{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T00:16:13Z","timestamp":1791332173234,"version":"4.3.1"},"reference-count":99,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2021,1,25]],"date-time":"2021-01-25T00:00:00Z","timestamp":1611532800000},"content-version":"vor","delay-in-days":2695,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013,10,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Cytosolic Ca2+ in guard cells plays an important role in stomatal movement responses to environmental stimuli. These cytosolic Ca2+ increases result from Ca2+ influx through Ca2+-permeable channels in the plasma membrane and Ca2+ release from intracellular organelles in guard cells. However, the genes encoding defined plasma membrane Ca2+-permeable channel activity remain unknown in guard cells and, with some exceptions, largely unknown in higher plant cells. Here, we report the identification of two Arabidopsis (Arabidopsis thaliana) cation channel genes, CNGC5 and CNGC6, that are highly expressed in guard cells. Cytosolic application of cyclic GMP (cGMP) and extracellularly applied membrane-permeable 8-Bromoguanosine 3\u2032,5\u2032-cyclic monophosphate-cGMP both activated hyperpolarization-induced inward-conducting currents in wild-type guard cells using Mg2+ as the main charge carrier. The cGMP-activated currents were strongly blocked by lanthanum and gadolinium and also conducted Ba2+, Ca2+, and Na+ ions. cngc5 cngc6 double mutant guard cells exhibited dramatically impaired cGMP-activated currents. In contrast, mutations in CNGC1, CNGC2, and CNGC20 did not disrupt these cGMP-activated currents. The yellow fluorescent protein-CNGC5 and yellow fluorescent protein-CNGC6 proteins localize in the cell periphery. Cyclic AMP activated modest inward currents in both wild-type and cngc5cngc6 mutant guard cells. Moreover, cngc5 cngc6 double mutant guard cells exhibited functional abscisic acid (ABA)-activated hyperpolarization-dependent Ca2+-permeable cation channel currents, intact ABA-induced stomatal closing responses, and whole-plant stomatal conductance responses to darkness and changes in CO2 concentration. Furthermore, cGMP-activated currents remained intact in the growth controlled by abscisic acid2 and abscisic acid insensitive1 mutants. This research demonstrates that the CNGC5 and CNGC6 genes encode unique cGMP-activated nonselective Ca2+-permeable cation channels in the plasma membrane of Arabidopsis guard cells.<\/jats:p>","DOI":"10.1104\/pp.113.225045","type":"journal-article","created":{"date-parts":[[2013,9,10]],"date-time":"2013-09-10T01:52:51Z","timestamp":1378777971000},"page":"578-590","source":"Crossref","is-referenced-by-count":127,"title":["Identification of Cyclic GMP-Activated Nonselective Ca2+-Permeable Cation Channels and Associated <i>CNGC5<\/i> and <i>CNGC6<\/i> Genes in Arabidopsis Guard Cells\n\u00a0\n\u00a0"],"prefix":"10.1093","volume":"163","author":[{"given":"Yong-Fei","family":"Wang","sequence":"first","affiliation":[{"name":"National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (Y.-F.W., H.-M.R.)"},{"name":"Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093\u20130116 (Y.-F.W., S.M., N.N., N.R., M.H., S.L., I.M., J.I.S.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shintaro","family":"Munemasa","sequence":"additional","affiliation":[{"name":"Division of Agricultural and Life Science, Graduate School of Environmental and Life Science, Okayama University, Okayama 7008530, Japan (S.M.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noriyuki","family":"Nishimura","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (Y.-F.W., H.-M.R.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui-Min","family":"Ren","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (Y.-F.W., H.-M.R.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadia","family":"Robert","sequence":"additional","affiliation":[{"name":"Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093\u20130116 (Y.-F.W., S.M., N.N., N.R., M.H., S.L., I.M., J.I.S.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"Han","sequence":"additional","affiliation":[{"name":"Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093\u20130116 (Y.-F.W., S.M., N.N., N.R., M.H., S.L., I.M., J.I.S.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irina","family":"Puz\u00f5rjova","sequence":"additional","affiliation":[{"name":"Institute of Technology, University of Tartu, 50411 Tartu, Estonia (I.P., H.K.); and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hannes","family":"Kollist","sequence":"additional","affiliation":[{"name":"Institute of Technology, University of Tartu, 50411 Tartu, Estonia (I.P., H.K.); and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen","family":"Lee","sequence":"additional","affiliation":[{"name":"Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093\u20130116 (Y.-F.W., S.M., N.N., N.R., M.H., S.L., I.M., J.I.S.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Izumi","family":"Mori","sequence":"additional","affiliation":[{"name":"Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093\u20130116 (Y.-F.W., S.M., N.N., N.R., M.H., S.L., I.M., J.I.S.)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julian I.","family":"Schroeder","sequence":"additional","affiliation":[{"name":"Division of Biological Sciences, Cell and Developmental Biology Section, and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093\u20130116 (Y.-F.W., S.M., N.N., N.R., M.H., S.L., I.M., J.I.S.)"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2013,9,9]]},"reference":[{"key":"2021052607391638500_b1","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1104\/pp.113.217539","article-title":"A suppressor screen of the chimeric AtCNGC11\/12 reveals residues important for intersubunit interactions of cyclic nucleotide-gated ion channels","volume":"162","author":"Abdel-Hamid","year":"2013","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b2","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1105\/tpc.106.045096","article-title":"Death don\u2019t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity","volume":"19","author":"Ali","year":"2007","journal-title":"Plant Cell"},{"key":"2021052607391638500_b3","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1093\/jxb\/erj012","article-title":"Expression of plant cyclic nucleotide-gated cation channels in yeast","volume":"57","author":"Ali","year":"2006","journal-title":"J Exp Bot"},{"key":"2021052607391638500_b4","first-page":"1785","article-title":"Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells","volume":"11","author":"Allen","year":"1999","journal-title":"Plant Cell"},{"key":"2021052607391638500_b5","doi-asserted-by":"crossref","first-page":"1649","DOI":"10.1105\/tpc.010448","article-title":"Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2","volume":"14","author":"Allen","year":"2002","journal-title":"Plant Cell"},{"key":"2021052607391638500_b6","doi-asserted-by":"crossref","first-page":"685","DOI":"10.2307\/3869872","article-title":"Two voltage-gated, calcium release channels coreside in the vacuolar membrane of broad bean guard cells","volume":"6","author":"Allen","year":"1994","journal-title":"Plant Cell"},{"key":"2021052607391638500_b7","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1046\/j.1365-313x.1999.00588.x","article-title":"A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants","volume":"20","author":"Arazi","year":"1999","journal-title":"Plant J"},{"key":"2021052607391638500_b8","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1038\/415977a","article-title":"MAP kinase signalling cascade in Arabidopsis innate immunity","volume":"415","author":"Asai","year":"2002","journal-title":"Nature"},{"key":"2021052607391638500_b9","doi-asserted-by":"crossref","first-page":"E96","DOI":"10.1073\/pnas.1101007108","article-title":"Guanylyl cyclase activity in plants?","volume":"108","author":"Ashton","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b10","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1105\/tpc.006999","article-title":"HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family","volume":"15","author":"Balagu\u00e9","year":"2003","journal-title":"Plant Cell"},{"key":"2021052607391638500_b11","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.cub.2012.11.022","article-title":"The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis","volume":"23","author":"Bauer","year":"2013","journal-title":"Curr Biol"},{"key":"2021052607391638500_b12","doi-asserted-by":"crossref","first-page":"E97","DOI":"10.1073\/pnas.1103313108","article-title":"Reply to Ashton. The putative guanylyl cyclase domain of AtPepR1 and similar plant receptors","volume":"108","author":"Berkowitz","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b13","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1111\/j.0022-2720.2004.01348.x","article-title":"FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells","volume":"214","author":"Bolte","year":"2004","journal-title":"J Microsc"},{"key":"2021052607391638500_b14","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1124\/mol.65.3.503","article-title":"Functional role of lipid raft microdomains in cyclic nucleotide-gated channel activation","volume":"65","author":"Brady","year":"2004","journal-title":"Mol Pharmacol"},{"key":"2021052607391638500_b15","doi-asserted-by":"crossref","first-page":"10593","DOI":"10.1073\/pnas.1116590109","article-title":"Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action","volume":"109","author":"Brandt","year":"2012","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b16","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.1093\/pcp\/pcs140","article-title":"A Ca2+-sensitive system mediates low-affinity K+ uptake in the absence of AKT1 in Arabidopsis plants","volume":"53","author":"Caballero","year":"2012","journal-title":"Plant Cell Physiol"},{"key":"2021052607391638500_b17","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1111\/j.1672-9072.2007.00524.x","article-title":"A putative calcium-permeable cyclic nucleotide-gated channel, CNGC18, regulates polarized pollen tube growth","volume":"49","author":"Chang","year":"2007","journal-title":"J Integr Plant Biol"},{"key":"2021052607391638500_b18","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1111\/j.1365-313X.2009.04108.x","article-title":"Dynamic regulation of guard cell anion channels by cytosolic free Ca2+ concentration and protein phosphorylation","volume":"61","author":"Chen","year":"2010","journal-title":"Plant J"},{"key":"2021052607391638500_b19","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1104\/pp.005645","article-title":"Calcium signaling through protein kinases: the Arabidopsis calcium-dependent protein kinase gene family","volume":"129","author":"Cheng","year":"2002","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b20","doi-asserted-by":"crossref","first-page":"9323","DOI":"10.1073\/pnas.150005697","article-title":"The Arabidopsis dnd1 \u201cdefense, no death\u201d gene encodes a mutated cyclic nucleotide-gated ion channel","volume":"97","author":"Clough","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b21","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1146\/annurev-arplant-070109-104628","article-title":"The language of calcium signaling","volume":"61","author":"Dodd","year":"2010","journal-title":"Annu Rev Plant Biol"},{"key":"2021052607391638500_b22","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1111\/j.1469-8137.2011.03661.x","article-title":"cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1","volume":"191","author":"Dubovskaya","year":"2011","journal-title":"New Phytol"},{"key":"2021052607391638500_b23","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/j.pbi.2004.07.009","article-title":"Guard cells: a dynamic signaling model","volume":"7","author":"Fan","year":"2004","journal-title":"Curr Opin Plant Biol"},{"key":"2021052607391638500_b24","doi-asserted-by":"crossref","first-page":"3333","DOI":"10.1105\/tpc.112.095844","article-title":"Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance","volume":"24","author":"Finka","year":"2012","journal-title":"Plant Cell"},{"key":"2021052607391638500_b25","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1093\/pcp\/pct021","article-title":"An IQ domain mediates the interaction with calmodulin in a plant cyclic nucleotide-gated channel","volume":"54","author":"Fischer","year":"2013","journal-title":"Plant Cell Physiol"},{"key":"2021052607391638500_b26","doi-asserted-by":"crossref","first-page":"14531","DOI":"10.1073\/pnas.0701781104","article-title":"A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen","volume":"104","author":"Frietsch","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b27","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1111\/j.1365-313X.2012.04969.x","article-title":"A heat-activated calcium-permeable channel\u2014Arabidopsis cyclic nucleotide-gated ion channel 6\u2014is involved in heat shock responses","volume":"70","author":"Gao","year":"2012","journal-title":"Plant J"},{"key":"2021052607391638500_b28","doi-asserted-by":"crossref","first-page":"8023","DOI":"10.1073\/pnas.0912030107","article-title":"Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities","volume":"107","author":"Geiger","year":"2010","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b29","doi-asserted-by":"crossref","first-page":"21425","DOI":"10.1073\/pnas.0912021106","article-title":"Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair","volume":"106","author":"Geiger","year":"2009","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b30","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/0896-6273(95)90252-X","article-title":"A histidine residue associated with the gate of the cyclic nucleotide-activated channels in rod photoreceptors","volume":"14","author":"Gordon","year":"1995","journal-title":"Neuron"},{"key":"2021052607391638500_b31","doi-asserted-by":"crossref","first-page":"4778","DOI":"10.1073\/pnas.95.8.4778","article-title":"Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells","volume":"95","author":"Grabov","year":"1998","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b32","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1104\/pp.119.1.277","article-title":"A steep dependence of inward-rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarization in guard cells","volume":"119","author":"Grabov","year":"1999","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b33","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1111\/j.1399-3054.2008.01157.x","article-title":"The cyclic nucleotide-gated channel, AtCNGC10, influences salt tolerance in Arabidopsis","volume":"134","author":"Guo","year":"2008","journal-title":"Physiol Plant"},{"key":"2021052607391638500_b34","first-page":"303","article-title":"The cyclic nucleotide-gated channel AtCNGC10 transports Ca2+ and Mg2+ in Arabidopsis","volume":"139","author":"Guo","year":"2010","journal-title":"Physiol Plant"},{"key":"2021052607391638500_b35","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1104\/pp.110.161703","article-title":"Opportunities to explore plant membrane organization with super-resolution microscopy","volume":"154","author":"Gutierrez","year":"2010","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b36","doi-asserted-by":"crossref","first-page":"4967","DOI":"10.1073\/pnas.080068897","article-title":"Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid","volume":"97","author":"Hamilton","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b37"},{"key":"2021052607391638500_b38","doi-asserted-by":"crossref","first-page":"2546","DOI":"10.1105\/tpc.112.100107","article-title":"A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis","volume":"24","author":"Hua","year":"2012","journal-title":"Plant Cell"},{"key":"2021052607391638500_b39","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1093\/aob\/mcr252","article-title":"Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses","volume":"109","author":"Hubbard","year":"2012","journal-title":"Ann Bot (Lond)"},{"key":"2021052607391638500_b40","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1016\/j.febslet.2007.02.017","article-title":"Cyclic nucleotide-gated channels in plants","volume":"581","author":"Kaplan","year":"2007","journal-title":"FEBS Lett"},{"key":"2021052607391638500_b41","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1146\/annurev-arplant-042809-112226","article-title":"Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling","volume":"61","author":"Kim","year":"2010","journal-title":"Annu Rev Plant Biol"},{"key":"2021052607391638500_b42","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1046\/j.1365-313X.2002.01414.x","article-title":"Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid","volume":"32","author":"K\u00f6hler","year":"2002","journal-title":"Plant J"},{"key":"2021052607391638500_b43","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1046\/j.1365-313X.1999.00422.x","article-title":"Characterisation of a novel gene family of putative cyclic nucleotide- and calmodulin-regulated ion channels in Arabidopsis thaliana","volume":"18","author":"K\u00f6hler","year":"1999","journal-title":"Plant J"},{"key":"2021052607391638500_b44","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1111\/j.1399-3054.2006.00851.x","article-title":"A novel device detects a rapid ozone-induced transient stomatal closure in intact Arabidopsis and its absence in abi2 mutant","volume":"129","author":"Kollist","year":"2007","journal-title":"Physiol Plant"},{"key":"2021052607391638500_b45","doi-asserted-by":"crossref","first-page":"2283","DOI":"10.1105\/tpc.11.12.2283","article-title":"T-DNA as an insertional mutagen in Arabidopsis","volume":"11","author":"Krysan","year":"1999","journal-title":"Plant Cell"},{"key":"2021052607391638500_b46","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1186\/1471-2229-9-140","article-title":"Salt-dependent regulation of a CNG channel subfamily in Arabidopsis","volume":"9","author":"Kugler","year":"2009","journal-title":"BMC Plant Biol"},{"key":"2021052607391638500_b47","doi-asserted-by":"crossref","first-page":"2623","DOI":"10.1093\/emboj\/cdg277","article-title":"NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis","volume":"22","author":"Kwak","year":"2003","journal-title":"EMBO J"},{"key":"2021052607391638500_b48","doi-asserted-by":"crossref","first-page":"1486","DOI":"10.1126\/science.292.5521.1486b","article-title":"The identity of plant glutamate receptors","volume":"292","author":"Lacombe","year":"2001","journal-title":"Science"},{"key":"2021052607391638500_b49","doi-asserted-by":"crossref","first-page":"1522","DOI":"10.1105\/tpc.112.097881","article-title":"Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+- and K+-permeable conductance in root cells","volume":"24","author":"Laohavisit","year":"2012","journal-title":"Plant Cell"},{"key":"2021052607391638500_b50","doi-asserted-by":"crossref","first-page":"21419","DOI":"10.1073\/pnas.0910601106","article-title":"A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells","volume":"106","author":"Lee","year":"2009","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b51","doi-asserted-by":"crossref","first-page":"35306","DOI":"10.1074\/jbc.M400311200","article-title":"Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells","volume":"279","author":"Lemtiri-Chlieh","year":"2004","journal-title":"J Biol Chem"},{"key":"2021052607391638500_b52","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1104\/pp.010832","article-title":"Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels","volume":"128","author":"Leng","year":"2002","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b53","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1105\/tpc.019000","article-title":"Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant","volume":"16","author":"Leonhardt","year":"2004","journal-title":"Plant Cell"},{"key":"2021052607391638500_b54","doi-asserted-by":"crossref","first-page":"6490","DOI":"10.1074\/jbc.M210983200","article-title":"Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana","volume":"278","author":"Ludidi","year":"2003","journal-title":"J Biol Chem"},{"key":"2021052607391638500_b55","doi-asserted-by":"crossref","first-page":"413","DOI":"10.4161\/psb.6.3.14356","article-title":"Cyclic nucleotide gated channel and Ca2+-mediated signal transduction during plant senescence signaling","volume":"6","author":"Ma","year":"2011","journal-title":"Plant Signal Behav"},{"key":"2021052607391638500_b56","doi-asserted-by":"crossref","first-page":"3167","DOI":"10.1105\/tpc.112.240810","article-title":"Calcium channels and acquired thermotolerance: here comes the sun and it\u2019s all right","volume":"24","author":"Mach","year":"2012","journal-title":"Plant Cell"},{"key":"2021052607391638500_b57","doi-asserted-by":"crossref","first-page":"12361","DOI":"10.1073\/pnas.220417197","article-title":"ABA activates multiple Ca2+ fluxes in stomatal guard cells, triggering vacuolar K+ (Rb+) release","volume":"97","author":"MacRobbie","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b58","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1104\/pp.106.092643","article-title":"Ca2+-dependent and -independent abscisic acid activation of plasma membrane anion channels in guard cells of Nicotiana tabacum","volume":"143","author":"Marten","year":"2007","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b59","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/343186a0","article-title":"Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure","volume":"343","author":"McAinsh","year":"1990","journal-title":"Nature"},{"key":"2021052607391638500_b60","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.2307\/3869479","article-title":"Visualizing changes in cytosolic-free Ca2+ during the response of stomatal guard cells to abscisic acid","volume":"4","author":"McAinsh","year":"1992","journal-title":"Plant Cell"},{"key":"2021052607391638500_b61","doi-asserted-by":"crossref","first-page":"2749","DOI":"10.1105\/tpc.106.044230","article-title":"An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses","volume":"18","author":"Miao","year":"2006","journal-title":"Plant Cell"},{"key":"2021052607391638500_b62","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1126\/science.1201101","article-title":"Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine","volume":"332","author":"Michard","year":"2011","journal-title":"Science"},{"key":"2021052607391638500_b63","doi-asserted-by":"crossref","first-page":"e327","DOI":"10.1371\/journal.pbio.0040327","article-title":"CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure","volume":"4","author":"Mori","year":"2006","journal-title":"PLoS Biol"},{"key":"2021052607391638500_b64","doi-asserted-by":"crossref","first-page":"1398","DOI":"10.1104\/pp.106.091298","article-title":"The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells: specific impairment of ion channel activation and second messenger production","volume":"143","author":"Munemasa","year":"2007","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b65","doi-asserted-by":"crossref","first-page":"2513","DOI":"10.1105\/tpc.010210","article-title":"Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants","volume":"13","author":"Murata","year":"2001","journal-title":"Plant Cell"},{"key":"2021052607391638500_b66","doi-asserted-by":"crossref","first-page":"3089","DOI":"10.1105\/tpc.007906","article-title":"Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production","volume":"14","author":"Mustilli","year":"2002","journal-title":"Plant Cell"},{"key":"2021052607391638500_b67","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1038\/msb.2010.28","article-title":"Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action","volume":"6","author":"Pandey","year":"2010","journal-title":"Mol Syst Biol"},{"key":"2021052607391638500_b68","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1126\/science.282.5387.287","article-title":"Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss","volume":"282","author":"Pei","year":"1998","journal-title":"Science"},{"key":"2021052607391638500_b69","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1038\/35021067","article-title":"Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells","volume":"406","author":"Pei","year":"2000","journal-title":"Nature"},{"key":"2021052607391638500_b70","doi-asserted-by":"crossref","first-page":"21193","DOI":"10.1073\/pnas.1000191107","article-title":"Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels","volume":"107","author":"Qi","year":"2010","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b71","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/338427a0","article-title":"Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells","volume":"338","author":"Schroeder","year":"1989","journal-title":"Nature"},{"key":"2021052607391638500_b72","doi-asserted-by":"crossref","first-page":"9305","DOI":"10.1073\/pnas.87.23.9305","article-title":"Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels","volume":"87","author":"Schroeder","year":"1990","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b73","doi-asserted-by":"crossref","first-page":"1944","DOI":"10.1073\/pnas.95.4.1944","article-title":"Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone","volume":"95","author":"Schuurink","year":"1998","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b74","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1104\/pp.87.3.583","article-title":"Calcium effects on stomatal movement in Commelina communis L.: use of EGTA to modulate stomatal response to light, KCl and CO2","volume":"87","author":"Schwartz","year":"1988","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b75","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1111\/j.1365-313X.2009.03872.x","article-title":"Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K channels in Arabidopsis guard cells","volume":"59","author":"Siegel","year":"2009","journal-title":"Plant J"},{"key":"2021052607391638500_b76","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1111\/j.1365-313X.2010.04141.x","article-title":"Ca2+-dependent activation of guard cell anion channels, triggered by hyperpolarization, is promoted by prolonged depolarization","volume":"62","author":"Stange","year":"2010","journal-title":"Plant J"},{"key":"2021052607391638500_b77","doi-asserted-by":"crossref","first-page":"1916","DOI":"10.1074\/jbc.M607926200","article-title":"The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells","volume":"282","author":"Suh","year":"2007","journal-title":"J Biol Chem"},{"key":"2021052607391638500_b78","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1046\/j.1365-313x.2000.00901.x","article-title":"Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance","volume":"24","author":"Sunkar","year":"2000","journal-title":"Plant J"},{"key":"2021052607391638500_b79","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1105\/tpc.105.038950","article-title":"Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane","volume":"18","author":"Sutter","year":"2006","journal-title":"Plant Cell"},{"key":"2021052607391638500_b80","doi-asserted-by":"crossref","first-page":"2970","DOI":"10.1002\/j.1460-2075.1994.tb06595.x","article-title":"Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell","volume":"13","author":"Thuleau","year":"1994","journal-title":"EMBO J"},{"key":"2021052607391638500_b81","doi-asserted-by":"crossref","first-page":"e55277","DOI":"10.1371\/journal.pone.0055277","article-title":"Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility","volume":"8","author":"Tunc-Ozdemir","year":"2013","journal-title":"PLoS ONE"},{"key":"2021052607391638500_b82","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1104\/pp.112.206888","article-title":"A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development","volume":"161","author":"Tunc-Ozdemir","year":"2013","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b83","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1007\/s11103-007-9239-7","article-title":"The chimeric cyclic nucleotide-gated ion channel ATCNGC11\/12 constitutively induces programmed cell death in a Ca2+ dependent manner","volume":"65","author":"Urquhart","year":"2007","journal-title":"Plant Mol Biol"},{"key":"2021052607391638500_b84","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1038\/nature06608","article-title":"SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling","volume":"452","author":"Vahisalu","year":"2008","journal-title":"Nature"},{"key":"2021052607391638500_b85","doi-asserted-by":"crossref","first-page":"9801","DOI":"10.1073\/pnas.160250397","article-title":"Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs","volume":"97","author":"V\u00e9ry","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b86","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1104\/pp.112.197509","article-title":"Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors","volume":"159","author":"Vincill","year":"2012","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b87","doi-asserted-by":"crossref","first-page":"3892","DOI":"10.1104\/pp.104.042754","article-title":"Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments","volume":"136","author":"Wang","year":"2004","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b88","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1146\/annurev.physiol.010908.163204","article-title":"Plant ion channels: gene families, physiology, and functional genomics analyses","volume":"71","author":"Ward","year":"2009","journal-title":"Annu Rev Physiol"},{"key":"2021052607391638500_b89","doi-asserted-by":"crossref","first-page":"669","DOI":"10.2307\/3869871","article-title":"Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure","volume":"6","author":"Ward","year":"1994","journal-title":"Plant Cell"},{"key":"2021052607391638500_b90","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1046\/j.1365-313X.2001.01032.x","article-title":"The role of calcium in ABA-induced gene expression and stomatal movements","volume":"26","author":"Webb","year":"2001","journal-title":"Plant J"},{"key":"2021052607391638500_b91","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1046\/j.1365-313X.1996.09030297.x","article-title":"Carbon dioxide induces increases in guard cell cytosolic free calcium","volume":"9","author":"Webb","year":"1996","journal-title":"Plant J"},{"key":"2021052607391638500_b92","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1104\/pp.110.161927","article-title":"Self-incompatibility in Papaver rhoeas activates nonspecific cation conductance permeable to Ca2+ and K+","volume":"155","author":"Wu","year":"2011","journal-title":"Plant Physiol"},{"key":"2021052607391638500_b93","doi-asserted-by":"crossref","first-page":"1645","DOI":"10.1038\/emboj.2011.68","article-title":"Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cell","volume":"30","author":"Xue","year":"2011","journal-title":"EMBO J"},{"key":"2021052607391638500_b94","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/1746-4811-4-6","article-title":"Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool","volume":"4","author":"Yang","year":"2008","journal-title":"Plant Methods"},{"key":"2021052607391638500_b95","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1093\/pcp\/pcf188","article-title":"ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis","volume":"43","author":"Yoshida","year":"2002","journal-title":"Plant Cell Physiol"},{"key":"2021052607391638500_b96","doi-asserted-by":"crossref","first-page":"7506","DOI":"10.1073\/pnas.0602225103","article-title":"CO2 signaling in guard cells: calcium sensitivity response modulation, a Ca2+-independent phase, and CO2 insensitivity of the gca2 mutant","volume":"103","author":"Young","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b97","doi-asserted-by":"crossref","first-page":"7819","DOI":"10.1073\/pnas.95.13.7819","article-title":"Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant","volume":"95","author":"Yu","year":"1998","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052607391638500_b98","doi-asserted-by":"crossref","first-page":"3019","DOI":"10.1105\/tpc.107.050666","article-title":"Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis","volume":"19","author":"Zhu","year":"2007","journal-title":"Plant Cell"},{"key":"2021052607391638500_b99","doi-asserted-by":"crossref","first-page":"1232","DOI":"10.1104\/pp.110.157545","article-title":"Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress","volume":"154","author":"Zou","year":"2010","journal-title":"Plant Physiol"}],"container-title":["Plant Physiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/plphys\/article-pdf\/163\/2\/578\/38113375\/plphys_v163_2_578.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/plphys\/article-pdf\/163\/2\/578\/38113375\/plphys_v163_2_578.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,26]],"date-time":"2021-05-26T07:46:44Z","timestamp":1622015204000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/plphys\/article\/163\/2\/578\/6110998"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,9,9]]},"references-count":99,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2013,9,9]]},"published-print":{"date-parts":[[2013,10,8]]}},"URL":"https:\/\/doi.org\/10.1104\/pp.113.225045","relation":{},"ISSN":["1532-2548"],"issn-type":[{"value":"1532-2548","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2013,10,1]]},"published":{"date-parts":[[2013,9,9]]}}}