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The allelochemical MDCA inhibits lignification and affects auxin homeostasis

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Steenackers, Ward Jan, Cesarino, Igor, Klíma, Petr, Quareshy, Mussa, Vanholme, Ruben, Corneillie, Sander, Kumpf, Robert P., Van de Wouwer, Dorien, Ljung, Karin, Goeminne, Geert, Novak, Ondrej, Zažímalová, Eva, Napier, R. (Richard), Boerjan, Wout A. and Vanholme, Bartel (2016) The allelochemical MDCA inhibits lignification and affects auxin homeostasis. Plant Physiology, 172 (2). pp. 874-888. doi:10.1104/pp.15.01972 ISSN 0032-0889.

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Official URL: http://dx.doi.org/10.1104/pp.15.01972

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Abstract

The phenylpropanoid 3,4-(methylenedioxy)cinnamic acid (MDCA) is a plant-derived compound first extracted from roots of Asparagus officinalis and further characterized as an allelochemical. Later on, MDCA was identified as an efficient inhibitor of 4-COUMARATE-CoA LIGASE (4CL), a key enzyme of the general phenylpropanoid pathway. By blocking 4CL, MDCA affects the biosynthesis of many important metabolites, which might explain its phytotoxicity. To decipher the molecular basis of the allelochemical activity of MDCA, we evaluated the effect of this compound on Arabidopsis thaliana seedlings. Metabolic profiling revealed that MDCA is converted in planta into piperonylic acid (PA), an inhibitor of CINNAMATE-4-HYDROXYLASE (C4H), the enzyme directly upstream of 4CL. The inhibition of C4H was also reflected in the phenolic profile of MDCA-treated plants. Treatment of in vitro grown plants resulted in an inhibition of primary root growth and a proliferation of lateral and adventitious roots. These observed growth defects were not the consequence of lignin perturbation, but rather the result of disturbing auxin homeostasis. Based on DII-VENUS quantification and direct measurement of cellular auxin transport, we concluded that MDCA disturbs auxin gradients by interfering with auxin efflux. In addition, mass spectrometry was used to show that MDCA triggers auxin biosynthesis, conjugation, and catabolism. A similar shift in auxin homeostasis was found in the c4h mutant ref3-2, indicating that MDCA triggers a cross talk between the phenylpropanoid and auxin biosynthetic pathways independent from the observed auxin efflux inhibition. Altogether, our data provide, to our knowledge, a novel molecular explanation for the phytotoxic properties of MDCA.

Item Type: Journal Article
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Journal or Publication Title: Plant Physiology
Publisher: American Society of Plant Biologists
ISSN: 0032-0889
Official Date: October 2016
Dates:
DateEvent
October 2016Published
9 August 2016Available
3 August 2016Accepted
18 December 2016Submitted
Volume: 172
Number: 2
Page Range: pp. 874-888
DOI: 10.1104/pp.15.01972
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 19 October 2016
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