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.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM059138-17
Application #
8466981
Study Section
Cellular Signaling and Regulatory Systems Study Section (CSRS)
Program Officer
Reddy, Michael K
Project Start
1999-05-01
Project End
2016-06-30
Budget Start
2013-07-01
Budget End
2014-06-30
Support Year
17
Fiscal Year
2013
Total Cost
$323,227
Indirect Cost
$113,339
Name
Purdue University
Department
Miscellaneous
Type
Schools of Earth Sciences/Natur
DUNS #
072051394
City
West Lafayette
State
IN
Country
United States
Zip Code
47907
Zhang, Qingzhu; Li, Yanqiang; Xu, Tao et al. (2016) The chromatin remodeler DDM1 promotes hybrid vigor by regulating salicylic acid metabolism. Cell Discov 2:16027
Hou, Yueh-Ju; Zhu, Yingfang; Wang, Pengcheng et al. (2016) Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling. PLoS Genet 12:e1005835
Zhao, Yang; Chan, Zhulong; Gao, Jinghui et al. (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci U S A 113:1949-54
Xing, Lu; Zhao, Yang; Gao, Jinghui et al. (2016) The ABA receptor PYL9 together with PYL8 plays an important role in regulating lateral root growth. Sci Rep 6:27177
Wang, Pengcheng; Zhu, Jian-Kang (2016) Assessing Kinase Activity in Plants with In-Gel Kinase Assays. Methods Mol Biol 1363:189-97
Zhu, Jian-Kang (2016) Abiotic Stress Signaling and Responses in Plants. Cell 167:313-324
Zhang, Qingzhu; Wang, Dong; Lang, Zhaobo et al. (2016) Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation. Proc Natl Acad Sci U S A 113:E4248-56
Yamamuro, Chizuko; Zhu, Jian-Kang; Yang, Zhenbiao (2016) Epigenetic Modifications and Plant Hormone Action. Mol Plant 9:57-70
Chan, Zhulong; Wang, Yanping; Cao, Minjie et al. (2016) RDM4 modulates cold stress resistance in Arabidopsis partially through the CBF-mediated pathway. New Phytol 209:1527-39
Zhan, Xiangqiang; Qian, Bilian; Cao, Fengqiu et al. (2015) An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and ABA responses. Nat Commun 6:8139

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