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Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating
Thursday, 2019/07/11 | 08:48:45

Koustav Maity, John M. Heumann, Aaron P. McGrath, Noah J. Kopcho, Po-Kai Hsu, Chang-Wook Lee, James H. Mapes, Denisse Garza, Srinivasan Krishnan, Garry P. Morgan, Kevin J. Hendargo, Thomas Klose, Steven D. Rees, Arturo Medrano-Soto, Milton H. Saier Jr., Miguel Piñeros, Elizabeth A. Komives, Julian I. Schroeder, Geoffrey Chang, and Michael H. B. Stowell

PNAS July 9, 2019 116 (28) 14309-14318

Significance

Environmental water deficiency and osmotic stress have been proposed to trigger the opening of osmolality-sensitive OSCA channels, leading to downstream signaling cascades necessary for abiotic stress resistance. We report the structural and functional analysis of OSCA1.2 from the crop plant rice. By combining biochemical, biophysical, and computational studies, we derive a model of how OSCA1.2 could mediate transport pathway gating under osmotic stress. Structure and functional analyses provide a molecular framework for studying proposed mechanosensing mechanisms in plants.

Abstract

Sensing and responding to environmental water deficiency and osmotic stresses are essential for the growth, development, and survival of plants. Recently, an osmolality-sensing ion channel called OSCA1 was discovered that functions in sensing hyperosmolality in Arabidopsis. Here, we report the cryo-electron microscopy (cryo-EM) structure and function of an OSCA1 homolog from rice (Oryza sativa; OsOSCA1.2), leading to a model of how it could mediate hyperosmolality sensing and transport pathway gating. The structure reveals a dimer; the molecular architecture of each subunit consists of 11 transmembrane (TM) helices and a cytosolic soluble domain that has homology to RNA recognition proteins. The TM domain is structurally related to the TMEM16 family of calcium-dependent ion channels and lipid scramblases. The cytosolic soluble domain possesses a distinct structural feature in the form of extended intracellular helical arms that are parallel to the plasma membrane. These helical arms are well positioned to potentially sense lateral tension on the inner leaflet of the lipid bilayer caused by changes in turgor pressure. Computational dynamic analysis suggests how this domain couples to the TM portion of the molecule to open a transport pathway. Hydrogen/deuterium exchange mass spectrometry (HDXMS) experimentally confirms the conformational dynamics of these coupled domains. These studies provide a framework to understand the structural basis of proposed hyperosmolality sensing in a staple crop plant, extend our knowledge of the anoctamin superfamily important for plants and fungi, and provide a structural mechanism for potentially translating membrane stress to transport regulation.

 

See https://www.pnas.org/content/116/28/14309

Figure 2: OsOSCA1.2 dimer interface and transport pathway. (A) OsOSCA1.2 surface representation. The TM domain is shown in gray, and the cytoplasmic domain is colored red and green. (B) View of OsOSCA1.2 from the cytoplasmic side. (C) Dimer interface residues. (D) Location of the predicted transport pathway in both subunits of OsOSCA1.2. The transport pathway is depicted as a cyan mesh. (E) Close-up view of the neck region, showing the residues “gating” the transport pathway.

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