The Evidence for Symplastic Phloem Loading

Turgeon, Robert; Beebe, Dwight U.

doi:10.1104/pp.96.2.349

Cited by 67 publications

(38 citation statements)

References 33 publications

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“…However, downregulation of SUT1 did not appreciably modify the V. phoeniceum vein images, except in the most severely downregulated line, and then not consistently. These results are similar to those in which sucrose transporter activity in RFO-transporting plants is inhibited with PCMBS (19). Apparently, when sucrose transporter activity is blocked, [ 14 C]sucrose enters the tissue by the non-saturable, PCMBSinsensitive uptake mechanism (36,37) and is then sequestered in the veins by diffusion through plasmodesmata and polymer trapping in the intermediary cells (34).…”

Section: Discussionsupporting

confidence: 77%

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Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading

Zhang

Turgeon

2009

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

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Sucrose is loaded into the phloem in the minor veins of leaves before export. Two active, species-specific loading mechanisms have been proposed. One involves transporter-mediated sucrose transfer from the apoplast into the sieve element-companion cell complex, so-called apoplastic loading. In the putative second mechanism, sucrose follows an entirely symplastic pathway, and the solute concentration is elevated by the synthesis of raffinose and stachyose in the phloem, not by transporter activity. Several sucrosetransporting plants have been shown to be apoplastic loaders by downregulating sucrose transporter 1 (SUT1), leading to accumulation of sugars and leaf chlorosis. In this study we compared the effect of downregulating SUT1 in Nicotiana tabacum, a sucrose transporter, and Verbascum phoeniceum, a species that transports raffinose and stachyose. To test the effectiveness of RNAi downregulation, we measured SUT1 mRNA levels and sucrose-H ؉ symport in leaf discs. Mild NtSUT1 downregulation in N. tabacum resulted in the pronounced phenotype associated with loading inhibition. In contrast, no such phenotype developed when VpSUT1 was downregulated in V. phoeniceum, leaving minimal sucrose transport activity. Only those plants with the most severe VpSUT1 downregulation accumulated more carbohydrate than usual and these plants were normal by other criteria: growth rate, photosynthesis, and ability to clear starch during the night. The results provide direct evidence that the mechanism of phloem loading in V. phoeniceum does not require active sucrose uptake from the apoplast and strongly supports the conclusion that the loading pathway is symplastic in this species.plasmodesmata ͉ raffinose ͉ stachyose P hloem loading provides the driving force for long-distance transport from leaves to sink organs in many plants by elevating the carbohydrate content and hydrostatic pressure in the sieve elements (SE) and companion cells (CC) of minor veins (1-3). In a large number of species, phloem loading is mediated by transporters on the plasma membranes of the SEs and CCs. These transporters drive sucrose, and in some cases sugar alcohol, from the apoplast into the SE-CC complex. The most direct proof of apoplastic loading has come from studies in which sucrose transporter 1 (SUT1/SUC2) is downregulated by antisense technology or DNA insertion (4-9). Such downregulation inhibits phloem loading and results in accumulation of sugars and starch, stunted growth, diminished photosynthesis, and leaf chlorosis. These experiments confirm the necessity of transmembrane transport of sucrose in these species and the indispensable role of SUT1 in apoplastic phloem loading.In species that load from the apoplast, relatively few plasmodesmata connect the SE-CC complex to surrounding cells (10,11). This is unsurprising given that extensive symplastic continuity would create a futile cycle of active loading from the apoplast and passive leakage back to mesophyll cells. However, in many other species plasmodesmata in the minor veins are numer...

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Section: Discussionsupporting

confidence: 77%

“…A ''polymer trap'' mechanism (18)(19)(20) has been proposed to explain how sucrose is loaded through plasmodesmata in RFO plants. According to this model, sucrose diffuses through plasmodesmata from mesophyll cells to intermediary cells, where it is converted into RFOs.…”

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confidence: 99%

Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading

Zhang

Turgeon

2009

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

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“…Physiological studies have indicated that an apoplastic loading step may not be required for delivery of assimilates to the phloem of stachyose-translocating plants (8,17,19,20). The present models, therefore, conjecture that synthesis of the raffinose oligosaccharides may take place within the intermediary cells from mesophyll-derived galactinol and sucrose.…”

Section: Introductionmentioning

confidence: 69%

“…The present models, therefore, conjecture that synthesis of the raffinose oligosaccharides may take place within the intermediary cells from mesophyll-derived galactinol and sucrose. These precursors are thought to be delivered to the intermediary cells via the abundant plasmodesmata that interconnect these cells and the mesophyll (19,20). If these models prove to be correct, then an additional spatial component will have been added to the carbon-partitioning story that probably does not exist for sucrose-translocating species.…”

Section: Introductionmentioning

confidence: 99%

Patterns of Assimilate Production and Translocation in Muskmelon (Cucumis melo L.)

Mitchell

Gadus²,

Madore³

1992

Plant Physiol.

119

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Continuous monitoring of steady-state carbon dioxide exchange rates in mature muskmelon (Cucumis melo L.) leaves showed diurnal patterns of photosynthesis and respiration that were translated into distinct patterns of accumulation and phloem export of soluble sugars and amino acids. Leaf soluble sugar patterns in general followed the pattern of photosynthetic activity observed in the leaf, whereas starch accumulated steadily throughout the light period. Sugar and starch levels declined through the dark phase. Phloem exudate analysis revealed that diurnal levels of the major transport sugars (stachyose and sucrose) in the phloem did not appear to correlate directly with the photosynthetic activity of the leaf but instead were inversely correlated with leaf starch accumulation and degradation. The amino acid pool in leaf tissues remained constant throughout the diurnal period; however, the relative contribution of individual amino acids to the total pool varied with the diurnal photosynthetic and respiratory activity of the leaf. In contrast, the phloem sap amino acid pool size was substantially larger in the light than in the dark, a result primarily due to enhanced export of glutamine, glutamate, and citrulline during the light period. The results indicate that the sugar and amino acid composition of cucurbit phloem sap is not constant but varies throughout the diurnal cycle in response to the metabolic activities of the source leaf.Rates of assimilate production in source leaves are determined both by biochemical regulation of key biosynthetic and degradative enzymes and by regulation of compartmentalization events that distribute assimilates between storage (chloroplast, vacuole) and transport (phloem) compartments (3,22). Export of photosynthetically fixed carbon from a source leaf is, therefore, dependent on the functioning of many complex metabolic events that control the production of phloem-mobile assimilates such as sucrose and delivery of these solutes to the phloem (3,6,18). In some plants, a direct correlation can be found between sucrose levels in the leaf and the rate of carbon export from the leaf, suggesting that the rate of phloem transport is controlled directly by the rate of sucrose synthesis (3,6,18 levels have no correlation with rates of export, suggesting possibly that it may not be the synthesis of sucrose but rather its delivery to the phloem system that is important in determining export rates (3,22). This may indicate a role for vacuolar transport processes in the control of export (3).At present, virtually all of our current information concerning biochemical regulation of carbon partitioning comes from plants that translocate sucrose exclusively (18). Recently, a renewed interest has been shown in carbon partitioning in those species that, in addition to sucrose, also synthesize and export the raffinose oligosaccharide, stachyose. The biochemistry of carbon partitioning between phloem-mobile and storage metabolites is far more complicated in these plants because of the additi...

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“…Immunological and physiological evidence obtained for cucurbit leaves now indicates that stachyose may be synthesized within the minor vein phloem from mesophyll-derived precursors (5). Current structural and physiological evidence also suggests that the delivery of these precursors may follow a symplastic pathway (5,15,18,19). In cucurbits, therefore, the effects of chilling on carbon partitioning within leaf tissues may be even more complex than is currently understood for sucrose-translocating species, in light of the importance of calcium balance in the control of solute movement through plasmodesmata (14).…”

mentioning

confidence: 99%

Patterns of Assimilate Production and Translocation in Muskmelon (Cucumis melo L.)

Mitchell¹,

Madore²

1992

Plant Physiol.

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The Evidence for Symplastic Phloem Loading

Cited by 67 publications

References 33 publications

Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading

Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading

Patterns of Assimilate Production and Translocation in Muskmelon (Cucumis melo L.)

Patterns of Assimilate Production and Translocation in Muskmelon (Cucumis melo L.)

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