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)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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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
Schools of Earth Sciences/Natur
West Lafayette
United States
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Zhao, Yang; Zhang, Zhengjing; Gao, Jinghui et al. (2018) Arabidopsis Duodecuple Mutant of PYL ABA Receptors Reveals PYL Repression of ABA-Independent SnRK2 Activity. Cell Rep 23:3340-3351.e5
Srivastava, Ashish Kumar; Lu, Yuming; Zinta, Gaurav et al. (2018) UTR-Dependent Control of Gene Expression in Plants. Trends Plant Sci 23:248-259
Wang, Pengcheng; Zhao, Yang; Li, Zhongpeng et al. (2018) Reciprocal Regulation of the TOR Kinase and ABA Receptor Balances Plant Growth and Stress Response. Mol Cell 69:100-112.e6
Zhang, Jinshan; Zhang, Hui; Botella, José Ramón et al. (2018) Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol 60:369-375
Yang, Yu; Wang, Wei; Chu, Zhaoqing et al. (2017) Roles of Nuclear Pores and Nucleo-cytoplasmic Trafficking in Plant Stress Responses. Front Plant Sci 8:574
Yang, Yu; La, Honggui; Tang, Kai et al. (2017) SAC3B, a central component of the mRNA export complex TREX-2, is required for prevention of epigenetic gene silencing in Arabidopsis. Nucleic Acids Res 45:181-197
Yan, Jun; Wang, Pengcheng; Wang, Bangshing et al. (2017) The SnRK2 kinases modulate miRNA accumulation in Arabidopsis. PLoS Genet 13:e1006753
Wang, Dong; Qu, Zhipeng; Yang, Lan et al. (2017) Transposable elements (TEs) contribute to stress-related long intergenic noncoding RNAs in plants. Plant J 90:133-146
Lang, Zhaobo; Wang, Yihai; Tang, Kai et al. (2017) Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc Natl Acad Sci U S A 114:E4511-E4519
Zhao, Chunzhao; Wang, Pengcheng; Si, Tong et al. (2017) MAP Kinase Cascades Regulate the Cold Response by Modulating ICE1 Protein Stability. Dev Cell 43:618-629.e5

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