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

Journal Article · Wed May 18 00:00:00 EDT 2016 · The Plant Cell

DOI:https://doi.org/10.1105/tpc.16.00091· OSTI ID:1737574

Stevenson, Sean Ross ^[1]; Kamisugi, Yasuko ^[1]; Trinh, Chi H. ^[1]; Schmutz, Jeremy ^[2]; Jenkins, Jerry W.  ^[2]; Grimwood, Jane  ^[2]; Muchero, Wellington ^[3]; Tuskan, Gerald A.  ^[3]; Rensing, Stefan A.  ^[4]; Lang, Daniel  ^[5]; Reski, Ralf  ^[5]; Melkonian, Michael ^[6]; Rothfels, Carl J. ^[7]; Li, Fay-Wei ^[8]; Larsson, Anders ^[9]; Wong, Gane Ka-Shu  ^[10]; Edwards, Thomas A. ^[1]; Cuming, Andrew C.  ^[1]

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1. Univ. of Leeds, Leeds (United Kingdom)
2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
4. Univ. of Marburg (Germany); Univ. of Freiburg (Germany)
5. Univ. of Freiburg (Germany)
6. Botanisches Inst., Koln (Germany)
7. Univ. of California, Berkeley, CA (United States)
8. Duke Univ., Durham, NC (United States)
9. Uppsala Univ. (Sweden)
10. Univ. of Alberta, Edmonton, AB (Canada); BGI-Shenzhen (China)

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. Lastly, 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.

• Research Organization: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
• Sponsoring Organization: USDOE Office of Science (SC), Biological and Environmental Research (BER); German Research Foundation (DFG); Biotechnology and Biological Sciences Research Council (BBSRC)
• Grant/Contract Number: AC02-05CH11231; RE 837/10-2; BB/F0017971/1; AC05-00OR22725
• OSTI ID: 1737574
• Alternate ID(s): OSTI ID: 1327711
• Journal Information: The Plant Cell, Vol. 28, Issue 6; ISSN 1040-4651
• Publisher: American Society of Plant Biologists
• Country of Publication: United States
• Language: English

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
abscisic acid
Physcomitrella patens
desiccation tolerance
MAP3
kinase
targeted mutagenesis
genetic mapping
land plant evolution