niyogi, Krishna K. Thu . "Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga". United States. doi:10.1038/s42003-019-0577-1. https://www.osti.gov/servlets/purl/1580873.
@article{osti_1580873,
title = {Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga},
author = {Roth, Melissa S. and Westcott, Daniel J. and Iwai, Masakazu and Niyogi, Krishna K.},
abstractNote = {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.},
doi = {10.1038/s42003-019-0577-1},
journal = {Communications Biology},
number = 1,
volume = 2,
place = {United States},
year = {2019},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Figure 1 Figure 1: Mutants reveal hexokinase1 as regulator of photosynthesis. (A) Gene structure of CzHXK1 with mutation location and type of hxk1 mutations as determined by whole-genome sequencing (See Methods). (B) Image of extracted pigments from representative samples of WT and hxk1 mutants after 84 h with and without glucose (Glc).more » (C) Maximum photosystem Ⅱ efficiency ($F$$v$ / $F$$m$) of hxk1 mutants is insensitive to glucose. Data represent means ± SD (n = 4 biological replicates, individual data points shown). (D) Photosynthetic apparatus of hxk1 mutants is insensitive to glucose. Immunoblot analysis of PSⅡ (D2, CP43), PSI (PsaA), cytochrome b6f (Cyt b6), light-harvesting complex of PSⅡ (LHCⅡ), light-harvesting complex of PSⅠ (LHCⅠ), and ATP synthase (AtpB) subunits after 84 h with and without glucose. The global AtpB antibody detected both the chloroplastic AtpB at ~50 kDa and the mitochondrial AtpB at ~70 kDa. Samples were normalized to total protein, and 10 μg of protein were loaded in each well. See Fig. 1G for stained total protein gel loading control. Images of the detected chemiluminescent signal on the complete membranes are available in Supplementary Fig. 4. (E) Net oxygen evolution (oxygen production in the light, 100 μmol photons m−2 s−1) of hxk1 mutants is insensitive to glucose. Data represent means ± SD (n = 3 biological replicates, individual data points shown). (F) Respiration (oxygen consumption in the dark) of hxk1 mutants is sensitive to glucose. Data represent means ± SD (n = 3 biological replicates, individual data points shown). (G) SDS-PAGE analysis of total protein extracted from whole cells and stained with Coomassie brilliant blue. Samples were normalized to total protein, and 10 μg of protein were loaded in each well. (H) Cell volume of hxk1 mutants increases with glucose. Data represent means ± SD (n = 4 biological replicates, individual data points shown).« less

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