title: Genetic Analysis of Physcomitrella patens Identifies ABSCISIC ACID NON-RESPONSIVE, a Regulator of ABA Responses Unique to Basal Land Plants and Required for Desiccation Tolerance.
abstract: The anatomically simple plants that first colonized land must have acquired molecular and biochemical adaptations to drought stress. Abscisic acid (ABA) coordinates responses leading to desiccation tolerance in all land plants. We identified ABA nonresponsive mutants in the model bryophyte Physcomitrella patens and genotyped a segregating population to map and identify the ABA NON-RESPONSIVE (ANR) gene encoding a modular protein kinase comprising an N-terminal PAS domain, a central EDR domain, and a C-terminal MAPKKK-like domain. anr mutants fail to accumulate dehydration tolerance-associated gene products in response to drought, ABA, or osmotic stress and do not acquire ABA-dependent desiccation tolerance. The crystal structure of the PAS domain, determined to 1.7-Å resolution, shows a conserved PAS-fold that dimerizes through a weak dimerization interface. Targeted mutagenesis of a conserved tryptophan residue within the PAS domain generates plants with ABA nonresponsive growth and strongly attenuated ABA-responsive gene expression, whereas deleting this domain retains a fully ABA-responsive phenotype. ANR orthologs are found in early-diverging land plant lineages and aquatic algae but are absent from more recently diverged vascular plants. We propose that ANR genes represent an ancestral adaptation that enabled drought stress survival of the first terrestrial colonizers but were lost during land plant evolution.
authors.affiliation: Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.
authors.forename: Sean R
authors.identifier: 0000-0001-5635-4340
authors.initials: SR
authors.lastname: Stevenson
authors.affiliation: Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.
authors.forename: Yasuko
authors.initials: Y
authors.lastname: Kamisugi
authors.affiliation: Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.
authors.forename: Chi H
authors.initials: CH
authors.lastname: Trinh
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, California 94598 HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806.
authors.forename: Jeremy
authors.initials: J
authors.lastname: Schmutz
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, California 94598 HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806.
authors.forename: Jerry W
authors.identifier: 0000-0002-8356-8325
authors.initials: JW
authors.lastname: Jenkins
authors.affiliation: Department of Energy Joint Genome Institute, Walnut Creek, California 94598 HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806.
authors.forename: Jane
authors.identifier: 0000-0003-0106-1289
authors.initials: J
authors.lastname: Grimwood
authors.affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.
authors.forename: Wellington
authors.initials: W
authors.lastname: Muchero
authors.affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.
authors.forename: Gerald A
authors.identifier: 0000-0003-0106-1289
authors.initials: GA
authors.lastname: Tuskan
authors.affiliation: University of Marburg, Plant Cell Biology, D-35043 Marburg, Germany BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79104 Freiburg, Germany.
authors.forename: Stefan A
authors.identifier: 0000-0002-0225-873X
authors.initials: SA
authors.lastname: Rensing
authors.affiliation: BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79104 Freiburg, Germany Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany.
authors.forename: Daniel
authors.identifier: 0000-0002-2166-0716
authors.initials: D
authors.lastname: Lang
authors.affiliation: BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79104 Freiburg, Germany Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany.
authors.forename: Ralf
authors.identifier: 0000-0002-5496-6711
authors.initials: R
authors.lastname: Reski
authors.affiliation: Botanisches Institut, D-50674 Köln, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Melkonian
authors.affiliation: Department of Integrative Biology, University of California, Berkeley California 94720-3140.
authors.forename: Carl J
authors.initials: CJ
authors.lastname: Rothfels
authors.affiliation: Department of Biology, Duke University, Durham, North Carolina 27708.
authors.forename: Fay-Wei
authors.initials: FW
authors.lastname: Li
authors.affiliation: Uppsala University, Systematic Biology, 752 36 Uppsala, Sweden.
authors.forename: Anders
authors.initials: A
authors.lastname: Larsson
authors.affiliation: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada Department of Medicine, University of Alberta, Edmonton, Alberta T6G 2E1, Canada BGI-Shenzhen, Shenzhen 518083, China.
authors.forename: Gane K-S
authors.identifier: 0000-0001-6108-5560
authors.initials: GK
authors.lastname: Wong
authors.affiliation: Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.
authors.forename: Thomas A
authors.initials: TA
authors.lastname: Edwards
authors.affiliation: Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom a.c.cuming@leeds.ac.uk.
authors.forename: Andrew C
authors.identifier: 0000-0003-2562-2052
authors.initials: AC
authors.lastname: Cuming
mesh_terms: D000040:Abscisic Acid / Q000494:pharmacology*; D019068:Bryopsida / Q000187:drug effects* / Q000235:genetics / Q000378:metabolism*; D018360:Crystallography, X-Ray; D003890:Desiccation; D055864:Droughts; D018506:Gene Expression Regulation, Plant / Q000187:drug effects / Q000235:genetics; D009154:Mutation; D009997:Osmotic Pressure; D010802:Phylogeny; D010940:Plant Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D017433:Protein Structure, Secondary
chemical_list: D010940:Plant Proteins; D000040:Abscisic Acid