Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos

Romsdahl, Trevor B.; Kambhampati, Shrikaar; Koley, Somnath; Yadav, Umesh P.; Alonso, Ana Paula; Allen, Doug K.; Chapman, Kent D.

doi:10.3390/metabo11030148

Title: Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos

Abstract

The combination of ¹³C-isotopic labeling and mass spectrometry imaging (MSI) offers an approach to analyze metabolic flux in situ. However, combining isotopic labeling and MSI presents technical challenges ranging from sample preparation, label incorporation, data collection, and analysis. Isotopic labeling and MSI individually create large, complex data sets, and this is compounded when both methods are combined. Therefore, analyzing isotopically labeled MSI data requires streamlined procedures to support biologically meaningful interpretations. Using currently available software and techniques, here we describe a workflow to analyze ¹³C-labeled isotopologues of the membrane lipid and storage oil lipid intermediate-phosphatidylcholine (PC). Our results with embryos of the oilseed crops, Camelina sativa and Thlaspi arvense (pennycress), demonstrated greater ¹³C-isotopic labeling in the cotyledons of developing embryos compared with the embryonic axis. Greater isotopic enrichment in PC molecular species with more saturated and longer chain fatty acids suggest different flux patterns related to fatty acid desaturation and elongation pathways. The ability to evaluate MSI data of isotopically labeled plant embryos will facilitate the potential to investigate spatial aspects of metabolic flux in situ.

Authors:

;

; Yadav, Umesh P.;

; Allen, Doug K.;

Publication Date:: Thu Mar 04 00:00:00 EST 2021

Research Org.:: Univ. of North Texas, Denton, TX (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NSF); US Department of Agriculture (USDA)

OSTI Identifier:: 1769213

Alternate Identifier(s):: OSTI ID: 1853579

Grant/Contract Number:: SC0020325; U01 CA235508; IOS-1829365; DBI-1827534; DBI-1427621

Resource Type:: Published Article

Journal Name:: Metabolites

Additional Journal Information:: Journal Name: Metabolites Journal Volume: 11 Journal Issue: 3; Journal ID: ISSN 2218-1989

Publisher:: MDPI AG

Country of Publication:: Switzerland

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; mass spectrometry imaging; MALDI (matrix assisted laser desorption/ionization); metabolomics; lipidomics; 13C-labeling; oilseed

Citation Formats


                    Romsdahl, Trevor B., Kambhampati, Shrikaar, Koley, Somnath, Yadav, Umesh P., Alonso, Ana Paula, Allen, Doug K., and Chapman, Kent D. Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos.  Switzerland: N. p., 2021. 
Web.  doi:10.3390/metabo11030148.

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                    Romsdahl, Trevor B., Kambhampati, Shrikaar, Koley, Somnath, Yadav, Umesh P., Alonso, Ana Paula, Allen, Doug K., & Chapman, Kent D. Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos.  Switzerland.  https://doi.org/10.3390/metabo11030148

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                    Romsdahl, Trevor B., Kambhampati, Shrikaar, Koley, Somnath, Yadav, Umesh P., Alonso, Ana Paula, Allen, Doug K., and Chapman, Kent D. Thu .  
"Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos".  Switzerland.  https://doi.org/10.3390/metabo11030148.

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@article{osti_1769213,

  title        = {Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos},

  author       = {Romsdahl, Trevor B. and Kambhampati, Shrikaar and Koley, Somnath and Yadav, Umesh P. and Alonso, Ana Paula and Allen, Doug K. and Chapman, Kent D.},

  abstractNote = {The combination of 13C-isotopic labeling and mass spectrometry imaging (MSI) offers an approach to analyze metabolic flux in situ. However, combining isotopic labeling and MSI presents technical challenges ranging from sample preparation, label incorporation, data collection, and analysis. Isotopic labeling and MSI individually create large, complex data sets, and this is compounded when both methods are combined. Therefore, analyzing isotopically labeled MSI data requires streamlined procedures to support biologically meaningful interpretations. Using currently available software and techniques, here we describe a workflow to analyze 13C-labeled isotopologues of the membrane lipid and storage oil lipid intermediate-phosphatidylcholine (PC). Our results with embryos of the oilseed crops, Camelina sativa and Thlaspi arvense (pennycress), demonstrated greater 13C-isotopic labeling in the cotyledons of developing embryos compared with the embryonic axis. Greater isotopic enrichment in PC molecular species with more saturated and longer chain fatty acids suggest different flux patterns related to fatty acid desaturation and elongation pathways. The ability to evaluate MSI data of isotopically labeled plant embryos will facilitate the potential to investigate spatial aspects of metabolic flux in situ.},

  doi          = {10.3390/metabo11030148},

  journal      = {Metabolites},

  number       = 3,

  volume       = 11,

  place        = {Switzerland},

  year         = {Thu Mar 04 00:00:00 EST 2021},

  month        = {Thu Mar 04 00:00:00 EST 2021}

}

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Title: Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos

Abstract

Citation Formats

On the Inverse Correlation of Protein and Oil: Examining the Effects of Altered Central Carbon Metabolism on Seed Composition Using Soybean Fast Neutron Mutants journal, December 2019

Ultra Performance Liquid Chromatography and High Resolution Mass Spectrometry for the Analysis of Plant Lipids journal, January 2011

Mass Spectrometry Imaging of Biomolecular Information journal, December 2014

13C-Metabolic Flux Analysis in Developing Flax (Linum usitatissinum L.) Embryos to Understand Storage Lipid Biosynthesis journal, December 2019

Carbon conversion efficiency and central metabolic fluxes in developing sunflower (Helianthus annuus L.) embryos: Metabolic fluxes in sunflower embryos journal, August 2007

Cloning of a cDNA encoding diacylglycerol acyltransferase from Arabidopsis thaliana and its functional expression journal, June 1999

Mass spectrometry imaging for plant biology: a review journal, October 2015

Correcting for natural isotope abundance and tracer impurity in MS-, MS/MS- and high-resolution-multiple-tracer-data from stable isotope labeling experiments with IsoCorrectoR journal, December 2018

Cellular Plasticity in Response to Suppression of Storage Proteins in the Brassica napus Embryo journal, April 2020

In Vitro Sugar Transport in Zea mays L. Kernels: II. Characteristics of Sugar Absorption and Metabolism by Isolated Developing Embryos journal, June 1987

Oil crops for the future journal, August 2020

Three-dimensional visualization of membrane phospholipid distributions in Arabidopsis thaliana seeds: A spatial perspective of molecular heterogeneity journal, February 2017

New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications journal, April 2011

Tracking the metabolic pulse of plant lipid production with isotopic labeling and flux analyses: Past, present and future journal, April 2015

Identification and stacking of crucial traits required for the domestication of pennycress journal, January 2020

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Phospholipid:diacylglycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants journal, May 2000

Heterogeneous Distribution of Erucic Acid in Brassica napus Seeds journal, January 2020

Metabolite fingerprinting of pennycress ( Thlaspi arvense L.) embryos to assess active pathways during oil synthesis journal, February 2015

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The role of light in soybean seed filling metabolism journal, April 2009

Assessing compartmentalized flux in lipid metabolism with isotopes journal, September 2016

Compartmentation of Triacylglycerol Accumulation in Plants journal, November 2011

Mass spectrometry imaging with high resolution in mass and space journal, May 2013

Spatial and Temporal Mapping of Key Lipid Species in Brassica napus Seeds journal, February 2017

Engineering industrial fatty acids in oilseeds journal, July 2012

Non-conventional pathways enable pennycress (Thlaspi arvense L.) embryos to achieve high efficiency of oil biosynthesis journal, February 2020

Metabolic networks in motion: 13 C‐based flux analysis journal, January 2006

Two Acyltransferases Contribute Differently to Linolenic Acid Levels in Seed Oil journal, February 2017

Acyl Editing and Headgroup Exchange Are the Major Mechanisms That Direct Polyunsaturated Fatty Acid Flux into Triacylglycerols journal, August 2012

Combining Salt Doping and Matrix Sublimation for High Spatial Resolution MALDI Imaging Mass Spectrometry of Neutral Lipids journal, September 2019

imzML — A common data format for the flexible exchange and processing of mass spectrometry imaging data journal, August 2012

Biotechnology tools and applications for development of oilseed crops with healthy vegetable oils journal, November 2020

The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene journal, September 1999

Compartment-specific labeling information in 13C metabolic flux analysis of plants journal, August 2007

Sublimation as a method of matrix application for mass spectrometric imaging journal, September 2007

Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. journal, January 1994

Ion Mobility-Mass Spectrometry Imaging Workflow journal, August 2020

The Transport of Sugars to Developing Embryos Is Not via the Bulk Endosperm in Oilseed Rape Seeds journal, June 2008

Fluxomics - connecting ‘omics analysis and phenotypes: Fluxomics - a systems biology tool journal, January 2013

MSiReader: An Open-Source Interface to View and Analyze High Resolving Power MS Imaging Files on Matlab Platform journal, March 2013

Spatial analysis of lipid metabolites and expressed genes reveals tissue-specific heterogeneity of lipid metabolism in high- and low-oil Brassica napus L. seeds journal, June 2018

Mitochondrial Metabolism in Developing Embryos of Brassica napus journal, September 2006

Quantifying plant phenotypes with isotopic labeling & metabolic flux analysis journal, February 2016

Carbon and Nitrogen Provisions Alter the Metabolic Flux in Developing Soybean Embryos journal, January 2013

Matrix assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) for direct visualization of plant metabolites in situ journal, February 2016

Charge Distribution between Different Classes of Glycerophospolipids in MALDI-MS Imaging journal, March 2020

On the Inverse Correlation of Protein and Oil: Examining the Effects of Altered Central Carbon Metabolism on Seed Composition Using Soybean Fast Neutron Mutants
journal, December 2019

Ultra Performance Liquid Chromatography and High Resolution Mass Spectrometry for the Analysis of Plant Lipids
journal, January 2011

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journal, December 2014

13C-Metabolic Flux Analysis in Developing Flax (Linum usitatissinum L.) Embryos to Understand Storage Lipid Biosynthesis
journal, December 2019

Carbon conversion efficiency and central metabolic fluxes in developing sunflower (Helianthus annuus L.) embryos: Metabolic fluxes in sunflower embryos
journal, August 2007

Cloning of a cDNA encoding diacylglycerol acyltransferase from Arabidopsis thaliana and its functional expression
journal, June 1999

Mass spectrometry imaging for plant biology: a review
journal, October 2015

Correcting for natural isotope abundance and tracer impurity in MS-, MS/MS- and high-resolution-multiple-tracer-data from stable isotope labeling experiments with IsoCorrectoR
journal, December 2018

Cellular Plasticity in Response to Suppression of Storage Proteins in the Brassica napus Embryo
journal, April 2020

In Vitro Sugar Transport in Zea mays L. Kernels: II. Characteristics of Sugar Absorption and Metabolism by Isolated Developing Embryos
journal, June 1987

Oil crops for the future
journal, August 2020

Three-dimensional visualization of membrane phospholipid distributions in Arabidopsis thaliana seeds: A spatial perspective of molecular heterogeneity
journal, February 2017

New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications
journal, April 2011

Tracking the metabolic pulse of plant lipid production with isotopic labeling and flux analyses: Past, present and future
journal, April 2015

Identification and stacking of crucial traits required for the domestication of pennycress
journal, January 2020

Tissue-specific differences in metabolites and transcripts contribute to the heterogeneity of ricinoleic acid accumulation in Ricinus communis L. (castor) seeds
journal, January 2019

Phospholipid:diacylglycerol acyltransferase: An enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants
journal, May 2000

Heterogeneous Distribution of Erucic Acid in Brassica napus Seeds
journal, January 2020

Metabolite fingerprinting of pennycress ( Thlaspi arvense L.) embryos to assess active pathways during oil synthesis
journal, February 2015

A Combined Metabolomics and Fluxomics Analysis Identifies Steps Limiting Oil Synthesis in Maize Embryos
journal, September 2019

The role of light in soybean seed filling metabolism
journal, April 2009

Assessing compartmentalized flux in lipid metabolism with isotopes
journal, September 2016

Compartmentation of Triacylglycerol Accumulation in Plants
journal, November 2011

Mass spectrometry imaging with high resolution in mass and space
journal, May 2013

Spatial and Temporal Mapping of Key Lipid Species in Brassica napus Seeds
journal, February 2017

Engineering industrial fatty acids in oilseeds
journal, July 2012

Non-conventional pathways enable pennycress (Thlaspi arvense L.) embryos to achieve high efficiency of oil biosynthesis
journal, February 2020

Metabolic networks in motion: ¹³ C‐based flux analysis
journal, January 2006

Two Acyltransferases Contribute Differently to Linolenic Acid Levels in Seed Oil
journal, February 2017

Acyl Editing and Headgroup Exchange Are the Major Mechanisms That Direct Polyunsaturated Fatty Acid Flux into Triacylglycerols
journal, August 2012

Combining Salt Doping and Matrix Sublimation for High Spatial Resolution MALDI Imaging Mass Spectrometry of Neutral Lipids
journal, September 2019

imzML — A common data format for the flexible exchange and processing of mass spectrometry imaging data
journal, August 2012

Biotechnology tools and applications for development of oilseed crops with healthy vegetable oils
journal, November 2020

The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene
journal, September 1999

Compartment-specific labeling information in 13C metabolic flux analysis of plants
journal, August 2007

Sublimation as a method of matrix application for mass spectrometric imaging
journal, September 2007

Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis.
journal, January 1994

Ion Mobility-Mass Spectrometry Imaging Workflow
journal, August 2020

The Transport of Sugars to Developing Embryos Is Not via the Bulk Endosperm in Oilseed Rape Seeds
journal, June 2008

Fluxomics - connecting ‘omics analysis and phenotypes: Fluxomics - a systems biology tool
journal, January 2013

MSiReader: An Open-Source Interface to View and Analyze High Resolving Power MS Imaging Files on Matlab Platform
journal, March 2013

Spatial analysis of lipid metabolites and expressed genes reveals tissue-specific heterogeneity of lipid metabolism in high- and low-oil Brassica napus L. seeds
journal, June 2018

Mitochondrial Metabolism in Developing Embryos of Brassica napus
journal, September 2006

Quantifying plant phenotypes with isotopic labeling & metabolic flux analysis
journal, February 2016

Carbon and Nitrogen Provisions Alter the Metabolic Flux in Developing Soybean Embryos
journal, January 2013

Matrix assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) for direct visualization of plant metabolites in situ
journal, February 2016

Charge Distribution between Different Classes of Glycerophospolipids in MALDI-MS Imaging
journal, March 2020