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Beet taproot plasma membrane sugar transport revisited

View ORCID ProfileAntonella Reyer, View ORCID ProfileNadia Bazihizina, Justyna Jaślan, View ORCID ProfileSönke Scherzer, View ORCID ProfileNadine Schäfer, View ORCID ProfileDawid Jaślan, Dirk Becker, View ORCID ProfileThomas D. Müller, View ORCID ProfileBenjamin Pommerrenig, H. Ekkehard Neuhaus, View ORCID ProfileIrene Marten, View ORCID ProfileRainer Hedrich
doi: https://doi.org/10.1101/2021.09.21.461191
Antonella Reyer
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Nadia Bazihizina
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
2Department of Agrifood Production and Environmental Sciences, Università degli Studi di Firenze, Viale delle Idee 30, 50019 Sesto Fiorentino, Florence, Italy
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Justyna Jaślan
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Sönke Scherzer
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Nadine Schäfer
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Dawid Jaślan
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
3Walther Straub Institute of Pharmacology and Toxicology, Faculty of Medicine, Ludwig Maximilians-Universität, 80336 Munich, Germany
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Dirk Becker
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Thomas D. Müller
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Benjamin Pommerrenig
4Plant Physiology, University of Kaiserslautern, 67663 Kaiserslautern, Germany
5Institute for Resistance Research and Stress Tolerance at the Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Tolerance, 06484 Quedlinburg, Germany
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H. Ekkehard Neuhaus
4Plant Physiology, University of Kaiserslautern, 67663 Kaiserslautern, Germany
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Irene Marten
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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Rainer Hedrich
1Julius-Maximilians-Universität (JMU), Biocenter, Department of Molecular Plant Physiology and Biophysics, D-97082 WuCrzburg, Germany
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  • For correspondence: rainer.hedrich@uni-wuerzburg.de
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SUMMARY

Sugar beet (Beta vulgaris) is the major sugar-producing crop in Europe and Northern America, as the taproot stores sucrose at a concentration of around 20%. Genome sequence analysis together with biochemical and electrophysiological approaches led to the identification and characterization of the TST sucrose transporter driving vacuolar sugar accumulation in the taproot. However, the sugar transporters mediating sucrose uptake across the plasma membrane of taproot parenchyma cells remained unknown. As with glucose, sucrose stimulation of taproot parenchyma cells caused inward proton fluxes and plasma membrane depolarization, indicating a sugar/proton symport mechanism. To decipher the nature of the corresponding proton-driven sugar transporters, we performed transcriptomic taproot profiling and identified the cold-induced PMT5a and STP13 transporters. When expressed in Xenopus laevis oocytes, BvPMT5a was characterized as a voltage- and H+-driven low-affinity glucose transporter, which does not transport sucrose. In contrast, BvSTP13 operated as a high-affinity H+/sugar symporter, transporting glucose better than sucrose, and being more cold-tolerant than BvPMT5a. Modeling of the BvSTP13 structure with bound mono- and disaccharides suggests plasticity of the binding cleft to accommodate the different saccharides. The identification of BvPMT5a and BvSTP13 as taproot sugar transporters could improve breeding of sugar beet to provide a sustainable energy crop.

Significance Statement In vivo electrophysiological studies with sugar beet taproots provide clear evidence for proton-coupled glucose and sucrose uptake into taproot parenchyma cells. In search for the molecular entities, the taproot-expressed BvPMT5a and BvSTP13 carriers were studied in detail, because they mediate proton-driven import of glucose and sucrose and thus provide proper candidates for sugar beet plasma membrane sugar-proton cotransporters.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The Supplemental Information has been updated and now also shows additional experiments; Figures 2 and 4 were revised for better illustration of the data; author affiliations were updated.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 20, 2023.
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Beet taproot plasma membrane sugar transport revisited
Antonella Reyer, Nadia Bazihizina, Justyna Jaślan, Sönke Scherzer, Nadine Schäfer, Dawid Jaślan, Dirk Becker, Thomas D. Müller, Benjamin Pommerrenig, H. Ekkehard Neuhaus, Irene Marten, Rainer Hedrich
bioRxiv 2021.09.21.461191; doi: https://doi.org/10.1101/2021.09.21.461191
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Beet taproot plasma membrane sugar transport revisited
Antonella Reyer, Nadia Bazihizina, Justyna Jaślan, Sönke Scherzer, Nadine Schäfer, Dawid Jaślan, Dirk Becker, Thomas D. Müller, Benjamin Pommerrenig, H. Ekkehard Neuhaus, Irene Marten, Rainer Hedrich
bioRxiv 2021.09.21.461191; doi: https://doi.org/10.1101/2021.09.21.461191

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