Abstract
The effect of N nutrition on root xylem (water) flow in Phaseolus vulgaris was studied by using the 1H NMR flow imaging technique. Plants pre-cultivated on CaSO4-solution were transferred to NMR-compatible split-root cuvettes filled with half-strength nitrate medium (2.5 mM). After 6 days full-strength (5 mM) nitrate medium was supplied to both compartments (NN treatment), or only to one compartment, whereas the other one was perfused with full-strength (5 mM) ammonium medium (NA treatment). Imaging was performed 7–8 days later. Root growth, xylem flow velocity and xylem pressure (measured with the xylem pressure probe) were largely unaffected by N nutrition. Under NA conditions, volume flow was significantly lower in ammonium- compared to nitrate-fed roots due to a reduced number of functional xylem elements. This was apparently not related to anatomical differences nor to an enhanced number of cavitated vessels in ammonium-fed roots. Vessels in these roots may become dysfunctional by clogging to prevent cavitation.
Similar content being viewed by others
Notes
Mean values ± SD throughout the paper. Significance was tested using Student’s T-test.
Xylem pressure is given in absolute values, i.e. 0 MPa corresponds to vacuum.
Abbreviations
- DW:
-
Dry weight
- NA:
-
Under split-root conditions, roots are either supplied with nitrate or ammonium nutrient solution
- NN:
-
Under split-root conditions, all roots are supplied with the same nitrate nutrient solution
- NMR:
-
Nuclear magnetic resonance
- Px :
-
Xylem pressure
- TSE:
-
Turbo-spin-echo
References
Adler PR, Wilcox GE, Markhart AH III (1996) Ammonium decreases muskmelon root system hydraulic conductivity. J Plant Nutr 19:1395–1403
Allen S, Raven JA, Sprent JI (1988) The role of long-distance transport in intracellular pH regulation in Phaseolus vulgaris grown with ammonium or nitrate as nitrogen source, or nodulated. J Exp Bot 39:513–528 doi:10.1093/jxb/39.5.513
Bentrup F-W (1996) NMR-microscopy: observing xylem and phloem conduits at work. Bot Acta 109:177–179
Bijlsma RJ, Lambers H, Kooijman SALM (2000) A dynamic whole-plant model of integrated metabolism of nitrogen and carbon. 1. Comparative ecological implications of ammonium-nitrate interactions. Plant Soil 220:49–69 doi:10.1023/A:1004779019486
Bottomley PA, Rogers HH, Forster TH (1986) NMR imaging shows water distribution and transport in plant root systems in-situ. Proc Natl Acad Sci USA 83:87–89 doi:10.1073/pnas.83.1.87
Bottomley PA, Rogers HH, Prior SA (1993) NMR imaging of root water distribution in intact Vicia faba L. plants in elevated atmospheric carbon dioxide. Plant Cell Environ 16:335–338 doi:10.1111/j.1365-3040.1993.tb00878.x
Bourgeois D, Decorps M (1991) Quantitative imaging of slow coherent motion by stimulated echoes with suppression of stationary water signal. J Magn Reson 94:20–33
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 doi:10.1016/0003-2697(76)90527-3
Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants. a critical review. J Plant Physiol 159:567–584 doi:10.1078/0176-1617-0774
Brown DP, Pratum TK, Bledsoe C, Ford ED, Cothern JS, Perry D (1991) Noninvasive studies of conifer roots by nuclear magnetic resonance NMR imaging of Douglas fir seedlings. Can J For Res 21:1559–1566 doi:10.1139/x91-217
Brück H, Guo S (2006) Influence of N-form on growth and photosynthesis of Phaseolus vulgaris L. plants. J Plant Nutr Soil Sci 169:849–856 doi:10.1002/jpln.200520570
Canny MJ (1990) Tansley Review No. 22: What becomes of the transpiration stream? New Phytol 114:341–368 doi:10.1111/j.1469-8137.1990.tb00404.x
Canny MJ (1993) The transpiration stream in the leaf apoplast: water and solutes. Philos Trans R Soc Lond Ser B 341:87–100 doi:10.1098/rstb.1993.0094
Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Steudle E (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot 51:61–70 doi:10.1093/jexbot/51.342.61
Feil B (1994) Growth and ammonium: nitrate uptake ratio of spring wheat cultivars under a homogeneous and a spatially separated supply of ammonium and nitrate. J Plant Nutr 17:717–728
Fernandez BE, Clothier JE, van Noordwijk M (2000) Water uptake. In: Smit AL, Bengough AG, Engels C, van Noordwijk M, Pellerin S, van de Geijn SC (eds) Root methods: a handbook. Springer, New York etc., pp 461–507
Guo S, Brück H, Sattelmacher B (2002) Effects of supplied nitrogen form on growth and water uptake of French bean (Phaseolus vulgaris L.) plants. Plant Soil 239:267–275 doi:10.1023/A:1015014417018
Guo S, Kaldenhoff R, Uehlein N, Sattelmacher B, Brueck H (2007a) Relationship between water and nitrogen uptake in nitrate- and ammonium-supplied Phaseolus vulgaris L. plants. J Plant Nutr Soil Sci 170:73–80 doi:10.1002/jpln.200625073
Guo S, Zhou Y, Shen Q, Zhang F (2007b) Effect of ammonium and nitrate nutrition on some physiological processes in higher plants—growth, photosynthesis, photorespiration, and water relations. Plant Biol 9:21–29 doi:10.1055/s-2006-924541
Haase A, Frahm J, Mattaei D, Hänicke W, Merboldt K-D (1986) FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J Magn Reson 67:258–266
Hennig J, Nauerth A, Friedburg H (1986) RARE imaging: a fast imaging method for clinical MR. Magn Reson Med 3:823–833 doi:10.1002/mrm.1910030602
Holbrook NM, Ahrens ET, Burns MJ, Zwieniecki MA (2001) In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiol 126:27–31 doi:10.1104/pp.126.1.27
Köckenberger W (2001) Functional imaging of plants by magnetic resonance experiments. Trends Plant Sci 6:286–292 doi:10.1016/S1360-1385(01)01984-7
Köckenberger W, Pope JM, Xia Y, Komor E, Jeffrey KR, Callaghan PT (1997) A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging. Planta 201:53–63 doi:10.1007/BF01258680
Kuchenbrod E, Landeck M, Thürmer F, Haase A, Zimmermann U (1996) Measurement of water flow in the xylem vessels of intact maize plants using flow-sensitive NMR imaging. Bot Acta 109:184–186
Kuchenbrod E, Kahler E, Thürmer F, Deichmann R, Zimmermann U, Haase A (1998) Functional magnetic resonance imaging in intact plants—quantitative observation of flow in plant vessels. Magn Res Imag 16:331–338 doi:10.1016/S0730-725X(97)00307-X
McCully ME (1994) Accumulation of high levels of potassium in developing xylem elements in roots of soybean and some other dicotyledons. Protopl 183:116–125 doi:10.1007/BF01276819
Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36 doi:10.1007/s11104-004-0965-1
Peuke AD, Kaiser WM (1996) Nitrate or ammonium uptake and transport, and rapid regulation of nitrate reduction in higher plants. Prog Bot 57:93–113
Peuke AD, 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 spectroscopy. Plant Cell Environ 24:491–503 doi:10.1046/j.1365-3040.2001.00704.x
Pritchard J, Ford-Lloyd B, Newbury HJL (2005) Roots as an integrated part of the translocation pathway. In: Holbrook NM, Zwieniecki M (eds) Vascular transport in plants. Elsevier, Amsterdam, pp 157–180
Radin JW (1990) Responses of transpiration and hydraulic conductance to root temperature in nitrogen- and phosphorus-deficient cotton seedlings. Plant Physiol 92:855–857
Radin JW, Boyer JS (1982) Control of leaf expansion by nitrogen nutrition in sunflower plants. Role of hydraulic conductivity and turgor. Plant Physiol 69:771–775
Radin JW, Matthews MA (1989) Water transport properties of cortical cells in roots of nitrogen- and phosphorus-deficient cotton seedlings. Plant Physiol 89:264–268
Rokitta M, Peuke AD, Zimmermann U, Haase A (1999a) Dynamic studies of phloem and xylem flow in fully differentiated plants by fast nuclear-magnetic-resonance microimaging. Protopl 209:126–131 doi:10.1007/BF01415708
Rokitta M, Zimmermann U, Haase A (1999b) Fast NMR flow measurements in plants using FLASH imaging. J Magn Reson 137:29–32 doi:10.1006/jmre.1998.1611
Romeis B (1989) Mikroskopische Technik, 17th edn. Urban and Schwarzenberg, München, Germany
Schneider H, Wistuba N, Miller B, Geßner P, Thürmer F, Melcher P, Meinzer F, Zimmermann U (1997) Diurnal variation in the radial reflection coefficient of intact maize roots determined with the xylem pressure probe. J Exp Bot 48:2045–2053
Schweizer P, Erismann KH (1985) Effect of nitrate and ammonium nutrition of nonnodulated Phaseolus vulgaris L. on phosphoenolpyruvate carboxylase and pyruvat kinase activity. Plant Physiol 78:455–458
Southon TE, Mattsson A, Jones RA (1992) NMR imaging of roots: effects after root freezing of containerised conifer seedlings. Physiol Plant 86:329–334 doi:10.1034/j.1399-3054.1992.860221.x
Van As H, Schaafsma TJ (1984) Noninvasive measurement of plant water flow by nuclear magnetic resonance. Biophys J 45:469–472
Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51:227–237 doi:10.1093/jexbot/51.343.227
Wang Y-H, Garvin DF, Kochian LV (2001) Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol 127:345–359 doi:10.1104/pp.127.1.345
Wegner LH, Zimmermann U (1998) Simultaneous recording of xylem pressure and trans-root potential in roots of intact glycophytes using a novel xylem pressure probe technique. Plant Cell Environ 21:849–865 doi:10.1046/j.1365-3040.1998.00335.x
Wistuba N, Reich R, Wagner H-J, Zhu JJ, Schneider H, Bentrup F-W, Haase A, Zimmermann U (2000) Xylem flow and its driving forces in a tropical liana: concomitant flow-sensitive NMR imaging and pressure probe measurements. Plant Biol 2:579–582 doi:10.1055/s-2000-16644
Zimmermann U, Schneider H, Wegner LH, Haase A (2004) Tansley review: water ascent in tall trees: Does evolution of land plants rely on a highly metastable state? New Phytol 162:575–613 doi:10.1111/j.1469-8137.2004.01083.x
Zwieniecki MA, Melcher P, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062 doi:10.1126/science.1057175
Acknowledgement
This work was supported by grants of the Deutsche Forschungsgemeinschaft to U.Z. and B.S. (SPP “Der Apoplast der höheren Pflanze”, grants No. Zi 99/10-3, Sa 359/12-3 and Sa 359/9) as well as to L.H.W. (We2766 1-1). We would also like to thank Günter Carl from the workshop of the Physics department in Würzburg for constructing the NMR split-root cuvettes, Mrs Stephanie Nieft for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: A.C. Borstlap.
Dedicated to the memory of the late Dr. Burkhard Sattelmacher, who passed away on November 21, 2005.
Rights and permissions
About this article
Cite this article
Schulze-Till, T., Kaufmann, I., Sattelmacher, B. et al. A 1H NMR study of water flow in Phaseolus vulgaris L. roots treated with nitrate or ammonium. Plant Soil 319, 307–321 (2009). https://doi.org/10.1007/s11104-008-9871-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-008-9871-2