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Integrated Metabolite and Transcript Profiling Identify a Biosynthetic Mechanism for Hispidol in Medicago truncatula Cell Cultures^{1,[C],[W],[OA]}

Plant Biology Division, Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (M.A.F., B.E.D., M.N., R.A.D., L.W.S.); Pharmacognosy Department, Faculty of Pharmacy, Cairo University, Cairo, Egypt 11562 (M.A.F.); Department of Biology, Colorado State University, Fort Collins, Colorado 80523 (B.E.D.); and Departamento de Química, Instituto de Ciências Exatas, Universidade Federal de Minas Gerais, Campus Pampulha, Belo Horizonte, Minas Gerais, 31270–901, Brazil (Â.d.F.)

Metabolic profiling of elicited barrel medic (Medicago truncatula) cell cultures using high-performance liquid chromatography coupled to photodiode and mass spectrometry detection revealed the accumulation of the aurone hispidol (6-hydroxy-2-[(4-hydroxyphenyl)methylidene]-1-benzofuran-3-one) as a major response to yeast elicitor. Parallel, large-scale transcriptome profiling indicated that three peroxidases, MtPRX1, MtPRX2, and MtPRX3, were coordinately induced with the accumulation of hispidol. MtPRX1 and MtPRX2 exhibited aurone synthase activity based upon in vitro substrate specificity and product profiles of recombinant proteins expressed in Escherichia coli. Hispidol possessed significant antifungal activity relative to other M. truncatula phenylpropanoids tested but has not been reported in this species before and was not found in differentiated roots in which high levels of the peroxidase transcripts accumulated. We propose that hispidol is formed in cell cultures by metabolic spillover when the pool of its precursor, isoliquiritigenin, builds up as a result of an imbalance between the upstream and downstream segments of the phenylpropanoid pathway, reflecting the plasticity of plant secondary metabolism. The results illustrate that integration of metabolomics and transcriptomics in genetically reprogrammed plant cell cultures is a powerful approach for the discovery of novel bioactive secondary metabolites and the mechanisms underlying their generation.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Lloyd W. Sumner (lwsumner{at}noble.org).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.141481

^* Corresponding author; e-mail lwsumner{at}noble.org.

Received May 18, 2009; accepted June 29, 2009; published July 1, 2009.