Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-19T05:05:47.479Z Has data issue: false hasContentIssue false

The Application of Contrast Media for In Vivo Feature Enhancement in X-Ray Computed Tomography of Soil-Grown Plant Roots

Published online by Cambridge University Press:  21 March 2017

Samuel D. Keyes*
Affiliation:
The Faculty of Engineering and the Environment, The University of Southampton, Southampton, SO17 1BJ, UK
Neil J. Gostling
Affiliation:
The Centre for Biological Sciences, The University of Southampton, Southampton, SO17 1BJ, UK
Jessica H. Cheung
Affiliation:
The Centre for Biological Sciences, The University of Southampton, Southampton, SO17 1BJ, UK
Tiina Roose
Affiliation:
The Faculty of Engineering and the Environment, The University of Southampton, Southampton, SO17 1BJ, UK
Ian Sinclair
Affiliation:
The Faculty of Engineering and the Environment, The University of Southampton, Southampton, SO17 1BJ, UK
Alan Marchant
Affiliation:
The Centre for Biological Sciences, The University of Southampton, Southampton, SO17 1BJ, UK
*
*Corresponding author. S.D.Keyes@soton.ac.uk
Get access

Abstract

The use of in vivo X-ray microcomputed tomography (μCT) to study plant root systems has become routine, but is often hampered by poor contrast between roots, soil, soil water, and soil organic matter. In clinical radiology, imaging of poorly contrasting regions is frequently aided by the use of radio-opaque contrast media. In this study, we present evidence for the utility of iodinated contrast media (ICM) in the study of plant root systems using μCT. Different dilutions of an ionic and nonionic ICM (Gastrografin 370 and Niopam 300) were perfused into the aerial vasculature of juvenile pea plants via a leaf flap (Pisum sativum). The root systems were imaged via μCT, and a variety of image-processing approaches used to quantify and compare the magnitude of the contrast enhancement between different regions. Though the treatment did not appear to significantly aid extraction of full root system architectures from the surrounding soil, it did allow the xylem and phloem units of seminal roots and the vascular morphology within rhizobial nodules to be clearly visualized. The nonionic, low-osmolality contrast agent Niopam appeared to be well tolerated by the plant, whereas Gastrografin showed evidence of toxicity. In summary, the use of iodine-based contrast media allows usually poorly contrasting root structures to be visualized nondestructively using X-ray μCT. In particular, the vascular structures of roots and rhizobial nodules can be clearly visualized in situ.

Type
Biological Science Applications
Copyright
© Microscopy Society of America 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

These authors contributed equally to this work

References

Ahmed, S., Naugler Klassen, T., Keyes, S., Daly, M., Jones, D.L., Mavrogordato, M., Sinclair, I. & Roose, T. (2016). Imaging the interaction of roots and phosphate fertiliser granules using 4D X-ray tomography. Plant and Soil 401, 125134.CrossRefGoogle Scholar
Almén, T. (1990). Contrast media: The relation of chemical structure, animal toxicity and adverse clinical effects. Am J Cardiol 66, F2F8.Google Scholar
Aloni, R. & Gad, A.E. (1982). Anatomy of the primary phloem fiber system in Pisum sativum . Am J Bot 69, 979984.Google Scholar
Alric, C., Taleb, J., Duc, G.L., et al. (2008). Gadolinium chelate coated gold nanoparticles as contrast agents for both X-ray computed tomography and magnetic resonance imaging. J Am Chem Soc 130, 59085915.Google Scholar
Anderson, M.A., Hung, A.Y.C., Mills, D. & Scott, M.S. (1995). Factors affecting the surface tension of soil solutions and solutions of humic acids. Soil Sci 160, 111116.Google Scholar
Andreucci, M., Solomon, R. & Tasanarong, A. (2014). Side effects of radiographic contrast media: Pathogenesis, risk factors, and prevention. BioMed Res Int 2014, 741018.CrossRefGoogle Scholar
Aylmore, A.G. (1993). Use of computer-assisted tomography in studying water movement around plant roots. Adv Agron 49, 154.CrossRefGoogle Scholar
Berry, M. (2003). Diagnostic Radiology: Urogenital Imaging. Kathmandu, Nepal: Jaypee Brothers, Medical Publishers.Google Scholar
Brooks, B. (1924). Intra-arterial injection of sodium iodide: Preliminary report. J Am Med Assoc 82, 10161019.Google Scholar
Calder, G., Hindle, C., Chan, J. & Shaw, P. (2015). An optical imaging chamber for viewing living plant cells and tissues at high resolution for extended periods. Plant Methods 11, 1.Google Scholar
Caldwell, M.M., Dawson, T.E. & Richards, J.H. (1998). Hydraulic lift: Consequences of water efflux from the roots of plants. Oecologia 113, 151161.Google Scholar
Carlson, W.D. (2006). Three-dimensional imaging of earth and planetary materials. Earth Planet Sci Lett 249, 133147.CrossRefGoogle Scholar
Christiansen, C. (2005). X-ray contrast media—An overview. Toxicology 209, 185187.CrossRefGoogle ScholarPubMed
Clausnitzer, V. & Hopmans, J.W. (2000). Pore-scale measurements of solute breakthrough using microfocus X-ray computed tomography. Water Resour Res 36, 20672079.Google Scholar
Cohan, R.H. & Ellis, J.H. (1999). Adverse reactions to iodinated radiographic contrast media. In Trends in Contrast Media, Thomsen, H.S., Muller, R.N. & Mattrey, R.F. (Eds.), pp. 117132. Heidelberg, Germany: Springer-Verlag.Google Scholar
Culligan, K.A., Wildenschild, D., Christensen, B.S.B., Gray, W.G., Rivers, M.L. & Tompson, A.F.B. (2004). Interfacial area measurements for unsaturated flow through a porous medium. Water Resour Res 40, W12413.Google Scholar
Cussler, E.L. (2009). Diffusion: Mass Transfer in Fluid Systems. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Dixon, H.H. & Joly, J. (1895). The path of the transpiration-current. Ann Bot IX, 403420.CrossRefGoogle Scholar
Flavel, R.J., Guppy, C.N., Tighe, M., Watt, M., McNeill, A. & Young, I.M. (2012). Non-destructive quantification of cereal roots in soil using high-resolution X-ray tomography. J Exp Bot 63, 25032511.Google Scholar
Fu, Q., Cheng, L., Guo, Y. & Turgeon, R. (2011). Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol 157, 15181527.Google Scholar
Garbout, A., Munkholm, L.J., Hansen, S.B., et al. (2012). The use of PET/CT scanning technique for 3D visualization and quantification of real-time soil/plant interactions. Plant Soil 352, 113127.Google Scholar
Gregory, P.J., Hutchison, D.J., Read, D.B., Jenneson, P.M., Gilboy, W.B. & Morton, E.J. (2003). Non-invasive imaging of roots with high-resolution X-ray micro-tomography. In Roots: The dynamic Interface between Plants and the Earth, Abe, J. J. (Ed.), pp. 351359. Amsterdam, Netherlands: Springer.Google Scholar
Hall, S.M. & Baker, D.A. (1972). The chemical composition of Ricinus phloem exudate. Planta 106, 131140.Google Scholar
Hallouard, F., Anton, N., Choquet, P., et al. (2010). Iodinated blood pool contrast media for preclinical X-ray imaging applications—A review. Biomaterials 31, 62496268.Google Scholar
Hayashi, H. & Chino, M. (1990). Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31, 247251.Google Scholar
Hayduk, W. & Laudie, H. (1974). Prediction of diffusion coefficients for nonelectrolytes in dilute aqueous solutions. AIChE J 20, 611615.Google Scholar
Heeraman, D.A., Hopmans, J.W. & Clausnitzer, V. (1997). Three dimensional imaging of plant roots in situ with x-ray computed tomography. Plant Soil 189, 167179.Google Scholar
Hocking, P.J. (1980). The composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauca Grah.). Ann Bot 45, 633643.Google Scholar
Holbrook, N.M. & Zwieniecki, M.A. (2011). Vascular Transport in Plants. Burlington, VT: Academic Press.Google Scholar
Hopmans, J.W., Vogel, T. & Koblik, P.D. (1992). X-ray tomography of soil water distribution in one-step outflow experiments. Soil Sci Soc Am J 56, 355362.Google Scholar
Jenneson, P.M., Gilboy, W.B., Morton, E.J. & Gregory, P.J. (2003). An X-ray micro-tomography system optimised for the low-dose study of living organisms. Appl Radiat Isot 58, 177181.Google Scholar
Jensen, S.C. & Peppers, M.P. (2013). Pharmacology and drug administration for imaging technologists. Maryland Heights, MO: Mosby Elsevier.Google Scholar
Kaestner, A., Lehmann, E. & Stampanoni, M. (2008). Imaging and image processing in porous media research. Adv Water Resour 31, 11741187.Google Scholar
Kemmochi, I. & Maru, H. (2004). Nondestructive discrimination of cabbage [Brassica oleracea capitata] plants infected with verticillium wilt using contrast media and an X-ray apparatus. J Jpn Soc Hortic Sci 73, 484490.CrossRefGoogle Scholar
Keyes, S.D., Daly, K.R., Gostling, N.J., Jones, D.L., Talboys, P., Pinzer, B.R., Boardman, R., Sinclair, I., Marchant, A. & Roose, T. (2013). High resolution synchrotron imaging of wheat root hairs growing in soil and image based modelling of phosphate uptake. New Phytol 198, 10231029.CrossRefGoogle ScholarPubMed
Kim, D., Park, S., Lee, J.H., Jeong, Y.Y. & Jon, S. (2007). Antibiofouling polymer-coated gold nanoparticles as a contrast agent for in vivo X-ray computed tomography imaging. J Am Chem Soc 129, 76617665.Google Scholar
Knoblauch, M., Peters, W.S., Ehlers, K. & van Bel, A.J.E. (2001). Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell 13, 12211230.Google Scholar
Lontoc-Roy, M., Dutilleul, P., Prasher, S.O., Han, L., Brouillet, T. & Smith, D.L. (2006). Advances in the acquisition and analysis of CT scan data to isolate a crop root system from the soil medium and quantify root system complexity in 3-D space. Geoderma 137, 231241.CrossRefGoogle Scholar
Maizel, A., von Wangenheim, D., Federici, F., Haseloff, J. & Stelzer, E.H.K. (2011). High‐resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68, 377385.Google Scholar
Mariani, G., Bruselli, L., Kuwert, T., Kim, E.E., Flotats, A., Israel, O., Dondi, M. & Watanabe, N. (2010). A review on the clinical uses of SPECT/CT. Eur J Nucl Med Mol Imaging 37, 19591985.Google Scholar
McClennan, B.L. (1990). Preston M. Hickey memorial lecture. Ionic and nonionic iodinated contrast media: Evolution and strategies for use. AJR Am J Roentgenol 155, 225233.CrossRefGoogle Scholar
Menon, M., Robinson, B., Oswald, S.E., Kaestner, A., Abbaspour, K.C., Lehmann, E. & Schulin, R. (2006). Visualisation of root growth in heterogeneously contaminated soil using neutron radiography. Eur J Soil Sci 58, 802810.Google Scholar
Mooney, S.J., Pridmore, T.P., Helliwell, J. & Bennett, M.J. (2012). Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant Soil 352, 122.CrossRefGoogle Scholar
Mullendore, D.L., Windt, C.W., Van As, H. & Knoblauch, M. (2010). Sieve tube geometry in relation to phloem flow. Plant Cell 22, 579593.Google Scholar
Munch, E. (1926). Dynamik der Saftstromungen. Ber Deut Bot Ges 44, 6871.Google Scholar
Oner-Sieben, S. & Lohaus, G. (2014). Apoplastic and symplastic phloem loading in Quercus robur and Fraxinus excelsior. J Exp Bot 65, 19051916.Google Scholar
Osborne, E.D., Sutherland, C.G., Scholl, A.J. & Rowntree, L.G. (1923). Roentgenography of urinary tract during excretion of sodium iodide. J Am Med Assoc 80, 368373.CrossRefGoogle Scholar
Otsu, N. (1979). A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern 9, 6266.Google Scholar
Payvandi, S., Daly, K.R., Jones, D.L., Talboys, P., Zygalakis, K.C. & Roose, T. (2014 a). A mathematical model of water and nutrient transport in xylem vessels of a wheat plant. Bull Math Biol 76, 566596.Google Scholar
Payvandi, S., Daly, K.R., Zygalakis, K.C. & Roose, T. (2014 b). Mathematical modelling of the phloem: The importance of diffusion on sugar transport at osmotic equilibrium. Bull Math Biol 76, 28342865.Google Scholar
Perret, J.S., Al-Belushi, M.E. & Deadman, M. (2007). Non-destructive visualisation and quantification of roots using computed tomography. Soil Biol Biochem 39, 391399.CrossRefGoogle Scholar
Peuke, A.D., Rokitta, M., Zimmermann, U., Schreiber, L. & Haase, A. (2001). Simultaneous measurement of water flow velocity and solute transport in xylem and phloem of adult plants of Ricinus communis over a daily time course by nuclear magnetic resonance spectrometry. Plant Cell Environ 24, 491503.CrossRefGoogle Scholar
Prodanovic, M., Lindquist, W.B. & Seright, R.S. (2006). Residual fluid blobs and contact angle measurements from X-ray images of fluid displacement. In XVI International Conference on Computational Methods in Water Resources, Copenhagen, Denmark, June 19–22, 2006.Google Scholar
Rabin, O., Perez, J.M., Grimm, J., Wojtkiewicz, G. & Weissleder, R. (2006). An X-ray computed tomography imaging agent based on long-circulating bismuth sulphide nanoparticles. Nat Mater 5, 118122.Google Scholar
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T. & Preibisch, S. (2012). Fiji: An open-source platform for biological-image analysis. Nat Methods 9, 676682.Google Scholar
Singh, J. & Daftary, A. (2008). Iodinated contrast media and their adverse reactions. J Nucl Med Technol 36, 6974.Google Scholar
Sjolund, R.D. (1997). The phloem sieve element: A river runs through it. Plant Cell 9, 11371146.Google Scholar
Sobrado, M.A. (2004). Influence of external salinity on the osmolality of xylem sap, leaf tissue and leaf gland secretion of the mangrove Laguncularia racemosa (L.) Gaertn. Trees 18, 422427.Google Scholar
Stuppy, W., Maisano, J.A., Colbert, M.W., Rudall, P.J. & Rowe, T.B. (2003). Three-dimensional analysis of plant structure using high-resolution X-ray computed tomography. Trends Plant Sci 8, 26.CrossRefGoogle ScholarPubMed
Thompson, M.V. (2006). Phloem: The long and the short of it. Trends Plant Sci 11, 2632.Google Scholar
Tiekstra, A.E., Else, M.A. & Jackson, M.B. (2000). External pressures based on leaf water potentials do not induce xylem sap to flow at rates of whole plant transpiration from roots of flooded or well-drained tomato and maize plants. Impact of shoot hydraulic resistances. Ann Bot 86, 665674.CrossRefGoogle Scholar
Tracy, S.R., Black, C.R., Roberts, J.A., Sturrock, C., Mairhofer, S., Craigon, J. & Mooney, S.J. (2012). Quantifying the impact of soil compaction on root system architecture in tomato (Solanum lycopersicum) by X-ray micro-computed tomography. Ann Bot 110, 511519.Google Scholar
Tyree, M.T., Salleo, S., Nardini, A., Gullo, M.A.L. & Mosca, R. (1999). Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiol 120, 1121.Google Scholar
Watson, B.T. (1976). Rapid propagation of changes in velocity of translocation along the phloem pathway of Helianthus annuus L. Ann Bot 40, 659667.Google Scholar
Wendel, F.M., Ternes, T.A., Richardson, S.D., Duirk, S.E., Pals, J.A., Wagner, E.D. & Plewa, M.J. (2016). Comparative toxicity of high-molecular weight iopamidol disinfection byproducts. Environ Sci Technol Lett 3, 8184.Google Scholar
Wildenschild, D., Armstrong, R.T., Herring, A.L., Young, I.M. & Carey, J.W. (2011). Exploring capillary trapping efficiency as a function of interfacial tension, viscosity, and flow rate. Energy Procedia 4, 49454952.CrossRefGoogle Scholar
Wildenschild, D., Vaz, C.M.P., Rivers, M.L., Rikard, D. & Christensen, B.S.B. (2002). Using X-ray computed tomography in hydrology: Systems, resolutions and limitations. J Hydrol 267, 285297.CrossRefGoogle Scholar
Wilson, J.L., Conrad, S.H., Mason, W.R., et al. (1990). Laboratory Investigation of Residual Liquid Organics. Washington, D.C.: US Environmental Protection Agency.Google Scholar
Wilson, J.L. (1990). Laboratory investigation of residual liquid organics from spills, leaks, and the disposal of hazardous wastes in groundwater. Ada, OK: Robert S. Kerr Environmental Research Laboratory, Office of Research and Development, US Environmental Protection Agency.Google Scholar