Home LiteratureArticle Details
PMID: 24329902 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

The New phytologist ·Vol. 202 ·No. 1 ·2014-04-00 ·Pages 188-197

Klemens PAW, Patzke K, Trentmann O, Poschet G, Büttner M, Schulz A, Marten I, Hedrich R, Neuhaus HE

Abstract

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.

Keywords
Arabidopsis glucose transport stress tolerance tonoplast vacuole
MeSH Terms
Adaptation, Physiological Arabidopsis/genetics,physiology Arabidopsis Proteins/genetics,metabolism Beta vulgaris Biocatalysis Biological Transport Carbohydrate Metabolism Electric Conductivity Freezing Gene Expression Regulation, Plant Germination Glucose/metabolism Light-Harvesting Protein Complexes/genetics,metabolism Monosaccharide Transport Proteins/genetics,metabolism Photosystem II Protein Complex/genetics,metabolism Plant Proteins/genetics,metabolism Plants, Genetically Modified Protons RNA, Messenger/genetics,metabolism Seeds/genetics,growth & development Signal Transduction Starch/metabolism Vacuoles/metabolism
Chemicals
Arabidopsis Proteins CAB1 protein, Arabidopsis Light-Harvesting Protein Complexes Monosaccharide Transport Proteins Photosystem II Protein Complex Plant Proteins Protons RNA, Messenger Starch Glucose
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Klemens Patrick A W
Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Str., D-67653, Kaiserslautern, Germany.
Patzke Kathrin
Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Str., D-67653, Kaiserslautern, Germany.
Trentmann Oliver
Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Str., D-67653, Kaiserslautern, Germany.
Poschet Gernot
Centre for Organismal Studies (COS), University of Heidelberg, Im Neuenheimer Feld 360, 69120, Heidelberg, Germany.
Büttner Michael
Centre for Organismal Studies (COS), University of Heidelberg, Im Neuenheimer Feld 360, 69120, Heidelberg, Germany.
Schulz Alexander
Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Julius-von-Sachs Platz 2, D-97082, Würzburg, Germany.
Marten Irene
Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Julius-von-Sachs Platz 2, D-97082, Würzburg, Germany.
Hedrich Rainer
Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Julius-von-Sachs Platz 2, D-97082, Würzburg, Germany.
Neuhaus H Ekkehard
Plant Physiology, University of Kaiserslautern, Erwin-Schrödinger-Str., D-67653, Kaiserslautern, Germany.
References (50)
50 references, click to expand
  1. Alberdi M, Corcuera LJ. 1991. Cold-acclimation in plants. Phytochemistry 30: 3177-3184.
  2. Bertl A, Blumwald E, Coronado R, Eisenberg R, Findlay G, Gradmann D, Hille B, Kohler K, Kolb HA, MacRobbie E. 1992. Electrical measurements on endomembranes. Science 258: 873-874.
  3. Beyhl D, Hörtensteiner S, Martinoia E, Farmer EE, Fromm J, Marten I, Hedrich R. 2009. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant Journal 58: 715-723.
  4. Büttner M, Sauer N. 2000. Monosaccharide transporters in plants: structure, function and physiology. Biochimica et Biophysica Acta 1465: 263-274.
  5. Carninci P, Nishiyama Y, Westover A, Itoh M, Nagaoka S, Sasaki N, Okazaki Y, Muramatsu M, Hayashizaki Y. 1998. Thermostabilization and thermoactivation of thermolabile enzymes by trehalose and its application for the synthesis of full length cDNA. Proceedings of the National Academy of Sciences, USA 95: 520-524.
  6. Chardon F, Bedu M, Calenge F, Klemens PA, Spinner L, Clement G, Chietera G, Leran S, Ferrand M, Lacombe B et al. 2013. Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Current Biology 23: 697-702.
  7. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527-532.
  8. Chiou TJ, Bush DR. 1996. Molecular cloning, immunochemical localization to the vacuole, and expression in transgenic yeast and tobacco of a putative sugar transporter from sugar beet. Plant Physiology 110: 511-520.
  9. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139: 5-17.
  10. Dekkers BJ, Schuurmans JA, Smeekens SC. 2004. Glucose delays seed germination in Arabidopsis thaliana. Planta 218: 579-588.
  11. Eom JS, Cho JI, Reinders A, Lee SW, Yoo Y, Tuan PQ, Choi SB, Bang G, Park YI, Cho MH et al. 2011. Impaired function of the tonoplast-localized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiology 157: 109-119.
  12. Flügge UI. 1999. Phosphate translocators in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 50: 27-45.
  13. Hanson J, Smeekens S. 2009. Sugar perception and signaling - an update. Current Opinion in Plant Biology 12: 562-567.
  14. Heldt HW. 2005. Plant biochemistry. Burlington, MA, USA: Elsevier Academic.
  15. Ivashikina N, Hedrich R. 2005. K+-currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. Plant Journal 41: 606-614.
  16. John P. 1992. Biosynthesis of the major crop products. Chichester, UK: John Wiley & Sons.
  17. Kaiser G, Heber U. 1984. Sucrose transport into vacuoles isolated from barley mesophyll protoplasts. Planta 161: 562-568.
  18. Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7: 193-195.
  19. Kiyosue T, Abe H, Yamaguchi-Shinozaki K, Shinozaki K. 1998. ERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter. Biochimica et Biophysica Acta 1370: 187-219.
  20. Koch KE. 1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 509-540.
  21. Krebs M, Beyhl D, Görlich E, Al-Rasheid KA, Marten I, Stierhof YD, Hedrich R, Schumacher K. 2010. Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proceedings of the National Academy of Sciences, USA 107: 3251-3256.
  22. Kruckeberg AL, Neuhaus HE, Feil R, Gottlieb LD, Stitt M. 1989. Decreased-activity mutants of phosphoglucose isomerase in the cytosol and chloroplasts of Clarkia xantiana. Biochemical Journal 261: 457-467.
  23. Leslie SB, Israeli E, Lighthart B, Crowe JH, Crowe LM. 1995. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Applied and Environment Microbiology 61: 3592-3597.
  24. Marsado F, Corcuera L, Alberdi M. 2000. Embryo physiological responses to cold by two cultivars of oat during germination. Crop Science 40: 1694-1701.
  25. Martinoia E, Maeshima M, Neuhaus HE. 2007. Vacuolar transporters and their essential role in plant metabolism. Journal of Experimental Botany 58: 83-102.
  26. Martinoia E, Meyer S, De Angeli A, Nagy R. 2012. Vacuolar transporters in their physiological context. Annual Review of Plant Biology 63: 163-213.
  27. McRae SR, Christopher JT, Smith JAC, Holtum JAM. 2002. Sucrose transport across the vacuolar membrane of Ananas comosus. Functional Plant Biology 29: 717-724.
  28. Monachello D, Allot M, Oliva S, Krapp A, Daniel-Vedele F, Barbier-Brygoo H, Ephritikhine G. 2009. Two anion transporters AtClCa and AtClCe fulfil interconnecting but not redundant roles in nitrate assimilation pathways. New Phytologist 183: 88-94.
  29. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. Science 300: 261-263.
  30. Neuhaus HE. 2007. Transport of primary metabolites across the plant vacuolar membrane. FEBS Letters 581: 2223-2226.
  31. Neuhaus HE, Quick WP, Siegl G, Stitt M. 1990. Control of photosynthate partitioning in spinach leaves: analysis of the interaction between feedforward and feedback regulation of sucrose synthesis. Planta 181: 583-592.
  32. Poschet G, Hannich B, Raab S, Jungkunz I, Klemens PA, Krueger S, Wic S, Neuhaus HE, Büttner M. 2011. A novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiology 157: 1664-1676.
  33. ap Rees T. 1994. Plant physiology. Virtue on both sides. Current Biology 4: 557-559.
  34. Ristic Z, Ashworth EN. 1993. Ultrastructural evidence that intracellular ice formation and possibly cavitation are the sources of freezing injury in supercooling wood tissue of Cornus florida L. Plant Physiology 103: 753-761.
  35. Rolland F, Moore B, Sheen J. 2002. Sugar sensing and signaling in plants. Plant Cell 14: 185-205.
  36. Ruiz-Medrano R, Xoconostle-Cazares B, Lucas J. 2001. The phloem as a conduit for inter-organ communication. Current Opinion in Plant Biology 4: 202-209.
  37. Sasaki H, Ichimura K, Oda M. 1996. Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Annals of Botany 78: 365-369.
  38. Schneider S, Hulpke S, Schulz A, Yaron I, Holl J, Imlau A, Schmitt B, Batz S, Wolf S, Hedrich R et al. 2012. Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. Plant Biology 14: 325-336.
  39. Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E, Poschet G, Büttner M, Schneider S, Sauer N, Hedrich R. 2011. Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant Journal 68: 129-136.
  40. Schulze WX, Schneider T, Starck S, Martinoia E, Trentmann O. 2012. Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant Journal 69: 529-541.
  41. Schulz-Lessdorf B, Hedrich R. 1995. Protons and calcium modulate SV-type channels in the vacuolar-lysosomal compartment - channel interaction with calmodulin inhibitors. Planta 197: 655-671.
  42. Schumacher K, Krebs M. 2010. The V-ATPase: small cargo, large effects. Current Opinion in Plant Biology 13: 724-730.
  43. Wanner LA, Junttila O. 1999. Cold-induced freezing tolerance in Arabidopsis. Plant Physiology 120: 391-400.
  44. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, Boles E. 1999. Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Letters 464: 123-128.
  45. Wingenter K, Schulz A, Wormit A, Wic S, Trentmann O, Hörmiller II, Heyer AG, Marten I, Hedrich R, Neuhaus HE. 2010. Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signalling and seed yield in Arabidopsis. Plant Physiology 154: 665-677.
  46. Wingenter K, Trentmann O, Winschuh I, Hörmiller II, Heyer AG, Reinders J, Schulz A, Geiger D, Hedrich R, Neuhaus HE. 2011. A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant Journal 68: 890-900.
  47. Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE. 2006. Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18: 3476-3490.
  48. Yamada K, Osakabe Y, Mizoi J, Nakashima K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K. 2010. Functional analysis of an Arabidopsis thaliana abiotic stress-inducible facilitated diffusion transporter for monosaccharides. Journal of Biological Chemistry 285: 1138-1146.
  49. Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2: 1565-1572.
  50. Zuther E, Büchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG. 2004. The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Letters 576: 169-173.
Article Info
Journal
The New phytologist
Abbr.
New Phytol
ISSN
1469-8137
Published
2014-04-00
Epub
2013-00-16
Pages
188-197
Language
English
Region
England
NLM ID
9882884
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com