Genetic analysis of Physcomitrella patens identifies ABSCISIC ACID NON-RESPONSIVE (ANR), a regulator of ABA responses unique to basal land plants and required for desiccation tolerance

DOI: 10.1105/tpc.16.00091

Authors: Sean Ross Stevenson (Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds) , Yasuko Kamisugi (Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds) , Chi H. Hung Trinh (Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds) , Jeremy Schmutz (Department of Energy Joint Genome Institute; Biosciences Division, Oak Ridge National Laboratory) , Jerry W. Jenkins (Department of Energy Joint Genome Institute; Biosciences Division, Oak Ridge National Laboratory) , Jane Grimwood (Department of Energy Joint Genome Institute; Biosciences Division, Oak Ridge National Laborator) , Wellington Muchero (Biosciences Division, Oak Ridge National Laboratory) , Gerald A Tuskan (Biosciences Division, Oak Ridge National Laboratory) , Stefan A Rensing (University of Marburg; University of Freiburg) , Daniel Lang (University of Freiburg;) , Ralf Reski (University of Freiburg) , Michael Melkonian (Botanisches Institut) , Carl J. Rothfels (Department of Integrative Biology) , Fay-wei Li (Duke University) , Anders Larsson (Uppsala University) , Gane Ka-shu Wong (University of Alberta; BGI-Shenzhen) , Thomas A. Edwards (University of Leeds) , Andrew C. Cuming (Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds)
Co-authored by industrial partner: No

Type: Journal Paper
Journal: The Plant Cell

State: Published (Approved)
Published: May 2016
Diamond Proposal Number(s): 10305

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.

Subject Areas: Biology and Bio-materials


Instruments: I24-Microfocus Macromolecular Crystallography

Documents:
tpc.16.00091.full.pdf

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