TY - JOUR
T1 - Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations
AU - Kim, Sunghoon
AU - Zeng, Weizhong
AU - Bernard, Shane
AU - Liao, Jun
AU - Venkateshwaran, Muthusubramanian
AU - Ane, Jean Michel
AU - Jiang, Youxing
N1 - Funding Information:
We thank N. Nguyen and Z. Keyser for manuscript preparation. The experimental results reported in this article derive from the work performed at Argonne National Laboratory, Structural Biology Center (19ID) and GM/CA (23ID) at the Advanced Photon Source, and from the work performed at the Berkeley Center for Structural Biology at the Advanced Light Source (ALS). Argonne is operated by the University of Chicago Argonne, LLC, for the U.S. Department of Energy, Office of Biological and Environmental Research under contract DE-AC02-06CH11357. The Berkeley Center for Structural Biology is supported in part by the National Institutes of Health, National Institute of General Medical Sciences, and the Howard Hughes Medical Institute. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. This work was supported in part by the Howard Hughes Medical Institute and by grants from the National Institute of Health (GM079179 to Y.J.), the Welch Foundation (Grant I-1578 to Y.J.), and the United States Department of Agriculture AFRI (Grant #2015-67013-22899 to M.V. and J.M.A.).
Publisher Copyright:
© 2019, The Author(s).
PY - 2019/12/1
Y1 - 2019/12/1
N2 - A family of plant nuclear ion channels, including DMI1 (Does not Make Infections 1) and its homologs CASTOR and POLLUX, are required for the establishment of legume-microbe symbioses by generating nuclear and perinuclear Ca2+ spiking. Here we show that CASTOR from Lotus japonicus is a highly selective Ca2+ channel whose activation requires cytosolic/nucleosolic Ca2+, 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 (Regulator of Conductance for K+) domains, and four subunits assemble into the gating ring architecture, similar to that of large conductance, Ca2+-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 Ca2+ sites. Our in vitro and in vivo assays also demonstrate the importance of these gating-ring Ca2+ binding sites to the physiological function of CASTOR as well as DMI1.
AB - A family of plant nuclear ion channels, including DMI1 (Does not Make Infections 1) and its homologs CASTOR and POLLUX, are required for the establishment of legume-microbe symbioses by generating nuclear and perinuclear Ca2+ spiking. Here we show that CASTOR from Lotus japonicus is a highly selective Ca2+ channel whose activation requires cytosolic/nucleosolic Ca2+, 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 (Regulator of Conductance for K+) domains, and four subunits assemble into the gating ring architecture, similar to that of large conductance, Ca2+-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 Ca2+ sites. Our in vitro and in vivo assays also demonstrate the importance of these gating-ring Ca2+ binding sites to the physiological function of CASTOR as well as DMI1.
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U2 - 10.1038/s41467-019-11698-5
DO - 10.1038/s41467-019-11698-5
M3 - Article
C2 - 31420535
AN - SCOPUS:85070799417
SN - 2041-1723
VL - 10
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 3703
ER -