Toward Mass Spectrometry Imaging in the Metabolomics Scale: Increasing Metabolic Coverage Through Multiple On-Tissue Chemical Modifications

Dueñas, Maria Emilia; Larson, Evan A.; Lee, Young Jin

doi:10.3389/fpls.2019.00860

Title: Toward Mass Spectrometry Imaging in the Metabolomics Scale: Increasing Metabolic Coverage Through Multiple On-Tissue Chemical Modifications

Journal Article · 12 July 2019 · Frontiers in Plant Science

DOI: https://doi.org/10.3389/fpls.2019.00860 · OSTI ID:1542477

Dueñas, Maria Emilia ^[1]; Larson, Evan A. ^[1]; Lee, Young Jin ^[1]

Iowa State University, Ames, IA (United States)

Exploring the metabolic differences directly on tissues is essential for the comprehensive understanding of how multicellular organisms function. Mass spectrometry imaging (MSI) is an attractive technique toward this goal; however, MSI in metabolomics scale has been hindered by multiple limitations. This is most notable for single cell level high-spatial resolution imaging because of the limited number of molecules in small sampling size and the low ionization yields of many metabolites. Several on-tissue chemical derivatization approaches have been reported to increase MSI signals of targeted compounds, especially in matrix-assisted laser desorption/ionization (MALDI)- MSI. Herein, we adopt a combination of chemical derivatization reactions, to selectively enhance metabolite signals of a specific functional group for each consecutive tissue section. Three well-known on-tissue derivatization methods were used as a proof of concept experiment: coniferyl aldehyde for primary amines, Girard’s reagent T for carbonyl groups, and 2-picolylamine for carboxylic acids. This strategy was applied to the cross-sections of leaves and roots from two different maize genotypes (B73 and Mo17), and enabled the detection of over six hundred new unique metabolite features compared to without modification. Statistical analysis indicated quantitative variation between metabolites in the tissue sections, while MS images revealed differences in localization of these metabolites. Combined, this untargeted approach facilitated the visualization of various classes of compounds, demonstrating the potential for untargeted MSI in the metabolomics scale.

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Research Organization:: Iowa State Univ., Ames, IA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); American Chemical Society (ACS); Society for Analytical Chemists of Pittsburgh (SACP)

OSTI ID:: 1542477

Alternate ID(s):: OSTI ID: 1903827

Journal Information:: Frontiers in Plant Science, Vol. 10; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 42 works

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References (78)

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High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf Dueñas, Maria Emilia; Klein, Adam T.; Alexander, Liza E. The Plant Journal, Vol. 89, Issue 4 https://doi.org/10.1111/tpj.13422	journal	February 2017
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Efficient Total Synthesis of 12-oxo-PDA and OPC-8:0 Ainai, Takayuki; Matsuumi, Michitaka; Kobayashi, Yuichi The Journal of Organic Chemistry, Vol. 68, Issue 20 https://doi.org/10.1021/jo0348571	journal	October 2003
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Direct imaging of single cells and tissue at sub-cellular spatial resolution using transmission geometry MALDI MS Zavalin, Andre; Todd, Erik M.; Rawhouser, Patrick D. Journal of Mass Spectrometry, Vol. 47, Issue 11 https://doi.org/10.1002/jms.3132	journal	November 2012
Matrix Recrystallization for MALDI-MS Imaging of Maize Lipids at High-Spatial Resolution Dueñas, Maria Emilia; Carlucci, Laura; Lee, Young Jin Journal of The American Society for Mass Spectrometry, Vol. 27, Issue 9 https://doi.org/10.1007/s13361-016-1422-0	journal	June 2016
Pyrylium Salts as Reactive Matrices for MALDI-MS Imaging of Biologically Active Primary Amines Shariatgorji, Mohammadreza; Nilsson, Anna; Källback, Patrik Journal of The American Society for Mass Spectrometry, Vol. 26, Issue 6 https://doi.org/10.1007/s13361-015-1119-9	journal	March 2015
High Spatial Resolution Imaging of Mouse Pancreatic Islets Using Nanospray Desorption Electrospray Ionization Mass Spectrometry Yin, Ruichuan; Kyle, Jennifer; Burnum-Johnson, Kristin Analytical Chemistry, Vol. 90, Issue 11 https://doi.org/10.1021/acs.analchem.8b00161	journal	April 2018
Microscopic imaging mass spectrometry assisted by on-tissue chemical derivatization for visualizing multiple amino acids in human colon cancer xenografts: Proteomics 2014 Toue, Sakino; Sugiura, Yuki; Kubo, Akiko PROTEOMICS, Vol. 14, Issue 7-8 https://doi.org/10.1002/pmic.201300041	journal	October 2013
Wax matters: absence of very-long-chain aldehydes from the leaf cuticular wax of the glossy11 mutant of maize compromises the prepenetration processes of Blumeria graminis: Maize glossy11 compromises powdery mildew prepenetration Hansjakob, A.; Riederer, M.; Hildebrandt, U. Plant Pathology, Vol. 60, Issue 6 https://doi.org/10.1111/j.1365-3059.2011.02467.x	journal	May 2011
Heterotic patterns of sugar and amino acid components in developing maize kernels Römisch-Margl, Lilla; Spielbauer, Gertraud; Schützenmeister, Andre Theoretical and Applied Genetics, Vol. 120, Issue 2 https://doi.org/10.1007/s00122-009-1190-3	journal	November 2009
Multi-matrix, dual polarity, tandem mass spectrometry imaging strategy applied to a germinated maize seed: toward mass spectrometry imaging of an untargeted metabolome Feenstra, Adam D.; Hansen, Rebecca L.; Lee, Young Jin The Analyst, Vol. 140, Issue 21 https://doi.org/10.1039/c5an01079a	journal	January 2015
Atmospheric pressure MALDI mass spectrometry imaging of tissues and cells at 1.4-μm lateral resolution Kompauer, Mario; Heiles, Sven; Spengler, Bernhard Nature Methods, Vol. 14, Issue 1 https://doi.org/10.1038/nmeth.4071	journal	November 2016
Laser Beam Filtration for High Spatial Resolution MALDI Imaging Mass Spectrometry Zavalin, Andre; Yang, Junhai; Caprioli, Richard Journal of The American Society for Mass Spectrometry, Vol. 24, Issue 7 https://doi.org/10.1007/s13361-013-0638-5	journal	May 2013
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Sodium-Doped Gold-Assisted Laser Desorption Ionization for Enhanced Imaging Mass Spectrometry of Triacylglycerols from Thin Tissue Sections Dufresne, Martin; Masson, Jean-François; Chaurand, Pierre Analytical Chemistry, Vol. 88, Issue 11 https://doi.org/10.1021/acs.analchem.6b01141	journal	May 2016
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On-Tissue Derivatization via Electrospray Deposition for Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Imaging of Endogenous Fatty Acids in Rat Brain Tissues Wu, Qian; Comi, Troy J.; Li, Bin Analytical Chemistry, Vol. 88, Issue 11 https://doi.org/10.1021/acs.analchem.6b01021	journal	May 2016
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Derivatization Strategies for the Detection of Triamcinolone Acetonide in Cartilage by Using Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Imaging Barré, Florian P. Y.; Flinders, Bryn; Garcia, João P. Analytical Chemistry, Vol. 88, Issue 24 https://doi.org/10.1021/acs.analchem.6b02491	journal	December 2016
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Direct imaging of single cells and tissue at sub-cellular spatial resolution using transmission geometry MALDI MS Zavalin, Andre; Todd, Erik M.; Rawhouser, Patrick D. Journal of Mass Spectrometry, Vol. 47, Issue 11 https://doi.org/10.1002/jms.3132	journal	November 2012
Microscopic imaging mass spectrometry assisted by on-tissue chemical derivatization for visualizing multiple amino acids in human colon cancer xenografts: Proteomics 2014 Toue, Sakino; Sugiura, Yuki; Kubo, Akiko PROTEOMICS, Vol. 14, Issue 7-8 https://doi.org/10.1002/pmic.201300041	journal	October 2013
Molecular histology analysis by matrix-assisted laser desorption/ionization imaging mass spectrometry using gold nanoparticles as matrix: Molecular histology analysis by MALDI-IMS using gold nanoparticles as matrix Tang, Ho-Wai; Wong, Melody Yee-Man; Lam, Wing Rapid Communications in Mass Spectrometry, Vol. 25, Issue 24 https://doi.org/10.1002/rcm.5281	journal	November 2011
Heterotic patterns of sugar and amino acid components in developing maize kernels Römisch-Margl, Lilla; Spielbauer, Gertraud; Schützenmeister, Andre Theoretical and Applied Genetics, Vol. 120, Issue 2 https://doi.org/10.1007/s00122-009-1190-3	journal	November 2009
Subcellular-level resolution MALDI-MS imaging of maize leaf metabolites by MALDI-linear ion trap-Orbitrap mass spectrometer Korte, Andrew R.; Yandeau-Nelson, Marna D.; Nikolau, Basil J. Analytical and Bioanalytical Chemistry, Vol. 407, Issue 8 https://doi.org/10.1007/s00216-015-8460-5	journal	January 2015
Microscopic visualization of testosterone in mouse testis by use of imaging mass spectrometry Shimma, Shuichi; Kumada, Henri-Obadja; Taniguchi, Hisanori Analytical and Bioanalytical Chemistry, Vol. 408, Issue 27 https://doi.org/10.1007/s00216-016-9594-9	journal	May 2016
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Reactions of Microsolvated Organic Compounds at Ambient Surfaces: Droplet Velocity, Charge State, and Solvent Effects Badu-Tawiah, Abraham K.; Campbell, Dahlia I.; Cooks, R. Graham Journal of The American Society for Mass Spectrometry, Vol. 23, Issue 6, p. 1077-1084 https://doi.org/10.1007/s13361-012-0365-3	journal	March 2012
Targeted Multiplex Imaging Mass Spectrometry in Transmission Geometry for Subcellular Spatial Resolution Thiery-Lavenant, Gwendoline; Zavalin, Andre I.; Caprioli, Richard M. Journal of The American Society for Mass Spectrometry, Vol. 24, Issue 4 https://doi.org/10.1007/s13361-012-0563-z	journal	February 2013
Laser Beam Filtration for High Spatial Resolution MALDI Imaging Mass Spectrometry Zavalin, Andre; Yang, Junhai; Caprioli, Richard Journal of The American Society for Mass Spectrometry, Vol. 24, Issue 7 https://doi.org/10.1007/s13361-013-0638-5	journal	May 2013
Implementation of a Gaussian Beam Laser and Aspheric Optics for High Spatial Resolution MALDI Imaging MS Zavalin, Andre; Yang, Junhai; Haase, Andreas Journal of The American Society for Mass Spectrometry, Vol. 25, Issue 6 https://doi.org/10.1007/s13361-014-0872-5	journal	April 2014
Pyrylium Salts as Reactive Matrices for MALDI-MS Imaging of Biologically Active Primary Amines Shariatgorji, Mohammadreza; Nilsson, Anna; Källback, Patrik Journal of The American Society for Mass Spectrometry, Vol. 26, Issue 6 https://doi.org/10.1007/s13361-015-1119-9	journal	March 2015
Matrix Recrystallization for MALDI-MS Imaging of Maize Lipids at High-Spatial Resolution Dueñas, Maria Emilia; Carlucci, Laura; Lee, Young Jin Journal of The American Society for Mass Spectrometry, Vol. 27, Issue 9 https://doi.org/10.1007/s13361-016-1422-0	journal	June 2016
Sputter-Coated Metal Screening for Small Molecule Analysis and High-Spatial Resolution Imaging in Laser Desorption Ionization Mass Spectrometry Hansen, Rebecca L.; Dueñas, Maria Emilia; Lee, Young Jin Journal of The American Society for Mass Spectrometry, Vol. 30, Issue 2 https://doi.org/10.1007/s13361-018-2081-0	journal	October 2018
Comparing two metabolic profiling approaches (liquid chromatography and gas chromatography coupled to mass spectrometry) for extra-virgin olive oil phenolic compounds analysis: A botanical classification perspective Bajoub, Aadil; Pacchiarotta, Tiziana; Hurtado-Fernández, Elena Journal of Chromatography A, Vol. 1428 https://doi.org/10.1016/j.chroma.2015.10.059	journal	January 2016
Optimization and Comparison of Multiple MALDI Matrix Application Methods for Small Molecule Mass Spectrometric Imaging Gemperline, Erin; Rawson, Stephanie; Li, Lingjun Analytical Chemistry, Vol. 86, Issue 20 https://doi.org/10.1021/ac5028534	journal	October 2014
In Situ Analysis of Small Populations of Adherent Mammalian Cells Using Laser Ablation Electrospray Ionization Mass Spectrometry in Transmission Geometry Jacobson, Rachelle S.; Thurston, Richard L.; Shrestha, Bindesh Analytical Chemistry, Vol. 87, Issue 24 https://doi.org/10.1021/acs.analchem.5b02971	journal	November 2015
On-Tissue Derivatization via Electrospray Deposition for Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Imaging of Endogenous Fatty Acids in Rat Brain Tissues Wu, Qian; Comi, Troy J.; Li, Bin Analytical Chemistry, Vol. 88, Issue 11 https://doi.org/10.1021/acs.analchem.6b01021	journal	May 2016
Sodium-Doped Gold-Assisted Laser Desorption Ionization for Enhanced Imaging Mass Spectrometry of Triacylglycerols from Thin Tissue Sections Dufresne, Martin; Masson, Jean-François; Chaurand, Pierre Analytical Chemistry, Vol. 88, Issue 11 https://doi.org/10.1021/acs.analchem.6b01141	journal	May 2016
Derivatization Strategies for the Detection of Triamcinolone Acetonide in Cartilage by Using Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Imaging Barré, Florian P. Y.; Flinders, Bryn; Garcia, João P. Analytical Chemistry, Vol. 88, Issue 24 https://doi.org/10.1021/acs.analchem.6b02491	journal	December 2016
High Spatial Resolution Imaging of Mouse Pancreatic Islets Using Nanospray Desorption Electrospray Ionization Mass Spectrometry Yin, Ruichuan; Kyle, Jennifer; Burnum-Johnson, Kristin Analytical Chemistry, Vol. 90, Issue 11 https://doi.org/10.1021/acs.analchem.8b00161	journal	April 2018
Efficient Total Synthesis of 12-oxo-PDA and OPC-8:0 Ainai, Takayuki; Matsuumi, Michitaka; Kobayashi, Yuichi The Journal of Organic Chemistry, Vol. 68, Issue 20 https://doi.org/10.1021/jo0348571	journal	October 2003
Atmospheric pressure MALDI mass spectrometry imaging of tissues and cells at 1.4-μm lateral resolution Kompauer, Mario; Heiles, Sven; Spengler, Bernhard Nature Methods, Vol. 14, Issue 1 https://doi.org/10.1038/nmeth.4071	journal	November 2016
Microencapsulated algal feeds as a sustainable replacement diet for broodstock in commercial bivalve aquaculture Willer, David F.; Furse, Samuel; Aldridge, David C. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-69645-0	journal	July 2020
Multi-matrix, dual polarity, tandem mass spectrometry imaging strategy applied to a germinated maize seed: toward mass spectrometry imaging of an untargeted metabolome Feenstra, Adam D.; Hansen, Rebecca L.; Lee, Young Jin The Analyst, Vol. 140, Issue 21 https://doi.org/10.1039/c5an01079a	journal	January 2015
The Metabolism of Acetaldehyde by Plant Tissues Fidler, J. C. Journal of Experimental Botany, Vol. 19, Issue 1 https://doi.org/10.1093/jxb/19.1.41	journal	January 1968
Amino Acid Export in Plants: A Missing Link in Nitrogen Cycling Okumoto, Sakiko; Pilot, Guillaume Molecular Plant, Vol. 4, Issue 3 https://doi.org/10.1093/mp/ssr003	journal	May 2011
Maize 9-Lipoxygenase ZmLOX3 Controls Development, Root-Specific Expression of Defense Genes, and Resistance to Root-Knot Nematodes Gao, Xiquan; Starr, James; Göbel, Cornelia Molecular Plant-Microbe Interactions, Vol. 21, Issue 1 https://doi.org/10.1094/mpmi-21-1-0098	journal	January 2008
Spatial Mapping and Profiling of Metabolite Distributions during Germination Feenstra, Adam D.; Alexander, Liza E.; Song, Zhihong Plant Physiology, Vol. 174, Issue 4 https://doi.org/10.1104/pp.17.00652	journal	June 2017
Wax matters: absence of very-long-chain aldehydes from the leaf cuticular wax of the glossy11 mutant of maize compromises the prepenetration processes of Blumeria graminis: Maize glossy11 compromises powdery mildew prepenetration Hansjakob, A.; Riederer, M.; Hildebrandt, U. Plant Pathology, Vol. 60, Issue 6 https://doi.org/10.1111/j.1365-3059.2011.02467.x	journal	May 2011
High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf Dueñas, Maria Emilia; Klein, Adam T.; Alexander, Liza E. The Plant Journal, Vol. 89, Issue 4 https://doi.org/10.1111/tpj.13422	journal	February 2017
Genome-wide association study for kernel composition and flour pasting behavior in wholemeal maize flour Alves, Mara Lisa; Carbas, Bruna; Gaspar, Daniel BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1729-7	journal	April 2019
Metabolomic Profiling of the Nectars of Aquilegia pubescens and A. Canadensis Noutsos, Christos; Perera, Ann M.; Nikolau, Basil J. PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0124501	journal	May 2015
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Synthesis and Functions of Jasmonates in Maize Borrego, Eli; Kolomiets, Michael Plants, Vol. 5, Issue 4 https://doi.org/10.3390/plants5040041	journal	November 2016
Changes in Polar Lipid Composition in Maize Seedlings Induced by Cadmium Stress ., Radhouane Chaffai; ., Mohamed Anis Elhammadi; ., Tini Nouhou Seybou International Journal of Agricultural Research, Vol. 2, Issue 2 https://doi.org/10.3923/ijar.2007.126.135	journal	February 2007

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59 BASIC BIOLOGICAL SCIENCES
mass spectrometry imaging
metabolomics
on-tissue derivatization
high-spatial resolution
maize
single cell

Title: Toward Mass Spectrometry Imaging in the Metabolomics Scale: Increasing Metabolic Coverage Through Multiple On-Tissue Chemical Modifications

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References (78)

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