Mechanisms of metabolic adaptation in the duckweed Lemna gibba : an integrated metabolic, transcriptomic and flux analysis

BMC Plant Biology · 10 authors, 5 centres

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TL;DR

Lemna gibba fronds grown with glutamine as the nitrogen source grew 1.4 times faster and accumulated more protein compared to nitrate-grown fronds. 13C-metabolic flux analysis revealed substantial reorganization of fluxes around the TCA cycle depending on nitrogen source, yet these flux changes could largely not be associated with changes in transcript abundance.

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Lemna gibba was grown under photomixotrophic conditions on liquid media with glucose as carbon source, comparing nitrate versus glutamine as nitrogen sources. Growth kinetics, biomass composition, metabolite levels, transcript abundance, and 13C-metabolic flux analysis were performed. Fronds grown on glutamine grew 1.4 times faster and accumulated more protein and less cell wall components than those on nitrate. Flux analysis showed the Calvin-Benson-Bassham cycle and oxidative pentose-phosphate pathway were highly active under both conditions, constituting a futile cycle with net ATP consumption. Substantial reorganization of fluxes around the TCA cycle led to differential formation of biosynthetic precursors for Asp and Gln family amino acids depending on the nitrogen source.

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preclinical research

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ORIGINAL PAPER

PMC10546790

Mechanisms of metabolic adaptation in the duckweed Lemna gibba : an integrated metabolic, transcriptomic and flux analysis

BMC Plant Biology

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ABSTRACT

Abstract Background Duckweeds are small, rapidly growing aquatic flowering plants. Due to their ability for biomass production at high rates they represent promising candidates for biofuel feedstocks. Duckweeds are also excellent model organisms because they can be maintained in well-defined liquid media, usually reproduce asexually, and because genomic resources are becoming increasingly available. To demonstrate the utility of duckweed for integrated metabolic studies, we examined the metabolic adaptation of growing Lemna gibba cultures to different nutritional conditions. Results To establish a framework for quantitative metabolic research in duckweeds we derived a central carbon metabolism network model of Lemna gibba based on its draft genome. Lemna gibba fronds were grown with nitrate or glutamine as nitrogen source. The two conditions were compared by quantification of growth kinetics, metabolite levels, transcript abundance, as well as by 13 C-metabolic flux analysis. While growing with glutamine, the fronds grew 1.4 times faster and accumulated more protein and less cell wall components compared to plants grown on nitrate. Characterization of photomixotrophic growth by 13 C-metabolic flux analysis showed that, under both metabolic growth conditions, the Calvin-Benson-Bassham cycle and the oxidative pentose-phosphate pathway are highly active, creating a futile cycle with net ATP consumption. Depending on the nitrogen source, substantial reorganization of fluxes around the tricarboxylic acid cycle took place, leading to differential formation of the biosynthetic precursors of the Asp and Gln families of proteinogenic amino acids. Despite the substantial reorganization of fluxes around the tricarboxylic acid cycle, flux changes could largely not be associated with changes in transcripts. Conclusions Through integrated analysis of growth rate, biomass composition, metabolite levels, and metabolic flux, we show that Lemna gibba is an excellent system for quantitative metabolic studies in plants. Our study showed that Lemna gibba adjusts to different nitrogen sources by reorganizing central metabolism. The observed disconnect between gene expression regulation and metabolism underscores the importance of metabolic flux analysis as a tool in such studies. Supplementary Information The online version contains supplementary material available at 10.1186/s12870-023-04480-9. Keywords: Duckweeds, Lemna gibba , Metabolic flux analysis, Metabolome analysis, Transcriptome analysis

CITATION EXPORT

Hai Shi, Evan Ernst, Nicolas Heinzel et al.. Mechanisms of metabolic adaptation in the duckweed Lemna gibba: an integrated metabolic, transcriptomic and flux analysis. BMC Plant Biology. (2023). https://doi.org/10.1186/s12870-023-04480-9

AUTHORS

10 · 5 CENTRES

Hai Shi, Evan Ernst, Nicolas Heinzel, Sean McCorkle, Hardy Rolletschek, Ljudmilla Borisjuk, Stefan Ortleb, Robert Martienssen, John Shanklin, Jorg Schwender

1Biology Department, Brookhaven National Laboratory, Upton, NY 11973 USA
2Cold Spring Harbor Laboratory, 1 Bungtown Rd, Cold Spring Harbor, NY 11724 USA
3Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724 USA
4Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, D–06466 Seeland OT Gatersleben, Germany
5Brookhaven National Laboratory, Computational Science Initiative, Upton, NY 11973 USA