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

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

doi:10.1021/acs.analchem.5b00459

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

Journal Article · Mon Apr 27 00:00:00 EDT 2015 · Analytical Chemistry

DOI:https://doi.org/10.1021/acs.analchem.5b00459· OSTI ID:1227451

Klein, Adam T. ^[1]; Yagnik, Gargey B. ^[1]; Hohenstein, Jessica D. ^[2]; Ji, Zhiyuan ^[3]; Zi, Jiachen ^[2]; Reichert, Malinda D. ^[2]; MacIntosh, Gustavo C. ^[2]; Yang, Bing ^[2]; Peters, Reuben J. ^[2]; Vela, Javier ^[2]; Lee, Young Jin ^[1]

Iowa State Univ., Ames, IA (United States); Ames Lab., Ames, IA (United States)
Iowa State Univ., Ames, IA (United States)
Shanghai Jiao Tong Univ., Shanghai (China); Iowa State Univ., Ames, IA (United States)

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.

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Research Organization:: Ames Laboratory (AMES), Ames, IA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: 2014-67013-21720; AC02-07CH11358

OSTI ID:: 1227451

Report Number(s):: IS-J-8639

Journal Information:: Analytical Chemistry, Vol. 87, Issue 10; ISSN 0003-2700

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 48 works

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References (49)

Improved imaging resolution in desorption electrospray ionization mass spectrometry Kertesz, Vilmos; Van Berkel, Gary J. Rapid Communications in Mass Spectrometry, Vol. 22, Issue 17 https://doi.org/10.1002/rcm.3662	journal	September 2008
Effector proteins that modulate plant–insect interactions Hogenhout, Saskia A.; Bos, Jorunn IB Current Opinion in Plant Biology, Vol. 14, Issue 4 https://doi.org/10.1016/j.pbi.2011.05.003	journal	August 2011
Plant immunity: towards an integrated view of plant–pathogen interactions Dodds, Peter N.; Rathjen, John P. Nature Reviews Genetics, Vol. 11, Issue 8 https://doi.org/10.1038/nrg2812	journal	June 2010
Improved spatial resolution in the imaging of biological tissue using desorption electrospray ionization Campbell, Dahlia I.; Ferreira, Christina R.; Eberlin, Livia S. Analytical and Bioanalytical Chemistry, Vol. 404, Issue 2 https://doi.org/10.1007/s00216-012-6173-6	journal	June 2012
Molecular Imaging of Biological Samples: Localization of Peptides and Proteins Using MALDI-TOF MS Caprioli, Richard M.; Farmer, Terry B.; Gile, Jocelyn Analytical Chemistry, Vol. 69, Issue 23 https://doi.org/10.1021/ac970888i	journal	December 1997
Mass Spectrometry Imaging of Cassette-Dosed Drugs for Higher Throughput Pharmacokinetic and Biodistribution Analysis Swales, John G.; Tucker, James W.; Strittmatter, Nicole Analytical Chemistry, Vol. 86, Issue 16 https://doi.org/10.1021/ac502217r	journal	July 2014
Chemical imaging of trichome specialized metabolites using contact printing and laser desorption/ionization mass spectrometry Li, Chao; Wang, Zhenzhen; Jones, A. Daniel Analytical and Bioanalytical Chemistry, Vol. 406, Issue 1 https://doi.org/10.1007/s00216-013-7444-6	journal	November 2013
Method for Simultaneous Imaging of Endogenous Low Molecular Weight Metabolites in Mouse Brain Using TiO ₂ Nanoparticles in Nanoparticle-Assisted Laser Desorption/Ionization-Imaging Mass Spectrometry Shrivas, Kamlesh; Hayasaka, Takahiro; Sugiura, Yuki Analytical Chemistry, Vol. 83, Issue 19 https://doi.org/10.1021/ac201602s	journal	October 2011
Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae Sana, Theodore R.; Fischer, Steve; Wohlgemuth, Gert Metabolomics, Vol. 6, Issue 3 https://doi.org/10.1007/s11306-010-0218-7	journal	May 2010
Plant terpenoid synthases: Molecular biology and phylogenetic analysis Bohlmann, J.; Meyer-Gauen, G.; Croteau, R. Proceedings of the National Academy of Sciences, Vol. 95, Issue 8 https://doi.org/10.1073/pnas.95.8.4126	journal	April 1998
Soybean defense responses to the soybean aphid Li, Yan; Zou, Jijun; Li, Min New Phytologist, Vol. 179, Issue 1 https://doi.org/10.1111/j.1469-8137.2008.02443.x	journal	July 2008
Phloem-sap feeding by animals: problems and solutions Douglas, A. E. Journal of Experimental Botany, Vol. 57, Issue 4 https://doi.org/10.1093/jxb/erj067	journal	January 2006
Spatial Mapping of Lipids at Cellular Resolution in Embryos of Cotton Horn, Patrick J.; Korte, Andrew R.; Neogi, Purnima B. The Plant Cell, Vol. 24, Issue 2 https://doi.org/10.1105/tpc.111.094581	journal	February 2012
Phytoalexins in defense against pathogens Ahuja, Ishita; Kissen, Ralph; Bones, Atle M. Trends in Plant Science, Vol. 17, Issue 2 https://doi.org/10.1016/j.tplants.2011.11.002	journal	February 2012
Methyl Salicylate, a Soybean Aphid-Induced Plant Volatile Attractive to the Predator Coccinella septempunctata Zhu, Junwei; Park, Kye-Chung Journal of Chemical Ecology, Vol. 31, Issue 8 https://doi.org/10.1007/s10886-005-5923-8	journal	July 2005
Molecular characterisation of a candidate gut sucrase in the pea aphid, Acyrthosiphon pisum Price, D. R. G.; Karley, A. J.; Ashford, D. A. Insect Biochemistry and Molecular Biology, Vol. 37, Issue 4 https://doi.org/10.1016/j.ibmb.2006.12.005	journal	April 2007
Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense Shroff, R.; Vergara, F.; Muck, A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 16 https://doi.org/10.1073/pnas.0711730105	journal	April 2008
The plant immune system Jones, Jonathan D. G.; Dangl, Jeffery L. Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05286	journal	November 2006
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 Hamm, Gregory; Carré, Vincent; Poutaraud, Anne Rapid Communications in Mass Spectrometry, Vol. 24, Issue 3 https://doi.org/10.1002/rcm.4395	journal	January 2010
Nanoparticle-Assisted Laser Desorption/Ionization Based Mass Imaging with Cellular Resolution Taira, Shu; Sugiura, Yuki; Moritake, Shinji Analytical Chemistry, Vol. 80, Issue 12 https://doi.org/10.1021/ac800081z	journal	May 2008
Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco Vogel-Adghough, Drissia; Stahl, Elia; Návarová, Hana Plant Signaling & Behavior, Vol. 8, Issue 11 https://doi.org/10.4161/psb.26366	journal	November 2013
In Vitro Antibacterial Activity of Sphaeropsidins and Chemical Derivatives toward Xanthomonas oryzae pv. oryzae , the Causal Agent of Rice Bacterial Blight Evidente, Antonio; Venturi, Vittorio; Masi, Marco Journal of Natural Products, Vol. 74, Issue 12 https://doi.org/10.1021/np200625m	journal	December 2011
Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity Návarová, Hana; Bernsdorff, Friederike; Döring, Anne-Christin The Plant Cell, Vol. 24, Issue 12 https://doi.org/10.1105/tpc.112.103564	journal	December 2012
Chlorophyll Loss Caused by Soybean Aphid (Hemiptera: Aphididae) Feeding on Soybean Diaz-montano, J.; Reese, J. C.; Schapaugh, W. T. Journal of Economic Entomology, Vol. 100, Issue 5 https://doi.org/10.1093/jee/100.5.1657	journal	October 2007
Nanospray desorption electrospray ionization: an ambient method for liquid-extraction surface sampling in mass spectrometry Roach, Patrick J.; Laskin, Julia; Laskin, Alexander The Analyst, Vol. 135, Issue 9 https://doi.org/10.1039/c0an00312c	journal	January 2010
Aphid saliva Miles, Peter W. Biological Reviews of the Cambridge Philosophical Society, Vol. 74, Issue 1 https://doi.org/10.1017/S0006323198005271	journal	February 1999
Use of mass spectrometry for imaging metabolites in plants: Mass spectrometry for imaging metabolites in plants Lee, Young Jin; Perdian, David C.; Song, Zhihong The Plant Journal, Vol. 70, Issue 1 https://doi.org/10.1111/j.1365-313X.2012.04899.x	journal	March 2012
Laser Microdissection: a Sample Preparation Technique for Plant Micrometabolic Profiling: Laser Microdissection Choi, Young Hae; Verpoorte, Robert; Fang, Jingjing Phytochemical Analysis, Vol. 25, Issue 4 https://doi.org/10.1002/pca.2477	journal	September 2013
Liquid extraction surface analysis mass spectrometry (LESA-MS) as a novel profiling tool for drug distribution and metabolism analysis: the terfenadine example: LESA-MS distribution analysis of terfenadine Eikel, Daniel; Vavrek, Marissa; Smith, Sheri Rapid Communications in Mass Spectrometry, Vol. 25, Issue 23 https://doi.org/10.1002/rcm.5274	journal	November 2011
Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins Schmelz, Eric A.; Huffaker, Alisa; Sims, James W. The Plant Journal, Vol. 79, Issue 4 https://doi.org/10.1111/tpj.12436	journal	March 2014
Mass spectrometry imaging of plant metabolites – principles and possibilities Bjarnholt, Nanna; Li, Bin; D'Alvise, Janina Nat. Prod. Rep., Vol. 31, Issue 6 https://doi.org/10.1039/C3NP70100J	journal	January 2014
High-Spatial and High-Mass Resolution Imaging of Surface Metabolites of Arabidopsis thaliana by Laser Desorption-Ionization Mass Spectrometry Using Colloidal Silver Jun, Ji Hyun; Song, Zhihong; Liu, Zhenjiu Analytical Chemistry, Vol. 82, Issue 8 https://doi.org/10.1021/ac902990p	journal	April 2010
Soybean seed coat cup unloading on plants with low-raffinose, low-stachyose seeds Kosina, Suzanne M.; Castillo, Alexander; Schnebly, Steven R. Seed Science Research, Vol. 19, Issue 3 https://doi.org/10.1017/S0960258509990043	journal	September 2009
Insect-Induced Daidzein, Formononetin and Their Conjugates in Soybean Leaves Murakami, Shinichiro; Nakata, Ryu; Aboshi, Takako Metabolites, Vol. 4, Issue 3 https://doi.org/10.3390/metabo4030532	journal	July 2014
Hymenopteran parasitoids synthesize 'honeydew-specific' oligosaccharides WÄCkers, F. L.; Lee, J. C.; Heimpel, G. E. Functional Ecology, Vol. 20, Issue 5 https://doi.org/10.1111/j.1365-2435.2006.01158.x	journal	October 2006
Fluorescent protein-based technologies: shedding new light on the plant endomembrane system: Fluorescent protein applications in plant endomembranes Sparkes, Imogen; Brandizzi, Federica The Plant Journal, Vol. 70, Issue 1 https://doi.org/10.1111/j.1365-313X.2011.04884.x	journal	March 2012
Lipidomics in situ: Insights into plant lipid metabolism from high resolution spatial maps of metabolites Horn, Patrick J.; Chapman, Kent D. Progress in Lipid Research, Vol. 54 https://doi.org/10.1016/j.plipres.2014.01.003	journal	April 2014
Analysis of Secondary Plant Metabolites by Indirect Desorption Electrospray Ionization Imaging Mass Spectrometry Thunig, Janina; Hansen, Steen H.; Janfelt, Christian Analytical Chemistry, Vol. 83, Issue 9 https://doi.org/10.1021/ac2004967	journal	May 2011
Electrospray sample deposition for matrix-assisted laser desorption/ionization(MALDI) and atmospheric pressure MALDI mass spectrometry with attomole detection limits Wei, Hui; Nolkrantz, Kerstin; Powell, David H. Rapid Communications in Mass Spectrometry, Vol. 18, Issue 11 https://doi.org/10.1002/rcm.1458	journal	May 2004
Metabolic profiling of laser microdissected vascular bundles of Arabidopsis thaliana Schad, Martina; Mungur, Rajsree; Fiehn, Oliver Plant Methods, Vol. 1, Issue 1 https://doi.org/10.1186/1746-4811-1-2	journal	August 2005
Comparative metabolite profiling of foxglove aphids (Aulacorthum solani Kaltenbach) on leaves of resistant and susceptible soybean strains Sato, Dan; Sugimoto, Masahiro; Akashi, Hiromichi Molecular BioSystems, Vol. 10, Issue 4 https://doi.org/10.1039/c3mb70595a	journal	January 2014
Mass spectrometric imaging as a high-spatial resolution tool for functional genomics: Tissue-specific gene expression of TT7 inferred from heterogeneous distribution of metabolites in Arabidopsis flowers Korte, Andrew R.; Song, Zhihong; Nikolau, Basil J. Anal. Methods, Vol. 4, Issue 2 https://doi.org/10.1039/C2AY05618F	journal	January 2012
Soybean Aphid Injury Effects on Shoot Nitrogen Components in Glycine max Riedell, Walter E.; Beckendorf, Eric A.; Catangui, Michael A. Crop Science, Vol. 53, Issue 1 https://doi.org/10.2135/cropsci2012.05.0286	journal	January 2013
Plant–aphid interactions: molecular and ecological perspectives Goggin, Fiona L. Current Opinion in Plant Biology, Vol. 10, Issue 4 https://doi.org/10.1016/j.pbi.2007.06.004	journal	August 2007
DESI Imaging of Small Molecules in Biological Tissues Cabral, Elaine C.; Ifa, Demian R. Mass Spectrometry Imaging of Small Molecules https://doi.org/10.1007/978-1-4939-1357-2_7	book	October 2014
Quantification of plant surface metabolites by matrix-assisted laser desorption-ionization mass spectrometry imaging: glucosinolates on Arabidopsis thaliana leaves Shroff, Rohit; Schramm, Katharina; Jeschke, Verena The Plant Journal, Vol. 81, Issue 6 https://doi.org/10.1111/tpj.12760	journal	March 2015
Structural Characterization of Chlorophyll-a by High Resolution Tandem Mass Spectrometry Wei, Juan; Li, Huilin; Barrow, Mark P. Journal of The American Society for Mass Spectrometry, Vol. 24, Issue 5 https://doi.org/10.1007/s13361-013-0577-1	journal	March 2013
QTL underlying the resistance to soybean aphid (Aphis glycines Matsumura) through isoflavone-mediated antibiosis in soybean cultivar ‘Zhongdou 27’ Meng, Fanli; Han, Yingpeng; Teng, Weili Theoretical and Applied Genetics, Vol. 123, Issue 8 https://doi.org/10.1007/s00122-011-1680-y	journal	August 2011
Honeydew Sugars and Osmoregulation in the Pea Aphid Acyrthosiphon Pisum Wilkinson, T. L.; Ashford, D. A.; Pritchard, J. Journal of Experimental Biology, Vol. 200, Issue 15 https://doi.org/10.1242/jeb.200.15.2137	journal	January 1997

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