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

• Published in: BMC plant biology Vol. 23; no. 1; pp. 1 - 458
• Main Authors: Shi, Hai, Ernst, Evan, Heinzel, Nicolas, McCorkle, Sean, Rolletschek, Hardy, Borisjuk, Ljudmilla, Ortleb, Stefan, Martienssen, Robert, Shanklin, John, Schwender, Jorg
• Format: Journal Article
• Language: English
• Published: London BioMed Central Ltd 03.10.2023; BioMed Central; Springer Science + Business Media; BMC
• Subjects: Adaptation; Adaptation (Physiology); Amino acids; Analysis; Aquatic plants; Biofuels; Biomass; Biomass energy; Botanical research; Carbon; Cell walls; Duckweed; Duckweeds; Floating plants; Flowering; Flowering plants; Fluctuations; Fluxes; Fronds; Gene expression; Genes; Genetic aspects; Genomes; Genomics; Glucose; Glutamine; Growth conditions; Growth kinetics; Lemna gibba; Lemnaceae; Lipids; Mass spectrometry; Metabolic flux; Metabolic flux analysis; Metabolism; Metabolites; Metabolome analysis; Monosaccharides; Nitrates; Nitrogen; Nitrogen sources; Pentose; Phosphates; Physiological aspects; Plants (botany); Scientific imaging; Sugars; Transcriptome analysis; Transcriptomics; Tricarboxylic acid cycle; United States
• ISSN: 1471-2229; 1471-2229
• DOI: 10.1186/s12870-023-04480-9

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. 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 .sup.13C-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 .sup.13C-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. 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.