Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating
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 inArabidopsis. In this paper, 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.more »
- Authors:
-
- Univ. of California, San Diego, La Jolla, CA (United States)
- Univ. of Colorado, Boulder, CO (United States)
- Cornell Univ., Ithaca, NY (United States)
- Purdue Univ., West Lafayette, IN (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Institute of General Medical Sciences (NIGMS); National Science Foundation (NSF)
- OSTI Identifier:
- 1600794
- Grant/Contract Number:
- U24 GM116789; GM060396
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 28; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; osmotic stress; channel; structure; cryo-EM; rice
Citation Formats
Maity, Koustav, Heumann, John M., McGrath, Aaron P., Kopcho, Noah J., Hsu, Po-Kai, Lee, Chang-Wook, Mapes, James H., Garza, Denisse, Krishnan, Srinivasan, Morgan, Garry P., Hendargo, Kevin J., Klose, Thomas, Rees, Steven D., Medrano-Soto, Arturo, Saier, Jr., Milton H., Piñeros, Miguel, Komives, Elizabeth A., Schroeder, Julian I., Chang, Geoffrey, and Stowell, Michael H. B. Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating. United States: N. p., 2019.
Web. doi:10.1073/pnas.1900774116.
Maity, Koustav, Heumann, John M., McGrath, Aaron P., Kopcho, Noah J., Hsu, Po-Kai, Lee, Chang-Wook, Mapes, James H., Garza, Denisse, Krishnan, Srinivasan, Morgan, Garry P., Hendargo, Kevin J., Klose, Thomas, Rees, Steven D., Medrano-Soto, Arturo, Saier, Jr., Milton H., Piñeros, Miguel, Komives, Elizabeth A., Schroeder, Julian I., Chang, Geoffrey, & Stowell, Michael H. B. Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating. United States. https://doi.org/10.1073/pnas.1900774116
Maity, Koustav, Heumann, John M., McGrath, Aaron P., Kopcho, Noah J., Hsu, Po-Kai, Lee, Chang-Wook, Mapes, James H., Garza, Denisse, Krishnan, Srinivasan, Morgan, Garry P., Hendargo, Kevin J., Klose, Thomas, Rees, Steven D., Medrano-Soto, Arturo, Saier, Jr., Milton H., Piñeros, Miguel, Komives, Elizabeth A., Schroeder, Julian I., Chang, Geoffrey, and Stowell, Michael H. B. 2019.
"Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating". United States. https://doi.org/10.1073/pnas.1900774116. https://www.osti.gov/servlets/purl/1600794.
@article{osti_1600794,
title = {Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating},
author = {Maity, Koustav and Heumann, John M. and McGrath, Aaron P. and Kopcho, Noah J. and Hsu, Po-Kai and Lee, Chang-Wook and Mapes, James H. and Garza, Denisse and Krishnan, Srinivasan and Morgan, Garry P. and Hendargo, Kevin J. and Klose, Thomas and Rees, Steven D. and Medrano-Soto, Arturo and Saier, Jr., Milton H. and Piñeros, Miguel and Komives, Elizabeth A. and Schroeder, Julian I. and Chang, Geoffrey and Stowell, Michael H. B.},
abstractNote = {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 inArabidopsis. In this paper, 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.},
doi = {10.1073/pnas.1900774116},
url = {https://www.osti.gov/biblio/1600794},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 28,
volume = 116,
place = {United States},
year = {Fri Jun 21 00:00:00 EDT 2019},
month = {Fri Jun 21 00:00:00 EDT 2019}
}
Web of Science
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Works referencing / citing this record:
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