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J. Biol. Chem., Vol. 279, Issue 43, 44817-44824, October 22, 2004

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UPS1 and UPS2 from Arabidopsis Mediate High Affinity Transport of Uracil and 5-Fluorouracil^*

Anja Schmidt, Yan-Hua Su, Reinhard Kunze¶, Susan Warner||, Matthew Hewitt||, Robert D. Slocum||, Uwe Ludewig, Wolf B. Frommer**, and Marcelo Desimone

From the Plant Physiology, ZMBP, Auf der Morgenstelle 1, D-72076 Tübingen, Germany, ^¶Botany Institute II, University of Cologne, Gyrhofstrasse 15, D-50931 Köln, Germany, ^||Department of Biological Sciences, Goucher College, Baltimore, Maryland 21204-2794, and ^**Carnegie Institution of Washington, Stanford, California 94305

Salvage pathways play an important role in providing nucleobases to cells, which are unable to synthesize sufficient amounts for their needs. Cellular uptake systems for pyrimidines have been described, but in higher eukaryotes, transporters for thymine and uracil have not been identified. Two plant transporters, AtUPS1 and PvUPS1, were recently identified as transporters for allantoin in Arabidopsis and French bean, respectively. However, Arabidopsis, in contrast to tropical legumes, uses mainly amino acids for long distance transport. Allantoin transport has not been described in the Brassicaceae. Thus, the physiological substrates of ureide permease (UPS) transporters in Arabidopsis may be compounds structurally related to allantoin. A detailed analysis of the substrate specificities of two members of the AtUPS family shows that AtUPS1 and AtUPS2 mediate high affinity uracil and 5-fluorouracil (a toxic uracil analogue) transport when expressed in yeast and Xenopus oocytes. Consistent with a function during germination and early seedling development, AtUPS1 expression is transiently induced during the early stages of seedling development followed by up-regulation of AtUPS2 expression. Arabidopsis ups2 insertion mutants and ups1 lines, in which transcript levels were reduced by post-transcriptional gene silencing, are more tolerant to 5-fluorouracil as compared with wild type plants. The results suggest that in Arabidopsis UPS transporters are the main transporters for uracil and potentially other nucleobases, whereas during evolution legumes may have taken advantage of the low selectivity of UPS proteins for long distance transport of allantoin.

Received for publication, May 17, 2004 , and in revised form, August 6, 2004.

^* This work was supported by the German Bundesministerium für Bildung und Forschung in the framework of Genomanalyse im biologischen System-Pflanze-GABI and by National Science Foundation Award MCB-0076881 (to R. D. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Supplemental Figs. 1–3.

These authors contributed equally.

To whom correspondence should be addressed. Tel.: 49-7071-29-73222; Fax: 49-7071-29-3287; E-mail: marcelo.desimone{at}zmbp.uni-tuebingen.de.

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