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

Sean R. Stevenson, Yasuko Kamisugi, Chi H. Trinh, Jeremy Schmutz, Jerry W. Jenkins, Jane Grimwood, Wellington Muchero, Gerald A. Tuskan, Stefan A. Rensing, Daniel Lang, Ralf Reski, Michael Melkonian, Carl J. Rothfels, Fay Wei Li, Anders Larsson, Gane K.S. Wong, Thomas A. Edwards, Andrew C. Cuming

Research output: Contribution to journalArticlepeer-review

87 Scopus citations

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.

Original languageEnglish
Pages (from-to)1310-1327
Number of pages18
JournalPlant Cell
Volume28
Issue number6
DOIs
StatePublished - Jun 2016

Funding

S.R.S. was supported by a Biotechnology and Biological Sciences Research Council (BBSRC) doctoral training grant to the University of Leeds Centre for Plant Sciences. A.C.C. and Y.K. gratefully acknowledge the receipt of BBSRC Research Grant BB/F0017971/1 to develop a P. patens forward genetics platform. The work conducted by the U.S. Department of Energy Joint Genome Institute (J.W.J., J.S., J.G., W.M., and G.A.T.) was supported by the Office of Science of the U.S. Department of Energy under Contract DE-AC02-05CH11231. S.A.R., D.L., and R.R. acknowledge funding from the Deutsche Forschungsgemeinschaft in the form of DFG Grant RE 837/10-2, and R.R. was supported by the Excellence Initiative of the German Federal and State Governments. The 1000 Plants (1KP) initiative, led by G.K.-S.W., is funded by the Alberta Ministry of Innovation and Advanced Education, Alberta Innovates Technology Futures (AITF), Innovates Centres of Research Excellence (iCORE), Musea Ventures, BGI-Shenzhen, and China National Genebank (CNGB). We thank Shengqiang Shu (Joint Genome Institute) for providing the cross-referencing between the V3.0, V3.1, and V3.3 P. patens locus IDs.

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