Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport

Carnegie Institution for Science, 260 Panama Street, Stanford, CA 94305, USA.
Science (Impact Factor: 33.61). 12/2011; 335(6065):207-11. DOI: 10.1126/science.1213351
Source: PubMed


Plants transport fixed carbon predominantly as sucrose, which is produced in mesophyll cells and imported into phloem cells
for translocation throughout the plant. It is not known how sucrose migrates from sites of synthesis in the mesophyll to the
phloem, or which cells mediate efflux into the apoplasm as a prerequisite for phloem loading by the SUT sucrose–H+ (proton) cotransporters. Using optical sucrose sensors, we identified a subfamily of SWEET sucrose efflux transporters. AtSWEET11
and 12 localize to the plasma membrane of the phloem. Mutant plants carrying insertions in AtSWEET11 and 12 are defective in phloem loading, thus revealing a two-step mechanism of SWEET-mediated export from parenchyma cells feeding
H+-coupled import into the sieve element–companion cell complex. We discuss how restriction of intercellular transport to the
interface of adjacent phloem cells may be an effective mechanism to limit the availability of photosynthetic carbon in the
leaf apoplasm in order to prevent pathogen infections.

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    • "ion triggers MTI in the host . Detailed comparisons between mock , DC3000hrpA - , and DC3000 treatments capture gene expression associated with MTI , effector - mediated suppression of MTI , and subsequent transcriptional changes associated with metabolic reconfigurations that favor pathogen nutrition , e . g . , deployment of SWEET transporters ( Chen et al . , 2010 , 2012 ) ."
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    ABSTRACT: Transcriptional reprogramming is integral to effective plant defense. Pathogen effectors act transcriptionally and posttranscriptionally to suppress defense responses. A major challenge to understanding disease and defense responses is discriminating between transcriptional reprogramming associated with microbial-associated molecular pattern (MAMP)-triggered immunity (MTI) and that orchestrated by effectors. A high-resolution time course of genome-wide expression changes following challenge with Pseudomonas syringae pv tomato DC3000 and the nonpathogenic mutant strain DC3000hrpA- allowed us to establish causal links between the activities of pathogen effectors and suppression of MTI and infer with high confidence a range of processes specifically targeted by effectors. Analysis of this information-rich data set with a range of computational tools provided insights into the earliest transcriptional events triggered by effector delivery, regulatory mechanisms recruited, and biological processes targeted. We show that the majority of genes contributing to disease or defense are induced within 6 h postinfection, significantly before pathogen multiplication. Suppression of chloroplast-associated genes is a rapid MAMP-triggered defense response, and suppression of genes involved in chromatin assembly and induction of ubiquitin-related genes coincide with pathogen-induced abscisic acid accumulation. Specific combinations of promoter motifs are engaged in fine-tuning the MTI response and active transcriptional suppression at specific promoter configurations by P. syringae.
    Preview · Article · Nov 2015 · The Plant Cell
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    • "Suc generated in mesophyll cells moves cell to cell, presumably via plasmodesmata, to enter the vascular bundle (Giaquinta, 1983). Efflux to the apoplasm occurs from phloem parenchyma cells through the SWEET transporters AtSWEET11 and AtSWEET12 (Chen et al., 2012). From the apoplasmic space, Suc is then actively accumulated into the CC-SE complex by Suc transporter/carrier proteins (SUTs or SUCs) energized by the proton motive force (pmf; Lalonde et al., 2004; Ayre, 2011). "
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    ABSTRACT: Plant productivity is determined in large part by the partitioning of assimilates between the sites of production and the sites of utilization. Proton-pumping pyrophosphatases (H+-PPases) are shown to participate in many energetic plant processes including general growth and biomass accumulation, CO2 fixation, nutrient acquisition, and stress responses. H+-PPases have a well-documented role in hydrolyzing pyrophosphate (PPi) and capturing the released energy to pump protons (H+) across the tonoplast and endomembranes to create proton motive force (pmf). Recently, an additional role for H+-PPases in phloem loading and biomass partitioning was proposed. In companion cells of the phloem, H+-PPases localize to the plasma membrane rather than endomembranes, and rather than hydrolyzing PPi to create pmf, pmf is utilized to synthesize PPi. Additional PPi in the companion cells promotes Suc oxidation and ATP synthesis, which the plasma membrane P-type ATPase in turn uses to create more pmf for phloem loading of sucrose via sucrose-H+ symporters (SUTs). To test this model, transgenic Arabidopsis thaliana plants were generated with constitutive and companion cell-specific overexpression of AVP1, encoding Type-1 Arabidopsis Vacuolar Pyrophosphatase-1. Plants with both constitutive and companion cell specific-overexpression accumulated more biomass in shoot and root systems. 14C-labelling experiments showed enhanced photosynthesis, phloem loading, phloem transport, and delivery to sink organs. These results support the model for an alternative H+-PPases function in the phloem by arguing that the increases in biomass observed with AVP1 overexpression stem from improved phloem loading and transport.
    Full-text · Article · Nov 2015 · Plant physiology
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    • "The atsweet11 or atsweet12 single mutants exhibit no aberrant phenotypes, possibly due to genetic redundancy. However, atsweet11;12 double mutants are mildly chlorotic and display slower growth and higher levels of starch and sugar accumulation in the leaves than do wild-type plants (Chen et al., 2012). Arabidopsis phloem-specific sucrose transporter (AtSUC2) is a phloem-specific SUT that is expressed specifically in companion cells (Stadler and Sauer, 1996). "
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    ABSTRACT: Yield in cereals is a function of grain number and size. Suc, the main carbohydrate product of photosynthesis in higher plants, is transported long distances from source leaves to sink organs such as seeds and roots. Here, we report that transgenic rice plants expressing the Arabidopsis phloem-specific sucrose transporter AtSUC2, which loads Suc into the phloem, showed an increase in grain yield of up to 16% relative to wild-type plants in field trials. Compared to wild-type plants, pPP2::AtSUC2 plants had larger spikelet hulls and larger and heavier grains. Grain filling was accelerated in the transgenic plants, and more photoassimilate was transported from the leaves to the grain. In addition, microarray analyses revealed that carbohydrate, amino acid, and lipid metabolism was enhanced in the leaves and grain of pPP2::AtSUC2 plants. Thus, enhancing sucrose loading represents a promising strategy to improve rice yield to feed the global population.
    Full-text · Article · Oct 2015 · Plant physiology
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