MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco.

We used dedicated magnetic resonance imaging (MRI) equipment and methods to study phloem and xylem transport in large potted plants. Quantitative flow profiles were obtained on a per-pixel basis, giving parameter maps of velocity, flow-conducting area and volume flow (flux). The diurnal xylem and phloem flow dynamics in poplar, castor bean, tomato and tobacco were compared. In poplar, clear diurnal differences in phloem flow profile were found, but phloem flux remained constant. In tomato, only small diurnal differences in flow profile were observed. In castor bean and tobacco, phloem flow remained unchanged. In all plants, xylem flow profiles showed large diurnal variation. Decreases in xylem flux were accompanied by a decrease in velocity and flow-conducting area. The diurnal changes in flow-conducting area of phloem and xylem could not be explained by pressure-dependent elastic changes in conduit diameter. The phloem to xylem flux ratio reflects what fraction of xylem water is used for phloem transport (Münch's counterflow). This ratio was large at night for poplar (0.19), castor bean (0.37) and tobacco (0.55), but low in tomato (0.04). The differences in phloem flow velocity between the four species, as well as within a diurnal cycle, were remarkably small (0.25-0.40 mm s(-1)). We hypothesize that upper and lower bounds for phloem flow velocity may exist: when phloem flow velocity is too high, parietal organelles may be stripped away from sieve tube walls; when sap flow is too slow or is highly variable, phloem-borne signalling could become unpredictable.

[1]  A. Bel,et al.  Ultrastructural features of well-preserved and injured sieve elements: Minute clamps keep the phloem transport conduits free for mass flow , 2000, Protoplasma.

[2]  M. V. Thompson.  Phloem: the long and the short of it. , 2006, Trends in plant science.

[3]  C. Windt,et al.  Effects of cold-girdling on flows in the transport phloem in Ricinus communis: is mass flow inhibited? , 2006, Plant, cell & environment.

[4]  E. Nikinmaa,et al.  Modeling xylem and phloem water flows in trees according to cohesion theory and Münch hypothesis , 2005, Trees.

[5]  Nick Gould,et al.  Direct measurements of sieve element hydrostatic pressure reveal strong regulation after pathway blockage. , 2004, Functional Plant Biology.

[6]  Y. Xia,et al.  A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging , 1997, Planta.

[7]  Shelagh M. Hall,et al.  Phloem transport in Ricinus: Its dependence on the water balance of the tissues , 1973, Planta.

[8]  Shelagh M. Hall,et al.  Phloem transport of 14C-labelled assimilates in Ricinus , 1971, Planta.

[9]  D. B. Fisher.  An evaluation of the Münch hypothesis for phloem transport in soybean , 2004, Planta.

[10]  M. R. Thorpe,et al.  Using the short-lived isotope 11C in mechanistic studies of photosynthate transport. , 2003, Functional plant biology : FPB.

[11]  N. Holbrook,et al.  Application of a single-solute non-steady-state phloem model to the study of long-distance assimilate transport. , 2003, Journal of theoretical biology.

[12]  A. Bel,et al.  The phloem, a miracle of ingenuity , 2003 .

[13]  Wolf B. Frommer,et al.  Phloem loading and unloading of sugars and amino acids , 2003 .

[14]  H. van As,et al.  Nuclear magnetic resonance imaging of membrane permeability changes in plants during osmotic stress , 2002 .

[15]  E. Nikinmaa,et al.  Time lags for xylem and stem diameter variations in a Scots pine tree , 2002 .

[16]  T. Scheenen,et al.  Functional imaging of plants: a nuclear magnetic resonance study of a cucumber plant. , 2002, Biophysical journal.

[17]  C. Offler,et al.  Role of membrane transport in phloem translocation of assimilates and water , 2001 .

[18]  W. Tanner,et al.  Transpiration, a prerequisite for long-distance transport of minerals in plants? , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[19]  T. Scheenen,et al.  Microscopic imaging of slow flow and diffusion: a pulsed field gradient stimulated echo sequence combined with turbo spin echo imaging. , 2001, Journal of magnetic resonance.

[20]  W. Köckenberger,et al.  Functional imaging of plants by magnetic resonance experiments. , 2001, Trends in plant science.

[21]  G Goldstein,et al.  Water transport in trees: current perspectives, new insights and some controversies. , 2001, Environmental and experimental botany.

[22]  Axel Haase,et al.  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 , 2001 .

[23]  A. V. van Bel,et al.  Reversible Calcium-Regulated Stopcocks in Legume Sieve Tubes , 2001, Plant Cell.

[24]  F. Vergeldt,et al.  Evaluation of algorithms for analysis of NMR relaxation decay curves. , 2000, Magnetic resonance imaging.

[25]  T. Scheenen,et al.  Quantification of water transport in plants with NMR imaging. , 2000, Journal of experimental botany.

[26]  E. Komor.  Source physiology and assimilate transport: the interaction of sucrose metabolism, starch storage and phloem export in source leaves and the effects on sugar status in phloem , 2000 .

[27]  T. Scheenen,et al.  Microscopic displacement imaging with pulsed field gradient turbo spin-echo NMR. , 2000, Journal of magnetic resonance.

[28]  E. Steudle,et al.  Water ascent in plants: do ongoing controversies have a sound basis? , 1999, Trends in plant science.

[29]  E. Komor,et al.  Assimilate export by leaves of Ricinus communis L. growing under normal and elevated carbon dioxide concentrations: the same rate during the day, a different rate at night , 1999, Planta.

[30]  A. D. Tomos,et al.  THE PRESSURE PROBE: A Versatile Tool in Plant Cell Physiology. , 1999, Annual review of plant physiology and plant molecular biology.

[31]  A Haase,et al.  Fast NMR flow measurements in plants using FLASH imaging. , 1999, Journal of magnetic resonance.

[32]  C. Grimmer.  Der Einfluß von erhöhten CO2- Konzentrationen auf den Export eines source-Blattes bei Ricinus communis L , 1999 .

[33]  B. Grodzinski,et al.  Estimating photosynthesis and concurrent export rates in C3 and C4 species at ambient and elevated CO21,2 , 1998, Plant physiology.

[34]  D. van Dusschoten,et al.  Quantitative T2 imaging of plant tissues by means of multi-echo MRI microscopy. , 1998, Magnetic resonance imaging.

[35]  Melvin T. Tyree,et al.  The Cohesion-Tension theory of sap ascent: current controversies , 1997 .

[36]  M. Tyree.  Review article. The cohesion-tension theory of sap ascent: current controversies , 1997 .

[37]  H. T. Edzes,et al.  Quantitative 1H-NMR imaging of water in white button mushrooms (Agaricus bisporus). , 1997, Magnetic resonance imaging.

[38]  S. Allen,et al.  Measurement of sap flow in plant stems , 1996 .

[39]  J. Pate,et al.  Effects of P deficiency on the uptake, flows and utilization of C, N and H2O within intact plants of Ricinus communis L. , 1996 .

[40]  P. Callaghan,et al.  Use of static and dynamic NMR microscopy to investigate the origins of contrast in images of biological tissues. , 1994, Biophysical chemistry.

[41]  A. Haase,et al.  Mechanisms of long-distance water transport in plants: a re-examination of some paradigms in the light of new evidence , 1993 .

[42]  W. Tanner,et al.  Does transpiration have an essential function in long-distance ion transport in plants ? , 1990 .

[43]  E. Steudle.  Methods for studying water relations of plant cells and tissues. , 1990 .

[44]  P. Callaghan,et al.  RAPID COMMUNICATION: NMR microscopy of dynamic displacements: k-space and q-space imaging , 1988 .

[45]  M. R. Thorpe,et al.  Measurement of Unloading and Reloading of Photo-assimilate within the Stem of Bean , 1987 .

[46]  S. Griffith,et al.  Sucrose Transport and Phloem Unloading in Stem of Vicia faba: Possible Involvement of a Sucrose Carrier and Osmotic Regulation. , 1986, Plant physiology.

[47]  J. Kallarackal,et al.  Phloem sap exudation in Ricinus communis: elastic responses and anatomical implications , 1985 .

[48]  P. Belton,et al.  NMR and compartmentation in biological tissues , 1985 .

[49]  J. Pate,et al.  Diurnal water balance of the cowpea fruit. , 1985, Plant physiology.

[50]  H. Van As,et al.  Noninvasive measurement of plant water flow by nuclear magnetic resonance. , 1984, Biophysical journal.

[51]  Jörg Kärger,et al.  The propagator representation of molecular transport in microporous crystallites , 1983 .

[52]  H. Ziegler.  Nature of Transported Substances , 1975 .

[53]  A. Ashford,et al.  Rapid Translocation in the Phloem of Wheat Roots , 1974 .

[54]  E. Macrobbie.  FACTS AND MECHANISMS: A COMPARATIVE SURVEY , 1971 .

[55]  C. E. Hartt.  Effect of Moisture Supply upon Translocation and Storage of C in Sugarcane. , 1967, Plant physiology.

[56]  D. Mortimer.  TRANSLOCATION OF THE PRODUCTS OF PHOTOSYNTHESIS IN SUGAR BEET PETIOLES , 1965 .

[57]  A. J. Peel,et al.  Studies in Sieve-tube Exudation through Aphid Mouth-parts: The Effects of Light and Girdling , 1962 .

[58]  E. Münch,et al.  Die stoffbewegungen in der Pflanze , 1931, Nature.

[59]  H. Dixon,et al.  Ascent of Sap , 1894, Nature.