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Volume 271, Number 44, Issue of November 1, 1996 pp. 27233-27236
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.

How Plants Dispose of Chlorophyll Catabolites
DIRECTLY ENERGIZED UPTAKE OF TETRAPYRROLIC BREAKDOWN PRODUCTS INTO ISOLATED VACUOLES

(Received for publication, May 6, 1996, and in revised form, August 26, 1996)

Brigitte Hinder Dagger , Maya Schellenberg Dagger , Simona Rodoni Dagger , Samuel Ginsburg Dagger , Esther Vogt § , Enrico Martinoia , Philippe Matile Dagger and Stefan Hörtensteiner Dagger

From the Dagger  Department of Plant Biology, University of Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland, the § Institute of Plant Sciences, Swiss Federal Institute of Technology, Universitätsstrasse 2, ETH-Z, CH-8092 Zürich, Switzerland, and the  Institut de Biologie Végétale, Université de Poitiers, 40 rue du Recteur Pineau, 86022 Poitiers, France

During the yellowing of leaves the porphyrin moiety of chlorophyll is cleaved into colorless linear tetrapyrrolic catabolites, which eventually are deposited in the central vacuoles of mesophyll cells. In senescent cotyledons of rape, Brassica napus, three nonfluorescent chlorophyll catabolites (NCCs), accounting for practically all the chlorophyll broken down, were found to be located in the vacuoles (vacuoplasts) prepared from protoplasts. Transport of catabolites across the tonoplast was studied with vacuoles isolated from barley mesophyll protoplasts in conjunction with a radiolabeled NCC, Bn-NCC-1, prepared from senescent rape cotyledons. The uptake of Bn-NCC-1 into vacuoles was against a concentration gradient and strictly dependent on MgATP and it followed saturation kinetics with a Km of approximately 100 µM. Although the hydrolysis of ATP was required, transport was apparently independent of the vacuolar proton pumps: accumulation of the NCC occurred both in the presence of the H+-ATPase inhibitor bafilomycin and after destroying the Delta pH between the vacuolar sap and the medium. ATP could be replaced by GTP or UTP, and the transport was inhibited in the presence of vanadate. Chlorophyll catabolites isolated from senescent barley leaves competed with the rape-specific substrate for uptake into the vacuoles. Compounds such as the glutathione conjugate of N-ethylmaleimide and taurocholate, which are known to be transported across the tonoplast in a primary active mode, did not significantly inhibit uptake of Bn-NCC-1. Although the heme catabolites biliverdin and bilirubin inhibited the uptake of the NCC, this effect is caused by unspecific binding to the vacuolar membrane rather than to the specific inhibition of carrier-mediated transport. Taken together, the results demonstrate that barley mesophyll vacuoles are constitutively equipped with a directly energized carrier that transports tetrapyrrolic catabolites of chlorophyll into the vacuole.


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