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The allelochemical MDCA inhibits lignification and affects auxin homeostasis

Ward Steenackers, Igor Cesarino, Petr Klima, Mussa Quareshy, Ruben Vanholme UGent, Sander Corneillie UGent, Robert Kumpf, Dorien Van de Wouwer, Karin Ljung, Geert Goeminne UGent, et al. (2016) PLANT PHYSIOLOGY. 172(2). p.874-888
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
CELL-SUSPENSION CULTURES, LATERAL ROOT-FORMATION, ARABIDOPSIS-THALIANA, LIGNIN BIOSYNTHESIS, PLANT DEVELOPMENT, SYSTEMS BIOLOGY, EXPRESSION, TRANSPORT, ACID, GROWTH
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
172
issue
2
pages
874 - 888
Web of Science type
Article
Web of Science id
000391147700021
JCR category
PLANT SCIENCES
JCR impact factor
6.456 (2016)
JCR rank
11/211 (2016)
JCR quartile
1 (2016)
ISSN
0032-0889
1532-2548
DOI
10.1104/pp.15.01972
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8510802
handle
http://hdl.handle.net/1854/LU-8510802
date created
2017-02-22 14:56:47
date last changed
2017-02-22 15:01:10
@article{8510802,
  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.},
  author       = {Steenackers, Ward and Cesarino, Igor and Klima, Petr and Quareshy, Mussa and Vanholme, Ruben and Corneillie, Sander and Kumpf, Robert and Van de Wouwer, Dorien and Ljung, Karin and Goeminne, Geert and Novak, Ondrej and Zazimalova, Eva and Napier, Richard and Boerjan, Wout and Vanholme, Bartel},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {CELL-SUSPENSION CULTURES,LATERAL ROOT-FORMATION,ARABIDOPSIS-THALIANA,LIGNIN BIOSYNTHESIS,PLANT DEVELOPMENT,SYSTEMS BIOLOGY,EXPRESSION,TRANSPORT,ACID,GROWTH},
  language     = {eng},
  number       = {2},
  pages        = {874--888},
  title        = {The allelochemical MDCA inhibits lignification and affects auxin homeostasis},
  url          = {http://dx.doi.org/10.1104/pp.15.01972},
  volume       = {172},
  year         = {2016},
}

Chicago
Steenackers, Ward, Igor Cesarino, Petr Klima, Mussa Quareshy, Ruben Vanholme, Sander Corneillie, Robert Kumpf, et al. 2016. “The Allelochemical MDCA Inhibits Lignification and Affects Auxin Homeostasis.” Plant Physiology 172 (2): 874–888.
APA
Steenackers, W., Cesarino, I., Klima, P., Quareshy, M., Vanholme, R., Corneillie, S., Kumpf, R., et al. (2016). The allelochemical MDCA inhibits lignification and affects auxin homeostasis. PLANT PHYSIOLOGY, 172(2), 874–888.
Vancouver
1.
Steenackers W, Cesarino I, Klima P, Quareshy M, Vanholme R, Corneillie S, et al. The allelochemical MDCA inhibits lignification and affects auxin homeostasis. PLANT PHYSIOLOGY. 2016;172(2):874–88.
MLA
Steenackers, Ward, Igor Cesarino, Petr Klima, et al. “The Allelochemical MDCA Inhibits Lignification and Affects Auxin Homeostasis.” PLANT PHYSIOLOGY 172.2 (2016): 874–888. Print.