Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions

In this study we describe a [15N] stable isotopic labeling study of amino acids in Spirodela polyrhiza (common duckweed) grown under three different light and carbon input conditions which represent unique potential metabolic modes. Plants were grown with a light cycle, either with supplemental sucr...

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Main Authors: Erin M. Evans, Dana M. Freund, Veronica M. Sondervan, Jerry D. Cohen, Adrian D. Hegeman
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-05-01
Series:Frontiers in Chemistry
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fchem.2018.00191/full
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author Erin M. Evans
Erin M. Evans
Dana M. Freund
Dana M. Freund
Veronica M. Sondervan
Jerry D. Cohen
Jerry D. Cohen
Adrian D. Hegeman
Adrian D. Hegeman
Adrian D. Hegeman
author_facet Erin M. Evans
Erin M. Evans
Dana M. Freund
Dana M. Freund
Veronica M. Sondervan
Jerry D. Cohen
Jerry D. Cohen
Adrian D. Hegeman
Adrian D. Hegeman
Adrian D. Hegeman
author_sort Erin M. Evans
collection DOAJ
description In this study we describe a [15N] stable isotopic labeling study of amino acids in Spirodela polyrhiza (common duckweed) grown under three different light and carbon input conditions which represent unique potential metabolic modes. Plants were grown with a light cycle, either with supplemental sucrose (mixotrophic) or without supplemental sucrose (photoautotrophic) and in the dark with supplemental sucrose (heterotrophic). Labeling patterns, pool sizes (both metabolically active and inactive), and kinetics/turnover rates were estimated for 17 of the proteinogenic amino acids. Estimation of these parameters followed several overall trends. First, most amino acids showed plateaus in labeling patterns of <100% [15N]-labeling, indicating the possibility of a large proportion of amino acids residing in metabolically inactive metabolite pools. Second, total pool sizes appear largest in the dark (heterotrophic) condition, whereas active pool sizes appeared to be largest in the light with sucrose (mixotrophic) growth condition. In contrast turnover measurements based on pool size were highest overall in the light with sucrose experiment, with the exception of leucine/isoleucine, lysine, and arginine, which all showed higher turnover in the dark. K-means clustering analysis also revealed more rapid turnover in the light treatments with many amino acids clustering in lower-turnover groups. Emerging insights from other research were also supported, such as the prevalence of alternate pathways for serine metabolism in non-photosynthetic cells. These data provide extensive novel information on amino acid pool size and kinetics in S. polyrhiza and can serve as groundwork for future metabolic studies.
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spelling doaj.art-db64f607c9fd43a4b5cf6cd25599c3832022-12-22T02:26:45ZengFrontiers Media S.A.Frontiers in Chemistry2296-26462018-05-01610.3389/fchem.2018.00191364869Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth ConditionsErin M. Evans0Erin M. Evans1Dana M. Freund2Dana M. Freund3Veronica M. Sondervan4Jerry D. Cohen5Jerry D. Cohen6Adrian D. Hegeman7Adrian D. Hegeman8Adrian D. Hegeman9Department of Horticultural Science, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesPlant and Microbial Genomics Institute, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesDepartment of Horticultural Science, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesPlant and Microbial Genomics Institute, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesDepartment of Horticultural Science, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesDepartment of Horticultural Science, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesPlant and Microbial Genomics Institute, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesDepartment of Horticultural Science, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesPlant and Microbial Genomics Institute, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesDepartment of Plant and Microbial Biology, University of Minnesota, Twin Cities, Saint Paul, MN, United StatesIn this study we describe a [15N] stable isotopic labeling study of amino acids in Spirodela polyrhiza (common duckweed) grown under three different light and carbon input conditions which represent unique potential metabolic modes. Plants were grown with a light cycle, either with supplemental sucrose (mixotrophic) or without supplemental sucrose (photoautotrophic) and in the dark with supplemental sucrose (heterotrophic). Labeling patterns, pool sizes (both metabolically active and inactive), and kinetics/turnover rates were estimated for 17 of the proteinogenic amino acids. Estimation of these parameters followed several overall trends. First, most amino acids showed plateaus in labeling patterns of <100% [15N]-labeling, indicating the possibility of a large proportion of amino acids residing in metabolically inactive metabolite pools. Second, total pool sizes appear largest in the dark (heterotrophic) condition, whereas active pool sizes appeared to be largest in the light with sucrose (mixotrophic) growth condition. In contrast turnover measurements based on pool size were highest overall in the light with sucrose experiment, with the exception of leucine/isoleucine, lysine, and arginine, which all showed higher turnover in the dark. K-means clustering analysis also revealed more rapid turnover in the light treatments with many amino acids clustering in lower-turnover groups. Emerging insights from other research were also supported, such as the prevalence of alternate pathways for serine metabolism in non-photosynthetic cells. These data provide extensive novel information on amino acid pool size and kinetics in S. polyrhiza and can serve as groundwork for future metabolic studies.https://www.frontiersin.org/article/10.3389/fchem.2018.00191/fullstable isotopenitrogenSpirodela polyrhizaduckweedautotrophicheterotrophic
spellingShingle Erin M. Evans
Erin M. Evans
Dana M. Freund
Dana M. Freund
Veronica M. Sondervan
Jerry D. Cohen
Jerry D. Cohen
Adrian D. Hegeman
Adrian D. Hegeman
Adrian D. Hegeman
Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions
Frontiers in Chemistry
stable isotope
nitrogen
Spirodela polyrhiza
duckweed
autotrophic
heterotrophic
title Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions
title_full Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions
title_fullStr Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions
title_full_unstemmed Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions
title_short Metabolic Patterns in Spirodela polyrhiza Revealed by 15N Stable Isotope Labeling of Amino Acids in Photoautotrophic, Heterotrophic, and Mixotrophic Growth Conditions
title_sort metabolic patterns in spirodela polyrhiza revealed by 15n stable isotope labeling of amino acids in photoautotrophic heterotrophic and mixotrophic growth conditions
topic stable isotope
nitrogen
Spirodela polyrhiza
duckweed
autotrophic
heterotrophic
url https://www.frontiersin.org/article/10.3389/fchem.2018.00191/full
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