Cellular detoxification in plants the role of glutathione S-conjugate transport
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1 Research Collection Doctoral Thesis Cellular detoxification in plants the role of glutathione S-conjugate transport Author(s): Tommasini, Roberto Publication Date: 1997 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETH Nr Cellular detoxification in plants: The role of glutathione S-conjugate transport A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of Doctor of Natural Sciences presented by Roberto Tommasini Dipl. Natw. ETH Zurich born December 18, 1963 in Uster Accepted on the recommendation of Prof. Dr. N. Amrhein, examiner Prof. Dr. E. Martinoia, co-examiner Dr. K. Kreuz, co-examiner Zurich 1997 Partially published in: Nature 364, (1993) Z. Naturforschung 48c, (1993) FEBS Lett. 352, (1994) Plant Physiol. Ill, (1996) Plant Physiol. Ill, (1996) Proc. Natl. Acad. Sci. USA 93, (1996)
3 2 Abstract The transport of glutathione S-conjugates (GS-conjugates) of e.g. N- ethylmaleimide (NEM) or metolachlor a chloroacetanilide herbicide, into isolated barley mesophyll vacuoles is a MgATP-dependent process. Uptake of NEM-GS as well as of metolachlor-gs into vacuoles is saturable and follows Michaelis-Menten kinetics. Bafilomycin, a very potent and specific inhibitor of the tonoplast H+-ATPase, failed to inhibit the MgATP-dependent uptake of GS-conjugate, while MgATP-dependent proton pumping, as well as the MgATP-dependent uptake of malate which is thought to be a secondary active process, were completely inhibited by bafilomycin. The GS-conjugate transport was also not driven by pyrophosphate, the substrate of the second vacuolar H+-pump. These results indicate that the energy-dependent uptake of GS-conjugates is not linked to the activity of either of the known vacuolar proton pumps. Strong inhibition of GS-conjugate uptake by vanadate (I5o 60 um), an inhibitor of P-type ATPases, also argues against an involvement of the tonoplast H+-ATPase. These observations and the fact that accumulation of GS-conjugates is observed in the presence of bafilomycin and NH4+, suggest that GS-conjugate uptake into plant vacuoles is mediated by a specific ATPase described here for the first time. Glutathione (GSH) in its oxidized form (GSSG) is also rapidly taken up into isolated barley vacuoles, while uptake of GSH is only marginal. GSSG transport is strictly MgATP-dependent and is inhibited by vanadate, but not by bafilomycin. We also investigated transport into intact protoplasts and leaf discs and found that the plasma membrane of leaf cells contains a specific transporter for GSH, which takes up GSSG and GS-conjugates in preference to GSH. Uptake of both GSH and GSSG was inhibited by GSconjugates, and GSSG inhibited the uptake of metolachlor-gs. In comparison, the uptake of the glucosyl conjugate of the herbicide derivative [5-hydroxyphenyl]primisulfuron into barley mesophyll vacuoles was investigated. This transport is also stimulated by MgATP, but is distinct from that described for GS-conjugates. Treatment of barley with different herbicide antidotes (safeners) revealed that the barley specific safener cloquintocet-mexyl causes a twofold increase in the vacuolar transport activities for both the glutathione and glucoside conjugates. Towards the isolation of the GS-conjugate transporter we have characterized a cadmium sensitive yeast strain (DTY 168) which is
4 3 also deficient in GS-conjugate transport (ycfla). Functional expression of the human GS-conjugate transporter MRP in the yeast mutant restored both cadmium resistance and GS-conjugate transport activity. Exploiting the sequence homology of MRP and YCF1, we isolated AtMRP, a homologoue at the amino acid level of Arabidopsis thaliana. Treatment of Arabidopsis thaliana plants with the herbicides IRL 1803 and primisulfuron resulted in a strong induction (30-50 times) on the transcript level compared to other homologoues of AtMRP. Zusammenfassung Der Transport der Glutathion S-Konjugate (GS-Konjugate) von Ethylmaleimid (NEM) und Metolachlor, ein Chloracetanilid Herbizid, in Gersten Mesophyll Vakuolen ist ein MgATP abhangiger Prozess. Die Aufnahme von NEM-GS wie auch von Metolachlor-GS in Vakuolen ist sattigbar und verlauft nach einer Michaelis-Menten Kinetik. Bafilomycin, ein spezifischer Inhibitor der Tonoplasten H+-ATPase, zeigt keinen Einfluss auf den Transport. Im Gegensatz dazu wurde der Protonen Transport, sowie der Transport von Malat, welcher ein sekundar aktivierter Transport ist, durch Bafilomycin vollstandig gehemmt. Der Transport von GS-Konjugaten ist auch nicht von Pyrophosphat abhangig, ein Substrat der zweiten Protonenpumpe am Tonoplasten. Diese Resultate zeigen, dass die energieabhangige Aufnahme von GS-Konjugaten nicht von den bislang bekannten Protonenpumpen abhangig ist. Eine starke Inhibierung der GS-Konjugat Aufnahme durch Vanadat (I50 60 um), ein Inhibitor der P-typ ATPasen, spricht ebenfalls gegen eine Beteiligung der vakuolaren Protonenpumpen. Aus diesen Beobachtungen und der Tatsache, dass eine Akkumulation von GS-Konjugaten in der Vakuole auch in Anwesenheit von Bafilomycin und NH4+ beobachtet werden kann, lasst sich schliessen, dass der Transport von GS-Konjugaten durch eine spezifische ATPase erfolgt, die hier erstmalig beschrieben wird. Oxidiertes Glutathion (GSSG) wird ebenfalls in isolierte Gersten Vakuolen aufgenommen, reduziertes Glutathion (GSH) dagegen nur marginal. Der Transport von GSSG ist ebenfalls strikt MgATP abhangig und ist durch Vanadat, aber nicht durch Bafilomycin hemmbar. Der Transport von GS-Konjugaten wurde auch an intakten Protoplasten und Blattscheiben untersucht. Dabei wurde gezeigt, dass Plasmamembranen
5 4 einen spezifischen Transporter fur GSH besitzen, wobei GSSG und GS- Konjugate bevorzugter aufgenommen von GSH und GSSG ist durch GS-Konjugate werden als GSH. Die Aufnahme hemmbar und GSSG hemmt die Aufnahme von Metolachlor-GS. Die Aufnahme des Herbizidglucosids [5-Hydroxyphenyl]primisulfuron in Gersten Mesophyllvakuolen wurde ebenfalls untersucht. Der Transport wird durch MgATP stimuliert und unterscheidet sich vom beschriebenen GS-Konjugat Transport. Eine Behandlung von Gerste mit verschiedenen Safenern ergab, dass der spezifische Safener Cloquintocet-mexyl in der Lage war, den Transport von GS-Konjugaten und des Herbizidglucosids zu verdoppeln. Im Hinblick auf die Isolierung des GS-Konjugat Transporters haben wir einen Cadmium sensitiven Hefestamm (DTY 168) charakterisiert, der auch GS- Konjugate nicht transportiern kann (ycfla). Die funktionelle Expression von MRP, dem GS-Konjugat Transporter des Menschen, in der Hefemutante resultierte in einer Wiederherstellung der Cadmiumtoleranz sowie des GS-Konjugat Transportes. Aufgrund der Sequenzhomologie mit YCF1 und MRP wurde die cdna von AtMRP isoliert, welche ein homologes Protein aus Arabidopsis thaliana kodiert. Behandlungen von Arabidopsis thaliana mit den Herbiziden IRL 1803 und Primisulfuron resultierten in einer starken Induktion (30-50 fach) von AtMRP spezifischen Transkripten.
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