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      The plant hormone ethylene restricts Arabidopsis growth via the epidermis

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          Significance

          Ethylene is a gaseous hormone that controls plant life throughout development. Being a simple hydrophobic molecule, it can freely enter cells; therefore, the cell type specificity of its action is challenging. By means of tissue-specific expression of two negative regulators of the signaling cascade, we selectively disrupted the ethylene signal in different cell types without affecting its biosynthesis. We demonstrate that ethylene restricts plant growth by dampening the effect of auxins in the outermost cell layer. We further show that this epidermis-specific signaling has an impact on the growth of neighboring cells, suggesting that the master controller of cell expansion resides in the epidermis, where it senses the environment and, subsequently drives growth, of the inner tissues.

          Abstract

          The gaseous hormone ethylene plays a key role in plant growth and development, and it is a major regulator of stress responses. It inhibits vegetative growth by restricting cell elongation, mainly through cross-talk with auxins. However, it remains unknown whether ethylene controls growth throughout all plant tissues or whether its signaling is confined to specific cell types. We employed a targeted expression approach to map the tissue site(s) of ethylene growth regulation. The ubiquitin E3 ligase complex containing Skp1, Cullin1, and the F-box protein EBF1 or EBF2 (SCF EBF1/2) target the degradation of EIN3, the master transcription factor in ethylene signaling. We coupled EBF1 and EBF2 to a number of cell type-specific promoters. Using phenotypic assays for ethylene response and mutant complementation, we revealed that the epidermis is the main site of ethylene action controlling plant growth in both roots and shoots. Suppression of ethylene signaling in the epidermis of the constitutive ethylene signaling mutant ctr1-1 was sufficient to rescue the mutant phenotype, pointing to the epidermis as a key cell type required for ethylene-mediated growth inhibition.

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          Most cited references64

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          Ethylene Biosynthesis and its Regulation in Higher Plants

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            A high-resolution root spatiotemporal map reveals dominant expression patterns.

            Transcriptional programs that regulate development are exquisitely controlled in space and time. Elucidating these programs that underlie development is essential to understanding the acquisition of cell and tissue identity. We present microarray expression profiles of a high-resolution set of developmental time points within a single Arabidopsis root and a comprehensive map of nearly all root cell types. These cell type-specific transcriptional signatures often predict previously unknown cellular functions. A computational pipeline identified dominant expression patterns that demonstrate transcriptional similarity between disparate cell types. Dominant expression patterns along the root's longitudinal axis do not strictly correlate with previously defined developmental zones, and in many cases, we observed expression fluctuation along this axis. Both robust co-regulation of gene expression and potential phasing of gene expression were identified between individual roots. Methods that combine these profiles demonstrate transcriptionally rich and complex programs that define Arabidopsis root development in both space and time.
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              CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.

              We isolated a recessive Arabidopsis mutant, ctr1, that constitutively exhibits seedling and adult phenotypes observed in plants treated with the plant hormone ethylene. The ctr1 adult morphology can be phenocopied by treatment of wild-type plants with exogenous ethylene and is due, at least in part, to inhibition of cell elongation. Seedlings and adult ctr1 plants show constitutive expression of ethylene-regulated genes. The epistasis of ctr1 and other ethylene response mutants has defined the position of CTR1 in the ethylene signal transduction pathway. The CTR1 gene has been cloned, and the DNA sequences of four mutant alleles were determined. The gene encodes a putative serine/threonine protein kinase that is most closely related to the Raf protein kinase family.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                24 April 2018
                11 April 2018
                11 April 2018
                : 115
                : 17
                : E4130-E4139
                Affiliations
                [1] aLaboratory of Functional Plant Biology, Department of Biology, Ghent University , B-9000 Ghent, Belgium;
                [2] bInstitut de Biologie Moléculaire des Plantes du CNRS , IBMP-CNRS-Unité Propre de Recherche 2357, Strasbourg, France
                Author notes
                4To whom correspondence should be addressed. Email: dominique.vanderstraeten@ 123456ugent.be .

                Edited by James J. Giovannoni, USDA-ARS Robert W. Holley Center and Boyce Thompson Institute for Plant Research, Ithaca, NY, and approved March 19, 2018 (received for review October 9, 2017)

                Author contributions: I.I.V., T.P., P.G., F.V., and D.V.D.S. designed research; I.I.V., E.Q., T.P., Y.D., and F.V. performed research; I.I.V., E.Q., T.P., Y.D., P.G., F.V., and D.V.D.S. analyzed data; I.I.V. and D.V.D.S. wrote the paper; and D.V.D.S. conceived and coordinated the project.

                1Present address: Institute of Plant Physiology and Genetics, Laboratory Regulation of Gene Expression, Bulgarian Academy of Sciences, Sofia 1113, Bulgaria.

                2Present address: Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates.

                3Present address: State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming 650201, China.

                Author information
                http://orcid.org/0000-0002-7755-1420
                Article
                201717649
                10.1073/pnas.1717649115
                5924893
                29643073
                db241e14-7601-433d-a272-2e8dbaf17ea0
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: Fonds Wetenschappelijk Onderzoek (FWO) 501100003130
                Award ID: G.0298.09
                Funded by: Fonds Wetenschappelijk Onderzoek (FWO) 501100003130
                Award ID: G.0656.13N
                Funded by: Universiteit Gent (UGent) 501100004385
                Award ID: BOF-BAS 01B02112
                Funded by: Agence Nationale de la Recherche (ANR) 501100001665
                Award ID: LABEX: ANR-10-LABX-0036_NETRNA
                Categories
                PNAS Plus
                Biological Sciences
                Plant Biology
                PNAS Plus

                ethylene,auxin,ein3 binding f-box factor ebf,root/shoot,arabidopsis

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