DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Investigation of the chemical interface in the soybean–aphid and rice–bacteria interactions using MALDI-mass spectrometry imaging

Abstract

Mass spectrometry imaging (MSI) is an emerging technology for high-resolution plant biology. It has been utilized to study plant–pest interactions, but limited to the surface interfaces. Here we expand the technology to explore the chemical interactions occurring inside the plant tissues. Two sample preparation methods, imprinting and fracturing, were developed and applied, for the first time, to visualize internal metabolites of leaves in matrix-assisted laser desorption ionization (MALDI)-MSI. This is also the first time nanoparticle-based ionization was implemented to ionize diterpenoid phytochemicals that were difficult to analyze with traditional organic matrices. The interactions between rice–bacterium and soybean–aphid were investigated as two model systems to demonstrate the capability of high-resolution MSI based on MALDI. Localized molecular information on various plant- or pest-derived chemicals provided valuable insight for the molecular processes occurring during the plant–pest interactions. Basically, salicylic acid and isoflavone based resistance was visualized in the soybean–aphid system and antibiotic diterpenoids in rice–bacterium interactions.

Authors:
 [1];  [1];  [2];  [3];  [2];  [2];  [2];  [2];  [2];  [2];  [1]
  1. Iowa State Univ., Ames, IA (United States); Ames Lab., Ames, IA (United States)
  2. Iowa State Univ., Ames, IA (United States)
  3. Shanghai Jiao Tong Univ., Shanghai (China); Iowa State Univ., Ames, IA (United States)
Publication Date:
Research Org.:
Ames Laboratory (AMES), Ames, IA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1227451
Report Number(s):
IS-J-8639
Journal ID: ISSN 0003-2700
Grant/Contract Number:  
2014-67013-21720; AC02-07CH11358
Resource Type:
Accepted Manuscript
Journal Name:
Analytical Chemistry
Additional Journal Information:
Journal Volume: 87; Journal Issue: 10; Journal ID: ISSN 0003-2700
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Klein, Adam T., Yagnik, Gargey B., Hohenstein, Jessica D., Ji, Zhiyuan, Zi, Jiachen, Reichert, Malinda D., MacIntosh, Gustavo C., Yang, Bing, Peters, Reuben J., Vela, Javier, and Lee, Young Jin. Investigation of the chemical interface in the soybean–aphid and rice–bacteria interactions using MALDI-mass spectrometry imaging. United States: N. p., 2015. Web. doi:10.1021/acs.analchem.5b00459.
Klein, Adam T., Yagnik, Gargey B., Hohenstein, Jessica D., Ji, Zhiyuan, Zi, Jiachen, Reichert, Malinda D., MacIntosh, Gustavo C., Yang, Bing, Peters, Reuben J., Vela, Javier, & Lee, Young Jin. Investigation of the chemical interface in the soybean–aphid and rice–bacteria interactions using MALDI-mass spectrometry imaging. United States. https://doi.org/10.1021/acs.analchem.5b00459
Klein, Adam T., Yagnik, Gargey B., Hohenstein, Jessica D., Ji, Zhiyuan, Zi, Jiachen, Reichert, Malinda D., MacIntosh, Gustavo C., Yang, Bing, Peters, Reuben J., Vela, Javier, and Lee, Young Jin. Mon . "Investigation of the chemical interface in the soybean–aphid and rice–bacteria interactions using MALDI-mass spectrometry imaging". United States. https://doi.org/10.1021/acs.analchem.5b00459. https://www.osti.gov/servlets/purl/1227451.
@article{osti_1227451,
title = {Investigation of the chemical interface in the soybean–aphid and rice–bacteria interactions using MALDI-mass spectrometry imaging},
author = {Klein, Adam T. and Yagnik, Gargey B. and Hohenstein, Jessica D. and Ji, Zhiyuan and Zi, Jiachen and Reichert, Malinda D. and MacIntosh, Gustavo C. and Yang, Bing and Peters, Reuben J. and Vela, Javier and Lee, Young Jin},
abstractNote = {Mass spectrometry imaging (MSI) is an emerging technology for high-resolution plant biology. It has been utilized to study plant–pest interactions, but limited to the surface interfaces. Here we expand the technology to explore the chemical interactions occurring inside the plant tissues. Two sample preparation methods, imprinting and fracturing, were developed and applied, for the first time, to visualize internal metabolites of leaves in matrix-assisted laser desorption ionization (MALDI)-MSI. This is also the first time nanoparticle-based ionization was implemented to ionize diterpenoid phytochemicals that were difficult to analyze with traditional organic matrices. The interactions between rice–bacterium and soybean–aphid were investigated as two model systems to demonstrate the capability of high-resolution MSI based on MALDI. Localized molecular information on various plant- or pest-derived chemicals provided valuable insight for the molecular processes occurring during the plant–pest interactions. Basically, salicylic acid and isoflavone based resistance was visualized in the soybean–aphid system and antibiotic diterpenoids in rice–bacterium interactions.},
doi = {10.1021/acs.analchem.5b00459},
journal = {Analytical Chemistry},
number = 10,
volume = 87,
place = {United States},
year = {Mon Apr 27 00:00:00 EDT 2015},
month = {Mon Apr 27 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 48 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Improved imaging resolution in desorption electrospray ionization mass spectrometry
journal, September 2008

  • Kertesz, Vilmos; Van Berkel, Gary J.
  • Rapid Communications in Mass Spectrometry, Vol. 22, Issue 17
  • DOI: 10.1002/rcm.3662

Effector proteins that modulate plant–insect interactions
journal, August 2011


Plant immunity: towards an integrated view of plant–pathogen interactions
journal, June 2010

  • Dodds, Peter N.; Rathjen, John P.
  • Nature Reviews Genetics, Vol. 11, Issue 8
  • DOI: 10.1038/nrg2812

Improved spatial resolution in the imaging of biological tissue using desorption electrospray ionization
journal, June 2012

  • Campbell, Dahlia I.; Ferreira, Christina R.; Eberlin, Livia S.
  • Analytical and Bioanalytical Chemistry, Vol. 404, Issue 2
  • DOI: 10.1007/s00216-012-6173-6

Molecular Imaging of Biological Samples:  Localization of Peptides and Proteins Using MALDI-TOF MS
journal, December 1997

  • Caprioli, Richard M.; Farmer, Terry B.; Gile, Jocelyn
  • Analytical Chemistry, Vol. 69, Issue 23
  • DOI: 10.1021/ac970888i

Mass Spectrometry Imaging of Cassette-Dosed Drugs for Higher Throughput Pharmacokinetic and Biodistribution Analysis
journal, July 2014

  • Swales, John G.; Tucker, James W.; Strittmatter, Nicole
  • Analytical Chemistry, Vol. 86, Issue 16
  • DOI: 10.1021/ac502217r

Chemical imaging of trichome specialized metabolites using contact printing and laser desorption/ionization mass spectrometry
journal, November 2013

  • Li, Chao; Wang, Zhenzhen; Jones, A. Daniel
  • Analytical and Bioanalytical Chemistry, Vol. 406, Issue 1
  • DOI: 10.1007/s00216-013-7444-6

Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae
journal, May 2010


Plant terpenoid synthases: Molecular biology and phylogenetic analysis
journal, April 1998

  • Bohlmann, J.; Meyer-Gauen, G.; Croteau, R.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 8
  • DOI: 10.1073/pnas.95.8.4126

Soybean defense responses to the soybean aphid
journal, July 2008


Phloem-sap feeding by animals: problems and solutions
journal, January 2006


Spatial Mapping of Lipids at Cellular Resolution in Embryos of Cotton
journal, February 2012

  • Horn, Patrick J.; Korte, Andrew R.; Neogi, Purnima B.
  • The Plant Cell, Vol. 24, Issue 2
  • DOI: 10.1105/tpc.111.094581

Phytoalexins in defense against pathogens
journal, February 2012


Methyl Salicylate, a Soybean Aphid-Induced Plant Volatile Attractive to the Predator Coccinella septempunctata
journal, July 2005


Molecular characterisation of a candidate gut sucrase in the pea aphid, Acyrthosiphon pisum
journal, April 2007

  • Price, D. R. G.; Karley, A. J.; Ashford, D. A.
  • Insect Biochemistry and Molecular Biology, Vol. 37, Issue 4
  • DOI: 10.1016/j.ibmb.2006.12.005

Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense
journal, April 2008

  • Shroff, R.; Vergara, F.; Muck, A.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 16
  • DOI: 10.1073/pnas.0711730105

The plant immune system
journal, November 2006

  • Jones, Jonathan D. G.; Dangl, Jeffery L.
  • Nature, Vol. 444, Issue 7117
  • DOI: 10.1038/nature05286

Determination and imaging of metabolites from Vitis vinifera leaves by laser desorption/ionisation time-of-flight mass spectrometry: Imaging of metabolites from Vitis vinifera leaves
journal, January 2010

  • Hamm, Gregory; Carré, Vincent; Poutaraud, Anne
  • Rapid Communications in Mass Spectrometry, Vol. 24, Issue 3
  • DOI: 10.1002/rcm.4395

Nanoparticle-Assisted Laser Desorption/Ionization Based Mass Imaging with Cellular Resolution
journal, May 2008

  • Taira, Shu; Sugiura, Yuki; Moritake, Shinji
  • Analytical Chemistry, Vol. 80, Issue 12
  • DOI: 10.1021/ac800081z

Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco
journal, November 2013

  • Vogel-Adghough, Drissia; Stahl, Elia; Návarová, Hana
  • Plant Signaling & Behavior, Vol. 8, Issue 11
  • DOI: 10.4161/psb.26366

In Vitro Antibacterial Activity of Sphaeropsidins and Chemical Derivatives toward Xanthomonas oryzae pv. oryzae , the Causal Agent of Rice Bacterial Blight
journal, December 2011

  • Evidente, Antonio; Venturi, Vittorio; Masi, Marco
  • Journal of Natural Products, Vol. 74, Issue 12
  • DOI: 10.1021/np200625m

Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity
journal, December 2012

  • Návarová, Hana; Bernsdorff, Friederike; Döring, Anne-Christin
  • The Plant Cell, Vol. 24, Issue 12
  • DOI: 10.1105/tpc.112.103564

Chlorophyll Loss Caused by Soybean Aphid (Hemiptera: Aphididae) Feeding on Soybean
journal, October 2007

  • Diaz-montano, J.; Reese, J. C.; Schapaugh, W. T.
  • Journal of Economic Entomology, Vol. 100, Issue 5
  • DOI: 10.1093/jee/100.5.1657

Nanospray desorption electrospray ionization: an ambient method for liquid-extraction surface sampling in mass spectrometry
journal, January 2010

  • Roach, Patrick J.; Laskin, Julia; Laskin, Alexander
  • The Analyst, Vol. 135, Issue 9
  • DOI: 10.1039/c0an00312c

Aphid saliva
journal, February 1999


Use of mass spectrometry for imaging metabolites in plants: Mass spectrometry for imaging metabolites in plants
journal, March 2012


Laser Microdissection: a Sample Preparation Technique for Plant Micrometabolic Profiling: Laser Microdissection
journal, September 2013

  • Choi, Young Hae; Verpoorte, Robert; Fang, Jingjing
  • Phytochemical Analysis, Vol. 25, Issue 4
  • DOI: 10.1002/pca.2477

Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins
journal, March 2014

  • Schmelz, Eric A.; Huffaker, Alisa; Sims, James W.
  • The Plant Journal, Vol. 79, Issue 4
  • DOI: 10.1111/tpj.12436

Mass spectrometry imaging of plant metabolites – principles and possibilities
journal, January 2014

  • Bjarnholt, Nanna; Li, Bin; D'Alvise, Janina
  • Nat. Prod. Rep., Vol. 31, Issue 6
  • DOI: 10.1039/C3NP70100J

Soybean seed coat cup unloading on plants with low-raffinose, low-stachyose seeds
journal, September 2009

  • Kosina, Suzanne M.; Castillo, Alexander; Schnebly, Steven R.
  • Seed Science Research, Vol. 19, Issue 3
  • DOI: 10.1017/S0960258509990043

Insect-Induced Daidzein, Formononetin and Their Conjugates in Soybean Leaves
journal, July 2014

  • Murakami, Shinichiro; Nakata, Ryu; Aboshi, Takako
  • Metabolites, Vol. 4, Issue 3
  • DOI: 10.3390/metabo4030532

Hymenopteran parasitoids synthesize 'honeydew-specific' oligosaccharides
journal, October 2006


Lipidomics in situ: Insights into plant lipid metabolism from high resolution spatial maps of metabolites
journal, April 2014


Analysis of Secondary Plant Metabolites by Indirect Desorption Electrospray Ionization Imaging Mass Spectrometry
journal, May 2011

  • Thunig, Janina; Hansen, Steen H.; Janfelt, Christian
  • Analytical Chemistry, Vol. 83, Issue 9
  • DOI: 10.1021/ac2004967

Electrospray sample deposition for matrix-assisted laser desorption/ionization(MALDI) and atmospheric pressure MALDI mass spectrometry with attomole detection limits
journal, May 2004

  • Wei, Hui; Nolkrantz, Kerstin; Powell, David H.
  • Rapid Communications in Mass Spectrometry, Vol. 18, Issue 11
  • DOI: 10.1002/rcm.1458

Metabolic profiling of laser microdissected vascular bundles of Arabidopsis thaliana
journal, August 2005

  • Schad, Martina; Mungur, Rajsree; Fiehn, Oliver
  • Plant Methods, Vol. 1, Issue 1
  • DOI: 10.1186/1746-4811-1-2

Comparative metabolite profiling of foxglove aphids (Aulacorthum solani Kaltenbach) on leaves of resistant and susceptible soybean strains
journal, January 2014

  • Sato, Dan; Sugimoto, Masahiro; Akashi, Hiromichi
  • Molecular BioSystems, Vol. 10, Issue 4
  • DOI: 10.1039/c3mb70595a

Soybean Aphid Injury Effects on Shoot Nitrogen Components in Glycine max
journal, January 2013


Plant–aphid interactions: molecular and ecological perspectives
journal, August 2007


DESI Imaging of Small Molecules in Biological Tissues
book, October 2014


Structural Characterization of Chlorophyll-a by High Resolution Tandem Mass Spectrometry
journal, March 2013

  • Wei, Juan; Li, Huilin; Barrow, Mark P.
  • Journal of The American Society for Mass Spectrometry, Vol. 24, Issue 5
  • DOI: 10.1007/s13361-013-0577-1

QTL underlying the resistance to soybean aphid (Aphis glycines Matsumura) through isoflavone-mediated antibiosis in soybean cultivar ‘Zhongdou 27’
journal, August 2011


Honeydew Sugars and Osmoregulation in the Pea Aphid Acyrthosiphon Pisum
journal, January 1997

  • Wilkinson, T. L.; Ashford, D. A.; Pritchard, J.
  • Journal of Experimental Biology, Vol. 200, Issue 15
  • DOI: 10.1242/jeb.200.15.2137

Works referencing / citing this record:

FERONIA mutation induces high levels of chloroplast-localized Arabidopsides which are involved in root growth
journal, November 2018

  • Hansen, Rebecca L.; Guo, Hongqing; Yin, Yanhai
  • The Plant Journal, Vol. 97, Issue 2
  • DOI: 10.1111/tpj.14123

Sample Preparation for Mass Spectrometry Imaging of Plant Tissues: A Review
journal, February 2016


Characterizing virus-induced gene silencing at the cellular level with in situ multimodal imaging
journal, May 2018


Metabolomics of Solanum lycopersicum Infected with Phytophthora infestans Leads to Early Detection of Late Blight in Asymptomatic Plants
journal, December 2018

  • Galeano Garcia, Paula; Neves dos Santos, Fábio; Zanotta, Samantha
  • Molecules, Vol. 23, Issue 12
  • DOI: 10.3390/molecules23123330

Recycling and metabolic flexibility dictate life in the lower oceanic crust
journal, March 2020


Metabolomics of Solanum lycopersicum Infected with Phytophthora infestans Leads to Early Detection of Late Blight in Asymptomatic Plants
journal, December 2018

  • Galeano Garcia, Paula; Neves dos Santos, Fábio; Zanotta, Samantha
  • Molecules, Vol. 23, Issue 12
  • DOI: 10.3390/molecules23123330

Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization
journal, March 2019

  • Hohenstein, Jessica D.; Studham, Matthew E.; Klein, Adam
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00310

Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to greenbugs
journal, February 2017

  • Donze-Reiner, Teresa; Palmer, Nathan A.; Scully, Erin D.
  • BMC Plant Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12870-017-0998-2

l -lysine metabolism to N -hydroxypipecolic acid: an integral immune-activating pathway in plants
journal, September 2018

  • Hartmann, Michael; Zeier, Jürgen
  • The Plant Journal, Vol. 96, Issue 1
  • DOI: 10.1111/tpj.14037

Characterizing virus-induced gene silencing at the cellular level with in situ multimodal imaging
journal, May 2018


Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization
journal, March 2019

  • Hohenstein, Jessica D.; Studham, Matthew E.; Klein, Adam
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00310

Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to greenbugs
journal, February 2017

  • Donze-Reiner, Teresa; Palmer, Nathan A.; Scully, Erin D.
  • BMC Plant Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12870-017-0998-2

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

  • Boughton, Berin A.; Thinagaran, Dinaiz; Sarabia, Daniel
  • Phytochemistry Reviews, Vol. 15, Issue 3
  • DOI: 10.1007/s11101-015-9440-2