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Title: 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 » 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.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [2];  [1];  [3];  [2];  [1]; ORCiD logo [4];  [1];  [1];  [1];  [3];  [1];  [1];  [1]; ORCiD logo [2]
+ Show Author Affiliations
  1. Univ. of California, San Diego, La Jolla, CA (United States)
  2. Univ. of Colorado, Boulder, CO (United States)
  3. Cornell Univ., Ithaca, NY (United States)
  4. 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:
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.
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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
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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. Fri . "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.
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@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},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
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}
}
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https://doi.org/10.1073/pnas.1900774116
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Works referenced in this record:

Cryo-EM structure of the mechanically activated ion channel OSCA1.2
journal, November 2018

  • Jojoa-Cruz, Sebastian; Saotome, Kei; Murthy, Swetha E.
  • eLife, Vol. 7
  • DOI: 10.7554/eLife.41845

OSCA/TMEM63 are an evolutionarily conserved family of mechanically activated ion channels
journal, November 2018

Screening Blockers Against a Potassium Channel with a Droplet Interface Bilayer Array
journal, November 2008

  • Syeda, Ruhma; Holden, Matthew A.; Hwang, William L.
  • Journal of the American Chemical Society, Vol. 130, Issue 46
  • DOI: 10.1021/ja804968g

Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments
journal, September 2006

  • Nour-Eldin, Hussam H.; Hansen, Bjarne G.; Nørholm, Morten H. H.
  • Nucleic Acids Research, Vol. 34, Issue 18
  • DOI: 10.1093/nar/gkl635

Piezo proteins are pore-forming subunits of mechanically activated channels
journal, February 2012

  • Coste, Bertrand; Xiao, Bailong; Santos, Jose S.
  • Nature, Vol. 483, Issue 7388
  • DOI: 10.1038/nature10812

The Transporter Classification Database (TCDB): recent advances
journal, November 2015

  • Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1103

X-ray structure of a calcium-activated TMEM16 lipid scramblase
journal, November 2014

  • Brunner, Janine D.; Lim, Novandy K.; Schenck, Stephan
  • Nature, Vol. 516, Issue 7530
  • DOI: 10.1038/nature13984

A Bayesian View on Cryo-EM Structure Determination
journal, January 2012

Conformational dynamics of P-glycoprotein in lipid nanodiscs and detergent micelles reveal complex motions on a wide time scale
journal, March 2018

  • Li, Mavis Jiarong; Guttman, Miklos; Atkins, William M.
  • Journal of Biological Chemistry, Vol. 293, Issue 17
  • DOI: 10.1074/jbc.RA118.002190

Constructing droplet interface bilayers from the contact of aqueous droplets in oil
journal, May 2013

  • Leptihn, Sebastian; Castell, Oliver K.; Cronin, Brid
  • Nature Protocols, Vol. 8, Issue 6
  • DOI: 10.1038/nprot.2013.061

OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis
journal, August 2014

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

EMRinger: side chain–directed model and map validation for 3D cryo-electron microscopy
journal, August 2015

  • Barad, Benjamin A.; Echols, Nathaniel; Wang, Ray Yu-Ruei
  • Nature Methods, Vol. 12, Issue 10
  • DOI: 10.1038/nmeth.3541

Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2
journal, November 2018

GEOCHEM-EZ: a chemical speciation program with greater power and flexibility
journal, October 2009

Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM
journal, December 2017

  • Paulino, Cristina; Kalienkova, Valeria; Lam, Andy K. M.
  • Nature, Vol. 552, Issue 7685
  • DOI: 10.1038/nature24652

Fiji: an open-source platform for biological-image analysis
journal, June 2012

  • Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2019

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

Structure of mammalian endolysosomal TRPML1 channel in nanodiscs
journal, October 2017

  • Chen, Qingfeng; She, Ji; Zeng, Weizhong
  • Nature, Vol. 550, Issue 7676
  • DOI: 10.1038/nature24035

Bioinformatic characterization of the Anoctamin Superfamily of Ca2+-activated ion channels and lipid scramblases
journal, March 2018

Calcium signalling in Arabidopsis thaliana responding to drought and salinity
journal, November 1997

Cryo-EM structures of the TMEM16A calcium-activated chloride channel
journal, December 2017

  • Dang, Shangyu; Feng, Shengjie; Tien, Jason
  • Nature, Vol. 552, Issue 7685
  • DOI: 10.1038/nature25024

DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes
journal, February 2014

  • Hou, Congcong; Tian, Wang; Kleist, Thomas
  • Cell Research, Vol. 24, Issue 5
  • DOI: 10.1038/cr.2014.14

Static light scattering to characterize membrane proteins in detergent solution
journal, October 2008

Hydrogen exchange mass spectrometry for the analysis of protein dynamics
journal, January 2005

  • Wales, Thomas E.; Engen, John R.
  • Mass Spectrometry Reviews, Vol. 25, Issue 1
  • DOI: 10.1002/mas.20064

Solvent accessibility of protein surfaces by amide H/2H exchange MALDI-TOF mass spectrometry
journal, November 2006

  • Truhlar, Stephanie M. E.; Croy, Carrie H.; Torpey, Justin W.
  • Journal of the American Society for Mass Spectrometry, Vol. 17, Issue 11
  • DOI: 10.1016/j.jasms.2006.07.023

Asymmetric Droplet Interface Bilayers
journal, May 2008

  • Hwang, William L.; Chen, Min; Cronin, Bríd
  • Journal of the American Chemical Society, Vol. 130, Issue 18
  • DOI: 10.1021/ja802089s

Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007

Membrane Topology and Predicted RNA-Binding Function of the ‘Early Responsive to Dehydration (ERD4)’ Plant Protein
journal, March 2012

A novel method for structure-based prediction of ion channel conductance properties
journal, March 1997

cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
journal, February 2017

  • Punjani, Ali; Rubinstein, John L.; Fleet, David J.
  • Nature Methods, Vol. 14, Issue 3
  • DOI: 10.1038/nmeth.4169

Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants
journal, March 2014

  • Choi, W. -G.; Toyota, M.; Kim, S. -H.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1319955111

Structure of the mechanosensitive OSCA channels
journal, September 2018

  • Zhang, Mingfeng; Wang, Dali; Kang, Yunlu
  • Nature Structural & Molecular Biology, Vol. 25, Issue 9
  • DOI: 10.1038/s41594-018-0117-6

Rapid hyperosmotic-induced Ca 2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters
journal, August 2016

  • Stephan, Aaron B.; Kunz, Hans-Henning; Yang, Eric
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 35
  • DOI: 10.1073/pnas.1519555113

Quantifying the local resolution of cryo-EM density maps
journal, November 2013

  • Kucukelbir, Alp; Sigworth, Fred J.; Tagare, Hemant D.
  • Nature Methods, Vol. 11, Issue 1
  • DOI: 10.1038/nmeth.2727

The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter
journal, January 2009

  • Mulligan, Christopher; Geertsma, Eric R.; Severi, Emmanuele
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 6
  • DOI: 10.1073/pnas.0809979106

Gctf: Real-time CTF determination and correction
journal, January 2016

A new generation of Ca2+ indicators with greatly improved fluorescence properties.
journal, March 1985

PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019

Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021

Insights on autophagosome–lysosome tethering from structural and biochemical characterization of human autophagy factor EPG5
journal, March 2021

  • Nam, Sung-Eun; Cheung, Yiu Wing Sunny; Nguyen, Thanh Ngoc
  • Communications Biology, Vol. 4, Issue 1
  • DOI: 10.1038/s42003-021-01830-x

X-ray structure of a calcium-activated TMEM16 lipid scramblase
text, January 2014

  • Brunner, Janine D.; Lim, Novandy K.; Schenck, Stephan
  • Nature Publishing Group
  • DOI: 10.5167/uzh-103990

A Bayesian view on cryo-EM structure determination
conference, May 2012

  • Scheres, Sjors H. W.
  • 2012 IEEE 9th International Symposium on Biomedical Imaging (ISBI 2012), 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI)
  • DOI: 10.1109/isbi.2012.6235807

PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.45787

Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM
text, January 2017

  • Paulino, Cristina; Kalienkova, Valeria; Lam, Andy K. M.
  • Nature Publishing Group
  • DOI: 10.5167/uzh-144591
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