Overexpression of a proton‐coupled vacuolar glucose exporter impairs freezing tolerance and seed germination

• Published in: The New phytologist 2014-04, Vol.202 (1), p.188-197
• Main Authors: Klemens, Patrick A. W, Patzke, Kathrin, Trentmann, Oliver, Poschet, Gernot, Büttner, Michael, Schulz, Alexander, Marten, Irene, Hedrich, Rainer, Neuhaus, H. Ekkehard
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological; ambient temperature; Arabidopsis; Arabidopsis - genetics; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Beta vulgaris; Biocatalysis; Biological Transport; Carbohydrate Metabolism; Cold; Cold tolerance; Cold treatment; Cytosol; Dehydration; Electric Conductivity; Exporters; Freezing; frost resistance; Gene Expression Regulation, Plant; Germination; Glucose; Glucose - metabolism; Glucose tolerance; glucose transport; Homology; Leaves; Light-Harvesting Protein Complexes - genetics; Light-Harvesting Protein Complexes - metabolism; Monosaccharide Transport Proteins - genetics; Monosaccharide Transport Proteins - metabolism; Monosaccharides; Photosystem II Protein Complex - genetics; Photosystem II Protein Complex - metabolism; Plant growth; Plant physiology; Plant Proteins - genetics; Plant Proteins - metabolism; Plants; Plants, Genetically Modified; Protein transport; Protons; RNA, Messenger - genetics; RNA, Messenger - metabolism; Saccharides; Seed germination; Seeds; Seeds - genetics; Seeds - growth & development; Signal Transduction; Starch - metabolism; stress tolerance; sugar beet; Sugar beets; Sugars; tonoplast; Transcription; Transgenic plants; vacuole; Vacuoles; Vacuoles - metabolism
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.12642

Arabidopsis vacuoles harbor, besides sugar transporter of the TMT‐type, an early response to dehydration like 6 (ERDL6) protein involved in glucose export into the cytosol. However, the mode of transport of ERDL6 and the plant's feedback to overexpression of its activity on essential properties such as, for example, seed germination or freezing tolerance, remain unexplored. Using patch‐clamp studies on vacuoles expressing AtERDL6 we demonstrated directly that this carrier operates as a proton‐driven glucose exporter. Overexpression of BvIMP, the closest sugar beet (Beta vulgaris) homolog to AtERDL6, in Arabidopsis leads surprisingly to impaired seed germination under both conditions, sugar application and low environmental temperatures, but not under standard conditions. Upon cold treatment, BvIMP overexpressor plants accumulated lower quantities of monosaccharides than the wild‐type, a response in line with the reduced frost tolerance of the transgenic Arabidopsis plants, and the fact that cold temperatures inhibits BvIMP transcription in sugar beet leaves. With these findings we show that the tight control of vacuolar sugar import and export is a key requisite for cold tolerance and seed germination of plants.