title: Ethylene-Mediated Regulation of A2-Type CYCLINs Modulates Hyponastic Growth in Arabidopsis.
abstract: Upward leaf movement (hyponastic growth) is frequently observed in response to changing environmental conditions and can be induced by the phytohormone ethylene. Hyponasty results from differential growth (i.e. enhanced cell elongation at the proximal abaxial side of the petiole relative to the adaxial side). Here, we characterize Enhanced Hyponasty-d, an activation-tagged Arabidopsis (Arabidopsis thaliana) line with exaggerated hyponasty. This phenotype is associated with overexpression of the mitotic cyclin CYCLINA2;1 (CYCA2;1), which hints at a role for cell divisions in regulating hyponasty. Indeed, mathematical analysis suggested that the observed changes in abaxial cell elongation rates during ethylene treatment should result in a larger hyponastic amplitude than observed, unless a decrease in cell proliferation rate at the proximal abaxial side of the petiole relative to the adaxial side was implemented. Our model predicts that when this differential proliferation mechanism is disrupted by either ectopic overexpression or mutation of CYCA2;1, the hyponastic growth response becomes exaggerated. This is in accordance with experimental observations on CYCA2;1 overexpression lines and cyca2;1 knockouts. We therefore propose a bipartite mechanism controlling leaf movement: ethylene induces longitudinal cell expansion in the abaxial petiole epidermis to induce hyponasty and simultaneously affects its amplitude by controlling cell proliferation through CYCA2;1. Further corroborating the model, we found that ethylene treatment results in transcriptional down-regulation of A2-type CYCLINs and propose that this, and possibly other regulatory mechanisms affecting CYCA2;1, may contribute to this attenuation of hyponastic growth.
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Joanna K
authors.initials: JK
authors.lastname: Polko
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Jop A
authors.initials: JA
authors.lastname: van Rooij
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Steffen
authors.initials: S
authors.lastname: Vanneste
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Ronald
authors.initials: R
authors.lastname: Pierik
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Ankie M H
authors.initials: AM
authors.lastname: Ammerlaan
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Marleen H
authors.initials: MH
authors.lastname: Vergeer-van Eijk
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Fionn
authors.initials: F
authors.lastname: McLoughlin
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Kerstin
authors.initials: K
authors.lastname: Gühl
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Gert
authors.initials: G
authors.lastname: Van Isterdael
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Laurentius A C J
authors.initials: LA
authors.lastname: Voesenek
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Frank F
authors.initials: FF
authors.lastname: Millenaar
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Tom
authors.initials: T
authors.lastname: Beeckman
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Anton J M
authors.initials: AJ
authors.lastname: Peeters
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.).
authors.forename: Athanasius F M
authors.initials: AF
authors.lastname: Marée
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology (J.K.P., R.P., A.M.H.A., M.H.V.-v.E., F.M., K.G., L.A.C.J.V., F.F.M., A.J.M.P., M.v.Z.), and Theoretical Biology and Bioinformatics (J.A.v.R.), Utrecht University, 3584 CH Utrecht, The Netherlands;Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.A.v.R., A.F.M.M.);Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium (S.V., G.V.I., T.B.) m.vanzanten@uu.nl.
authors.forename: Martijn
authors.initials: M
authors.lastname: van Zanten
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000502:physiology* / Q000528:radiation effects; D049109:Cell Proliferation; D056751:Cyclin A2 / Q000235:genetics / Q000378:metabolism*; D015536:Down-Regulation; D005030:Ethylenes / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D018546:Hypocotyl / Q000235:genetics / Q000254:growth & development / Q000502:physiology / Q000528:radiation effects; D008027:Light; D008954:Models, Biological; D010937:Plant Growth Regulators / Q000378:metabolism*; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000502:physiology / Q000528:radiation effects
chemical_list: D056751:Cyclin A2; D005030:Ethylenes; D010937:Plant Growth Regulators; C036216:ethylene