NMR Imaging of Air Spaces and Metabolites in Fruit and Vegetables

  • Maja Musse
  • Henk Van As
Reference work entry


This chapter deals with the principles and the applications of magnetic resonance imaging (MRI) for assessment of the distribution and of the amount of intercellular gas-filled spaces and major metabolites in fruit and vegetable tissues. Combining this information with measurements of water characteristics could enable the use of MRI in an integrative approach to plant characterization.

In MRI, the presence of gas-filled intercellular spaces in plant tissues impacts the NMR relaxation behavior of water molecules because gas and water have different magnetic susceptibilities. This phenomenon can be exploited for the noninvasive detection of certain physiological disorders in fruit and vegetable tissues or for quantification of the spatial distribution of apparent microporosity. On the other hand, the amount and the distribution of major metabolites (sugars, starch, lipids, etc.) can be accessed by MRI using approaches based on differences in relaxation times or on chemical shift between water and metabolites protons. Here we provide an overview of the theoretical aspects of MRI methods and a description of different approaches. The imaging protocols for specific applications for both air space and metabolite imaging are discussed with respect to their application to fruits and vegetables.


Magnetic resonance imaging (MRI) Relaxation times Microporosity Gas volume fraction Magnetic susceptibility Proton exchange Sugars Starch Lipids Localized spectroscopy Single-voxel spectroscopy (SVS) Chemical shift imaging (CSI) Chemical shift selective imaging (CSSI) Quality defects 


  1. 1.
    Verboven P, Kerckhofs G, Mebatsion HK, Ho QT, Temst K, Wevers M, et al. Three-dimensional gas exchange pathways in pome fruit characterized by synchrotron X-ray computed tomography. Plant Physiol. 2008;147(2):518–27.CrossRefGoogle Scholar
  2. 2.
    Ting VJL, Silcock P, Bremer PJ, Biasioli F. X-ray micro-computer tomographic method to visualize the microstructure of different apple cultivars. J Food Sci. 2013;78(11):E1735–E42.CrossRefGoogle Scholar
  3. 3.
    Herremans E, Verboven P, Bongaers E, Estrade P, Verlinden BE, Wevers M, et al. Characterisation of ‘Braeburn’ browning disorder by means of X-ray micro-CT. Postharvest Biol Technol. 2013;75:114–24.CrossRefGoogle Scholar
  4. 4.
    Yablonskiy DA, Haacke EM. Theory of NMR signal behavior in magnetically inhomogeneous tissues: the static dephasing regime. Magn Reson Med. 1994;32(6):749–63.CrossRefGoogle Scholar
  5. 5.
    Duce SL, Carpenter TA, Hall LD, Hills BP. An investigation of the origins of contrast in NMR spin echo images of plant tissue. Magn Reson Imaging. 1992;10:289–97.CrossRefGoogle Scholar
  6. 6.
    Donker HCW, Van As H, Edzes HT, Jans AWH. NMR imaging of white button mushroom (Agaricus bisporis) at various magnetic fields. Magn Reson Imaging. 1996;14(10):1205–15.CrossRefGoogle Scholar
  7. 7.
    McCarthy MJ, Zion B, Chen P, Ablett S, Darke AH, Lillford PJ. Diamagnetic susceptibility changes in apple tissue after bruising. J Sci Food Agric. 1995;67(1):13–20.CrossRefGoogle Scholar
  8. 8.
    Mazhar M, Joyce D, Cowin G, Brereton I, Hofman P, Collins R, et al. Non-destructive H-1-MRI assessment of flesh bruising in avocado (Persea americana M.) cv. Hass. Postharvest Biol Technol. 2015;100:33–40.CrossRefGoogle Scholar
  9. 9.
    Chen P, McCarthy MJ, Kauten R. NMR for internal quality evaluation of fruits and vegetables. Trans ASAE. 1989;32(5):1747–53.CrossRefGoogle Scholar
  10. 10.
    Herremans E, Melado-Herreros A, Defraeye T, Verlinden B, Hertog M, Verboven P, et al. Comparison of X-ray CT and MRI of watercore disorder of different apple cultivars. Postharvest Biol Technol. 2014 Jan;87:42–50.CrossRefGoogle Scholar
  11. 11.
    Clark CJ, MacFall JS, Bieleski RL. Loss of watercore from ‘Fuji’ apple observed by magnetic resonance imaging. Sci Hortic. 1998;73(4):213–27.CrossRefGoogle Scholar
  12. 12.
    Musse M, Quellec S, Cambert M, Devaux MF, Lahaye M, Mariette F. Monitoring the postharvest ripening of tomato fruit using quantitative MRI and NMR relaxometry. Postharvest Biol Technol. 2009;53(1–2):22–35.CrossRefGoogle Scholar
  13. 13.
    Musse M, De Guio F, Quellec S, Cambert M, Challois S, Davenel A. Quantification of microporosity in fruit by MRI at various magnetic fields: comparison with X-ray microtomography. Magn Reson Imaging. 2010;28(10):1525–34.CrossRefGoogle Scholar
  14. 14.
    Winisdorffer G, Musse M, Quellec S, Devaux M-F, Lahaye M, Mariette F. MRI investigation of subcellular water compartmentalization and gas distribution in apples. Magn Reson Imaging. 2015;33(5):671–80.CrossRefGoogle Scholar
  15. 15.
    Winisdorffer G, Musse M, Quellec S, Barbacci A, Le Gall S, Mariette F, et al. Analysis of the dynamic mechanical properties of apple tissue and relationships with the intracellular water status, gas distribution, histological properties and chemical composition. Postharvest Biol Technol. 2015;104:1–16.CrossRefGoogle Scholar
  16. 16.
    Hills BP, Wright KM, Belton PS. Proton NMR-studies of chemical and diffusive exchange in carbohydrate systems. Mol Phys. 1989;67(6):1309–26.CrossRefGoogle Scholar
  17. 17.
    Hills BP, Duce SL. The influence of chemical and diffusive exchange on water proton transverse relaxation in plant tissues. Magn Reson Imaging. 1990;8(3):321–31.CrossRefGoogle Scholar
  18. 18.
    Van As H. Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. J Exp Bot. 2007;58(4):743–56.Google Scholar
  19. 19.
    Raffo A, Gianferri R, Barbieri R, Brosio E. Ripening of banana fruit monitored by water relaxation and diffusion H-1-NMR measurements. Food Chem. 2005;89(1):149–58.CrossRefGoogle Scholar
  20. 20.
    Průšová A. Light on phloem transport (an MRI approach). Wageningen: Wageningen University; 2016.Google Scholar
  21. 21.
    Shaarani SM, Cardenas-Blanco A, Amin MHG, Soon NG, Hall LD. Monitoring development and ripeness of oil palm fruit (Elaeis guneensis) by MRI and bulk NMR. Int J Agric Biol. 2010;12(1):101–5.Google Scholar
  22. 22.
    Jagannathan NR, Govindaraju V, Raghunathan P. In-vivo magnetic resonance study of the histochimistry of coconut (Cocos-nucifera). Magn Reson Imaging. 1995;13(6):885–92.CrossRefGoogle Scholar
  23. 23.
    Vozzo JA, Halloin JM, Cooper TG, Potchen EJ. Use of NMR spectroscopy and magnetic resonance imaging for discriminating Juglans nigra L. seeds. Seed Sci Technol. 1996;24(3):457–63.Google Scholar
  24. 24.
    Borisjuk L, Rolletschek H, Neuberger T. Nuclear magnetic resonance imaging of lipid in living plants. Prog Lipid Res. 2013;52(4):465–87.CrossRefGoogle Scholar
  25. 25.
    Kotyk JJ, Pagel MD, Deppermann KL, Colletti RF, Hoffman NG, Yannakakis EJ, et al. High-throughput determination of oil content in corn kernels using nuclear magnetic resonance imaging. J Am Oil Chem Soc. 2005;82(12):855–62.CrossRefGoogle Scholar
  26. 26.
    Clerjon S, Bonny JM. Diffusion-weighted NMR micro-imaging of lipids: application to food products. In: Renou JP, Belton PS, Webb GA, editors. Magnetic resonance in food science: an exciting future. Cambridge: Royal Society of Chemistry Special Publications; 2011. p. 182–9.CrossRefGoogle Scholar
  27. 27.
    Kockenberger W. Nuclear magnetic resonance micro-imaging in the investigation of plant cell metabolism. J Exp Bot. 2001;52:641–52.CrossRefGoogle Scholar
  28. 28.
    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(4):1183–7.CrossRefGoogle Scholar
  29. 29.
    Srimany A, George C, Naik HR, Pinto DG, Chandrakumar N, Pradeep T. Developmental patterning and segregation of alkaloids in areca nut (seed of Areca catechu) revealed by magnetic resonance and mass spectrometry imaging. Phytochemistry. 2016;125:35–42.CrossRefGoogle Scholar
  30. 30.
    Ishida N, Ogawa H, Koizumi M, Kano H. Ontogenetic changes of the water status and accumulated soluble compounds in growing cherry fruits studied by NMR imaging. Magn Reson Chem. 1997;35:S22–S8.CrossRefGoogle Scholar
  31. 31.
    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(1):17–25.CrossRefGoogle Scholar
  32. 32.
    Glidewell SM. NMR imaging of developing barley grains. J Cereal Sci. 2006;43(1):70–8.CrossRefGoogle Scholar
  33. 33.
    Kockenberger W. Functional imaging of plants by magnetic resonance experiments. Trends Plant Sci. 2001;6(7):286–92.CrossRefGoogle Scholar
  34. 34.
    Pope JM, Rumpel H, Kuhn W, Walker R, Leach D, Sarafis V. Applications of chemical-shift selective NMR microscopy to the noninvasive histochemistry of plant materials. Magn Reson Imaging. 1991;9(3):357–63.CrossRefGoogle Scholar
  35. 35.
    Brescia MA, Pugliese T, Hardy E, Sacco A. Compositional and structural investigations of ripening of table olives, Bella della Daunia, by means of traditional and magnetic resonance imaging analyses. Food Chem. 2007;105(1):400–4.CrossRefGoogle Scholar
  36. 36.
    Lakshminarayana MR, Joshi S, Gowda GAN, Khetrapal CL. Spatial-distribution of oil in groundnut and sunflower seeds by nuclear magnetic resonance imaging. J Biosci. 1992;17(1):87–93.CrossRefGoogle Scholar
  37. 37.
    Neuberger T, Sreenivasulu N, Rokitta M, Rolletschek H, Gobel C, Rutten T, et al. Quantitative imaging of oil storage in developing crop seeds. Plant Biotechnol J. 2008;6(1):31–45.Google Scholar
  38. 38.
    Gersbach PV, Reddy N. Non-invasive localization of thymol accumulation in Carum copticum (Apiaceae) fruits by chemical shift selective magnetic resonance imaging. Ann Bot. 2002;90(2):253–7.CrossRefGoogle Scholar
  39. 39.
    Pope JM, Jonas D, Walker RR. Application of NMR microimaging to the study of water, lipid and carbohydrate distribution in grape berries. Protoplasma. 1993;173(3-4):177–86.CrossRefGoogle Scholar
  40. 40.
    Fuchs J, Neuberger T, Rolletschek H, Schiebold S, Nguyen TH, Borisjuk N, et al. A noninvasive platform for imaging and quantifying oil storage in submillimeter tobacco seed. Plant Physiol. 2013;161(2):583–93.CrossRefGoogle Scholar
  41. 41.
    Xia Y, Jelinski LW. Imaging law-concentration metabolites in the presence of a large background signal. J Magn Reson Ser B. 1995;107(1):1–9.CrossRefGoogle Scholar
  42. 42.
    Rumpel H, Pope JM. The application of 3D chemical-shift microscopy to noninvasive histochemistry. Magn Reson Imaging. 1992;10(2):187–94.CrossRefGoogle Scholar
  43. 43.
    Hernando D, Kellman P, Haldar JP, Liang ZP. Robust water/fat separation in the presence of large field inhomogeneities using a graph cut algorithm. Magn Reson Med. 2010;63(1):79–90.Google Scholar
  44. 44.
    Picaud J, Collewet G, Idier J. Quantification of mass fat fraction in fish using water–fat separation MRI. Magn Reson Imaging. 2016;34(1):44–50.CrossRefGoogle Scholar
  45. 45.
    Heidenreich M, Köckenberger W, Kimmich R, Chandrakumar N, Bowtell R. Investigation of carbohydrate metabolism and transport in castor bean seedlings by cyclic J cross polarization imaging and spectroscopy. J Magn Reson. 1998;132(1):109–24.CrossRefGoogle Scholar
  46. 46.
    Melkus G, Rolletschek H, Fuchs J, Radchuk V, Grafahrend-Belau E, Sreenivasulu N, et al. Dynamic C-13/H-1 NMR imaging uncovers sugar allocation in the living seed. Plant Biotechnol J. 2011;9(9):1022–37.CrossRefGoogle Scholar
  47. 47.
    Olt S, Krotz E, Komor E, Rokitta M, Haase A. Na-23 and H-1 NMR microimaging of intact plants. J Magn Reson. 2000;144(2):297–304.CrossRefGoogle Scholar
  48. 48.
    Munz E, Jakob PM, Borisjuk L. The potential of nuclear magnetic resonance to track lipids in planta. Biochimie. 2016;130:97–108.CrossRefGoogle Scholar
  49. 49.
    Van As H, van Duynhoven J. MRI of plants and foods. J Magn Reson. 2013;229:25–34.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.IRSTEA, UR OPAALERennesFrance
  2. 2.Univ Bretagne LoireRennesFrance
  3. 3.Laboratory of Biophysics and Wageningen NMR CentreWageningen UniversityWageningenThe Netherlands

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