MRSI vs CEST MRI to understand tomato metabolism in ripening fruit: is there a better contrast?

A Correction to this article is available

This article has been updated


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.

Graphical abstract

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Data availability

Data are available at the following link:

Change history


CaCl2 :

Calcium chloride


Chemical exchange saturation transfer


Chemical shift imaging


Fast low angle shot


Field of view


2-Aminobutyric acid


French National Research Institute for Agriculture, Food and Environment

MTRasym :

Magnetization transfer ratio asymmetry


Magnetic resonance


Magnetic resonance imaging


Magnetic resonance spectroscopy imaging


Nuclear magnetic resonance


Rapid acquisition with relaxation enhancement




Signal to noise ratio


Water saturation shift referencing


  1. 1.

    Lauterbur PC. Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature. 1973;242:190–1.

    CAS  Article  Google Scholar 

  2. 2.

    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.

    Article  Google Scholar 

  3. 3.

    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.

    Article  Google Scholar 

  4. 4.

    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.

    CAS  Article  Google Scholar 

  5. 5.

    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.

    CAS  Article  Google Scholar 

  6. 6.

    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.

    CAS  Article  Google Scholar 

  7. 7.

    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.

    CAS  Article  Google Scholar 

  8. 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.

    CAS  Article  Google Scholar 

  9. 9.

    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.

    Article  Google Scholar 

  10. 10.

    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.

    CAS  Article  Google Scholar 

  11. 11.

    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.

    Article  Google Scholar 

  12. 12.

    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.

    Article  Google Scholar 

  13. 13.

    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.

    Article  Google Scholar 

  14. 14.

    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.

    CAS  Article  Google Scholar 

  15. 15.

    Renou JP, Foucat L, Bonny JM. Magnetic resonance imaging studies of water interactions in meat. Food Chem. 2003;82:35–9.

    CAS  Article  Google Scholar 

  16. 16.

    Van As H, van Duynhoven J. MRI of plants and foods. J Magn Reson. 2013;229:25–34.

    Article  Google Scholar 

  17. 17.

    Andy E. Inside Insides. 2010. Accessed 20/09/09.

  18. 18.

    Borisjuk L, Rolletschek H, Neuberger T. Surveying the plant’s world by magnetic resonance imaging. Plant J. 2012;70:129–46.

    CAS  Article  Google Scholar 

  19. 19.

    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.

    CAS  Article  Google Scholar 

  20. 20.

    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.

    CAS  Article  Google Scholar 

  21. 21.

    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.

    CAS  Article  Google Scholar 

  22. 22.

    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.

    Article  Google Scholar 

  23. 23.

    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.

    CAS  Article  Google Scholar 

  24. 24.

    Podda R, Delli Castelli D, Digilio G, Gullino ML, Aime S. Asparagine in plums detected by CEST–MRI. Food Chem. 2015;169:1–4.

    CAS  Article  Google Scholar 

  25. 25.

    Gillaspy G, Ben-David H, Gruissem W. Fruits: a developmental perspective. Plant Cell. 1993;5:1439–51.

  26. 26.

    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.

  27. 27.

    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.

    CAS  Article  Google Scholar 

  28. 28.

    Bergougnoux V. The history of tomato: from domestication to biopharming. Biotechnol Adv. 2014;32:170–89.

    CAS  Article  Google Scholar 

  29. 29.

    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.

  30. 30.

    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.

    CAS  Article  Google Scholar 

  31. 31.

    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.

    Article  Google Scholar 

  32. 32.

    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.

    CAS  Article  Google Scholar 

  33. 33.

    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.

    Article  Google Scholar 

  34. 34.

    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.

    Article  Google Scholar 

  35. 35.

    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.

    Article  Google Scholar 

  36. 36.

    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.

    Article  Google Scholar 

  37. 37.

    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.

    CAS  Article  Google Scholar 

  38. 38.

    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.

  39. 39.

    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.

    CAS  Article  Google Scholar 

  40. 40.

    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.

    CAS  Article  Google Scholar 

  41. 41.

    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.

    Google Scholar 

  42. 42.

    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.

    CAS  Article  Google Scholar 

  43. 43.

    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.

    CAS  Article  Google Scholar 

Download references


We thank Isabelle Atienza for growing the tomato plants and Florie Cassiau for help with ESM Fig. S1 drawing.

Code availability

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).

Author information




Guilhem Pagés: conceptualization, investigation, writing—original draft, review, and editing. Catherine Deborde: conceptualization, writing—original draft, and review. Martine Lemaire-Chamley: funding acquisition, resources, writing—original draft, and review. Annick Moing: supervision, writing—original draft, and review. Jean-Marie Bonny: supervision, writing—review.

Corresponding author

Correspondence to Guilhem Pagés.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Publisher’s note

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

Supplementary information


(PDF 698 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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).

Download citation


  • Chemical exchange saturation transfer (CEST)
  • Magnetic resonance spectroscopy imaging (MRSI)
  • Metabolites
  • Ripe fruit
  • Sugars
  • Tomato