title: Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest.
abstract: Despite its relevance for agricultural production, environmental stress-induced growth inhibition, which is responsible for significant yield reductions, is only poorly understood. Here, we investigated the molecular mechanisms underlying cell cycle inhibition in young proliferating leaves of the model plant Arabidopsis thaliana when subjected to mild osmotic stress. A detailed cellular analysis demonstrated that as soon as osmotic stress is sensed, cell cycle progression rapidly arrests, but cells are kept in a latent ambivalent state allowing a quick recovery (pause). Remarkably, cell cycle arrest coincides with an increase in 1-aminocyclopropane-1-carboxylate levels and the activation of ethylene signaling. Our work showed that ethylene acts on cell cycle progression via inhibition of cyclin-dependent kinase A activity independently of EIN3 transcriptional control. When the stress persists, cells exit the mitotic cell cycle and initiate the differentiation process (stop). This stop is reflected by early endoreduplication onset, in a process independent of ethylene. Nonetheless, the potential to partially recover the decreased cell numbers remains due to the activity of meristemoids. Together, these data present a conceptual framework to understand how environmental stress reduces plant growth.
authors.affiliation: Department of Plant Systems Biology, VIB, 9052 Ghent, Belgium.
authors.forename: Aleksandra
authors.initials: A
authors.lastname: Skirycz
authors.forename: Hannes
authors.initials: H
authors.lastname: Claeys
authors.forename: Stefanie
authors.initials: S
authors.lastname: De Bodt
authors.forename: Akira
authors.initials: A
authors.lastname: Oikawa
authors.forename: Shoko
authors.initials: S
authors.lastname: Shinoda
authors.forename: Megan
authors.initials: M
authors.lastname: Andriankaja
authors.forename: Katrien
authors.initials: K
authors.lastname: Maleux
authors.forename: Nubia Barbosa
authors.initials: NB
authors.lastname: Eloy
authors.forename: Frederik
authors.initials: F
authors.lastname: Coppens
authors.forename: Sang-Dong
authors.initials: SD
authors.lastname: Yoo
authors.forename: Kazuki
authors.initials: K
authors.lastname: Saito
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 / Q000187:drug effects / Q000502:physiology*; D049109:Cell Proliferation; D018844:Cyclin-Dependent Kinases / Q000037:antagonists & inhibitors / Q000378:metabolism*; D005030:Ethylenes / Q000494:pharmacology*; D018506:Gene Expression Regulation, Plant; D020411:Oligonucleotide Array Sequence Analysis; D009995:Osmosis; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D018520:Plant Shoots / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D030821:Plants, Genetically Modified / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D015398:Signal Transduction / Q000502:physiology*; D013312:Stress, Physiological; D013997:Time Factors; D059467:Transcriptome
chemical_list: D000598:Amino Acids, Cyclic; D029681:Arabidopsis Proteins; D005030:Ethylenes; C023863:1-aminocyclopropane-1-carboxylic acid; C036216:ethylene; D018844:Cyclin-Dependent Kinases