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The role of Vacuolar Hexose Exporters during Stress Response and Development

Fachliche Zuordnung Pflanzenphysiologie
Förderung Förderung von 2008 bis 2015
Projektkennung Deutsche Forschungsgemeinschaft (DFG) - Projektnummer 61498647
 
Erstellungsjahr 2016

Zusammenfassung der Projektergebnisse

Subcellular sugar partitioning in plants is strongly regulated in adaptation to developmental cues and changes in external conditions. We have identified the vacuolar glucose exporter ERD6-like 6 (ERDL6), which has a significant impact on cellular glucose homeostasis. ERDL6 expression is induced in response to factors that activate vacuolar glucose pools like darkness, heat stress and wound response. On the other hand, ERDL6 transcript levels drop during conditions that trigger glucose accumulation in the vacuole like cold, salt and osmotic stress, drought and external sugar supply. Accordingly, sugar analyses revealed that erdl6 mutants have elevated vacuolar glucose levels and glucose flux across the tonoplast is impaired under stress conditions. Establishing the nonaqueous fractionation technique allowed us to clearly assign these changes in glucose levels to the vacuole. Using patch-clamp studies on vacuoles of erdl6 mutant lines we demonstrated directly that this carrier operates as a proton-driven glucose exporter. Complementation studies of the erdl6 knockout plants expressing ERDL6 variants with phosphosite mutations suggest that phosphorylation stimulates ERDL6 activity. ERDL6 has a strong impact on the composition of seed reserves, since the levels of glucose, protein and lipids increased more than two-fold in erdl6 mutant seeds. However, the concentration of phloem sugars in these mutants is not elevated but slightly decreased, indicating that not long-distance supply by increased leaf sugars lead to seed improvement but rather local effects. Lack of ERDL6-driven glucose export from the vacuole has mild impact on several developmental processes, as seed germination and pollen germination rates were reduced and flowering initiation was slightly delayed. However, in contrast to other mutants accumulating cellular sugars, freezing tolerance was not affected in erdl6 mutants. Analysis of the erdl6 mutant transcriptome revealed that vacuolar glucose export is connected to cellulose synthesis as well as jasmonic acid (JA) synthesis and signalling. A group of cellulose synthesis genes was significantly induced, leading to increased cellulose levels in cell walls and in turn to improved seedling development under etiolation conditions. Further, several JA synthesis genes as well as the master regulator of JA signalling, MYC2, and JAZ-type co-regulators were significantly upregulated. Interestingly, MYC2 and JAZ9 can directly interact with the ERDL6 promoter, and in turn the ERDL6-wound induction is strongly repressed in myc2 mutants (and even more pronounced in myc2,3,4 mutants). We were not able to clearly define the role of ERDL4, another ERD6 homolog, since erdl4 knockout plants did not show changes in cellular sugars and expression of ERDL4 in the erdl6 knockout did not complement this mutant. However, the additional lack of ERDL4 in erdl6 mutants led to a further increase in glucose levels, a more pronounced delay in flowering time and further reduction in pollen germination rates. In the functional network of tonoplast transporters, ERDL6 acts as antagonist to the TMT tonoplast monosaccharide transporters, since over-expression of ERDL6 in the tmt1,2 mutant background restores WT glucose levels, while the additional lack of ERDL6 in the tmt1,2-dKO further reduced vacuolar glucose. These data suggest that a concerted action of ERDL6 and TMTs regulates vacuolar sugar partitioning and determines plant performance during stress response and development.

Projektbezogene Publikationen (Auswahl)

  • (2010) The Arabidopsis sugar transporter (AtSTP) family: an update. Plant Biology 12: 35-41
    Büttner, M.
    (Siehe online unter https://doi.org/10.1111/j.1438-8677.2010.00383.x)
  • (2011) A Novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Phys. 157: 1664-1676
    Poschet, G., Hannich, B., Raab, S., Jungkunz, I., Klemens, P.A.W., Krueger, S., Wic, S., Neuhaus, H.E. and Büttner, M.
    (Siehe online unter https://doi.org/10.1104/pp.111.186825)
  • (2011) A Novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiol. 157:1664-76
    Poschet, G., Hannich, B., Raab, S., Jungkunz, I., Klemens, P.A.W., Krueger, S., Wic, S., Neuhaus, H.E. and Büttner, M.
    (Siehe online unter https://doi.org/10.1104/pp.111.186825)
  • (2011) Proton-driven sucrose symport and antiport is provided by the vacuolar transporters SUC4 and TMT1/2. Plant J. 68: 129-136
    Schulz, A., Beyhl, D., Marten, I., Wormit, A., Neuhaus, E., Poschet, G., Büttner, M., Schneider, S., Sauer, N. and Hedrich, R.
    (Siehe online unter https://doi.org/10.1111/j.1365-313X.2011.04672.x)
  • (2014) Overexpression of a proton-coupled vacuolar glucose exporter impairs freezing tolerance and seed germination. New Phytol. 202: 188-197
    Klemens, P.A.W., Patzke, K., Trentmann, O., Poschet, G., Büttner, M., Schulz, A., Marten, I., Hedrich, R. and Neuhaus, H.E.
    (Siehe online unter https://doi.org/10.1111/nph.12642)
 
 

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