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cis-Cinnamic Acid Is a Novel, Natural Auxin Efflux Inhibitor That Promotes Lateral Root Formation

W. Steenackers, P. Klíma, M. Quareshy, I. Cesarino, RP. Kumpf, S. Corneillie, P. Araújo, T. Viaene, G. Goeminne, MK. Nowack, K. Ljung, J. Friml, JJ. Blakeslee, O. Novák, E. Zažímalová, R. Napier, W. Boerjan, B. Vanholme,

. 2017 ; 173 (1) : 552-565. [pub] 20161111

Jazyk angličtina Země Spojené státy americké

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/bmc18016920

Auxin steers numerous physiological processes in plants, making the tight control of its endogenous levels and spatiotemporal distribution a necessity. This regulation is achieved by different mechanisms, including auxin biosynthesis, metabolic conversions, degradation, and transport. Here, we introduce cis-cinnamic acid (c-CA) as a novel and unique addition to a small group of endogenous molecules affecting in planta auxin concentrations. c-CA is the photo-isomerization product of the phenylpropanoid pathway intermediate trans-CA (t-CA). When grown on c-CA-containing medium, an evolutionary diverse set of plant species were shown to exhibit phenotypes characteristic for high auxin levels, including inhibition of primary root growth, induction of root hairs, and promotion of adventitious and lateral rooting. By molecular docking and receptor binding assays, we showed that c-CA itself is neither an auxin nor an anti-auxin, and auxin profiling data revealed that c-CA does not significantly interfere with auxin biosynthesis. Single cell-based auxin accumulation assays showed that c-CA, and not t-CA, is a potent inhibitor of auxin efflux. Auxin signaling reporters detected changes in spatiotemporal distribution of the auxin response along the root of c-CA-treated plants, and long-distance auxin transport assays showed no inhibition of rootward auxin transport. Overall, these results suggest that the phenotypes of c-CA-treated plants are the consequence of a local change in auxin accumulation, induced by the inhibition of auxin efflux. This work reveals a novel mechanism how plants may regulate auxin levels and adds a novel, naturally occurring molecule to the chemical toolbox for the studies of auxin homeostasis.

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$a Steenackers, Ward $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a cis-Cinnamic Acid Is a Novel, Natural Auxin Efflux Inhibitor That Promotes Lateral Root Formation / $c W. Steenackers, P. Klíma, M. Quareshy, I. Cesarino, RP. Kumpf, S. Corneillie, P. Araújo, T. Viaene, G. Goeminne, MK. Nowack, K. Ljung, J. Friml, JJ. Blakeslee, O. Novák, E. Zažímalová, R. Napier, W. Boerjan, B. Vanholme,
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$a Auxin steers numerous physiological processes in plants, making the tight control of its endogenous levels and spatiotemporal distribution a necessity. This regulation is achieved by different mechanisms, including auxin biosynthesis, metabolic conversions, degradation, and transport. Here, we introduce cis-cinnamic acid (c-CA) as a novel and unique addition to a small group of endogenous molecules affecting in planta auxin concentrations. c-CA is the photo-isomerization product of the phenylpropanoid pathway intermediate trans-CA (t-CA). When grown on c-CA-containing medium, an evolutionary diverse set of plant species were shown to exhibit phenotypes characteristic for high auxin levels, including inhibition of primary root growth, induction of root hairs, and promotion of adventitious and lateral rooting. By molecular docking and receptor binding assays, we showed that c-CA itself is neither an auxin nor an anti-auxin, and auxin profiling data revealed that c-CA does not significantly interfere with auxin biosynthesis. Single cell-based auxin accumulation assays showed that c-CA, and not t-CA, is a potent inhibitor of auxin efflux. Auxin signaling reporters detected changes in spatiotemporal distribution of the auxin response along the root of c-CA-treated plants, and long-distance auxin transport assays showed no inhibition of rootward auxin transport. Overall, these results suggest that the phenotypes of c-CA-treated plants are the consequence of a local change in auxin accumulation, induced by the inhibition of auxin efflux. This work reveals a novel mechanism how plants may regulate auxin levels and adds a novel, naturally occurring molecule to the chemical toolbox for the studies of auxin homeostasis.
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$a Klíma, Petr $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Quareshy, Mussa $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a Cesarino, Igor $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden (K.L., O.N.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany CAS and Faculty of Science of Palacký University, CZ-78371 Olomouc, Czech Republic (O.N.).
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$a Kumpf, Robert P $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Araújo, Pedro $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Viaene, Tom $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Nowack, Moritz K $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Friml, Jiří $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Blakeslee, Joshua J $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.).
700    1_
$a Novák, Ondřej $u Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.). Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.). School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.). Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.). 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.). Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.). Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. 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.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Laboratory 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, 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.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium (W.S., I.C., R.P.K., S.C., P.A., T.V., G.G., M.K.N., W.B., B.V.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Institute of Experimental Botany, Czech Academy of Sciences, CZ-16502 Prague, Czech Republic (P.K., E.Z.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.Q., R.N.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Department of Botany, Institute of Biosciences, University of São Paulo, Butantã, São Paulo 03178-200, Brazil (I.C.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. 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.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Institute of Science and Technology, Austria, 3400 Klosterneuburg, Austria (J.F.); bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Department of Horticulture and Crop Science, The Ohio State University/Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (J.J.B.); and bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be. Laboratory 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, CZ-78371 Olomouc, Czech Republic (O.N.) bartel.vanholme@psb.vib-ugent.be wout.boerjan@psb.vib-ugent.be.
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