Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations

• Published in: Nature communications Vol. 10; no. 1; pp. 1 - 12
• Main Authors: Kim, Sunghoon, Zeng, Weizhong, Bernard, Shane, Liao, Jun, Venkateshwaran, Muthusubramanian, Ane, Jean-Michel, Jiang, Youxing
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 16.08.2019; Nature Publishing Group; Nature Portfolio
• Subjects: 13; 13/106; 13/109; 14/33; 38/35; 631/449/2676/2678; 631/45/269/1146; 631/535/1266; 631/57/2270/1140; 82/16; 82/29; 82/80; 82/83; 9/74; BASIC BIOLOGICAL SCIENCES; Binding sites; Calcium channels; Calcium conductance; Calcium ions; Calcium-binding protein; Channel gating; Domains; Homology; Humanities and Social Sciences; Ion channels; ion transport; Legumes; multidisciplinary; Potassium channels; Potassium channels (calcium-gated); Potassium conductance; Resistance; rhizobial symbiosis; Science; Science (multidisciplinary); Symbiosis; x-ray crystallography
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-019-11698-5

A family of plant nuclear ion channels, including DMI1 ( D oes not M ake I nfections 1 ) and its homologs CASTOR and POLLUX, are required for the establishment of legume-microbe symbioses by generating nuclear and perinuclear Ca 2+ spiking. Here we show that CASTOR from Lotus japonicus is a highly selective Ca 2+ channel whose activation requires cytosolic/nucleosolic Ca 2+ , contrary to the previous suggestion of it being a K + channel. Structurally, the cytosolic/nucleosolic ligand-binding soluble region of CASTOR contains two tandem RCK ( R egulator of C onductance for K + ) domains, and four subunits assemble into the gating ring architecture, similar to that of large conductance, Ca 2+ -gated K + (BK) channels despite the lack of sequence similarity. Multiple ion binding sites are clustered at two locations within each subunit, and three of them are identified to be Ca 2+ sites. Our in vitro and in vivo assays also demonstrate the importance of these gating-ring Ca 2+ binding sites to the physiological function of CASTOR as well as DMI1. CASTOR is a Lotus japonicus ion channel required for nuclear Ca 2+ spiking and establishing rhizobial and mycorrhizal symbioses. Here, via structural and functional analysis, Kim et al . show that CASTOR is a Ca 2+ -selective channel activated via Ca 2+ binding to a soluble gating ring consisting of tandem RCK domains.