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. 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.

Drought Stress Responses and Resistance in Plants: From Cellular Responses to Long-Distance Intercellular Communication

“…CALCIUM-PERMEABLE STRESS-GATED CATION CHANNEL1 (CSC1)/OSCA1.2 is a homolog in the OSCA family and has been reported as a hyperosmolality-gated calcium-permeable channel protein (Hou et al, 2014). CSC1/ OSCA1.2 also mediated calcium fluxes in plant cells in response to osmotic stress conditions, although the detailed function of CSC1/OSCA1.2 in plant tissues remains unclear (Liu et al, 2018;Maity et al, 2019).…”

Systematic Analysis of the Maize OSCA Genes Revealing ZmOSCA Family Members Involved in Osmotic Stress and ZmOSCA2.4 Confers Enhanced Drought Tolerance in Transgenic Arabidopsis

“…Previous studies of Arabidopsis and rice have shown that OSCA family members contain DUF221 domain and have been identified to contain 15 and 11 members, respectively, with multiple genes associated with osmotic stress [13,26]. Each OSCA protein in the Arabidopsis and rice genomes contained 11 transmembrane domains [27,28]. In contrast, nine ZmOSCAs contained 9-11 transmembrane domains, and ZmOSCA1.1a and ZmOSCA3.1 proteins contained only four and two transmembrane domains, respectively (Table 1), which indicates that ZmOSCAs had experienced greater genetic variation during evolution.…”

Cryo-EM structures of human TMEM120A and TMEM120B

“…The ion permeation path of most MSCs, including MscL and MscS 8 from bacteria, NOMPC 9 from fly, and TRAAK 10 and Piezo 11,12 from mammal, are along the symmetric axis. The dimeric TMEM120A is reminiscent of OSCAs [13][14][15][16] from plant, whose ion permeation path are along each protomer. Although TMEM120A shows the ability to permeate ions as measured in bilayer system, our results indicate TMEM120A does not response to poking or stretch mechanical stimuli in heterologous expression system.…”