TY - JOUR

T1 - The novel chloroplast glucose transporter pGlcT2 affects adaptation to extended light periods

AU - Valifard, Marzieh

AU - Fernie, Alisdair R.

AU - Kitashova, Anastasia

AU - Nägele, Thomas

AU - Schröder, Rebekka

AU - Meinert, Melissa

AU - Pommerrenig, Benjamin

AU - Mehner-Breitfeld, Denise

AU - Witte, Claus Peter

AU - Brüser, Thomas

AU - Keller, Isabel

AU - Neuhaus, H. Ekkehard

N1 - Funding Information: We are grateful to Katja Bettenbrock for donation of her E. coli ptsG/manXYZ mutant strain. The authors would also like to thank Ruth Wartenberg (Plant Physiology, University of Kaiserslautern) for excellent technical assistance and analysis of promoter-pGlcT2-GUS plants. We also thank Sibylle Traupe and Inge Reupke (Microbiology, Leibniz University Hannover) for excellent technical assistance. M. V. B. P. C-P. W. T. B. I. K. H. E. N. Conceptualization; M. V. A. R. F. A. K. T. N. R. S. M. M. B. P. D. M-B, C-P. W. T. B. I. K. Investigation; M. V. I. K. Visualization; A. R. F. T. N. T. B. H. E. N. Funding acquisition; A. R. F. T. N. B. P. H. E. N. Writing - Review & Editing. Funding Information: This work was financially supported by the Deutsche Forschungsgemeinschaft (DFG) within the Collaborative Research Center 175, The Green Hub, Projects B03, B04 and D03 to H. E. N., A. F. and T. N., respectively. Further support was provided by a grant of the Alexander von Humboldt Foundation to M. V., the German Federal State Lower Saxony to T. B. and by the German Federal State Rhineland Palatinate (Program BioComp) to H. E. N.

PY - 2023/6

Y1 - 2023/6

N2 - Intracellular sugar compartmentation is critical in plant development and acclimation to challenging environmental conditions. Sugar transport proteins are present in plasma membranes and in membranes of organelles such as vacuoles, the Golgi apparatus, and plastids. However, there may exist other transport proteins with uncharacterized roles in sugar compartmentation. Here we report one such novel transporter of the Monosaccharide Transporter Family, the closest phylogenetic homolog of which is the chloroplast-localized glucose transporter pGlcT and that we therefore term plastidic glucose transporter 2 (pGlcT2). We show, using gene-complemented glucose uptake deficiency of an Escherichia coli ptsG/manXYZ mutant strain and biochemical characterization, that this protein specifically facilitates glucose transport, whereas other sugars do not serve as substrates. In addition, we demonstrate pGlcT2-GFP localized to the chloroplast envelope and that pGlcT2 is mainly produced in seedlings and in the rosette center of mature Arabidopsis plants. Therefore, in conjunction with molecular and metabolic data, we propose pGlcT2 acts as a glucose importer that can limit cytosolic glucose availability in developing pGlcT2-overexpressing seedlings. Finally, we show both overexpression and deletion of pGlcT2 resulted in impaired growth efficiency under long day and continuous light conditions, suggesting pGlcT2 contributes to a release of glucose derived from starch mobilization late in the light phase. Together, these data indicate the facilitator pGlcT2 changes the direction in which it transports glucose during plant development and suggest the activity of pGlcT2 must be controlled spatially and temporarily in order to prevent developmental defects during adaptation to periods of extended light.

AB - Intracellular sugar compartmentation is critical in plant development and acclimation to challenging environmental conditions. Sugar transport proteins are present in plasma membranes and in membranes of organelles such as vacuoles, the Golgi apparatus, and plastids. However, there may exist other transport proteins with uncharacterized roles in sugar compartmentation. Here we report one such novel transporter of the Monosaccharide Transporter Family, the closest phylogenetic homolog of which is the chloroplast-localized glucose transporter pGlcT and that we therefore term plastidic glucose transporter 2 (pGlcT2). We show, using gene-complemented glucose uptake deficiency of an Escherichia coli ptsG/manXYZ mutant strain and biochemical characterization, that this protein specifically facilitates glucose transport, whereas other sugars do not serve as substrates. In addition, we demonstrate pGlcT2-GFP localized to the chloroplast envelope and that pGlcT2 is mainly produced in seedlings and in the rosette center of mature Arabidopsis plants. Therefore, in conjunction with molecular and metabolic data, we propose pGlcT2 acts as a glucose importer that can limit cytosolic glucose availability in developing pGlcT2-overexpressing seedlings. Finally, we show both overexpression and deletion of pGlcT2 resulted in impaired growth efficiency under long day and continuous light conditions, suggesting pGlcT2 contributes to a release of glucose derived from starch mobilization late in the light phase. Together, these data indicate the facilitator pGlcT2 changes the direction in which it transports glucose during plant development and suggest the activity of pGlcT2 must be controlled spatially and temporarily in order to prevent developmental defects during adaptation to periods of extended light.

KW - Arabidopsis thaliana

KW - chloroplast

KW - glucose transport

KW - membrane protein

KW - photosynthesis

UR - http://www.scopus.com/inward/record.url?scp=85160006647&partnerID=8YFLogxK

U2 - 10.1016/j.jbc.2023.104741

DO - 10.1016/j.jbc.2023.104741

M3 - Article

C2 - 37088133

AN - SCOPUS:85160006647

VL - 299

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 6

M1 - 104741

ER -