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 zofingiensisreversibly 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:
-
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). 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. https://doi.org/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. https://doi.org/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 zofingiensisreversibly 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 = {Thu Sep 19 00:00:00 EDT 2019},
month = {Thu Sep 19 00:00:00 EDT 2019}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Interaction between Starch Breakdown, Acetate Assimilation, and Photosynthetic Cyclic Electron Flow in Chlamydomonas reinhardtii
journal, June 2012
- Johnson, Xenie; Alric, Jean
- Journal of Biological Chemistry, Vol. 287, Issue 31
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
The Ability of a Charophyte Alga Hexokinase to Restore Glucose Signaling and Glucose Repression of Gene Expression in a Glucose-Insensitive Arabidopsis Hexokinase Mutant Depends on Its Catalytic Activity
journal, December 2018
- Ulfstedt, Mikael; Hu, Guo-Zhen; Eklund, D. Magnus
- Frontiers in Plant Science, Vol. 9
Glucose repression can be alleviated by reducing glucose phosphorylation rate in Saccharomyces cerevisiae
journal, February 2018
- Lane, Stephan; Xu, Haiqing; Oh, Eun Joong
- Scientific Reports, Vol. 8, Issue 1
Master regulators in plant glucose signaling networks
journal, March 2014
- Sheen, Jen
- Journal of Plant Biology, Vol. 57, Issue 2
Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling
journal, April 2003
- Moore, B.
- Science, Vol. 300, Issue 5617
Isozymes of Plant Hexokinase: Occurrence, Properties and Functions
journal, July 2007
- Claeyssen, Eric; Rivoal, Jean
- ChemInform, Vol. 38, Issue 27
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions
journal, October 2007
- Merchant, S. S.; Prochnik, S. E.; Vallon, O.
- Science, Vol. 318, Issue 5848, p. 245-250
The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains
journal, November 2012
- Breuer, Guido; Lamers, Packo P.; Martens, Dirk E.
- Bioresource Technology, Vol. 124
Subdiffraction-resolution live-cell imaging for visualizing thylakoid membranes
journal, July 2018
- Iwai, Masakazu; Roth, Melissa S.; Niyogi, Krishna K.
- The Plant Journal, Vol. 96, Issue 1
Isozymes of plant hexokinase: Occurrence, properties and functions
journal, March 2007
- Claeyssen, Éric; Rivoal, Jean
- Phytochemistry, Vol. 68, Issue 6
Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine
journal, March 2006
- Li, Y.
- Genome Research, Vol. 16, Issue 3
Dynamic and diverse sugar signaling
journal, October 2016
- Li, Lei; Sheen, Jen
- Current Opinion in Plant Biology, Vol. 33
Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009
- Li, H.; Durbin, R.
- Bioinformatics, Vol. 25, Issue 14
Plant Hexokinases are Multifaceted Proteins
journal, April 2017
- Aguilera-Alvarado, G. Paulina; S�nchez-Nieto, Sobeida
- Plant and Cell Physiology, Vol. 58, Issue 7
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
journal, July 1998
- Field, C. B.
- Science, Vol. 281, Issue 5374
Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings: Dynamics of transcriptional and metabolic responses to sucrose
journal, January 2007
- Osuna, Daniel; Usadel, Bjorn; Morcuende, Rosa
- The Plant Journal, Vol. 49, Issue 3
Transcriptome analysis of Chlorella zofingiensis to identify genes and their expressions involved in astaxanthin and triacylglycerol biosynthesis
journal, July 2016
- Huang, Weiping; Ye, Jingrun; Zhang, Jingjing
- Algal Research, Vol. 17
A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids
journal, April 1984
- Wessel, D.; Flügge, U. I.
- Analytical Biochemistry, Vol. 138, Issue 1
A central integrator of transcription networks in plant stress and energy signalling
journal, August 2007
- Baena-González, Elena; Rolland, Filip; Thevelein, Johan M.
- Nature, Vol. 448, Issue 7156
SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms
journal, June 2006
- Rolland, Filip; Baena-Gonzalez, Elena; Sheen, Jen
- Annual Review of Plant Biology, Vol. 57, Issue 1
Nitrogen-depleted Chlorella zofingiensis produces astaxanthin, ketolutein and their fatty acid esters: a carotenoid metabolism study
journal, May 2014
- Mulders, Kim J. M.; Weesepoel, Yannick; Bodenes, Pierre
- Journal of Applied Phycology, Vol. 27, Issue 1
Nutritional Control of cell Pigmentation in Chlorella Protothecoides with Special Reference to the Degeneration of Chloroplast Induced by Glucose1
journal, May 1964
- Shihira-Ishikawa, Ikuko; Hase, Eiji
- Plant and Cell Physiology, Vol. 5, Issue 2
Glucose–TOR signalling reprograms the transcriptome and activates meristems
journal, March 2013
- Xiong, Yan; McCormack, Matthew; Li, Lei
- Nature, Vol. 496, Issue 7444
Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production
journal, May 2017
- Roth, Melissa S.; Cokus, Shawn J.; Gallaher, Sean D.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 21
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Chlorella zofingiensis as an Alternative Microalgal Producer of Astaxanthin: Biology and Industrial Potential
journal, June 2014
- Liu, Jin; Sun, Zheng; Gerken, Henri
- Marine Drugs, Vol. 12, Issue 6
Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis
journal, February 2019
- Roth, Melissa S.; Gallaher, Sean D.; Westcott, Daniel J.
- The Plant Cell, Vol. 31, Issue 3
Glucose sensing and the mitochondrial alternative pathway are involved in the regulation of astaxanthin biosynthesis in the dark-grown Chlorella zofingiensis (Chlorophyceae)
journal, July 2008
- Li, Yantao; Huang, Junchao; Sandmann, Gerhard
- Planta, Vol. 228, Issue 5
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w
journal, April 2012
- Cingolani, Pablo; Platts, Adrian; Wang, Le Lily
- Fly, Vol. 6, Issue 2
Localization of the Primary Metabolic Block Produced by 2-Deoxyglucose
journal, February 1957
- Wick, Arne N.; Drury, Douglas R.; Nakada, Henry I.
- Journal of Biological Chemistry, Vol. 224, Issue 2
The chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii: Isolation, characterization and immunological cross-reactivity to higher-plant polypeptides
journal, February 1991
- Bassi, Roberto; Wollman, Francis-Andr�
- Planta, Vol. 183, Issue 3
Glucose sensing and the mitochondrial alternative pathway are involved in the regulation of astaxanthin biosynthesis in the dark-grown Chlorella zofingiensis (Chlorophyceae)
journal, July 2008
- Li, Yantao; Huang, Junchao; Sandmann, Gerhard
- Planta, Vol. 228, Issue 5
Nitrogen-depleted Chlorella zofingiensis produces astaxanthin, ketolutein and their fatty acid esters: a carotenoid metabolism study
journal, May 2014
- Mulders, Kim J. M.; Weesepoel, Yannick; Bodenes, Pierre
- Journal of Applied Phycology, Vol. 27, Issue 1
Master regulators in plant glucose signaling networks
journal, March 2014
- Sheen, Jen
- Journal of Plant Biology, Vol. 57, Issue 2
Transcriptome analysis of Chlorella zofingiensis to identify genes and their expressions involved in astaxanthin and triacylglycerol biosynthesis
journal, July 2016
- Huang, Weiping; Ye, Jingrun; Zhang, Jingjing
- Algal Research, Vol. 17
The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains
journal, November 2012
- Breuer, Guido; Lamers, Packo P.; Martens, Dirk E.
- Bioresource Technology, Vol. 124
Dynamic and diverse sugar signaling
journal, October 2016
- Li, Lei; Sheen, Jen
- Current Opinion in Plant Biology, Vol. 33
Pigment and Structural Changes in Chlorella zofingiensis upon Light and Nitrogen Stress
journal, July 1995
- Bar, Etan; Rise, Moshe; Vishkautsan, Marina
- Journal of Plant Physiology, Vol. 146, Issue 4
A central integrator of transcription networks in plant stress and energy signalling
journal, August 2007
- Baena-González, Elena; Rolland, Filip; Thevelein, Johan M.
- Nature, Vol. 448, Issue 7156
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
A type 2C protein phosphatase activates high-affinity nitrate uptake by dephosphorylating NRT2.1
journal, March 2021
- Ohkubo, Yuri; Kuwata, Keiko; Matsubayashi, Yoshikatsu
- Nature Plants, Vol. 7, Issue 3
Targeted introduction of heritable point mutations into the plant mitochondrial genome
journal, March 2022
- Forner, Joachim; Kleinschmidt, Dennis; Meyer, Etienne H.
- Nature Plants, Vol. 8, Issue 3
Targeted A-to-G base editing of chloroplast DNA in plants
journal, December 2022
- Mok, Young Geun; Hong, Sunghyun; Bae, Su-Ji
- Nature Plants, Vol. 8, Issue 12
Glucose repression can be alleviated by reducing glucose phosphorylation rate in Saccharomyces cerevisiae
journal, February 2018
- Lane, Stephan; Xu, Haiqing; Oh, Eun Joong
- Scientific Reports, Vol. 8, Issue 1
Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production
journal, May 2017
- Roth, Melissa S.; Cokus, Shawn J.; Gallaher, Sean D.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 21
Hexokinase 2 Is an Intracellular Glucose Sensor of Yeast Cells That Maintains the Structure and Activity of Mig1 Protein Repressor Complex
journal, February 2016
- Vega, Montserrat; Riera, Alberto; Fernández-Cid, Alejandra
- Journal of Biological Chemistry, Vol. 291, Issue 14
The Glucose-regulated Nuclear Localization of Hexokinase 2 in Saccharomyces cerevisiae Is Mig1-dependent
journal, January 2004
- Ahuatzi, Deifilia; Herrero, Pilar; de la Cera, Tamara
- Journal of Biological Chemistry, Vol. 279, Issue 14
Plant Hexokinases are Multifaceted Proteins
journal, April 2017
- Aguilera-Alvarado, G. Paulina; S�nchez-Nieto, Sobeida
- Plant and Cell Physiology, Vol. 58, Issue 7
Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine
journal, March 2006
- Li, Y.
- Genome Research, Vol. 16, Issue 3
Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis
journal, February 2019
- Roth, Melissa S.; Gallaher, Sean D.; Westcott, Daniel J.
- The Plant Cell, Vol. 31, Issue 3
Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling
journal, April 2003
- Moore, B.
- Science, Vol. 300, Issue 5617
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
journal, July 1998
- Field, C. B.
- Science, Vol. 281, Issue 5374
Transcriptome and de novo analysis of Rosa xanthina f. spontanea in response to cold stress
journal, October 2021
- Zhuang, Defeng; Ma, Ce; Xue, Li
- BMC Plant Biology, Vol. 21, Issue 1
RNA Purification from the Unicellular Green Alga, Chromochloris zofingiensis
journal, January 2018
- Gallaher, Sean; Roth, Melissa
- BIO-PROTOCOL, Vol. 8, Issue 7
Hexokinase as a Sugar Sensor in Higher Plants
journal, January 1997
- Jang, Jyan-Chyun; Leon, Patricia; Zhou, Li
- The Plant Cell, Vol. 9, Issue 1
Chlorella zofingiensis as an Alternative Microalgal Producer of Astaxanthin: Biology and Industrial Potential
journal, June 2014
- Liu, Jin; Sun, Zheng; Gerken, Henri
- Marine Drugs, Vol. 12, Issue 6
Works referencing / citing this record:
New Insights into Xanthophylls and Lipidomic Profile Changes Induced by Glucose Supplementation in the Marine Diatom Nitzschia laevis
journal, July 2022
- Mao, Xuemei; Wang, Xia; Ge, Mengdie
- Marine Drugs, Vol. 20, Issue 7
Figures / Tables found in this record: