A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging

Köckenberger, Walter; Pope, James Gray; Xia, Yang; Jeffrey, Kenneth R.; Komor, Ewald; Callaghan, Paul T.

doi:10.1007/bf01258680

Cited by 152 publications

(106 citation statements)

References 33 publications

(37 reference statements)

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“…Wider and shorter tubes (relays) will promote faster propagation of pressure and concentration waves, faster propagation of hormonal signals and decrease the turgor pressure differences along the phloem in both of the phloem construction scenarios. The actual flow velocities that have been measured in intact plants fall somewhere between 0.2 to 0.5 mm/s (0.7 -2 m/hour) (Köckenberger, 1997;Peuke et al, 2001;Windt et al, 2006). The flow velocity predicted by our model in the base case (Fig.…”

Section: Different Phloem Construction Criteriamentioning

confidence: 71%

Linking phloem function to structure: Analysis with a coupled xylem–phloem transport model

Hölttä

Mencuccini

Nikinmaa

2009

Journal of Theoretical Biology

199

188

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Cite this article as: T. Hölttä, M. Mencuccini and E. Nikinmaa, Linking phloem function to structure: Analysis with a coupled xylem-phloem transport model, Journal of Theoretical Biology (2009Biology ( ), doi:10.1016Biology ( /j.jtbi.2009 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. We carried out a theoretical analysis of phloem transport based on Münch hypothesis by developing a coupled xylem-phloem transport model. Results showed that the maximum sugar transport rate of the phloem was limited by solution viscosity and that transport requirements were strongly affected by prevailing xylem water potential. The minimum number of xylem and phloem conduits required to sustain transpiration and assimilation, respectively, were calculated. At its maximum sugar transport rate, the phloem functioned with a high turgor pressure difference between the sugar sources and sinks but the turgor pressure difference was reduced if additional parallel conduits were added or solute relays were introduced. Solute relays were shown to decrease the number of parallel sieve tubes needed for phloem transport, leading to a more uniform turgor pressure and allowing faster information transmission within the phloem. Because xylem water potential affected both xylem and phloem transport, the conductance of the two systems was found to be coupled such that large structural investments in the xylem reduced the need for investment in the phloem and vice versa.

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Section: Different Phloem Construction Criteriamentioning

confidence: 71%

Linking phloem function to structure: Analysis with a coupled xylem–phloem transport model

Hölttä

Mencuccini

Nikinmaa

2009

Journal of Theoretical Biology

199

188

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“…5A. The lower osmotic pressure differences, which could be the result of a lowered rate of photosynthesis, would require higher P os values to move water cell-to-cell and support the high rate of xylem to phloem recycling that occurs in plants (38). Rehydratating a partially dehydrated plant may be speeded up if the P os of the cell membranes is higher.…”

Section: Discussionmentioning

confidence: 99%

The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells

Morillón

Chrispeels

2001

Proc. Natl. Acad. Sci. U.S.A.

141

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The transpiration stream that passes through a plant may follow an apoplastic route, with low resistance to flow, or a cell-to-cell route, in which cellular membranes impede water flow. However, passage of water through membranes can be facilitated by aquaporins thereby decreasing resistance. We investigated the relationship between transpiration, which can be down-regulated by abscisic acid (ABA) or by high humidity, and the osmotic water permeability (P os) of protoplasts. By using leaf protoplasts of wild-type (wt) Arabidopsis thaliana plants and of mutants that are low in ABA (aba1) or insensitive to ABA (abi1 and abi2), we found that protoplasts from aba1 and abi mutants have very low P os values compared with those from wt plants when the plants are grown at 45% relative humidity. High values of P os were found 3 h after the addition of ABA to the culture medium of aba1 plants; addition of ABA to abi plants did not restore the P os to wt levels. There was no such increase in P os when excised leaves of aba1 plants were treated with ABA. When the transpiration stream was attenuated by growing the plants at 85% relative humidity, the P os of protoplasts from all plants (wt and mutants) was higher. We suggest that attenuation of the transpiration stream in whole plants is required for the up-regulation of the P os of the membranes, and that this up-regulation, which does not require ABA, is mediated by the activation of aquaporins in the plasma membrane. P lant growth requires a tradeoff between the need to acquire CO 2 for photosynthesis and the need to minimize water loss from the leaves. Water lost through the transpiration stream is replaced by water that is taken up from the soil. The force that drives this water uptake is the tension created by the evaporation of water from the leaf cells. Water that moves through living tissues can follow an apoplastic or cell-to-cell path. Careful measurements of the hydraulic properties of plant tissues and organs show that the relative contribution of each pathway to overall hydraulic conductivity may change substantially depending on the intensity of water flow and other factors (1). When the rate of water flow is high (open stomates, low relative humidity), water flows along the apoplast and around the protoplasts because the apoplastic path has the lower hydraulic resistance. Conversely, when the rate of water flow is small, a larger proportion of water follows the cell-to-cell path and needs to pass through cellular membranes (and possibly through plasmodesmata). Water flow along this path has a much higher hydraulic resistance and can be modulated by aquaporins, proteins that facilitate transmembrane water transport (2-4). An important unanswered question is whether the magnitude of flow in the apoplastic path affects the resistance in the cell-to-cell path.In plants, aquaporins form a family of 35-37 sequence-related proteins (5, 6) that transport water and neutral solutes, such as glycerol, across membranes. Aquaporins have been found in the tonoplast (vacuol...

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“…NMR flow imaging does not only give information about the average flow velocity, such as heat pulse based methods do, but gives access to all properties of the flowing water, such as the flow conducting area, the distribution of flow velocities, and the volume flow, all on a per pixel basis (Scheenen et al, 2000b). So far, studies have been conducted measuring flow in the stem of a variety of plants, ranging from castor bean seedlings (Kö ckenberger et al, 1997) to fully developed tomato, castor bean, and tobacco (Nicotiana tabacum) plants, and a small poplar tree (Populus spp. ; Windt et al, 2006).…”

Section: Nmr Flow Imagingmentioning

confidence: 99%

Most Water in the Tomato Truss Is Imported through the Xylem, Not the Phloem: A Nuclear Magnetic Resonance Flow Imaging Study

2009

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In this study, we demonstrate nuclear magnetic resonance flow imaging of xylem and phloem transport toward a developing tomato (Solanum lycopersicum) truss. During an 8-week period of growth, we measured phloem and xylem fluxes in the truss stalk, aiming to distinguish the contributions of the two transport tissues and draw up a balance between influx and efflux. It is commonly estimated that about 90% of the water reaches the fruit by the phloem and the remaining 10% by the xylem. The xylem is thought to become dysfunctional at an early stage of fruit development. However, our results do not corroborate these findings. On the contrary, we found that xylem transport into the truss remained functional throughout the 8 weeks of growth. During that time, at least 75% of the net influx into the fruit occurred through the external xylem and about 25% via the perimedullary region, which contains both phloem and xylem. About one-half of the net influx was lost due to evaporation. Halfway through truss development, a xylem backflow appeared. As the truss matured, the percentage of xylem water that circulated into the truss and out again increased in comparison with the net uptake, but no net loss of water from the truss was observed. The circulation of xylem water continued even after the fruits and pedicels were removed. This indicates that neither of them was involved in generating or conducting the circulation of sap. Only when the main axis of the peduncle was cut back did the circulation stop.

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A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging

Cited by 152 publications

References 33 publications

Linking phloem function to structure: Analysis with a coupled xylem–phloem transport model

Linking phloem function to structure: Analysis with a coupled xylem–phloem transport model

The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells

Most Water in the Tomato Truss Is Imported through the Xylem, Not the Phloem: A Nuclear Magnetic Resonance Flow Imaging Study

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