Detecting and responding to environmental perturbations are important for all organisms. One of the most important distinguishing features of plants is that they are sessile and therefore must endure environmental challenges. We are interested in understanding the genetic and epigenetic basis of plant adaptation to ionic and osmotic imbalances. Through a genetic screen and subsequent molecular and biochemical analysis, we discovered a calcium signaling pathway in which the calcium-binding protein SOS3 interacts with and activates the protein kinase SOS2, which then activates the plasma membrane Na+/H+ antiporter SOS1 and other ion transporters by phosphorylation to achieve ion homeostasis under salt stress. In addition to ionic imbalance, hyperosmotic stress is another important aspect of salt stress. Recently, we found that a group of protein kinases (i.e., SnRK2s) related to the SOS2 subfamily of protein kinases (i.e., SnRK3s) are essential for the signaling of osmotic stress and the stress hormone abscisic acid (ABA). We elucidated the mechanism of SnRK2 activation in response to ABA and reconstituted in vitro the ABA signaling pathway leading from the PYR/PYL/ACAR family of soluble ABA receptors (PYLs) to the activation of SnRK2s;activation of SnRK2s leads to phosphorylation of transcription factors. We have exciting preliminary data suggesting that several PYLs are involved in osmosensing or upstream signaling to activate SnRK2s in an ABA- independent manner. We propose to build on this preliminary data in order to elucidate the mechanism of osmotic stress sensing and signaling. We will investigate the function of PYLs in osmosensing and osmotic stress activation of SnRK2 protein kinases. Other regulators of SnRK2s under osmotic stress will be identified from protein interaction screens. In a complementary approach, we will dissect osmotic stress signaling through genetic and chemical genetic screens facilitated by transgenic plants expressing the firefly luciferase reporter gene under the osmotic stress responsive NCED3 or RD29A promoter. Furthermore, we will capitalize on our expertise in both stress biology and epigenetics to explore the epigenetic basis of stress resistance and mechanisms of transgenerational epigenetic inheritance by genome- wide profiling of DNA methylation in stress-challenged plants and by testing the adaptability of cells from various mutants in the epigenetic pathways. The proposed work will continue to advance new concepts and bridge major gaps in the understanding of how eukaryotes adapt to challenging environments.

Public Health Relevance

Water and ion homeostasis are fundamental properties of all living cells, and malfunctions in these have been linked to many diseases in humans. Supported by NIH funding, we have discovered a signaling pathway for intracellular Na+ and K+ homeostasis in the model organism Arabidopsis thaliana in response to high salt conditions, and have elucidated a core pathway for the sensing and signaling of the phytohormone abscisic acid. The research proposed here will continue to generate exciting new knowledge on how multicellular eukaryotic organisms cope with environmental challenges.

National Institute of Health (NIH)
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Cellular Signaling and Regulatory Systems Study Section (CSRS)
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Reddy, Michael K
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Purdue University
Earth Sciences/Resources
West Lafayette
United States
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Qian, Weiqiang; Miki, Daisuke; Lei, Mingguang et al. (2014) Regulation of active DNA demethylation by an ?-crystallin domain protein in Arabidopsis. Mol Cell 55:361-71
Zhu, Xiaohong; Taylor, Aaron; Zhang, Shenyu et al. (2014) Measuring spatial and temporal Ca2+ signals in Arabidopsis plants. J Vis Exp :e51945
Shi, Haitao; Ye, Tiantian; Zhu, Jian-Kang et al. (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65:4119-31
Zhao, Yang; Xing, Lu; Wang, Xingang et al. (2014) The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Sci Signal 7:ra53
Yamamuro, Chizuko; Miki, Daisuke; Zheng, Zhimin et al. (2014) Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation. Nat Commun 5:4062
Zhang, Huiming; Tang, Kai; Qian, Weiqiang et al. (2014) An Rrp6-like protein positively regulates noncoding RNA levels and DNA methylation in Arabidopsis. Mol Cell 54:418-30
Lei, Mingguang; La, Honggui; Lu, Kun et al. (2014) Arabidopsis EDM2 promotes IBM1 distal polyadenylation and regulates genome DNA methylation patterns. Proc Natl Acad Sci U S A 111:527-32
Zhao, Yang; Chan, Zhulong; Xing, Lu et al. (2013) The unique mode of action of a divergent member of the ABA-receptor protein family in ABA and stress signaling. Cell Res 23:1380-95
Zhang, Huiming; Wang, Bangshing; Duan, Cheng-Guo et al. (2013) Chemical probes in plant epigenetics studies. Plant Signal Behav 8:
Bai, Ge; Yang, Da-Hai; Zhao, Yang et al. (2013) Interactions between soybean ABA receptors and type 2C protein phosphatases. Plant Mol Biol 83:651-64

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