Pathway of Phloem Unloading of Sucrose in Corn Roots

Giaquinta, Robert T.; Lin, Willy; Sadler, Nancy L.; Franceschi, Vincent R.

doi:10.1104/pp.72.2.362

Cited by 147 publications

(98 citation statements)

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“…Sadler, V.R. Franceschi [1983] Plant Physiol 72: 362-367), which grow apical to the end of the phloem and must build all biomass with carbon supplied from the shoot or kernel. We derived an expression for the growthsustaining Suc flux, which is the minimum longitudinal flux that would be required to meet the carbon demands of growth in the root apical meristem.…”

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Nonvascular, Symplasmic Diffusion of Sucrose Cannot Satisfy the Carbon Demands of Growth in the Primary Root Tip of Zea mays L

1994

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Nonvascular, symplasmic transport of sucrose (Suc) was investigated theoretically in the primary root tip of maize (Zea mays 1.cv WF9 x Mo 17) seedlings. Symplasmic diffusion has been assumed to be the mechanism of transport of Suc to cells in the root apical meristem (R.T. Ciaquinta, W. Lin, N.L. Sadler, V.R. Franceschi [1983] Plant Physiol 72: 362-367), which grow apical to the end of the phloem and must build all biomass with carbon supplied from the shoot or kernel. We derived an expression for the growthsustaining Suc flux, which is the minimum longitudinal flux that would be required to meet the carbon demands of growth in the root apical meristem. We calculated this flux from data on root growth velocity, area, and biomass density, taking into account construction and maintenance respiration and the production of mucilage by the root cap. We then calculated the conductivity of the symplasmic pathway for diffusion, from anatomical data on cellular dimensions and the frequency and dimensions of plasmodesmata, and from two estimates of the diffusive conductance of a plasmodesma, derived from independent data. Then, the concentration gradients required to drive a growth-sustaining Suc flux by diffusion alone were calculated but were found not to be physiologically reasonable. We also calculated the hydraulic conductivity of the plasmodesmatal pathway and found that mass flow of Suc solution through plasmodesmata would also be insufficient, by itself, to satisfy the carbon demands of growth. However, much of the demand for water to cause cell expansion could be met by the water unloaded from the phloem while unloading Suc to satisfy the carbon demands of growth, and the hydraulic conductivity of plasmodesmata is high enough that much of that water could move symplasmically. Either our current understanding of plasmodesmatal ultrastructure and function is flawed, or alternative transport mechanisms must exist for Suc transport to the meristem.Understanding the control of plant growth and development must include an understanding of the transport of photoassimilates from sources into developing sinks. Transport of solutes through the differentiated phloem is explained well by quantitative treatments of Miinch's (1930) pressure flow hypothesis (Christy and Femer, 1973;Tyree et al., 1974a;Ross and Tyree, 1980), and experimental data are in reasonably good agreement with their predictions (cf. Zimmermann and Brown, 1971; Pickard et al.,

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“…Work by Giaquinta et al (1983) and Dick and ap Rees (1975) indicated that transport of Suc in primary maize roots is entirely symplasmic. If so, the transport characteristics would be affected by the transport capacity of plasmodesmata.…”

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Nonvascular, Symplasmic Diffusion of Sucrose Cannot Satisfy the Carbon Demands of Growth in the Primary Root Tip of Zea mays L

1994

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“…The hydrolysis products of sucrose, fructose, and glucose, are also known to play key roles in carbohydrate movement in those plant species which employ sucrose hydrolysis between assimilate source and sink (4,8,9 , unpublished) showed that asymmetrically labeled sucrose is inverted during accumulation by isolated cotton embryos. The uptake of glucose and fructose and the effect of these sugars upon sucrose influx in cotton root and leaf discs was therefore investigated.…”

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“…The hydrolysis products of sucrose, fructose, and glucose, are also known to play key roles in carbohydrate movement in those plant species which employ sucrose hydrolysis between assimilate source and sink (4,8,9). Hampson et al (1 1, 12) analyzed carbohydrate accumulation by excised cotton hypocotyl and concluded that cellular invertase is functionally absent in this tissue.…”

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Sugar Uptake by Cotton Tissues

Hendrix¹

1984

Plant Physiol.

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The tissue accumulation of sucrose, glucose, and fructose has been studied in cultured cotton (Gossypium hirsutum L.) roots and leaf discs. Sucrose uptake by both tissues from high apoplastic concentrations was independent of pH but has a slightly acidic pH optimum from low concentrations. Like other higher plant tissues, cotton root cells accumulate sucrose via a 'saturable,' inhibitor-sensitive mechanism and a linear, inhibitor-resistant mechanism. The linear mechanism of sucrose uptake is not as pronounced in leaf disc data as it is in root data. Further, sucrose uptake by cotton leaf discs is more resistant than uptake by root cells to pH alterations, inhibitors, and monosaccharides in the uptake medium. The saturable phase of sucrose influx into cotton root is eliminated by glucose, fructose, and high pH. Sucrose influx into both tissues is not altered by osmotica up to 200 milliOsmolar. Sucrose accumulated by both tissues is rapidly converted to other chemical forms, especially in root tissue where only approximately 50% remains as neutral sugars 1 hour following the start of radiolabel exposure. Although the entry of radiolabeled sucrose is faster in abraded leaf discs, they give the same response patterns to pH, inhibitors, and monosaccharide as do unabraded discs.The sucrose accumulation kinetics of cotton roots and leaf discs differ. These differences may be related to the physiological roles (source versus sink) of the two tissues in the intact plant.Cell accumulation of sugar in cells from the apoplastic compartment is of major importance to short distance carbohydrate movement in plant tissues (5, 6). Sucrose accumulation in tissues isolated from several plant species seems to consist of a saturable component, most apparent at low sucrose levels, plus a nonsaturable component ( 17,18,21). Evidence for this interpretation of these kinetics stems from, among other things, the elimination of the saturable, but not the nonsaturable, component of sucrose uptake by inhibitors, particularly the organic mercurials. The specificity of the mercurials in blocking sucrose accumulation has been demonstrated by Giaquinta (6, 7) who found they caused a sharp decrease in sucrose influx but did not effect (at the concentrations employed) Beta leaf photosynthesis, sucrose efflux, respiration, or hexose uptake.The primary translocation product in cotton is thought to be sucrose (1 1). The hydrolysis products of sucrose, fructose, and glucose, are also known to play key roles in carbohydrate movement in those plant species which employ sucrose hydrolysis between assimilate source and sink (4,8,9 , unpublished) showed that asymmetrically labeled sucrose is inverted during accumulation by isolated cotton embryos. The uptake of glucose and fructose and the effect of these sugars upon sucrose influx in cotton root and leaf discs was therefore investigated.Since it is generally agreed that phloem capacity is not the limiting factor in photoassimilate movement between source and sink cells, cell uptake from the apopl...

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“…24). In expanding leaves (19,26), and roots (11), a symplastic pathway has been indicated. The pathway for phloem unloading and uptake of phloem solutes into expanding cells in the elongation zone of stems has not been well characterized.…”

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Coupling of Solute Transport and Cell Expansion in Pea Stems

Schmalstig

Cosgrove²

1990

Plant Physiol.

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Cells located in the elongation zone of stems and roots expand considerably before they are displaced from the growing zone, yet they exhibit little net dilution. For instance, in maize roots the cell sap osmotic pressure is uniform throughout the growth zone (22) and in pea epicotyls there is only a slight decrease (from 9.2-8.3 bar) in the growing region (4). Thus, the rate of unloading from the phloem (a major source of osmoticum in these tissues) appears to be closely coordinated with the local expansion rate.In contrast to the observations on intact plants, excised segments often exhibit considerable dilution during growth (23). Likewise in seedlings from which cotyledons were excised, growth resulted in dilution ofthe cell sap (18). Evidently the usual coupling between expansion and solute uptake can be broken, and cell expansion can still take place despite reduction or blockage of normal solute import.The nature of the coupling between cell expansion and import of phloem solutes depends on the pathway and the mechanism of exit of solutes from the phloem and entry into expanding cells. A pathway through the apoplast is indicated in mature stems (12) and roots (27) Every 20 min after addition, 10 ,uL of distilled water was spread over the cotyledon surfaces to keep the L-glucose solution wet. Fluorescein as the sodium salt was added as a 1.0% solution in a 1.5% agar block (5 x 5 x 2 mm) to the cotyledon surfaces cut as for L-glucose addition. All transport experiments were done in a box kept at 100% RH to reduce transpiration.After 1 h for sucrose and 2 h for other compounds, the epicotyl was cut into sections consisting of the plumule and hook and pieces from 4 to 60 mm ( Fig. 1)

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Pathway of Phloem Unloading of Sucrose in Corn Roots

Cited by 147 publications

References 11 publications

Nonvascular, Symplasmic Diffusion of Sucrose Cannot Satisfy the Carbon Demands of Growth in the Primary Root Tip of Zea mays L

Nonvascular, Symplasmic Diffusion of Sucrose Cannot Satisfy the Carbon Demands of Growth in the Primary Root Tip of Zea mays L

Sugar Uptake by Cotton Tissues

Coupling of Solute Transport and Cell Expansion in Pea Stems

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