Cryo-EM structure of OSCA1.2 from Oryza sativa: Mechanical basis of potential membrane hyperosmolality-gating

Authors: MAITY, KOUSTAV - University Of California, San Diego; HEUMANN, JOHN - University Of Colorado; MCGRATH, AARON - University Of California, San Diego; KOPCHO, NOAH - University Of California, San Diego; HSU, PO-KAI - University Of California, San Diego; LEE, CHANG-WOOK - University Of California, San Diego; MAPES, JAMES - University Of Colorado; GARZO, DENISSE - University Of California, San Diego; KRISHNA, SRINIVASAN - Boyce Thompson Institute; MORGAN, GAYY - University Of Colorado; HENDARGO, KEVIN - University Of California, San Diego; KLOSE, THOMAS - Purdue University; REES, STEVEN - University Of California, San Diego; MEDRANO-SOTO, ARTURO - University Of California, San Diego; SAIER, MILTON - University Of California, San Diego; Pineros, Miguel; KOMIVES, ELIZABETH - University Of California, San Diego; SCHROEDER, JULIAN - University Of California, San Diego; CHANG, GEOFFREY - University Of California, San Diego; STOWELL, MICHAEL - University Of Colorado

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/16/2019
Publication Date: N/A
Citation: N/A

Interpretive Summary: Environmental factors such as low rainfall, extreme temperatures, and salinity, among others, contribute to drought that affects agricultural productivity and food security. In plants, OSCA proteins are thought to be capable of recognizing and decoding drought-related stress. Using a multidisciplinary approach by combining biochemical, biophysical and computational studies, we have inferred a structural model for an OSCA protein from rice. This model allowed us to understand the mechanism by which this OSCA protein senses physical forces, such as those experienced during drought, and translates them into biological (biochemical) signals, thereby evoking a variety of physiological and molecular responses. This study provides the basis to understand how crop plants respond and adapt in response to changes in the environment.

Technical 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 calciumdependent 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. The 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.