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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Heavy Metal Stress and Sulfate Uptake in Maize Roots¹

Dipartimento di Produzione Vegetale, Università degli Studi di Milano, 20133 Milan, Italy (F.F.N., C.L., B.C., G.A.S.); and Biochimie and Physiologie Moléculaire des Plantes, Institut National de la Recherche Agronomique (Unité 386), Centre National de la Recherche Scientifique (Unité Mixte de Recherche 5004), Ecole Nationale Supérieure Agronomique de Montpellier, Université Montpellier 2, 34060 Montpellier, cedex 1, France (P.F., J.-C.D.)

ZmST1;1, a putative high-affinity sulfate transporter gene expressed in maize (Zea mays) roots, was functionally characterized and its expression patterns were analyzed in roots of plants exposed to different heavy metals (Cd, Zn, and Cu) interfering with thiol metabolism. The ZmST1;1 cDNA was expressed in the yeast (Saccharomyces cerevisiae) sulfate transporter mutant CP154-7A. Kinetic analysis of sulfate uptake isotherm, determined on complemented yeast cells, revealed that ZmST1;1 has a high affinity for sulfate (K_m value of 14.6 ± 0.4 µM). Cd, Zn, and Cu exposure increased both ZmST1;1 expression and root sulfate uptake capacity. The metal-induced sulfate uptakes were accompanied by deep alterations in both thiol metabolism and levels of compounds such as reduced glutathione (GSH), probably involved as signals in sulfate uptake modulation. Cd and Zn exposure strongly increased the level of nonprotein thiols of the roots, indicating the induction of additional sinks for reduced sulfur, but differently affected root GSH contents that decreased or increased following Cd or Zn stress, respectively. Moreover, during Cd stress a clear relation between the ZmST1;1 mRNA abundance increment and the entity of the GSH decrement was impossible to evince. Conversely, Cu stress did not affect nonprotein thiol levels, but resulted in a deep contraction of GSH pools. Our data suggest that during heavy metal stress sulfate uptake by roots may be controlled by both GSH-dependent or -independent signaling pathways. Finally, some evidence suggesting that root sulfate availability in Cd-stressed plants may limit GSH biosynthesis and thus Cd tolerance are discussed.

The author responsible for the distribution of materials integral to the finding presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Gian Attilio Sacchi (gianattilio.sacchi@unimi.it).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.076240.

^* Corresponding author; e-mail gianattilio.sacchi{at}unimi.it; fax 39–0250316521.

Received December 23, 2005; returned for revision April 28, 2006; accepted May 2, 2006.

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