Surveying the plant's world by magnetic resonance imaging

Plant Journal

Volumn 70, Issue 1, 2012, Pages 129-146

  Borisjuk, Ljudmilla ^a   Rolletschek, Hardy ^a   Neuberger, Thomas ^b,c  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

abiotic biotic stress; biodiversity; MRI; non invasive imaging; plant metabolism; seed

Indexed keywords

GENE FUNCTION; IN-VIVO; INTERNAL STRUCTURE; NON-INVASIVE IMAGING; PHYSIOLOGICAL PROCESS; PLANT METABOLISM; PLANT PHYSIOLOGY; PLANT SCIENCE; POTENTIAL BENEFITS; TEMPORAL RESOLUTION;

BIODIVERSITY; GENES; MAGNETIC RESONANCE IMAGING; METABOLISM; PHYSIOLOGY;

SEED;

WATER;

BIODIVERSITY; ENVIRONMENT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; METABOLOMICS; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW; SYSTEMS BIOLOGY;

BIODIVERSITY; ENVIRONMENT; HOST-PATHOGEN INTERACTIONS; MAGNETIC RESONANCE IMAGING; METABOLOMICS; PLANT PHYSIOLOGICAL PROCESSES; PLANTS; STRESS, PHYSIOLOGICAL; SYSTEMS BIOLOGY; WATER;

EID: 84859121620     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04927.x     Document Type: Review

References (165)

1. Alonso, G., Perez-Donoso, L., Greve, C., Walton, J.H., Shackel, K.A., and, Labavitch, J.M., (2007) Xylella fastidiosa infection and ethylene exposure result in xylem and water movement disruption in grapevine shoots. Plant Physiol. 143, 1024-1036.
2. Alonso, A.P., Valc, D.L., and, Shachar-Hill, Y., (2011) Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering. Metab. Eng. 13, 96-107.
3. Araus, J.L., Slafer, G.A., Reynolds, M.P., and, Royo, C., (2002) Plant breeding and drought in C-3 cereals: what should we breed for? Ann. Bot. 89, 925-940.
4. Bax, A., Griffey, R.H., and, Hawkins, B.L., (1983) Correlation of proton and nitrogen-15 chemical shifts by multiple quantum NMR. J. Magn. Reson. 55, 301-315.
5. Beck, E.H., Fettig, S., Knake, C., Hartig, K., and, Bhattarai, T., (2007) Specific and unspecific responses of plants to cold and drought stress. J. Biosci. 32, 501-510.
6. Bentsink, L., Hanson, J., Hanhart, C.J., et al. (2010) Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways. Proc. Natl Acad. Sci. USA, 107, 4264-4269.
7. Blossfeld, S., Le Marié, C.A., Van Dusschoten, D., Suessmilch, S., and, Kuhn, A.J., (2011) Non-invasive investigation of root growth via NMR imaging. Commun. Agric. Appl. Biol. Sci. 76, 11-13.
8. Blümich, B., Perlo, J., and, Casanova, F., (2008) Mobile single sided NMR. Prog. Nucl. Magn. Reson. Spectr. 52, 197-269.
9. Blümler, P., Windt, C.W., and, van Dusschoten, D., (2009) Magnetic resonance of plants. Nova Acta Leopold., 96 (357), 17-30.
10. Borisjuk, L., Wang, T.L., Rolletschek, H., Wobus, U., and, Weber, H., (2002) A pea seed mutant affected in the differentiation of the embryonic epidermis is impaired in embryo growth and seed maturation. Development 129, 1595-1607.
11. Borisjuk, L., Nguyen, T.H., Neuberger, T., et al. (2005) Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds. New Phytol. 167, 761-776.
12. Borisjuk, L., Rolletschek, H., Fuchs, J., Melkus, G., and, Neuberger, T., (2011) Recent applications of 'low field' and 'high field' magnetic resonance in seed research. Materials 4, 1426-1439.
13. Borompichaichartkul, C., Moran, G., Srzednicki, G., and, Price, W.S., (2005) Nuclear magnetic resonance (NMR) and magnetic resonance imaging (MRI) studies of corn at subzero temperatures. J. Food Eng. 69, 199-205.
14. Bottomley, P.A., Rogers, H.H., and, Foster, T.H., (1986) NMR imaging shows water distribution and transport in plant root systems in situ. Proc. Natl Acad. Sci. USA, 83, 87-89.
15. Bourgeois, D., Remy, C., Lefur, Y., Devoulon, P., Benabid, A.L., and, Decorps, M., (1991) Proton spectroscopic imaging: a tool for studying intracerebral tumor models in rat. Magn. Reson. Med. 21, 10-20.
16. Boyer, J.S., (1982) Plant productivity and environment. Science, 218, 443-448.
17. Brown, J.M., Johnson, G.A., and, Kramer, P.J., (1986) In vivo magnetic resonance microscopy of changing water content in Pelargonium hortorum roots. Plant Physiol. 82, 1158-1160.
18. Callaghan, P.T., (1993) Principles of Nuclear Magnetic Resonance Microscopy. Oxford: Oxford University Press, p. 492.
19. Capitani, D., Brilli, F., Mannina, L., Proietti, N., and, Loreto, F., (2009) In situ investigation of leaf water status by portable unilateral nuclear magnetic resonance. Plant Physiol. 149, 1638-1647.
20. Chaumon, F., Moshelion, M., and, Daniels, M.J., (2005) Regulation of plant aquaporin activity. Biol. Cell 97, 749-764.
21. Chudek, J.A., and, Hunter, G., (1997) Magnetic resonance imaging of plants. Prog. Nucl. Magn. Reson. Spectrosc. 31, 43-62.
22. Ciobanu, L., and, Pennington, C.H., (2004) 3D micron-scale MRI of single biological cells. Solid State NMR, 25, 138-141.
23. Ciobanu, L., Seeber, D.A, and, Pennington, C.H., (2002) 3D MR microscopy with resolution 3.7 μm by 3.3 μm by 3.3 μm. J. Magn. Reson. 158, 178-182.
24. Clearwater, M.J., and, Clark, C.J., (2003) In vivo magnetic resonance imaging of xylem vessel contents in woody lianas. Plant Cell Environ. 26, 1205-1214.
25. De Graaf, R., (2007) In vivo NMR Spectroscopy. Principles and Techniques, 2nd edn. Chichester: John Wiley & Sons Ldt.
26. 13C]-NMR spectroscopy of cerebral metabolism. NMR Biomed. 16, 339-357.
27. Dixon, H.H., and, Joly, J., (1894) On the ascent of sap. Ann. Bot. 8, 468-470.
28. Drakakaki, G., Christou, P., and, Stöger, E., (2000) Constitutive expression of soybean ferritin cDNA in transgenic wheat and rice results in increased iron levels in vegetative tissues but not in seeds. Transgenic Res. 9, 445-52.
29. Fast Seefeldt, H., van den Berg, F., Köckenberger, W., Engelsen, S.B., and, Wollenweber, B., (2007) Water mobility in the endosperm of high beta-glucan barley mutants as studied by nuclear magnetic resonance imaging. Magn. Reson. Imaging 25, 425-32.
30. Faust, M., Wang, P.C., and, Maas, J., (1997) The use of magnetic resonance imaging in plant science. Hort. Rev. 20, 225-266.
31. Garnczarska, M., Zalewski, T., and, Kempka, M., (2007a) Water uptake and distribution in germinating lupine seeds studied by magnetic resonance imaging and NMR spectroscopy. Physiol. Plant. 130, 23-32.
32. Garnczarska, M., Zalewski, T., and, Kempka, M., (2007b) Changes in water status and water distribution in maturing lupin seeds studied by MR imaging and NMR spectroscopy. J. Exp. Bot. 58, 3961-3969.
33. Gilad, A.A., Ziv, K., McMahon, M.T., van Zijl, P.C.M., Neeman, M., and, Bulte, J.W.M., (2008) MRI reporter genes. J. Nucl. Med. 49, 1905-1908.
34. Glidewell, S.M., (2006) NMR imaging of developing barley grains. J. Cereal. Sci. 50, 70-78.
35. Glidewell, S.M., Williamson, B., Duncan, G.H., Chudek, J.A., and, Hunter, G., (1999) The development of blackcurrant fruit from flower to maturity: a comparative study by 3D nuclear magnetic resonance (NMR) micro-imaging and conventional histology. New Phytol. 141, 85-98.
36. Glover, P., and, Mansfield, P., (2002) Limits to magnetic resonance microscopy. Rep. Prog. Phys. 65, 1489-1511.
37. Golovina, E.A., Van As, H., and, Hoekstra, F.A., (2010) Membrane chemical stability and seed longevity. Eur. Biophys. J. 39, 657-668.
38. Goodman, B.A., Williamson, B., Simpson, E.J., Chudek, J.A., Hunter, G., and, Prior, D.A.M., (1996) High field NMR microscopic imaging of cultivated strawberry fruit. Magn. Reson. Imaging 14, 187-196.
39. Goodson, B., (2006) Mobilizing magnetic resonance. PhysicsWorld 5, 28-33.
40. Gruwel, M.L., Yin, X.S., Edney, M.J., Schroeder, S.W., MacGregor, A.W., and, Abrams, S., (2002) Barley viability during storage: use of magnetic resonance as a potential tool to study viability loss. J. Agric. Food. Chem. 50, 667-676.
41. Gruwel, M.L., Ghosh, P.K., Latta, P., and, Jayas, D.S., (2008) On the diffusion constant of water in wheat. J. Agric. Food. Chem. 56, 59-62.
42. Gussoni, M., Greco, F., Vezzoli, A., Osuga, T., and, Zetta, L., (2001) Magnetic resonance imaging of molecular transport in living morning glory stems. Magn. Reson. Imaging 19, 1311-1322.
43. Haacke, E.M, Brown, R.W., Thompson, M.R., and, Venkatesan, R., (1999) Magnetic Resonance Imaging: Physical Principles and Sequence Design. New York: John Wiley & Sons LTD.
44. Haase, A., Frahm, J., Matthei, D., and, Merbold, K.D., (1986) FLASH imaging: rapid NMR imaging using low flip angle pulses. J. Magn. Reson. 67, 258-266.
45. Haishi, T., Uematsu, T., Matsuda, Y., and, Kose, K., (2001) Development of a 1.0 T MR microscope using a Nd-Fe-B permanent magnet. Magn. Reson. Imaging 19, 875-880.
46. Haishi, T., Koizumi, H., Arai, T., Koizumi, M., and, Kano, H., (2011) Rapid detection of infestation of apple fruits by the peach fruit moth, Carposina sasakii Matsumura, larvae using a 0.2-T dedicated magnetic resonance imaging apparatus. Appl. Magn. Reson. 41, 1-18.
47. Halbach, K., (1980) Design of permanent multipole magnets with oriented rare-earth cobalt material. Nucl. Inst. Meth. 169, 1-10.
48. Hayden, D.M., Rolletschek, H., Borisjuk, L., Corwin, J., Kliebenstein, D.J., Grimberg, A., Stymne, S., and, Dehesh, K., (2011) Cofactome analyses reveal enhanced flux of carbon into oil for potential biofuel production. Plant J. 67, 1018-1028.
49. Heidenreich, M., Köckenberger, W., Kimmich, R., Chandrakumara, N., and, Bowtell, R., (1998) Investigation of carbohydrate metabolism and transport in castor bean seedlings by cyclic J cross polarization imaging and spectroscopy. J. Magn. Reson. 132, 109-124.
50. Hill, P.J., Stritzker, J., Scadeng, M., Geissinger, U., Haddad, D., Basse-Lüsebrink, T.C., Gbureck, U., Jakob, P., and, Szalay, A.A., (2011) Magnetic resonance imaging of tumors colonized with bacterial ferritin-expressing Escherichia coli. PLoS ONE 6, e25409.
51. Hillnhütter, C., Sikora, R.A., Oerke, E.-C., and, van Dusschoten, D., (2011) Nuclear magnetic resonance: a tool for imaging belowground damage caused by Heterodera schachtii and Rhizoctonia solani on sugar beet. J. Exp. Bot. 63, 319-327.
52. Hinshaw, W.S., Bottomley, P.A., and, Holland, G.N., (1979) A demonstration of the resolution of NMR imaging in biological systems. Experientia, 35, 1268-1269.
53. Holbrook, N.M., Ahrens, E.T., Burns, M.J., and, Zwieniecki, M.A., (2001) In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiol. 126, 27-31.
54. Hölttä, T., Vesala, T., Sevanto, S., Perämäki, M., and, Nikinmaa, E., (2006) Modeling xylem and phloem water flows in trees according to cohesion theory and Munch hypothesis. Trees Structure and Function, 20, 67-78.
55. Horigane, A.K., Takahashi, H., Maruyama, S., Ohtsubo, K., and, Yoshida, M., (2006) Water penetration into rice grains during soaking observed by gradient echo magnetic resonance imaging. J. Cereal. Sci. 44, 307-316.
56. Hurd, R.E., and, John, B.K., (1991) Gradient-enhanced proton-detected heteronuclear multiple-quantum coherence spectroscopy. J. Magn. Reson. 91, 648-653.
57. Ide, H., Price, W.S., Arata, Y., and, Ishikawa, M., (1998) Freezing behaviors in leaf buds of cold-hardy conifers visualized by NMR microscopy. Tree Physiol. 18, 451-458.
58. Ishida, N., Koizumi, M., and, Kano, H., (2000) The NMR microscope: a unique and promising tool for plant science. Ann. Bot. 86, 259-278.
59. Ishida, N., Naito, S., and, Kano, H., (2004) Loss of moisture from harvested rice seeds on MRI. Magn. Reson. Imaging 22, 871-875.
60. Ishikawa, M., Price, W.S., Ide, H., and, Arata, Y., (1997) Visualization of freezing behaviors in leaf and flower buds of full-moon maple by nuclear magnetic resonance microscopy. Plant Physiol. 115, 1515-1524.
61. Ishimaru, T., Horigane, A.K., Ida, M., Iwasawa, N., San-oh, Y.A., Nakazono, M., Nishizawa, N.K., Masumura, T., Kondo, M., and, Yoshida, M., (2009) Formation of grain chalkiness and changes in water distribution in developing rice caryopses grown under high-temperature stress. J. Cereal. Sci. 50, 166-174.
62. Jahnke, S., Menzel, M.I., van Dusschoten, D., et al. (2009) Combined MRI-PET dissects dynamic changes in plant structures and functions. Plant J. 59, 634-644.
63. Jiang, T., Ding, B.-O., Li, F.-J, and, Yang, C.-P., (2006) Differential expression of endogenous ferritin genes and iron homeostasis alteration in transgenic tobacco overexpressing soybean ferritin gene. Acta genetica Sinica 33, 1120-1126.
64. Kalcsits, L., Kendall, E., Silim, S., and, Tanino, K., (2009) Magnetic resonance microimaging indicates water diffusion correlates with dormancy induction in cultured hybrid poplar (Populus spp.) buds. Tree Physiol. 29, 1269-1277.
65. Katsuhara, M., Hanba, Y.T., Shiratake, K., and, Maeshima, M., (2008) Expanding roles of plant aquaporins in plasma membranes and cell organelles. Funct. Plant Biol. 35, 1-14.
66. Kaufmann, I., Schulze-Till, T., Schneider, H.U., Zimmermann, U., Jakob, P., and, Wegner, L.H., (2009) Functional repair of embolized vessels in maize roots after temporal drought stress, as demonstrated by magnetic resonance imaging. New Phytol. 184, 245-256.
67. Ki, S., Sugihara, F., Kasahara, K., Tochio, H., Shirakawa, M., and, Kokubo, T., (2007) Magnetic resonance-based visualization of gene expression in mammalian cells using a bacterial polyphosphate kinase reporter gene. BioTechniques, 42, 209-215.
68. Kikuchi, K., Koizumi, M., Ishida, N., and, Kano, H., (2006) Water uptake by dry bean observed by micro-magnetic resonance imaging. Ann. Bot. 98, 545-553.
69. Kimura, T., Geya, Y., Terada, Y., Kose, K., Haishi, T., Gemma, H., and, Sekozawa, Y., (2011) Development of a mobile magnetic resonance imaging system for outdoor tree measurements. Rev. Sci. Instrum. 82, 053704.
70. Köckenberger, W., (2001) Functional imaging of plants by magnetic resonance experiments. Trends Plant Sci. 6, 286-292.
71. Köckenberger, W., and, Granwehr, J., (2009) MR microscopy. In Encyclopedia of Spectroscopy and Spectrometry (, Lindon, J., Tranter, G., and, Koppenaal, D., eds.). London: Academic Press, pp. 1654-1662.
72. Köckenberger, W., Pope, J.M., Xia, Y., Jeffrey, K.R., Komor, E., and, Callaghan, P.T., (1997) A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging. Planta, 201, 53-63.
73. Köckenberger, W., De Panfilis, C., Santoro, D., Dahiya, P., and, Rawsthorne, S., (2004) High resolution NMR microscopy of plants and fungi. J. Microsc. 214, 182-189.
74. Koizumi, M., Kikuchi, K., Isobe, S., Ishida, N., Naito, S., and, Kano, H., (2008) Role of seed coat in imbibing soybean seeds observed by micro-magnetic resonance imaging. Ann. Bot. 102, 343-352.
75. Lauterbur, P.C., (1973) Image formation by induced local interactions: examples of employing nuclear magnetic resonance. Nature, 242, 190-191.
76. Lee, S.C., Kim, K., Kim, J., Lee, S., Yi, J.H., Kim, S.W., Ha, K.S., and, Cheong, C., (2001) One micrometer resolution NMR microscopy. J. Magn. Reson. 150, 207-213.
77. Lee, K., Avondo, J., Morrison, H., Blot, L., Stark, M., Sharpe, J., Bangham, A., and, Coen, E., (2006) Visualizing plant development and gene expression in three dimensions using optical projection tomography. Plant Cell, 18, 2145-2156.
78. Levitt, H.M., (2008) Spin dynamics: Basics of Nuclear Magnetic Resonance. England, UK: John Wiley & Sons LTD.
79. Liu, X.L., Covington, M.F., Fankhauser, C., Chory, J., and, Wagner, D.R., (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell, 13, 1293-1304.
80. Liu, Y.B., Wang, G., Liu, J., Zhao, X., Tan, H.J., and, Li, X.R., (2007) Anatomical, morphological and metabolic acclimation in the resurrection plant Reaumuria soongorica during dehydration and rehydration. J. Arid Environ. 70, 183-194.
81. Liu, G., Bulte, J.W., and, Gilad, A.A., (2011) CEST MRI reporter genes. Methods Mol. Biol. 711, 271-80.
82. Livet, J., Weissman, T.A., Kang, H., Draft, R.W., Lu, J., Bennis, R.A., Sanes, J.R., and, Lichtman, J.W., (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature, 450, 56-62.
83. Lopes, M.S., Araus, J.L., van Heerden, P.D.R., and, Foyer, C.H., (2011) Enhancing drought tolerance in C4 crops. J. Exp. Bot. 62, 3135-3153.
84. MacFall, J.S., Spaine, P., Doudrick, R., and, Johnson, G.A., (1994) Alterations in growth and water-transport processes in fusiform rust galls of pine, determined by magnetic resonance microscopy. Phytopathology, 84, 288-293.
85. Manz, B., Müller, K., Kucera, B., Volke, F., and, Leubner-Metzger, G., (2005) Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant Physiol. 138, 1538-1551.
86. Melkus, G., Rolletschek, H., Radchuk, R., Fuchs, J., Rutten, T., Wobus, U., Altmann, T., Jakob, P., and, Borisjuk, L., (2009) The metabolic role of legume endosperm: a non-invasive imaging study. Plant Physiol. 151, 1139-1154.
87. 13C/1H NMR imaging uncovers sugar allocation in the living seed. Plant Biotechnol. J. 9, 1022-1037.
88. Metzler, A., Izquierdo, M., Ziegler, A., Köckenberger, W., Komor, E., von Kienlin, M., and, Haase, A., (1995) Plant histochemistry by correlation peak imaging. Proc. Natl Acad. Sci. USA, 92, 11912-11915.
89. Millard, M.M., Veisz, O.B., Krizek, D.T., and, Line, M., (1995) Magnetic resonance imaging (MRI) of water during cold acclimation and freezing in winter wheat. Plant Cell Environ. 18, 535-544.
90. Mispelter, J., Lupu, M., and, Briguet, A., (2006) NMR Probeheads: For Biophysical and Biomedical Experiments. London, UK: Imperial College Press.
91. Molina-Cano, J.L., Sopena, A., Polo, J.P., Bergareche, C., Moralejo, M.A., Swanston, J.S., and, Glidewell, S.M., (2002) Relationships between barley hordeins and malting quality in a mutant of cv. Triumph. II. Genetic and environmental effects on water uptake. J. Cereal. Sci. 36, 39-50.
92. Mullendore, D.L., Windt, C.W., Van As, H., and, Knoblauch, M., (2010) Sieve tube geometry in relation to phloem flow. Plant Cell, 22, 579-593.
93. Münch, E., (1930) Die Stoffbewegungen in der Pflanze. Jena, Germany: Gustav Fischer.
94. Musse, M., Quellec, S., Devaux, M-F., Cambert, M., Lahaye, M., and, Mariette, F., (2009) An investigation of the structural aspects of the tomato fruit by means of quantitative nuclear magnetic resonance imaging. Magn. Reson. Imaging 27, 709-719.
95. Nagata, T., Kiyono, M., and, Pan-Hou, H., (2006) Engineering expression of bacterial polyphosphate kinase in tobacco for mercury remediation. Appl. Microbiol. Biotechnol. 72, 777-782.
96. Nagel, M., and, Börner, A., (2010) The longevity of crop seeds stored under ambient conditions. Seed Science Research, 20, 1-12.
97. Neuberger, T., and, Webb, A.G., (2009) Radiofrequency coils for magnetic resonance microscopy and microimaging. NMR Biomed. 22, 975-981.
98. Neuberger, T., Sreenivasulu, N., Rokitta, M., et al. (2008) Quantitative imaging of oil storage in developing crop seeds. Plant Biotechnol. J. 6, 31-45.
99. Neuberger, T., Rolletschek, H., Webb, A., and, Borisjuk, L., (2009) Non-invasive mapping of lipids in plant tissue using magnetic resonance imaging. Methods Mol. Biol. 579, 485-496.
100. Osuga, T., and, Tatsuoka, H., (1999) Effect of 1.5 T steady magnetic field on neuroconduction of a bullfrog sciatic nerve in a partially active state within several hours after extraction. Magn. Reson. Imaging 17, 791-794.
101. Paul, A.L., Ferl, R.J., and, Meisel, M.W., (2006) High magnetic field induced changes of gene expression in Arabidopsis. Biomagn. Res. Technol. 22, 7.
102. Pearce, R.B., Sumer, S., Doran, S.J., Carpenter, T.A., and, Hall, L.D., (1994) Non-invasive imaging of fungal colonization and host response in the living sapwood of sycamore (Acer pseudoplatanus L.) using nuclear magnetic resonance. Physiol. Mol. Plant Pathol. 45, 359-384.
103. Pennisi, E., (2008) Plant genetics: the blue revolution, drop by drop, gene by gene. Science, 320, 171-173.
104. Peuke, A.D., Rokitta, M., Zimmermann, U., Schreiber, L., and, 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, 491-503.
105. Peuke, A.D., Windt, C., and, Van As, H., (2006) Effects of cold-girdling on flows in the transport phloem in Ricinus communis: is mass flow inhibited? Plant Cell Environ. 29, 15-25.
106. Pohlmeier, A., Oros-Peusquens, A., Javaux, M., Menzel, M.I., Vanderborght, J., Kaffanke, J., Romanzetti, S., Lindenmair, J., Vereecken, H., and, Shah, N.J., (2008) Changes in soil water content resulting from Ricinus root uptake monitored by magnetic resonance imaging. Vadose Zone J 7, 1010-1017.
107. Price, W.S., Ide, H., Arata, Y., and, Ishikawa, M., (1997) Visualization of freezing behaviours in flower bud tissues of cold hardy Rhododendron japonicum by nuclear magnetic resonance micro-imaging. Aust. J. Plant Physiol. 24, 599-605.
108. 31P NMR investigation of Gadolinium uptake in maize roots. J. Inorg. Biochem. 38, 265-275.
109. Radchuk, V., Borisjuk, L., Radchuk, R., Steinbiss, H.-H., Rolletschek, H., Broeders, S., and, Wobus, U., (2006) Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell 18, 1652-1666.
110. Raich, H., and, Blümler, P., (2004) Design and construction of a dipolar Halbach array with an homogeneous field from identical bar-magnets-NMR-Mandhalas. Conc. Magn. Reson. B: Magn. Reson. Eng. 23B, 16-25.
111. Ratcliffe, R.G., (2010) Plant science applications of NMR. In Encyclopedia of Spectroscopy and Spectrometry, 2nd edn, vol. 3. (, Lindon, J., Tranter, G., and, Koppenaal, D., eds.). London: Academic Press.
112. Ratcliffe, R.G., Roscher, A., and, Shachar-Hill, Y., (2001) Plant NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 39, 267-300.
113. Rathjen, J.R., Strounina, E.V., and, Mares, D.J., (2009) Water movement into dormant and non-dormant wheat (Triticum aestivum L.) grains. J. Exp. Bot. 60, 1619-1631.
114. 1H magnetic resonance imaging and complementary analytical techniques to characterize developmental changes in the Zantedeschia Spreng. tuber. J. Exp. Bot. 51, 2009-2020.
115. Roh, M.S., (2005) Flowering and inflorescence development of Lachenalia aloides'Pearsonii' as influenced by bulb storage and forcing temperature. Sci. Hortic. 104, 305-323.
116. Roh, M.S., Bentz, J.-A., Wang, P., Li, E., and, Koshioka, M., (2004) Maturity and temperature stratification affect the germination of Sytrax japonicus seeds. J. Hort. Sci. Biotech. 79, 645-651.
117. Rokitta, M., Zimmermann, U., and, Haase, A., (1999) Fast NMR flow measurements in plants using FLASH imaging. J. Magn. Reson. 137, 29-32.
118. Rokitta, M., Rommel, E., Zimmermann, U., and, Haase, A., (2000) Portable nuclear magnetic resonance imaging system. Rev. Sci. Instrum. 71, 4257-4262.
119. Rolletschek, H., Melkus, G., Grafahrend-Belau, E., Fuchs, J., Heinzel, N., Schreiber, F., Jakob, P.M., and, Borisjuk, L., (2011) Combined non-invasive imaging and modelling approaches reveal metabolic compartmentation in the cereal endosperm. Plant Cell, 23, 3041-3054.
120. 13C] glutamate turnover in human brain. Proc. Natl Acad. Sci. USA, 89, 9603-9606.
121. Ruan, R., and, Litchfeld, J.B., (1992) Determination of water distribution and mobility inside maize kernels during steeping using magnetic resonance imaging. Ceral Chem. 69, 13-17.
122. Salleo, S., Lo Gullo, M.A., Trifilo, P., and, Nardini, A., (2004) New evidence for the role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant Cell Environ. 27, 1065-1076.
123. 1H magnetic resonance imaging. BMC Plant Biol. 10, 188.
124. Scheenen, T.W.J., Vergeldt, F.J., Windt, C.W., de Jager, P.A., and, Van As, H., (2001) Microscopic imaging of slow flow and diffusion: a pulsed field gradient stimulated echo sequence combined with turbo spin echo imaging. J. Magn. Reson. 151, 94-100.
125. Scheenen, T., Heemskerk, A., de Jager, A., Vergeldt, F., and, Van As, H., (2002) Functional imaging of plants: a nuclear magnetic resonance study of a cucumber plant. Biophys. J. 82, 481-92.
126. Scheenen, T.W., Vergeldt, F.J., Heemskerk, A.M., and, Van As, H., (2007) Intact plant magnetic resonance imaging to study dynamics in long-distance sap flow and flow-conducting surface area. Plant Physiol. 144, 1157-1165.
127. Schneider, H., Manz, B., Westhoff, M., et al. (2003) The impact of lipid distribution, composition and mobility on xylem water refilling of the resurrection plant Myrothamnus flabellifolia. New Phytol. 159, 487-505.
128. Schulze-Till, T., Kaufmann, I., Sattelmacher, B., Jakob, P., Haase, A., Guo, S., Zimmermann, U., and, Wegner, L., (2009) A 1H NMR study of water flow in Phaseolus vulgaris L. roots treated with nitrate or ammonium. Plant Soil, 319, 307-321.
129. Serganova, I., Ponomarev, V., and, Blasberg, R., (2007) Human reporter genes: potential use in clinical studies. Nucl. Med. Biol. 34, 791-807.
130. Shaarani, S.M., Cárdenas-Blanco, A., Amin, M.H.G., Soon, N.G., and, Hall, L.D., (2010) Monitoring development and ripeness of oil palm fruit (Elaeis guneensis) by MRI and bulk NMR. Int. J. Agric. Biol. 12, 101-105.
131. Sidhu, O.P., Pathre, A.S., Snehi, S.K., Raj, S.K., Roy, R., and, Khetrapal, C.L., (2010) Metabolic and histopathological alterations of Jatropha mosaic begomovirus-infected Jatropha curcas L. by HR-MAS NMR spectroscopy and magnetic resonance imaging. Planta 232, 85-93.
132. Simon, M., and, Mattson, J.S., (1996) The Pioneers of NMR and Magnetic Resonance in Medicine: The Story of MRI. Ramat Gan, Israel: Bar-Ilan University Press. ISBN 0-9619243-1-4.
133. Soher, B.J., van Zijl, P.C., Duyn, J.H., and, Barker, P.B., (1996) Quantitative proton MR spectroscopic imaging of the human brain. Magn. Reson. Med. 35, 356-363.
134. Sweetlove, L.J., and, Ratcliffe, R.G., (2011) Flux-balance modeling of plant metabolism. Front. Plant. Sci. 2, 38.
135. Szimtenings, M., Olt, S., and, Haase, A., (2003) Flow encoded NMR spectroscopy for quantification of metabolite flow in intact plants. J. Magn. Reson. 161, 70-76.
136. Takase, T., Ishikawa, H., Murakami, H., Kikuchi, J., Sato-Nara, K., and, Suzuki, H., (2011) The circadian clock modulates water dynamics and aquaporin expression in Arabidopsis roots. Plant Cell Physiol. 52, 373-383.
137. Tanino, K.K., Kalcsits, L., Silim, S., Kendall, E., and, Gray, G.R., (2010) Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol. Biol. 73, 49-65.
138. Terskikh, V.V., Feurtado, J.A., Ren, C., Abrams, S.R., and, Kermode, A.R., (2005) Water uptake and oil distribution during imbibition of seeds of western pine (Pinus monticola Dougl. ex D. Don) monitored in vivo using magnetic resonance imaging. Planta, 221, 17-27.
139. 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn. Reson. Med., 41, 649-656.
140. Truernit, E., Bauby, H., Dubreucq, B., Grandjean, O., Runions, J., Barthélémy, J., and, Palauqui, J.-C., (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell, 20, 1494-1503.
141. Tse, T.Y., Spanswick, R.M., and, Jelinski, L.W., (1996) Quantitative evaluation of NMR and MRI methods to measure sucrose concentrations in plants. Protoplasma 194, 54-62.
142. Umebayashi, T., Fukuda, K., Haishi, T., Sotooka, R., Zuhair, S., and, Otsuki, K., (2011) The developmental process of xylem embolisms in pine wilt disease monitored by multipoint imaging using compact magnetic resonance imaging. J. Exp. Bot. 59, 3371-3381.
143. Utsuzawa, S., Fukuda, K., and, Sakaue, D., (2005) Use of magnetic resonance microscopy for the nondestructive observation of xylem cavitation caused by pine wilt disease. Phytopathology, 95, 737-743.
144. Van As, H., (2007) Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. J. Exp. Bot. 58, 743-756.
145. Van As, H., Reinders, J.E.A., de Jager, P.A., van der Sanden, P.A.C.M., and, Schaafsma, T.J., (1994) In situ plant water-balance studies using a portable NMR spectrometer. J. Exp. Bot. 45, 61-67.
146. Van As, H., Scheenen, T., and, Vergeldt, F.J., (2009) MRI of intact plants. Photosynth. Res. 102, 213-222.
147. Van der Toorn, A., Zemah, H., Van As, H., Bendel, P., and, Kamenetsky, R., (2000) Developmental changes and water status in tulip bulbs during storage: visualization by RMN imaging. J. Exp. Bot. 51, 1277-1287.
148. Van der Weerd, L., (2002a) Magnetic Resonance Imaging of Plants: Plant Water Status and Drought Stress Response. PhD Thesis, Laboratory of Biophysics, Wageningen University, Wageningen, The Netherlands.
149. Van der Weerd, L., Claessens, M.M.A.E., Ruttink, T., Vergeldt, F.J., Schaafsma, T.J., and, Van As, H., (2001) Quantitative NMR microscopy of osmotic stress responses in maize and pearl millet. J. Exp. Bot. 52, 2333-2343.
150. Van der Weerd, L., Claessens, M.M.A.E., Efdé, C., and, Van As, H., (2002b) Nuclear magnetic resonance imaging of membrane permeability changes in plants during osmotic stress. Plant Cell Environ. 25, 1538-1549.
151. Van Voorthuysen, T., Regierer, B., Springer, F., Dijkema, C., Vreugdenhil, D., and, Kossmann, J., (2000) Introduction of poly-phosphate as a novel phosphate pool in the chloroplast of transgenic potato plants modifies carbohydrate partitioning. J. Biotechnol. 77, 65-80.
152. Van Wuytswinkel, O., Vansuyt, G., Grignon, N., Fourcroy, P., and, Briat, J.F., (1999) Iron homeostasis alteration in transgenic tobacco overexpressing ferritin. Plant J. 17, 93-97.
153. Vanhamme, L., van den Boogaart, A., and, van Huffel, S., (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J. Magn. Reson. 129, 35-43.
154. Verscht, J., Kalusche, B., Köhler, J., Koeckenberger, W., Metzler, A., Haase, A., and, Komor, E., (1998) The kinetics of sucrose concentration in the phloem of individual vascular bundles of the Ricinus communis seedling measured by nuclear magnetic resonance microimaging. Planta, 205, 132-139.
155. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J.H., and, Zhu, J.K., (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45, 523-539.
156. Wenzler, M., Hölscher, D., Oerther, T., and, Schneider, B., (2008) Nectar formation and floral nectary anatomy of Anigozanthos flavidus- a combined magnetic resonance imaging and spectroscopy study. J. Exp. Bot. 59, 3425-3434.
157. Windt, C.W., Vergeldt, F.J., De Jager, P.A., and, Van As, H., (2006) 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 Environ. 29, 1715-1729.
158. Windt, C.W., Gerkema, E., and, Van As, H., (2009) Most water in the tomato truss Is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study. Plant Physiol. 151, 830-842.
159. Windt, C.W., Soltner, H., van Dusschoten, D., and, Blümler, P., (2011) A portable Halbach magnet that can be opened and closed without force: the NMR-CUFF. J. Magn. Reson. 208, 27-33.
160. Wojtyla, L., Garnczarska, M., Zalewski, T., Bednarski, W., Ratajczak, L., and, Jurga, S., (2006) A comparative study of water distribution, free radical production and activation of antioxidative metabolism in germinating pea seeds. J. Plant Physiol. 163, 1207-1220.
161. Wright, S.M., Brown, D.G., Porter, J.R., Spence, D.C., Esparza, E., Cole, D.C., and, Huson, F.R., (2002) A desktop magnetic resonance imaging system. MAGMA 13, 177-185.
162. Yadav, S.K., (2009) Cold stress tolerance mechanisms in plants. A review. Agron. Sustain. Dev. 30, 515-527.
163. Yamazaki, T., Kawamura, Y., Minami, A., and, Uemur, M., (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell, 20, 3389-3404.
164. Yooyongwech, S., Horigane, A.K., Yoshida, M., Yamaguchi, M., Sekozawa, Y., Sugaya, S., and, Gemma, H., (2008) Changes in aquaporin gene expression and magnetic resonance imaging of water status in peach tree flower buds during dormancy. Physiol. Plant. 134, 522-533.
165. Zhang, H.-J., Wei, Z.-G., Zhao, H.-Y., Yang, H.-X., Li, H.-X., and, Hu, F., (2009) Effects of low-molecular-weight organic acids on Gadolinium accumulation and transportation in tomato plants. Biol. Trace Elem. Res. 127, 81-93.