SUT2, a Putative Sucrose Sensor in Sieve Elements

Abstract

In leaves, sucrose uptake kinetics involve high-and low-affinity components. A family of low-and high-affinity sucrose transporters (SUT) was identified. SUT1 serves as a high-affinity transporter essential for phloem loading and long-distance transport in solanaceous species. SUT4 is a low-affinity transporter with an expression pattern overlapping that of SUT1. Both SUT1 and SUT4 localize to enucleate sieve elements of tomato. New sucrose transporter-like proteins, named SUT2, from tomato and Arabidopsis contain extended cytoplasmic domains, thus structurally resembling the yeast sugar sensors SNF3 and RGT2. Features common to these sensors are low codon bias, environment of the start codon, low expression, and lack of detectable transport activity. In contrast to LeSUT1 , which is induced during the sink-to-source transition of leaves, SUT2 is more highly expressed in sink than in source leaves and is inducible by sucrose. LeSUT2 protein colocalizes with the low-and high-affinity sucrose transporters in sieve elements of tomato petioles, indicating that multiple SUT mRNAs or proteins travel from companion cells to enucleate sieve elements. The SUT2 gene maps on chromosome V of potato and is linked to a major quantitative trait locus for tuber starch content and yield. Thus, the putative sugar sensor identified colocalizes with two other sucrose transporters, differs from them in kinetic properties, and potentially regulates the relative activity of low-and high-affinity sucrose transport into sieve elements. INTRODUCTIONSucrose, the major product of photosynthesis in mature leaves, is loaded into the vascular tissue for translocation to heterotrophic tissues to support their growth. In solanaceous plants, SUT1 is essential for phloem loading into sieve elements (Riesmeier et al., 1994;Kühn et al., 1996;Bürkle et al., 1998). SUT1 serves as a high-affinity transporter for sucrose ( K m ‫ف‬ 1 mM; Riesmeier et al., 1993), whereas SUT4, with a K m of ‫ف‬ 11 mM, is a low-affinity sucrose transporter (Weise et al., 2000). Both proteins colocalize in sieve elements (Kühn et al., 1997;Weise et al., 2000). Localization of SUT1 protein in sieve elements and SUT1 mRNA at the orifices of plasmodesmata interconnecting companion cells and sieve elements, together with the high turnover of both SUT1 mRNA and protein, indicate that trafficking of mRNA or protein occurs from companion cells into enucleate sieve elements by way of plasmodesmata (Kühn et al., 1997).Sugar transport is highly regulated, and sucrose-specific signaling pathways are involved in controlling transport activity (Chiou and Bush, 1998), potentially by using protein phosphorylation (Roblin et al., 1998). Overexpression of pyruvate decarboxylase in potato leads to a 10-fold increase in sugar export, demonstrating the capacity to regulate sugar export from leaves within a wide dynamic range (Tadege et al., 1998). This poses the question of how regulation is coordinated between sieve elements that contain the transporters and companion cells in which transcri...

Untitled

“…The expression pattern of the high affinity AtSUC2 [4] and the low affinity AtSUT4 [10], and the putative sucrose sensor AtSUT2 [11] overlaps in minor veins of leaves of mature plants (Fig. 1A).…”

“…To confirm the targeting of the NubG-fusion proteins to the plasma membrane and to show their functionality, NubG-AtSUC2 and NubG-AtSUT4 were tested for their ability to complement growth of the yeast strain SUSY7/ura3 on sucrose [11,30]. In both cases, the N-terminal fusion of NubG to the sucrose transporters did not impair their transport function, as demonstrated by the growth of SUSY7/ura3 containing the respective fusion proteins on sucrose as the sole carbon source (Fig.…”

“…Considering the hypothesized function of AtSUT2 as a sucrose sensor [11], one can envisage a model in which a putative sucrose sensor can directly modulate the transport activity of an interacting sucrose transporter through cooperative effects. It became obvious from analyses in yeast, that certain micro-environments of the plasma membrane, the so called lipid rafts, can change in composition due to intra- or extracellular stimuli [43], which in turn may favor certain protein-protein interactions resulting in the activation of signaling cascades or transport processes.…”

“…Functionality of the sucrose transporter-NubG-fusions was tested using yeast strain SUSY7/ura3 [11,30] transformed with plasmids bearing respective fusion constructs. To test for growth on sucrose, three colonies from each transformation were resuspended in 5 mL water and 50 μL aliquots were plated both on yeast minimal medium supplemented with tryptophan and either glucose (2%), or sucrose (2%, pH 4).…”

“…In contrast, AtSUT4 serves as a low affinity transporter and is potentially involved in phloem loading in minor veins [10]. SUT2 was characterized as weak low affinity transporter, and based on circumstantial evidence it has been speculated that SUT2 may be a candidate for a postulated sucrose sensor fulfilling similar functions as the yeast sugar sensors SNF3 and RGT2 [11]. The other Arabidopsis genes are highly related to SUC1 and SUC2, indicating recent gene amplification events, but function of these genes is still not defined.…”