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The Allelochemical MDCA Inhibits Lignification and Affects Auxin Homeostasis

W. Steenackers, I. Cesarino, P. Klíma, M. Quareshy, R. Vanholme, S. Corneillie, RP. Kumpf, D. Van de Wouwer, K. Ljung, G. Goeminne, O. Novák, E. Zažímalová, R. Napier, W. Boerjan, B. Vanholme,

. 2016 ; 172 (2) : 874-888. [pub] 20160809

Language English Country United States

Document type Journal Article

Persistent link   https://www.medvik.cz/link/bmc18017105

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.

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$a Steenackers, Ward $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a The Allelochemical MDCA Inhibits Lignification and Affects Auxin Homeostasis / $c W. Steenackers, I. Cesarino, P. Klíma, M. Quareshy, R. Vanholme, S. Corneillie, RP. Kumpf, D. Van de Wouwer, K. Ljung, G. Goeminne, O. Novák, E. Zažímalová, R. Napier, W. Boerjan, B. Vanholme,
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$a 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.
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$a Cesarino, Igor $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Klíma, Petr $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Quareshy, Mussa $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a Vanholme, Ruben $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Corneillie, Sander $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Kumpf, Robert Peter $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a Van de Wouwer, Dorien $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Ljung, Karin $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Goeminne, Geert $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a Novák, Ondřej $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Zažímalová, Eva $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Napier, Richard $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Boerjan, Wout $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.) bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be.
700    1_
$a Vanholme, Bartel $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.V., S.C., R.P.K., D.V.d.W., G.G., W.B., B.V.);Department of Botany, Institute of Biosciences, University of São Paulo, 05508-090 Butantã, São Paulo, Brazil (I.C.);Institute of Experimental Botany, the Czech Academy of Sciences, 16502 Prague, the Czech Republic (P.K., E.Z.);School of Life Sciences, University of Warwick, CV4 7AL Coventry, United Kingdom (M.Q., R.N.);Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.); andLaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, Šlechtitelů 27, CZ-78371 Olomouc, Czech Republic (O.N.) bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be.
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