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J. Biol. Chem., Vol. 280, Issue 23, 21867-21881, June 10, 2005

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Detoxification and Transcriptome Response in Arabidopsis Seedlings Exposed to the Allelochemical Benzoxazolin-2(3H)-one^*

Scott R. Baerson, Adela Sánchez-Moreiras¶||, Nuria Pedrol-Bonjoch**, Margot Schulz, Isabelle A. Kagan, Ameeta K. Agarwal¶¶, Manuel J. Reigosa¶, and Stephen O. Duke

From the United States Department of Agriculture, Agricultural Research Service, Natural Products Utilization Research Unit, University, Mississippi 38677, ^¶Laboratorio de Ecofisioloxia Vexetal, Facultade de Ciencias, Universidade de Vigo, Vigo 36310, Spain, ^**Área de Nutrición, Pastos y Forrajes, SERIDA, Estación Experimental "La Mata," Grado 33820, Spain, Institut für Molekulare Physiologie und Biotechnologie der Pflanzen, Universität Bonn, Biozentrum Karlrobert Kreiten Strasse 13, 53115 Bonn, Germany, and ^¶¶National Center for Natural Products Research, University of Mississippi, University, Mississippi 38677

Benzoxazolin-2(3H)-one (BOA) is an allelochemical most commonly associated with monocot species, formed from the O-glucoside of 2,4-dihydroxy-2H-1,4-benzoxazin-3(4H)-one by a two-step degradation process. The capacity of Arabidopsis to detoxify exogenously supplied BOA was analyzed by quantification of the major known metabolites BOA-6-OH, BOA-6-O-glucoside, and glucoside carbamate, revealing that detoxification occurs predominantly through O-glucosylation of the intermediate BOA-6-OH, most likely requiring the sequential action of as-yet-unidentified cytochrome P450 and UDP-glucosyltransferase activities. Transcriptional profiling experiments were also performed with Arabidopsis seedlings exposed to BOA concentrations, representing I₅₀ and I₈₀ levels based on root elongation inhibition assays. One of the largest functional categories observed for BOA-responsive genes corresponded to protein families known to participate in cell rescue and defense, with the majority of these genes potentially associated with chemical detoxification pathways. Further experiments using a subset of these genes revealed that many are also transcriptionally induced by a variety of structurally diverse xenobiotic compounds, suggesting they comprise components of a coordinately regulated, broad specificity xenobiotic defense response. The data significantly expand upon previous studies examining plant transcriptional responses to allelochemicals and other environmental toxins and provide novel insights into xenobiotic detoxification mechanisms in plants.

Received for publication, January 19, 2005 , and in revised form, April 8, 2005.

^* This work was supported in part by a fellowship under the Organization for Economic Cooperation and Development Cooperative Research Programme, Biological Resource Management for Sustainable Agriculture Systems (to N. P.-B.). 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 www.jbc.org) contains Table I.

^|| Present address: Dept. of Biochemistry, Max-Planck-Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745 Jena, Germany.

Present address: United States Department of Agriculture, Agricultural Research Service, Forage-Animal Production Research Unit, N220 Agricultural Sciences North, Lexington, KY 40546.

To whom correspondence should be addressed: United States Department of Agriculture, Agricultural Research Service, Natural Products Utilization Research Unit, P. O. Box 8048, University, MS 38677. Tel.: 662-915-7965; Fax: 662-915-1035; E-mail: sbaerson{at}olemiss.edu.

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