Besides structural information, magnetic resonance imaging (MRI) is crucial to reveal the presence and gradients of metabolites in organs constituted of several tissues. In plant science, such knowledge is key to better understand fruit development and metabolism. Routine methods based on fixation for cytological studies or dissection for metabolite measurements induce biases and plant sample destruction. Magnetic resonance spectroscopy imaging (MSRI) leads to one NMR spectrum per pixel while chemical exchange saturation transfer (CEST) MRI allows mapping metabolites having exchangeable protons. As both methods present different advantages and drawbacks, we compared them to map metabolites in ripe tomato fruits. We demonstrated that MRSI was difficult to interpret due to large spatial chemical shift variations while CEST MRI produced promising image mapping of the main carbohydrates and amino acids. It showed that glucose/fructose was mostly located in the locular tissue, whereas glutamate/glutamine/GABA was found inside the columella.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Data are available at the following link: https://data.inrae.fr/dataset.xhtml?persistentId=doi:10.15454/PYMPNP
- CaCl2 :
Chemical exchange saturation transfer
Chemical shift imaging
Fast low angle shot
Field of view
French National Research Institute for Agriculture, Food and Environment
- MTRasym :
Magnetization transfer ratio asymmetry
Magnetic resonance imaging
Magnetic resonance spectroscopy imaging
Nuclear magnetic resonance
Rapid acquisition with relaxation enhancement
Signal to noise ratio
Water saturation shift referencing
Lauterbur PC. Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature. 1973;242:190–1.
Mlynárik V, Gambarota G, Frenkel H, Gruetter R. Localized short-echo-time proton MR spectroscopy with full signal-intensity acquisition. Magn Reson Med. 2006;56:965–70.
Lecocq A, Le Fur Y, Maudsley AA, Le Troter A, Sheriff S, Sabati M, et al. Whole-brain quantitative mapping of metabolites using short echo three-dimensional proton MRSI. J Magn Reson Imag. 2015;42:280–9.
Wiesinger F, Weidl E, Menzel MI, Janich MA, Khegai O, Glaser SJ, et al. IDEAL spiral CSI for dynamic metabolic MR imaging of hyperpolarized [1-13C]pyruvate. Magn Reson Med. 2012;68:8–16.
Clatworthy MR, Kettunen MI, Hu D-E, Mathews RJ, Witney TH, Kennedy BWC, et al. Magnetic resonance imaging with hyperpolarized [1,4-13C2]fumarate allows detection of early renal acute tubular necrosis. Proc Natl Acad Sci U S A. 2012;109:13374–9.
Chan KWY, McMahon MT, Kato Y, Liu G, Bulte JWM, Bhujwalla ZM, et al. Natural D-glucose as a biodegradable MRI contrast agent for detecting cancer. Magn Reson Med. 2012;68:1764–73.
Nasrallah FA, Pages G, Kuchel PW, Golay X, Chuang K-H. Imaging brain deoxyglucose uptake and metabolism by glucoCEST MRI. J Cerebr Blood Flow Met. 2013;33:1270–8.
Ling W, Regatte RR, Navon G, Jerschow A. Assessment of glycosaminoglycan concentration in vivo by chemical exchange-dependent saturation transfer (gagCEST). Proc Natl Acad Sci U S A. 2008;105:2266–70.
Schmitt B, Zbýň Š, Stelzeneder D, Jellus V, Paul D, Lauer L, et al. Cartilage quality assessment by using glycosaminoglycan chemical exchange saturation transfer and 23Na MR imaging at 7 T. Radiology. 2011;260:257–64.
Cai K, Haris M, Singh A, Kogan F, Greenberg JH, Hariharan H, et al. Magnetic resonance imaging of glutamate. Nature Med. 2012;18:302–6.
Pépin J, Francelle L, Carrillo-de Sauvage M-A, de Longprez L, Gipchtein P, Cambon K, et al. In vivo imaging of brain glutamate defects in a knock-in mouse model of Huntington’s disease. Neuroimage. 2016;139:53–64.
Yan G, Zhang T, Dai Z, Yi M, Jia Y, Nie T, et al. A potential magnetic resonance imaging technique based on chemical exchange saturation transfer for in vivo γ-aminobutyric acid imaging. PLoS One. 2016;11:e0163765.
Jia G, Abaza R, Williams JD, Zynger DL, Zhou J, Shah ZK, et al. Amide proton transfer MR imaging of prostate cancer: a preliminary study. J Magn Reson Imag. 2011;33:647–54.
Zhou J, Payen J-F, Wilson DA, Traystman RJ, van Zijl PCM. Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nature Med. 2003;9:1085–90.
Renou JP, Foucat L, Bonny JM. Magnetic resonance imaging studies of water interactions in meat. Food Chem. 2003;82:35–9.
Van As H, van Duynhoven J. MRI of plants and foods. J Magn Reson. 2013;229:25–34.
Andy E. Inside Insides. 2010. http://insideinsides.blogspot.com/. Accessed 20/09/09.
Borisjuk L, Rolletschek H, Neuberger T. Surveying the plant’s world by magnetic resonance imaging. Plant J. 2012;70:129–46.
Hesse L, Bunk K, Leupold J, Speck T, Masselter T. Structural and functional imaging of large and opaque plant specimens. J Exp Bot. 2019;70:3659–78.
Windt CW, Vergeldt FJ, De Jager PA, Van As H. MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Env. 2006;29:1715–29.
Galed G, Fernández-Valle ME, Martinez A, Heras A. Application of MRI to monitor the process of ripening and decay in citrus treated with chitosan solutions. Magn Reson Imag. 2004;22:127–37.
Musse M, Quellec S, Devaux M-F, Cambert M, Lahaye M, Mariette F. An investigation of the structural aspects of the tomato fruit by means of quantitative nuclear magnetic resonance imaging. Magn Reson Imag. 2009;27:709–19.
Baek S, Lim J, Lee JG, McCarthy MJ, Kim SM. Investigation of the maturity changes of cherry tomato using magnetic resonance imaging. Appl Sci. 2020;10:5188.
Podda R, Delli Castelli D, Digilio G, Gullino ML, Aime S. Asparagine in plums detected by CEST–MRI. Food Chem. 2015;169:1–4.
Gillaspy G, Ben-David H, Gruissem W. Fruits: a developmental perspective. Plant Cell. 1993;5:1439–51.
Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova VJ, et al. Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol. 2008;148:730–50.
Mounet F, Lemaire-Chamley M, Maucourt M, Cabasson C, Giraudel J-L, Deborde C, et al. Quantitative metabolic profiles of tomato flesh and seeds during fruit development: complementary analysis with ANN and PCA. Metabolomics. 2007;3:273–88.
Bergougnoux V. The history of tomato: from domestication to biopharming. Biotechnol Adv. 2014;32:170–89.
Quinet M, Angosto T, Yuste-Lisbona FJ, Blanchard-Gros R, Bigot S, Martinez J-P, et al. Tomato fruit development and metabolism. Front Plant Sci. 2019;10.
Lemaire-Chamley M, Mounet F, Deborde C, Maucourt M, Jacob D, Moing A. NMR-based tissular and developmental metabolomics of tomato fruit. Metabolites. 2019;9:93.
Meyerspeer M, Scheenen T, Schmid AI, Mandl T, Unger E, Moser E. Semi-LASER localized dynamic 31P magnetic resonance spectroscopy in exercising muscle at ultra-high magnetic field. Magn Reson Med. 2011;65:1207–15.
Pohmann R, von Kienlin M. Accurate phosphorus metabolite images of the human heart by 3D acquisition-weighted CSI. Magn Reson Med. 2001;45:817–26.
Tkáč I, Starčuk Z, Choi IY, Gruetter R. In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med. 1999;41:649–56.
Le Fur Y, Nicoli F, Guye M, Confort-Gouny S, Cozzone PJ, Kober F. Grid-free interactive and automated data processing for MR chemical shift imaging data. Magn Reson Mat Phys Biol Med. 2010;23:23–30.
Kim M, Gillen J, Landman BA, Zhou J, van Zijl PCM. Water saturation shift referencing (WASSR) for chemical exchange saturation transfer (CEST) experiments. Magn Reson Med. 2009;61:1441–50.
van Zijl PCM, Yadav NN. Chemical exchange saturation transfer (CEST): what is in a name and what isn’t? Magn Reson Med. 2011;65:927–48.
Wu B, Warnock G, Zaiss M, Lin C, Chen M, Zhou Z, et al. An overview of CEST MRI for non-MR physicists. EJNMMI Phys. 2016;3:19.
Deborde C, Moing A, Roch L, Jacob D, Rolin D, Giraudeau P. Plant metabolism as studied by NMR spectroscopy. Prog Nucl Magn Reson Spectrosc. 2017;102-103:61–97.
Banerjee A, George C, Bharathwaj S, Chandrakumar N. Postharvest ripening study of sweet lime (Citrus limettioides) in situ by volume-localized NMR spectroscopy. J Agric Food Chem. 2009;57:1183–7.
Cheng Y-C, Wang T-T, Chen J-H, Lin T-T. Spatial–temporal analyses of lycopene and sugar contents in tomatoes during ripening using chemical shift imaging. Postharvest Biol Technol. 2011;62:17–25.
Musse M, Van As H. NMR imaging of air spaces and metabolites in fruit and vegetables. In: Webb GA, editor. Modern magnetic resonance. Cham: Springer International Publishing; 2017. p. 1–15.
Vidot K, Rivard C, Van Vooren G, Siret R, Lahaye M. Metallic ions distribution in texture and phenolic content contrasted cider apples. Postharvest Biol Technol. 2020;160:111046.
Nakamura J, Morikawa-Ichinose T, Fujimura Y, Hayakawa E, Takahashi K, Ishii T, et al. Spatially resolved metabolic distribution for unraveling the physiological change and responses in tomato fruit using matrix-assisted laser desorption/ionization–mass spectrometry imaging (MALDI–MSI). Anal Bioanal Chem. 2017;409:1697–706.
We thank Isabelle Atienza for growing the tomato plants and Florie Cassiau for help with ESM Fig. S1 drawing.
MATLAB codes are available upon request from the corresponding author.
This work was partially supported by the IB2019_GelSeed project of the INRAE BAP division and MetaboHUB (ANR-11-INBS-0010).
Conflict of interest
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised: During production the typesetter wrongly captured the manuscript as ESM file, therefore it has been mistakenly published instead of the supplementary information
About this article
Cite this article
Pagés, G., Deborde, C., Lemaire-Chamley, M. et al. MRSI vs CEST MRI to understand tomato metabolism in ripening fruit: is there a better contrast?. Anal Bioanal Chem 413, 1251–1257 (2021). https://doi.org/10.1007/s00216-020-03101-w
- Chemical exchange saturation transfer (CEST)
- Magnetic resonance spectroscopy imaging (MRSI)
- Ripe fruit