Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating

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.

doi:10.1073/pnas.1900774116

Title: Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating

Journal Article · Fri Jun 21 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1900774116· OSTI ID:1600794

Maity, Koustav ^[1]; Heumann, John M. ^[2]; McGrath, Aaron P. ^[1]; Kopcho, Noah J. ^[1]; Hsu, Po-Kai ^[1]; Lee, Chang-Wook ^[1]; Mapes, James H. ^[2]; Garza, Denisse ^[1]; Krishnan, Srinivasan ^[3]; Morgan, Garry P. ^[2]; Hendargo, Kevin J. ^[1];

^[4]; Rees, Steven D. ^[1]; Medrano-Soto, Arturo ^[1]; Saier, Jr., Milton H. ^[1]; Piñeros, Miguel ^[3]; Komives, Elizabeth A. ^[1]; Schroeder, Julian I. ^[1]; Chang, Geoffrey ^[1];

^[2]

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)

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institute of General Medical Sciences (NIGMS); National Science Foundation (NSF)

Grant/Contract Number:: U24 GM116789; GM060396

OSTI ID:: 1600794

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, Issue 28; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 39 works

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References (46)

Cryo-EM structure of the mechanically activated ion channel OSCA1.2 Jojoa-Cruz, Sebastian; Saotome, Kei; Murthy, Swetha E. eLife, Vol. 7 https://doi.org/10.7554/eLife.41845	journal	November 2018
OSCA/TMEM63 are an evolutionarily conserved family of mechanically activated ion channels Murthy, Swetha E.; Dubin, Adrienne E.; Whitwam, Tess eLife, Vol. 7 https://doi.org/10.7554/eLife.41844	journal	November 2018
Screening Blockers Against a Potassium Channel with a Droplet Interface Bilayer Array Syeda, Ruhma; Holden, Matthew A.; Hwang, William L. Journal of the American Chemical Society, Vol. 130, Issue 46 https://doi.org/10.1021/ja804968g	journal	November 2008
Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments Nour-Eldin, Hussam H.; Hansen, Bjarne G.; Nørholm, Morten H. H. Nucleic Acids Research, Vol. 34, Issue 18 https://doi.org/10.1093/nar/gkl635	journal	September 2006
Piezo proteins are pore-forming subunits of mechanically activated channels Coste, Bertrand; Xiao, Bailong; Santos, Jose S. Nature, Vol. 483, Issue 7388 https://doi.org/10.1038/nature10812	journal	February 2012
The Transporter Classification Database (TCDB): recent advances Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1103	journal	November 2015
X-ray structure of a calcium-activated TMEM16 lipid scramblase Brunner, Janine D.; Lim, Novandy K.; Schenck, Stephan Nature, Vol. 516, Issue 7530 https://doi.org/10.1038/nature13984	journal	November 2014
A Bayesian View on Cryo-EM Structure Determination Scheres, Sjors H. W. Journal of Molecular Biology, Vol. 415, Issue 2 https://doi.org/10.1016/j.jmb.2011.11.010	journal	January 2012
Conformational dynamics of P-glycoprotein in lipid nanodiscs and detergent micelles reveal complex motions on a wide time scale Li, Mavis Jiarong; Guttman, Miklos; Atkins, William M. Journal of Biological Chemistry, Vol. 293, Issue 17 https://doi.org/10.1074/jbc.RA118.002190	journal	March 2018
Constructing droplet interface bilayers from the contact of aqueous droplets in oil Leptihn, Sebastian; Castell, Oliver K.; Cronin, Brid Nature Protocols, Vol. 8, Issue 6 https://doi.org/10.1038/nprot.2013.061	journal	May 2013
OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis Yuan, Fang; Yang, Huimin; Xue, Yan Nature, Vol. 514, Issue 7522 https://doi.org/10.1038/nature13593	journal	August 2014
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
EMRinger: side chain–directed model and map validation for 3D cryo-electron microscopy Barad, Benjamin A.; Echols, Nathaniel; Wang, Ray Yu-Ruei Nature Methods, Vol. 12, Issue 10 https://doi.org/10.1038/nmeth.3541	journal	August 2015
Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2 Liu, Xin; Wang, Jiawei; Sun, Linfeng Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07564-5	journal	November 2018
GEOCHEM-EZ: a chemical speciation program with greater power and flexibility Shaff, Jon E.; Schultz, Benjamin A.; Craft, Eric J. Plant and Soil, Vol. 330, Issue 1-2 https://doi.org/10.1007/s11104-009-0193-9	journal	October 2009
Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM Paulino, Cristina; Kalienkova, Valeria; Lam, Andy K. M. Nature, Vol. 552, Issue 7685 https://doi.org/10.1038/nature24652	journal	December 2017
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Structure of mammalian endolysosomal TRPML1 channel in nanodiscs Chen, Qingfeng; She, Ji; Zeng, Weizhong Nature, Vol. 550, Issue 7676 https://doi.org/10.1038/nature24035	journal	October 2017
Bioinformatic characterization of the Anoctamin Superfamily of Ca2+-activated ion channels and lipid scramblases Medrano-Soto, Arturo; Moreno-Hagelsieb, Gabriel; McLaughlin, Daniel PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0192851	journal	March 2018
Calcium signalling in Arabidopsis thaliana responding to drought and salinity Knight, Heather; Trewavas, Anthony J.; Knight, Marc R. The Plant Journal, Vol. 12, Issue 5 https://doi.org/10.1046/j.1365-313X.1997.12051067.x	journal	November 1997
Cryo-EM structures of the TMEM16A calcium-activated chloride channel Dang, Shangyu; Feng, Shengjie; Tien, Jason Nature, Vol. 552, Issue 7685 https://doi.org/10.1038/nature25024	journal	December 2017
DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes Hou, Congcong; Tian, Wang; Kleist, Thomas Cell Research, Vol. 24, Issue 5 https://doi.org/10.1038/cr.2014.14	journal	February 2014
Two-electrode Voltage-clamp Recordings in Xenopus laevis Oocytes：Reconstitution of Abscisic Acid Activation of SLAC1 Anion Channel via PYL9 ABA Receptor Wang, Cun; Zhang, Jingbo; Schroeder, Julian BIO-PROTOCOL, Vol. 7, Issue 2 https://doi.org/10.21769/BioProtoc.2114	journal	January 2017
Static light scattering to characterize membrane proteins in detergent solution Slotboom, Dirk Jan; Duurkens, Ria H.; Olieman, Kees Methods, Vol. 46, Issue 2 https://doi.org/10.1016/j.ymeth.2008.06.012	journal	October 2008
Hydrogen exchange mass spectrometry for the analysis of protein dynamics Wales, Thomas E.; Engen, John R. Mass Spectrometry Reviews, Vol. 25, Issue 1 https://doi.org/10.1002/mas.20064	journal	January 2005
Solvent accessibility of protein surfaces by amide H/2H exchange MALDI-TOF mass spectrometry Truhlar, Stephanie M. E.; Croy, Carrie H.; Torpey, Justin W. Journal of the American Society for Mass Spectrometry, Vol. 17, Issue 11 https://doi.org/10.1016/j.jasms.2006.07.023	journal	November 2006
Asymmetric Droplet Interface Bilayers Hwang, William L.; Chen, Min; Cronin, Bríd Journal of the American Chemical Society, Vol. 130, Issue 18 https://doi.org/10.1021/ja802089s	journal	May 2008
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Membrane Topology and Predicted RNA-Binding Function of the ‘Early Responsive to Dehydration (ERD4)’ Plant Protein Rai, Archana; Suprasanna, Penna; D'Souza, Stanislaus F. PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0032658	journal	March 2012
A novel method for structure-based prediction of ion channel conductance properties Smart, O. S.; Breed, J.; Smith, G. R. Biophysical Journal, Vol. 72, Issue 3 https://doi.org/10.1016/S0006-3495(97)78760-5	journal	March 1997
cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination Punjani, Ali; Rubinstein, John L.; Fleet, David J. Nature Methods, Vol. 14, Issue 3 https://doi.org/10.1038/nmeth.4169	journal	February 2017
Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants Choi, W. -G.; Toyota, M.; Kim, S. -H. Proceedings of the National Academy of Sciences, Vol. 111, Issue 17 https://doi.org/10.1073/pnas.1319955111	journal	March 2014
Structure of the mechanosensitive OSCA channels Zhang, Mingfeng; Wang, Dali; Kang, Yunlu Nature Structural & Molecular Biology, Vol. 25, Issue 9 https://doi.org/10.1038/s41594-018-0117-6	journal	September 2018
Rapid hyperosmotic-induced Ca ²⁺ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters Stephan, Aaron B.; Kunz, Hans-Henning; Yang, Eric Proceedings of the National Academy of Sciences, Vol. 113, Issue 35 https://doi.org/10.1073/pnas.1519555113	journal	August 2016
Quantifying the local resolution of cryo-EM density maps Kucukelbir, Alp; Sigworth, Fred J.; Tagare, Hemant D. Nature Methods, Vol. 11, Issue 1 https://doi.org/10.1038/nmeth.2727	journal	November 2013
The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter Mulligan, Christopher; Geertsma, Eric R.; Severi, Emmanuele Proceedings of the National Academy of Sciences, Vol. 106, Issue 6 https://doi.org/10.1073/pnas.0809979106	journal	January 2009
Gctf: Real-time CTF determination and correction Zhang, Kai Journal of Structural Biology, Vol. 193, Issue 1 https://doi.org/10.1016/j.jsb.2015.11.003	journal	January 2016
A new generation of Ca2+ indicators with greatly improved fluorescence properties. Grynkiewicz, G.; Poenie, M.; Tsien, R. Y. Journal of Biological Chemistry, Vol. 260, Issue 6 https://doi.org/10.1016/S0021-9258(19)83641-4	journal	March 1985
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Insights on autophagosome–lysosome tethering from structural and biochemical characterization of human autophagy factor EPG5 Nam, Sung-Eun; Cheung, Yiu Wing Sunny; Nguyen, Thanh Ngoc Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-01830-x	journal	March 2021
X-ray structure of a calcium-activated TMEM16 lipid scramblase Brunner, Janine D.; Lim, Novandy K.; Schenck, Stephan Nature Publishing Group https://doi.org/10.5167/uzh-103990	text	January 2014
A Bayesian view on cryo-EM structure determination Scheres, Sjors H. W. 2012 IEEE 9th International Symposium on Biomedical Imaging (ISBI 2012), 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI) https://doi.org/10.1109/isbi.2012.6235807	conference	May 2012
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM Paulino, Cristina; Kalienkova, Valeria; Lam, Andy K. M. Nature Publishing Group https://doi.org/10.5167/uzh-144591	text	January 2017

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Title: Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating

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