title: Ethylene Response Factor6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis.
abstract: Leaf growth is a complex developmental process that is continuously fine-tuned by the environment. Various abiotic stresses, including mild drought stress, have been shown to inhibit leaf growth in Arabidopsis (Arabidopsis thaliana), but the underlying mechanisms remain largely unknown. Here, we identify the redundant Arabidopsis transcription factors ETHYLENE RESPONSE FACTOR5 (ERF5) and ERF6 as master regulators that adapt leaf growth to environmental changes. ERF5 and ERF6 gene expression is induced very rapidly and specifically in actively growing leaves after sudden exposure to osmotic stress that mimics mild drought. Subsequently, enhanced ERF6 expression inhibits cell proliferation and leaf growth by a process involving gibberellin and DELLA signaling. Using an ERF6-inducible overexpression line, we demonstrate that the gibberellin-degrading enzyme GIBBERELLIN 2-OXIDASE6 is transcriptionally induced by ERF6 and that, consequently, DELLA proteins are stabilized. As a result, ERF6 gain-of-function lines are dwarfed and hypersensitive to osmotic stress, while the growth of erf5erf6 loss-of-function mutants is less affected by stress. Besides its role in plant growth under stress, ERF6 also activates the expression of a plethora of osmotic stress-responsive genes, including the well-known stress tolerance genes STZ, MYB51, and WRKY33. Interestingly, activation of the stress tolerance genes by ERF6 occurs independently from the ERF6-mediated growth inhibition. Together, these data fit into a leaf growth regulatory model in which ERF5 and ERF6 form a missing link between the previously observed stress-induced 1-aminocyclopropane-1-carboxylic acid accumulation and DELLA-mediated cell cycle exit and execute a dual role by regulating both stress tolerance and growth inhibition.
authors.affiliation: Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium.
authors.forename: Marieke
authors.initials: M
authors.lastname: Dubois
authors.forename: Aleksandra
authors.initials: A
authors.lastname: Skirycz
authors.forename: Hannes
authors.initials: H
authors.lastname: Claeys
authors.forename: Katrien
authors.initials: K
authors.lastname: Maleux
authors.forename: Stijn
authors.initials: S
authors.lastname: Dhondt
authors.forename: Stefanie
authors.initials: S
authors.lastname: De Bodt
authors.forename: Robin
authors.initials: R
authors.lastname: Vanden Bossche
authors.forename: Liesbeth
authors.initials: L
authors.lastname: De Milde
authors.forename: Takeshi
authors.initials: T
authors.lastname: Yoshizumi
authors.forename: Minami
authors.initials: M
authors.lastname: Matsui
authors.forename: Dirk
authors.initials: D
authors.lastname: Inzé
mesh_terms: D000598:Amino Acids, Cyclic / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development / Q000502:physiology; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D002453:Cell Cycle; D002455:Cell Division; D055864:Droughts; D005030:Ethylenes / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D018745:Genome, Plant / Q000235:genetics; D005875:Gibberellins / Q000378:metabolism; D005938:Glucocorticoids; D008954:Models, Biological; D020411:Oligonucleotide Array Sequence Analysis; D009997:Osmotic Pressure; D010937:Plant Growth Regulators / Q000378:metabolism*; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D030821:Plants, Genetically Modified; D015398:Signal Transduction; D013312:Stress, Physiological; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism; D014867:Water / Q000502:physiology*
chemical_list: C582788:AT5G47230 protein, Arabidopsis; D000598:Amino Acids, Cyclic; D029681:Arabidopsis Proteins; C582825:ERF6 protein, Arabidopsis; D005030:Ethylenes; D005875:Gibberellins; D005938:Glucocorticoids; D010937:Plant Growth Regulators; D014157:Transcription Factors; D014867:Water; C023863:1-aminocyclopropane-1-carboxylic acid; C036216:ethylene
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