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

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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.

Abstract

In plants, exogenous glucose represses photosynthesis but this phenomenon has been little studied in green algae. Roth et. al. discover through a forward genetics screen in C. zofingiensis that hexokinase 1 is needed to turn off photosynthesis in the presence of glucose and for glucose-mediated upregulation of lipid metabolism.

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Glc-TOR signalling leads transcriptome reprogramming and meristem activation

Yan Xiong, Matthew P. McCormack, Lei Li … (2013)

Meristems encompass stem/progenitor cells that sustain postembryonic growth of all plant organs. How meristems are activated and sustained by nutrient signalling remains enigmatic in photosynthetic plants. Combining chemical manipulations and chemical genetics at the photoautotrophic transition checkpoint, we reveal that shoot photosynthesis-derived glucose drives target-of-rapamycin (TOR) signalling relays through glycolysis and mitochondrial bioenergetics to control root meristem activation, which is decoupled from direct glucose sensing, growth-hormone signalling, and stem-cell maintenance. Surprisingly, glucose-TOR signalling dictates transcriptional reprogramming of remarkable gene sets involved in central and secondary metabolism, cell cycle, transcription, signalling, transport and folding. Systems, cellular and genetic analyses uncover TOR phosphorylation of E2Fa transcription factor for an unconventional activation of S-phase genes, and glucose-signalling defects in e2fa root meristems. Our findings establish pivotal roles of glucose-TOR signalling in unprecedented transcriptional networks wiring central metabolism and biosynthesis for energy and biomass production, and integrating localized stem/progenitor-cell proliferation through inter-organ nutrient coordination to control developmental transition and growth.

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Localization of the primary metabolic block produced by 2-deoxyglucose.

N Wick, H Nakada, D. R. Drury … (1957)

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Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings.

Daniel Osuna, Björn Usadel, Rosa Morcuende … (2007)

Arabidopsis seedlings were subjected to 2 days of carbon starvation, and then resupplied with 15 mm sucrose. The transcriptional and metabolic response was analyzed using ATH1 arrays, real-time quantitative (q)RT-PCR analysis of >2000 transcription regulators, robotized assays of enzymes from central metabolism and metabolite profiling. Sucrose led within 30 min to greater than threefold changes of the transcript levels for >100 genes, including 20 transcription regulators, 15 ubiquitin-targeting proteins, four trehalose phosphate synthases, autophagy protein 8e, several glutaredoxins and many genes of unknown function. Most of these genes respond to changes of endogenous sugars in Arabidopsis rosettes, making them excellent candidates for upstream components of sugar signaling pathways. Some respond during diurnal cycles, consistent with them acting in signaling pathways that balance the supply and utilization of carbon in normal growth conditions. By 3 h, transcript levels change for >1700 genes. This includes a coordinated induction of genes involved in carbohydrate synthesis, glycolysis, respiration, amino acid and nucleotide synthesis, DNA, RNA and protein synthesis and protein folding, and repression of genes involved in amino acid and lipid catabolism, photosynthesis and chloroplast protein synthesis and folding. The changes of transcripts are followed by a delayed activation of central metabolic pathways and growth processes, which use intermediates from these pathways. Sucrose and reducing sugars accumulate during the first 3-8 h, and starch for 24 h, showing that there is a delay until carbon utilization for growth recommences. Gradual changes of enzyme activities and metabolites are found for many metabolic pathways, including glycolysis, nitrate assimilation, the shikimate pathway and myoinositol, proline and fatty acid metabolism. After 3-8 h, there is a decrease of amino acids, followed by a gradual increase of protein.

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Author and article information

Contributors

Melissa S. Roth:

ORCID: http://orcid.org/0000-0001-7389-5982

Melissa.S.Roth@gmail.com

Krishna K. Niyogi:

ORCID: http://orcid.org/0000-0001-7229-2071

niyogi@berkeley.edu

Journal

Journal ID (nlm-ta): Commun Biol

Journal ID (iso-abbrev): Commun Biol

Title: Communications Biology

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2399-3642

Publication date (Electronic): 19 September 2019

Publication date PMC-release: 19 September 2019

Publication date Collection: 2019

Volume: 2

Electronic Location Identifier: 347

Affiliations

[1 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, Howard Hughes Medical Institute, Department of Plant and Microbial Biology, , University of California, ; Berkeley, CA 94720-3102 USA

[2 ]ISNI 0000 0001 2231 4551, GRID grid.184769.5, Molecular Biophysics and Integrated Bioimaging Division, , Lawrence Berkeley National Laboratory, ; Berkeley, CA 94720 USA

Author information

Melissa S. Roth http://orcid.org/0000-0001-7389-5982

Daniel J. Westcott http://orcid.org/0000-0002-1828-2582

Masakazu Iwai http://orcid.org/0000-0002-0986-9015

Krishna K. Niyogi http://orcid.org/0000-0001-7229-2071

Article

Publisher ID: 577

DOI: 10.1038/s42003-019-0577-1

PMC ID: 6753101

PubMed ID: 31552300

SO-VID: 4ec5b682-ce86-4d81-a35e-3483bd50d651

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 15 May 2019

Date accepted : 14 August 2019

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Keywords: photosynthesis,biodiesel,cellular microbiology,plant physiology,plant molecular biology

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Keywords: photosynthesis, biodiesel, cellular microbiology, plant physiology, plant molecular biology

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

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Journal of Green Building

Most cited references 18

Glc-TOR signalling leads transcriptome reprogramming and meristem activation

Localization of the primary metabolic block produced by 2-deoxyglucose.

Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings.

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