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Formation of the vascular system of developing bean (Phaseolus limensis L.) seeds according to nuclear magnetic resonance microtomography

  • Plant Developmental Biology
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Abstract

1H magnetic resonance microtomography imaging was applied to study vascular systems in developing bean (Phaseolus limensis L.) seeds. Using the gradient echo method, we recorded 2D tomographic sections in the sagittal and axial planes of the fruits sampled from a vegetating plant on days 10, 17, 24, and 31 after fertilization. Any vascular connection between the tissues of maternal plant (bean pod and seed coat) and the embryo were undetectable. The embryo has an autonomous branched network of procambial strands in the cotyledons, converging to the embryonic axis. The bean pods are covered with a network of vascular bundles; large vascular strands run along the dorsal and ventral sutures. The seed coat vascular bundles are formed in the process of seed ripening and are represented by a developed vascular system multiply branching in the middle part of the ground parenchyma at the stage of physiological maturity. They are connected with the source of assimilates via the lateral pod veins and a large vascular bundle, entering the seed below the hilum via the placenta. Assimilates enter the external part of the seed coat, which contains no vascular bundles, via the funiculus vascular bundles and hilum tissue.

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References

  • Aleksandrov, V.G., Anatomiya rastenii (Anatomy of Plants), Moscow: Sovetskaya nauka, 1954.

    Google Scholar 

  • Aniskin, V.I. and Saprykina, E.G., On Water Permeability of Seeds of Forage Legumes and Lupins, Sel. Semenovod., 1962, no. 4, pp. 18–22.

  • Van As, H., Scheenen, T.W.J., and Vergeldt, F.J., MRI of Intact Plants, Photosynth. Res., 2009, vol. 102, pp. 213–222.

    Article  PubMed  Google Scholar 

  • Bailey, I.W. and Swamy, B.G.L., The Conduplicate Carpel of Dicotiledons and Its Initial Trends of Specification, Am. J. Bot., 1951, vol. 38, pp. 373–379.

    Article  Google Scholar 

  • Blümich, B. and Kuhn, W., Magnetic Resonance Microscopy: Methods and Application in Materials Science, Agriculture and Biomedicine, New York: VCH Publishers. B, 1992.

    Google Scholar 

  • Busse, J.S. and Evert, R.F., Pattern of Differentiation of the First Vascular Elements in the Embryo and Seedling of Arabidopsis thaliana, Int. J. Plant Sci., 1999, vol. 160, pp. 1–13.

    Article  Google Scholar 

  • Callaghan, P.T., Principles of Nuclear Magnetic Resonance Microscopy, Oxford: Oxford Univ. Press, 1991.

    Google Scholar 

  • Chudek, J.A. and Hunter, G., Magnetic Resonance Imaging of Plants, Progr. Nucl. Mag. Res. Sp., 1997, vol. 31, pp. 43–62.

    Article  CAS  Google Scholar 

  • Ciobanu, L., Webb, A.G., and Pennington, C.H., Magnetic Resonance Imaging of Biological Cells, Progr. Nucl. Mag. Res. Sp., 2003, vol. 42, pp. 69–93.

    Article  CAS  Google Scholar 

  • Connelly, A., Lohman, J.A.B., Loughman, B.C., et al., High Resolution Imaging of Plant Tissue by NMR, J. Exp. Bot., 1987, vol. 38, pp. 1713–1723.

    Article  CAS  Google Scholar 

  • Van Dongen, J.T., Ammerlaan, A.M.H., Wouterlood, M., et al., Structure of the Developing Pea Seed Coat and the Post-Phloem Transport Pathway of Nutrients, Ann. Bot., 2003, vol. 91, pp. 729–737.

    Article  PubMed  Google Scholar 

  • Esau, K., Anatomiya semennykh rastenii (Anatomy of Seed Plants), Book 2, Moscow: Mir, 1980.

    Google Scholar 

  • Farrar, T.C. and Becker, E.D., Pulse and Fourier Transform NMR: Introduction to Theory and Methods, New York: Academic Press.B, 1971.

    Google Scholar 

  • Fiziologiya sel’skokhozyaistvennykh rastenii (Physiology of Crop Plants), vol. 6: Zernobobovye rasteniya. Mnogoletnie travy. Khlebnye zlaki (Leguminous Plants. Perennial Grasses. Crop Plants), Turkov, N.S., Ed., Moscow: Mosk. Gos. Univ., 1970.

    Google Scholar 

  • Foster, M.P. and Hutchinson, J.M.S., Practical NMR Imaging, Oxford: IRL Press. B, 1987.

    Google Scholar 

  • Garnczarska, M., Zalewski, T., and Kempka, M., Water Uptake and Distribution in Germinating Lupine Seeds Studied by Magnetic Resonance Imaging and NMR Spectroscopy, Physiologia Plantarum, 2007, vol. 130, pp. 23–32.

    Article  CAS  Google Scholar 

  • Garnczarska, M., Zalewski, T., and Wojtyla, L., A Comparative Study of Water Distribution and Dehydrin Protein Localization in Maturing Pea Seeds, J. Plant Physiol., 2008, vol. 165, pp. 1940–1946.

    Article  PubMed  CAS  Google Scholar 

  • Glidewell, S.M., Williamson, B., Goodman, B.A., et al., An NMR Microscopic Study of Grape (Vitis vinifera L.), Protoplasma, 1997, vol. 198, pp. 27–35.

    Article  Google Scholar 

  • Glidewell, S.M., NMR Imaging of Developing Barley Grains, J. Cereal Sci., 2006, vol. 43, pp. 70–78.

    Article  CAS  Google Scholar 

  • Goodman, B.A., Williamson, B., and Chudek, J.A., Nuclear Magnetic Resonance (NMR) Micro-Imaging of Raspberry Fruit: Further Studies on the Origin of the Image, New Phytol., 1992, vol. 122, pp. 529–535.

    Article  Google Scholar 

  • Gyngell, M.L., The Application of Steady-State Free Precession in Rapid 2DFT NMR Imaging: FAST and CEFAST Sequences, Magn. Res. Imag., 1988, vol. 6, pp. 415–419.

    Article  CAS  Google Scholar 

  • Hausser, K.H. and Kalbitzer, H.R., NMR in Medicine and Biology: Structure Determination, Tomography, in vivo Spectroscopy, Berlin: Springer-Verlag, 1991.

    Google Scholar 

  • Horigane, A.K., Takahashi, H., Maruyama, S., et al., Water Penetration into Rice Grains during Soaking Observed by Gradient Echo Magnetic Resonance Imaging, J. Cereal Sci., 2006, vol. 44, pp. 307–316.

    Article  CAS  Google Scholar 

  • Ishida, N., Koizumi, M., and Kano, H., The NMR Microscope: A Unique and Promising Tool for Plant Science, Ann. Bot., 2000, vol. 86, pp. 259–278.

    Article  CAS  Google Scholar 

  • Ishida, N., Naito, S., and Kano, H., Loss of Moisture from Harvested Rice Seeds on MRI, Magn. Res. Imag., 2004, vol. 22, pp. 871–875.

    Article  Google Scholar 

  • Köckenberger, W., Pope, J.M., Xia, Y., et al., A Non-Invasive Measurement of Phloem and Xylem Water Flow in Castor Bean Seedlings by Nuclear Magnetic Resonance Microimaging, Planta, 1997, vol. 201, pp. 53–63.

    Article  Google Scholar 

  • Köckenberger, W., Functional Imaging of Plants by Magnetic Resonance Experiments, Trends Plant Sci., 2001, vol. 6, no. 7, pp. 286–292.

    Article  PubMed  Google Scholar 

  • Köckenberger, W., De Panfilis, C., Santoro, D., et al., High Resolution NMR Microscopy of Plants and Fungi, J. Microsc., 2004, vol. 214, pp. 182–189.

    Article  PubMed  Google Scholar 

  • Kikuchi, K., Koizumi, M., Ishida, N., et al., Water Uptake by Dry Beans Observed by Micro-Magnetic Resonance Imaging, Ann. Bot., 2006, vol. 98, pp. 545–553.

    Article  PubMed  Google Scholar 

  • Koptyug, I.V. and Sagdeev, R.Z., Modern Physicochemical Applications of NMR Tomography. The Specificity of the Method and Its Application to the Study of LiquidContaining Objects, Usp. Khim., 2002, vol. 71, no. 7, pp. 672–699.

    Google Scholar 

  • Lauterbur, P.C., Image Formation by Induced Local Interactions: Examples Employing Nuclear Magnetic Resonance, Nature, 1973, vol. 242, pp. 190–191.

    Article  CAS  Google Scholar 

  • MacFall, J.S. and Johnson, G.A., The Architecture of Plant Vasculature and Transport as Seen with Magnetic Resonance Microscopy, Can. J. Bot., 1994, vol. 72, pp. 1561–1573.

    Article  Google Scholar 

  • Manz, B., Muller, K., Kucera, B., et al., Water Uptake and Distribution in Germinating Tobacco Seeds Investigated in vivo by Nuclear Magnetic Resonance Imaging, Plant Physiol., 2005, vol. 138, pp. 1538–1551.

    Article  PubMed  CAS  Google Scholar 

  • Morris, P.G., Nuclear Magnetic Resonance Imaging in Medicine and Biology, Oxford: Clarendon Press, 1986.

    Google Scholar 

  • Murray, D.R., Nutritive Role of Seed Coats in Developing Legume Seeds, Am. J. Bot., 1987, vol. 74, pp. 1122–1137.

    Article  CAS  Google Scholar 

  • Öpik H., Development of Cotyledon cell Structure in Ripening Phaseolus vulgaris Seeds, J. Exp. Bot., 1968, vol. 19, no. 58, pp. 64–76.

    Article  Google Scholar 

  • Pate, J.S., Kuo, J., Van Bel, A.J.E., et al., Diurnal Water Balance of the Cowpea Fruit, Plant Physiol., 1985, vol. 77, pp. 148–156.

    Article  PubMed  CAS  Google Scholar 

  • Patrick, J.W. and Offler, C.E., Compartmentation of Transport and Transfer Events in Developing Seeds, J. Exp. Bot., 2001, vol. 52, pp. 551–564.

    Article  PubMed  CAS  Google Scholar 

  • Peoples, M.B., Pate, J.S., Atkins, C.A., et al., Economy of Water, Carbon and Nitrogen in the Developing Cowpea Fruit, Plant Physiol., 1985, vol. 77, pp. 142–147.

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer, P.E. and Gerasimowicz, W.V., Nuclear Magnetic Resonance in Agriculture, Boca Raton.: CRC Press, 1989.

    Google Scholar 

  • Pietrzak, L.N., Fregeau-reid, J., Chatson, B., et al., Observation on Water Distribution in Soybean Seed during Hydration Processes Using Nuclear Magnetic Resonance Imaging, Can. J. Plant Sci., 2002, vol. 82, pp. 513–519.

    Article  Google Scholar 

  • Reeve, R.M. and Brown, M.S., Histological Development of the Green Bean Pod as Related to Culinary Texture. 1. Early Stages of Pod Development, J. Food Sci., 1968, vol. 33 P, pp. 321–326.

    Article  Google Scholar 

  • Rinki, P.A., Magnitnyi rezonans v meditsine (Magnetic Resonance in Medicine), Moscow: Geotar-Med, 2003.

    Google Scholar 

  • Scheenen, T.W.J., Van Dusschoten, D., de Jager, P.A., et al., Quantification of Water Transport in Plants with NMR Imaging, J. Exp. Bot., 2000, vol. 51, pp. 1751–1759.

    Article  PubMed  CAS  Google Scholar 

  • Scheenen, T.W.J., Vergeldt, F.J., Heemskerk, A.M., et al., Intact Plant Magnetic Resonance Imaging to Study Dynamics in Long-Distance Sap Flow-Conducting Surface Area, Plant Physiol., 2007, vol. 144, pp. 1157–1165.

    Article  PubMed  CAS  Google Scholar 

  • Sterling, C., Development of the Seed Coat of Lima Bean (Phaseolus lunatus L.), Bull. Torrey Bot. Club, 1954, vol. 81, no. 4, pp. 271–287.

    Article  Google Scholar 

  • Thorne, J.H., Phloem Unloading of C and N Assimilates in Developing Seeds, Ann. Rev. Plant Physiol., 1985, vol. 36, pp. 317–343.

    Article  CAS  Google Scholar 

  • Tsinger, N.V., Semya, ego razvitie i fiziologicheskie svoistva (Seed, Its Development and Physiological Properties), Moscow: Akad. Nauk SSSR, 1958.

    Google Scholar 

  • Verscht, J., Kalusche, B., Köhler, J., et al., The Kinetics of Sucrose Concentration in the Phloem of Individual Vascular Bundles of the Ricinus communis Seedling Measured by Nuclear Magnetic Resonance Microimaging, Planta, 1998, vol. 205, pp. 132–139.

    Article  CAS  Google Scholar 

  • Vinogradova, I.S. and Falaleev, O.V., Application of Magnetic Resonance Microtomography for Studying the Internal Structure of Plants, Sel’skokhoz. Biol., 2010a, no. 3, pp. 118–124.

  • Vinogradova, I.S. and Falaleev, O.V., Application of Magnetic Resonance Microtomography for Studying the Internal Structure of Legume Seeds, Vestnik Ross. Akad. Sel’skokhoz. Nauk, 2010b, no. 6, pp. 10–12.

  • Weber, H., Borisjuk, L., and Wobus, U., Molecular Physiology of Legume Seed Development, Annu. Rev. Plant Biol., 2005, vol. 56, pp. 253–279.

    Article  PubMed  CAS  Google Scholar 

  • Williamson, B., Goodman, B.A., Chudek, J.A., et al., The Vascular Architecture of the Fruit Receptacle of Red Raspberry Determined by 3D NMR Microscopy and Surface-Rendering Techniques, New Phytol., 1994, vol. 128, pp. 39–44.

    Article  Google Scholar 

  • Xia, Y., Sarafis, V., Campbell, E.O., et al., Non Invasive Imaging of Water Flow in Plants by NMR Microscopy, Protoplasma, 1993, vol. 173, pp. 170–176.

    Article  Google Scholar 

  • Yakovlev, G.P., Bobovye zemnogo shara (Legumes of the World), Leningrad: Nauka, Leningr. Otd., 1991.

    Google Scholar 

  • Zhang, W.H., Zhou, Y., Dibley, K.E., et al., Nutrient Loading in Developing Seeds, Funct. Plant Biol., 2007, vol. 34, pp. 314–331.

    Article  CAS  Google Scholar 

  • Zhou, Y., Setz, N., Niemietz, C., et al., Aquaporins and Unloading of Phloem-Imported Water in Coats of Developing Bean Seeds, Plant, Cell Environ., 2007, vol. 30, pp. 1566–1577.

    Article  CAS  Google Scholar 

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Correspondence to I. S. Vinogradova.

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Original Russian Text © I.S. Vinogradova, O.V. Falaleev, 2012, published in Ontogenez, 2012, Vol. 43, No. 1, pp. 28–38.

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Vinogradova, I.S., Falaleev, O.V. Formation of the vascular system of developing bean (Phaseolus limensis L.) seeds according to nuclear magnetic resonance microtomography. Russ J Dev Biol 43, 25–34 (2012). https://doi.org/10.1134/S1062360412010079

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