1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 72, 2021
  5. Article

Annual Review of Plant Biology

Volume 72, 2021

Recent Advances in the Physiology of Ion Channels in Plants

Abstract

Our knowledge of plant ion channels was significantly enhanced by the first application of the patch-clamp technique to isolated guard cell protoplasts over 35 years ago. Since then, research has demonstrated the importance of ion channels in the control of gas exchange in guard cells, their role in nutrient uptake in roots, and the participation of calcium-permeable cation channels in the regulation of cell signaling affected by the intracellular concentrations of this second messenger. In recent years, through the employment of reverse genetics, mutant proteins, and heterologous expression systems, research on ion channels has identified mechanisms that modify their activity through protein–protein interactions or that result in activation and/or deactivation of ion channels through posttranslational modifications. Additional and confirmatory information on ion channel functioning has been derived from the crystallization and molecular modeling of plant proteins that, together with functional analyses, have helped to increase our knowledge of the functioning of these important membrane proteins that may eventually help to improve crop yield. Here, an update on the advances obtained in plant ion channel function during the last few years is presented.

Keyword(s): AKT1, cryogenic electron microscopy, KAT1, SLAC1, TPC1, traffic
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081519-035925
2021-06-17
2024-05-07
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-081519-035925.html?itemId=/content/journals/10.1146/annurev-arplant-081519-035925&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Balagué C, Lin B, Alcon C, Flottes G, Malmström S et al. 2003. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:2365–79
     [Google Scholar]
  2. 2. 
    Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse J-M, Gambale F et al. 2011. Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu. Rev. Plant Biol. 62:25–51
     [Google Scholar]
  3. 3. 
    Basu D, Haswell ES. 2017. Plant mechanosensitive ion channels: an ocean of possibilities. Curr. Opin. Plant Biol. 40:43–48
     [Google Scholar]
  4. 4. 
    Becker D, Geiger D, Dunkel M, Roller A, Bertl A et al. 2004. AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner. PNAS 101:4415621–26
     [Google Scholar]
  5. 5. 
    Brandt B, Brodsky DE, Xue S, Negi J, Iba K et al. 2012. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. PNAS 109:2610593–98Reconstitution of the signaling pathway regulating SLAC1 in Xenopus oocytes.
     [Google Scholar]
  6. 6. 
    Brandt B, Munemasa S, Wang C, Nguyen D, Yong T et al. 2015. Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4:e03599Identification of the requirement of simultaneous phosphorylation of two phosphorylation sites in SLAC1.
     [Google Scholar]
  7. 7. 
    Catterall WA. 2010. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 67:6915–28
     [Google Scholar]
  8. 8. 
    Charpentier M, Sun J, Vaz Martins T, Radhakrishnan GV, Findlay K et al. 2016. Nuclear-localized cyclic nucleotide–gated channels mediate symbiotic calcium oscillations. Science 352:62891102–5Identification of the association of CNGC15 with the DMI1 channel to modulate nuclear Ca2+ oscillations.
     [Google Scholar]
  9. 9. 
    Chen Y-H, Hu L, Punta M, Bruni R, Hillerich B et al. 2010. Homologue structure of the SLAC1 anion channel for closing stomata in leaves. Nature 467:73191074–80Application of X-ray analyses to protein crystals to obtain the three-dimensional structure of SLAC1.
     [Google Scholar]
  10. 10. 
    Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L et al. 2007. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:2223–39
     [Google Scholar]
  11. 11. 
    Chiasson DM, Haage K, Sollweck K, Brachmann A, Dietrich P, Parniske M. 2017. A quantitative hypermorphic CNGC allele confers ectopic calcium flux and impairs cellular development. eLife 6:e25012
     [Google Scholar]
  12. 12. 
    Chin K, DeFalco TA, Moeder W, Yoshioka K. 2013. The Arabidopsis cyclic nucleotide-gated ion channels AtCNGC2 and AtCNGC4 work in the same signaling pathway to regulate pathogen defense and floral transition. Plant Physiol 163:2611–24
     [Google Scholar]
  13. 13. 
    Chiu JC, Brenner ED, DeSalle R, Nitabach MN, Holmes TC, Coruzzi GM. 2002. Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana. Mol. Biol. Evol. 19:71066–82
     [Google Scholar]
  14. 14. 
    Corratgé-Faillie C, Ronzier E, Sanchez F, Prado K, Kim JH et al. 2017. The Arabidopsis guard cell outward potassium channel GORK is regulated by CPK33. FEBS Lett 591:131982–92
     [Google Scholar]
  15. 15. 
    Cubero-Font P, Maierhofer T, Jaslan J, Rosales MA, Espartero J et al. 2016. Silent S-type anion channel subunit SLAH1 gates SLAH3 open for chloride root-to-shoot translocation. Curr. Biol. 26:162213–20
     [Google Scholar]
  16. 16. 
    Dadacz-Narloch B, Beyhl D, Larisch C, López-Sanjurjo EJ, Reski R et al. 2011. A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. Plant Cell 23:72696–707
     [Google Scholar]
  17. 17. 
    De Angeli A, Baetz U, Francisco R, Zhang J, Chaves MM, Regalado A. 2013. The vacuolar channel VvALMT9 mediates malate and tartrate accumulation in berries of Vitis vinifera. Planta 238:2283–91
     [Google Scholar]
  18. 18. 
    De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S et al. 2006. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:7105939–42
     [Google Scholar]
  19. 19. 
    De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S et al. 2009. CLC-mediated anion transport in plant cells. Philos. Trans. R. Soc. B 364: 1514.195–201
     [Google Scholar]
  20. 20. 
    De Angeli A, Zhang J, Meyer S, Martinoia E. 2013. AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat. Commun. 4:1804
     [Google Scholar]
  21. 21. 
    De Bortoli S, Teardo E, Szabò I, Morosinotto T, Alboresi A. 2016. Evolutionary insight into the ionotropic glutamate receptor superfamily of photosynthetic organisms. Biophys. Chem. 218:14–26
     [Google Scholar]
  22. 22. 
    DeFalco TA, Marshall CB, Munro K, Kang H-G, Moeder W et al. 2016. Multiple calmodulin-binding sites positively and negatively regulate Arabidopsis CYCLIC NUCLEOTIDE-GATED CHANNEL12. Plant Cell 28:1738–51
     [Google Scholar]
  23. 23. 
    DeFalco TA, Moeder W, Yoshioka K. 2016. Opening the gates: insights into cyclic nucleotide-gated channel-mediated signaling. Trends Plant Sci 21:11903–6
     [Google Scholar]
  24. 24. 
    Dunkel M, Latz A, Schumacher K, Müller T, Becker D, Hedrich R. 2008. Targeting of vacuolar membrane localized members of the TPK channel family. Mol. Plant 1:6938–49
     [Google Scholar]
  25. 25. 
    Eisenach C, Chen ZH, Grefen C, Blatt MR. 2012. The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K+ channel activity with vegetative growth. Plant J 69:2241–51
     [Google Scholar]
  26. 26. 
    Eisenach C, Papanatsiou M, Hillert EK, Blatt MR. 2014. Clustering of the K+ channel GORK of Arabidopsis parallels its gating by extracellular K+. Plant J 78:2203–14
     [Google Scholar]
  27. 27. 
    Fischer C, Defalco TA, Karia P, Snedden WA, Moeder W et al. 2017. Calmodulin as a Ca2+-sensing subunit of Arabidopsis cyclic nucleotide-gated channel complexes. Plant Cell Physiol 58:71208–21
     [Google Scholar]
  28. 28. 
    Frietsch S, Wang Y-F, Sladek C, Poulsen LR, Romanowsky SM et al. 2007. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. PNAS 104:3614531–36
     [Google Scholar]
  29. 29. 
    Furuichi T, Sasaki T, Tsuchiya Y, Ryan PR, Delhaize E, Yamamoto Y. 2010. An extracellular hydrophilic carboxy-terminal domain regulates the activity of TaALMT1, the aluminum-activated malate transport protein of wheat. Plant J 64:147–55
     [Google Scholar]
  30. 30. 
    Gao F, Han X, Wu J, Zheng S, Shang Z et al. 2012. A heat-activated calcium-permeable channel—Arabidopsis cyclic nucleotide-gated ion channel 6—is involved in heat shock responses. Plant J 70:61056–69
     [Google Scholar]
  31. 31. 
    Gao QF, Fei CF, Dong JY, Gu LL, Wang YF. 2014. Arabidopsis CNGC18 is a Ca2+-permeable channel. Mol. Plant 7:4739–43
     [Google Scholar]
  32. 32. 
    Gao QF, Gu LL, Wang HQ, Fei CF, Fang X et al. 2016. Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. PNAS 113:3096–101
     [Google Scholar]
  33. 33. 
    Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D et al. 1998. Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–55
     [Google Scholar]
  34. 34. 
    Geiger D, Scherzer S, Mumm P, Marten I, Ache P et al. 2010. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. PNAS 107:178023–28
     [Google Scholar]
  35. 35. 
    Geiger D, Scherzer S, Mumm P, Stange A, Marten I et al. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. PNAS 106:5021425–30Reconstitution of the signaling pathway regulating SLAC1 in an in vitro kinase assay.
     [Google Scholar]
  36. 36. 
    Ger MF, Rendon G, Tilson JL, Jakobsson E 2010. Domain-based identification and analysis of glutamate receptor ion channels and their relatives in prokaryotes. PLOS ONE 5:10e12827
     [Google Scholar]
  37. 37. 
    Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJM 2007. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. PNAS 104:2510726–31
     [Google Scholar]
  38. 38. 
    Grefen C, Karnik R, Larson E, Lefoulon C, Wang Y et al. 2015. A vesicle-trafficking protein commandeers Kv channel voltage sensors for voltage-dependent secretion. Nat. Plants 1:815108
     [Google Scholar]
  39. 39. 
    Guo J, Bai X, Jiang Y, Zeng W, Chen Q, She J 2018. Structural insights into the voltage and phospholipid activation of the mammalian TPC1 channel. Nature 556:7699130–34
     [Google Scholar]
  40. 40. 
    Guo J, Zeng W, Chen Q, Lee C, Chen L et al. 2016. Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature 531:7593196–201Application of X-ray analyses to protein crystals to obtain the three-dimensional structure of TPC1.
     [Google Scholar]
  41. 41. 
    Gutermuth T, Lassig R, Portes M-T, Maierhofer T, Romeis T et al. 2013. Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25:114525–43
     [Google Scholar]
  42. 42. 
    Guzel Deger A, Scherzer S, Nuhkat M, Kedzierska J, Kollist H et al. 2015. Guard cell SLAC1-type anion channels mediate flagellin-induced stomatal closure. New Phytol 208:1162–73
     [Google Scholar]
  43. 43. 
    Hamilton ES, Jensen GS, Maksaev G, Katims A, Sherp AM, Haswell ES. 2015. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350:6259438–41
     [Google Scholar]
  44. 44. 
    Hamilton ES, Schlegel AM, Haswell ES. 2014. United in diversity: mechanosensitive ion channels in plants. Annu. Rev. Plant Biol. 66:113–37
     [Google Scholar]
  45. 45. 
    Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K. 2006. Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat. Cell Biol. 8:4391–97
     [Google Scholar]
  46. 46. 
    Haswell ES, Meyerowitz EM. 2006. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol. 16:11–11
     [Google Scholar]
  47. 47. 
    Hedrich R. 2012. Ion channels in plants. Physiol. Rev. 92:41777–811
     [Google Scholar]
  48. 48. 
    Hedrich R, Flügge UI, Fernandez JM. 1986. Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Lett 204:2228–32
     [Google Scholar]
  49. 49. 
    Hedrich R, Geiger D. 2017. Biology of SLAC1-type anion channels—from nutrient uptake to stomatal closure. New Phytol 216:146–61
     [Google Scholar]
  50. 50. 
    Hedrich R, Mueller TD, Becker D, Marten I 2018. Structure and function of TPC1 vacuole SV channel gains shape. Mol. Plant 11:6764–75
     [Google Scholar]
  51. 51. 
    Hedrich R, Neher E. 1987. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329:6142833–36
     [Google Scholar]
  52. 52. 
    Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K et al. 2011. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21:71116–30
     [Google Scholar]
  53. 53. 
    Herdean A, Nziengui H, Zsiros O, Solymosi K, Garab G et al. 2016. The Arabidopsis thylakoid chloride channel AtCLCe functions in chloride homeostasis and regulation of photosynthetic electron transport. Front. Plant Sci. 7:115
     [Google Scholar]
  54. 54. 
    Herdean A, Teardo E, Nilsson AK, Pfeil BE, Johansson ON et al. 2016. A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat. Commun. 7:111654
     [Google Scholar]
  55. 55. 
    Hoekenga OA, Maron LG, Piñeros MA, Cançado GMA, Shaff J et al. 2006. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. PNAS 103:259738–43
     [Google Scholar]
  56. 56. 
    Honsbein A, Sokolovski S, Grefen C, Campanoni P, Pratelli R et al. 2009. A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. Plant Cell 21:92859–77
     [Google Scholar]
  57. 57. 
    Hõrak H, Sierla M, Tõldsepp K, Wang C, Wang Y-S et al. 2016. A dominant mutation in the HT1 kinase uncovers roles of MAP kinases and GHR1 in CO2-induced stomatal closure. Plant Cell 28:102493–509
     [Google Scholar]
  58. 58. 
    Hoshi T. 1995. Regulation of voltage dependence of the KAT1 channel by intracellular factors. J. Gen. Physiol. 105:309–28
     [Google Scholar]
  59. 59. 
    Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F et al. 2003. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. PNAS 100:95549–54
     [Google Scholar]
  60. 60. 
    Hou C, Tian W, Kleist T, He K, Garcia V et al. 2014. DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res 24:5632–35Identification of osmosensitive calcium-permeable cation channels.
     [Google Scholar]
  61. 61. 
    Hu H, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue S et al. 2010. Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat. Cell Biol. 12:187–93
     [Google Scholar]
  62. 62. 
    Hua D, Wang C, He J, Liao H, Duan Y et al. 2012. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24:62546–61
     [Google Scholar]
  63. 63. 
    Isayenkov S, Isner J-C, Maathuis FJM. 2011. Rice two-pore K+ channels are expressed in different types of vacuoles. Plant Cell 23:2756–68
     [Google Scholar]
  64. 64. 
    Ishibashi K, Suzuki M, Imai M. 2000. Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem. Biophys. Res. Commun. 270:2370–76
     [Google Scholar]
  65. 65. 
    Isner JC, Begum A, Nuehse T, Hetherington AM, Maathuis FJM. 2018. KIN7 kinase regulates the vacuolar TPK1 K+ channel during stomatal closure. Curr. Biol. 28:3466–72.E4
     [Google Scholar]
  66. 66. 
    Jaślan D, Mueller TD, Becker D, Schultz J, Cuin TA et al. 2016. Gating of the two-pore cation channel AtTPC1 in the plant vacuole is based on a single voltage-sensing domain. Plant Biol 18:5750–60
     [Google Scholar]
  67. 67. 
    Jegla T, Busey G, Assmann SM 2018. Evolution and structural characteristics of plant voltage-gated K+ channels. Plant Cell 30:2898–909
     [Google Scholar]
  68. 68. 
    Johnson AA, Guziewicz KE, Lee CJ, Kalathur RC, Pulido JS et al. 2017. Bestrophin 1 and retinal disease. Prog. Retin. Eye Res. 58:45–69
     [Google Scholar]
  69. 69. 
    Kaplan B, Sherman T, Fromm H. 2007. Cyclic nucleotide-gated channels in plants. FEBS Lett 581:122237–46
     [Google Scholar]
  70. 70. 
    Karnik R, Grefen C, Bayne R, Honsbein A, Kohler T et al. 2013. Arabidopsis Sec1/Munc18 protein SEC11 is a competitive and dynamic modulator of SNARE binding and SYP121-dependent vesicle traffic. Plant Cell 25:41368–82
     [Google Scholar]
  71. 71. 
    Karnik R, Lefoulon C, Blatt MR, Zhang B, Gonzalez W et al. 2016. Commandeering channel voltage sensors for secretion, cell turgor, and volume control. Trends Plant Sci 22:181–95
     [Google Scholar]
  72. 72. 
    Keller BU, Hedrich R, Raschke K. 1989. Voltage-dependent anion channels in the plasma membrane of guard cells. Nature 341:6241450–53
     [Google Scholar]
  73. 73. 
    Kim T-H, Böhmer M, Hu H, Nishimura N, Schroeder JI. 2010. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61:561–91
     [Google Scholar]
  74. 74. 
    Kochian LV. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:237–60
     [Google Scholar]
  75. 75. 
    Kong D, Hu HC, Okuma E, Lee Y, Lee HS et al. 2016. L-Met activates Arabidopsis GLR Ca2+ channels upstream of ROS production and regulates stomatal movement. Cell Rep 17:102553–61
     [Google Scholar]
  76. 76. 
    Kong D, Ju C, Parihar A, Kim S, Cho D, Kwak JM. 2015. Arabidopsis glutamate receptor homolog3.5 modulates cytosolic Ca2+ level to counteract effect of abscisic acid in seed germination. Plant Physiol 167:41630–42
     [Google Scholar]
  77. 77. 
    Kovermann P, Meyer S, Hörtensteiner S, Picco C, Scholz-Starke J et al. 2007. The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:61169–80
     [Google Scholar]
  78. 78. 
    Kugler A, Köhler B, Palme K, Wolff P, Dietrich P. 2009. Salt-dependent regulation of a CNG channel subfamily in Arabidopsis. BMC Plant Biol 9:140
     [Google Scholar]
  79. 79. 
    Ladwig F, Dahlke RI, Stührwohldt N, Hartmann J, Harter K, Sauter M. 2015. Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1. Plant Cell 27:61718–29
     [Google Scholar]
  80. 80. 
    Lam HM, Chiu J, Hsieh MH, Meisel L, Oliveira IC et al. 1998. Glutamate-receptor genes in plants. Nature 396:6707125–26
     [Google Scholar]
  81. 81. 
    Larisch N, Schulze C, Galione A, Dietrich P. 2012. An N-terminal dileucine motif directs two-pore channels to the tonoplast of plant cells. Traffic 13:71012–22
     [Google Scholar]
  82. 82. 
    Latz A, Becker D, Hekman M, Müller T, Beyhl D et al. 2007. TPK1, a Ca2+-regulated Arabidopsis vacuole two-pore K+ channel is activated by 14-3-3 proteins. Plant J 52:3449–59
     [Google Scholar]
  83. 83. 
    Latz A, Mehlmer N, Zapf S, Mueller TD, Wurzinger B et al. 2013. Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium-dependent protein kinases (CDPKs). Mol. Plant 6:41274–89
     [Google Scholar]
  84. 84. 
    Lee CP, Maksaev G, Jensen GS, Murcha MW, Wilson ME et al. 2016. MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress. Plant J 88:5809–25
     [Google Scholar]
  85. 85. 
    Lee JS, Wilson ME, Richardson RA, Haswell ES. 2019. Genetic and physical interactions between the organellar mechanosensitive ion channel homologs MSL1, MSL2, and MSL3 reveal a role for inter-organellar communication in plant development. Plant Direct 3:3e00124
     [Google Scholar]
  86. 86. 
    Lee SC, Lan W, Buchanan BB, Luan S 2009. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. PNAS 106:5021419–24
     [Google Scholar]
  87. 87. 
    Lee SC, Lan W-Z, Kim B-G, Li L, Cheong YH et al. 2007. A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. PNAS 104:4015959–64
     [Google Scholar]
  88. 88. 
    Lefoulon C, Boeglin M, Moreau B, Véry AA, Szponarski W et al. 2016. The Arabidopsis AtPP2CA protein phosphatase inhibits the GORK K+ efflux channel and exerts a dominant suppressive effect on phosphomimetic-activating mutations. J. Biol. Chem. 291:126521–33
     [Google Scholar]
  89. 89. 
    Lefoulon C, Waghmare S, Karnik R, Blatt MR. 2018. Gating control and K+ uptake by the KAT1 K+ channel leveraged through membrane anchoring of the trafficking protein SYP121. Plant Cell Environ 41:112668–77
     [Google Scholar]
  90. 90. 
    Li F, Wang J, Ma C, Zhao Y, Wang Y et al. 2013. Glutamate receptor-like channel3.3 is involved in mediating glutathione-triggered cytosolic calcium transients, transcriptional changes, and innate immunity responses in Arabidopsis. Plant Physiol 162:31497–509
     [Google Scholar]
  91. 91. 
    Li L, Kim BG, Cheong YH, Pandey GK, Luan S 2006. A Ca2+ signaling pathway regulates a K+ channel for low-K response. PNAS 103:12625–30
     [Google Scholar]
  92. 92. 
    Ligaba A, Dreyer I, Margaryan A, Schneider DJ, Kochian L, Piñeros M. 2013. Functional, structural and phylogenetic analysis of domains underlying the Al sensitivity of the aluminum-activated malate/anion transporter, TaALMT1. Plant J 76:5766–80
     [Google Scholar]
  93. 93. 
    Luan S. 2009. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:137–42
     [Google Scholar]
  94. 94. 
    Maathuis FJM. 2011. Vacuolar two-pore K+ channels act as vacuolar osmosensors. New Phytol 191:184–91
     [Google Scholar]
  95. 95. 
    Maierhofer T, Diekmann M, Offenborn JN, Lind C, Bauer H et al. 2014. Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci. Signal. 7:342ra86
     [Google Scholar]
  96. 96. 
    Maierhofer T, Lind C, Huttl S, Scherzer S, Papenfuss M et al. 2014. A single-pore residue renders the Arabidopsis root anion channel SLAH2 highly nitrate selective. Plant Cell 26:62554–67
     [Google Scholar]
  97. 97. 
    Maity K, Heumann JM, McGrath AP, Kopcho NJ, Hsu P-K et al. 2019. Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating. PNAS 116:2814309–18Application of X-ray analyses to protein crystals to obtain the three-dimensional structure of OSCA1.
     [Google Scholar]
  98. 98. 
    Marmagne A, Vinauger-Douard M, Monachello D, De Longevialle AF, Charon C et al. 2007. Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively. J. Exp. Bot. 58:123385–93
     [Google Scholar]
  99. 99. 
    Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K et al. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:41646–67
     [Google Scholar]
  100. 100. 
    Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y. 2006. Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol 142:145–53
     [Google Scholar]
  101. 101. 
    Mattera R, Boehm M, Chaudhuri R, Prabhu Y, Bonifacino JS. 2011. Conservation and diversification of dileucine signal recognition by adaptor protein (AP) complex variants. J. Biol. Chem. 286:32022–30
     [Google Scholar]
  102. 102. 
    Meena MK, Prajapati R, Krishna D, Divakaran K, Pandey Y et al. 2019. The Ca2+ channel CNGC19 regulates Arabidopsis defense against Spodoptera herbivory. Plant Cell 31:71539–62
     [Google Scholar]
  103. 103. 
    Meyer S, Mumm P, Imes D, Endler A, Weder B et al. 2010. AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63:61054–62
     [Google Scholar]
  104. 104. 
    Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B et al. 2011. Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J 67:2247–57
     [Google Scholar]
  105. 105. 
    Michard E, Lima PT, Borges F, Silva AC, Portes MT et al. 2011. Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332:434–37
     [Google Scholar]
  106. 106. 
    Michard E, Simon AA, Tavares B, Wudick MM, Feijó JA. 2017. Signaling with ions: the keystone for apical cell growth and morphogenesis in pollen tubes. Plant Physiol 173:191–111
     [Google Scholar]
  107. 107. 
    Mikosch M, Hurst A, Hertel B, Homann U. 2006. Diacidic motif is required for efficient transport of the K+ channel KAT1 to the plasma membrane. Plant Physiol 142:3923–30
     [Google Scholar]
  108. 108. 
    Miller EA, Beilharz TH, Malkus PN, Lee MCS, Hamamoto S et al. 2003. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:4497–509
     [Google Scholar]
  109. 109. 
    Moeder W, Urquhart W, Ung H, Yoshioka K. 2011. The role of cyclic nucleotide-gated ion channels in plant immunity. Mol. Plant 4:3442–52
     [Google Scholar]
  110. 110. 
    Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF et al. 2006. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure. PLOS Biol 4:101749–62
     [Google Scholar]
  111. 111. 
    Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:7463422–26
     [Google Scholar]
  112. 112. 
    Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H et al. 2008. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–86
     [Google Scholar]
  113. 113. 
    Nguyen CT, Depré S, Thomine S, Filleur S, Jossier M et al. 2016. Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol 57:4764–75
     [Google Scholar]
  114. 114. 
    Nguyen TH, Huang S, Meynard D, Chaine C, Michel R et al. 2017. A dual role for the OsK5.2 ion channel in stomatal movements and K+ loading into xylem sap. Plant Physiol 174:42409–18
     [Google Scholar]
  115. 115. 
    Ortiz-Ramírez C, Michard E, Simon AA, Damineli DSC, Hernández-Coronado M et al. 2017. GLUTAMATE RECEPTOR-LIKE channels are essential for chemotaxis and reproduction in mosses. Nature 549:767091–95
     [Google Scholar]
  116. 116. 
    Pantoja O, Gelli A, Blumwald E. 1992. Characterization of vacuolar malate and K+ channels under physiological conditions. Plant Physiol 100:31137–41
     [Google Scholar]
  117. 117. 
    Pantoja O, Smith JAC. 2002. Sensitivity of the plant vacuolar malate channel to pH, Ca2+ and anion-channel blockers. J. Membr. Biol. 186:131–42
     [Google Scholar]
  118. 118. 
    Pei Z, Ward J, Schroeder J. 1999. Magnesium sensitizes slow vacuolar channels to physiological cytosolic calcium and inhibits fast vacuolar channels in fava bean guard cell vacuoles. Plant Physiol 121:3977–86
     [Google Scholar]
  119. 119. 
    Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J et al. 2005. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:7031404–8
     [Google Scholar]
  120. 120. 
    Pineros MA. 2001. A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol 125:1292–305
     [Google Scholar]
  121. 121. 
    Price MB, Kong D, Okumoto S. 2013. Inter-subunit interactions between Glutamate-Like Receptors in Arabidopsis. Plant Signal. Behav. 8:12e27034
     [Google Scholar]
  122. 122. 
    Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M et al. 2002. AtKC1, a silent Arabidopsis potassium channel α-subunit modulates root hair K+ influx. PNAS 99:64079–84
     [Google Scholar]
  123. 123. 
    Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD 2002. Aluminum activates an anion channel in the apical cells of wheat roots. PNAS 94:126547–52
     [Google Scholar]
  124. 124. 
    Saito S, Hamamoto S, Moriya K, Matsuura A, Sato Y et al. 2018. N-myristoylation and S-acylation are common modifications of Ca2+-regulated Arabidopsis kinases and are required for activation of the SLAC1 anion channel. New Phytol 218:41504–21
     [Google Scholar]
  125. 125. 
    Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K et al. 2010. Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol 51:3354–65
     [Google Scholar]
  126. 126. 
    Sasaki T, Tsuchiya Y, Ariyoshi M, Ryan PR, Furuichi T, Yamamoto Y. 2014. A domain-based approach for analyzing the function of aluminum-activated malate transporters from wheat (Triticum aestivum) and Arabidopsis thaliana in Xenopus oocytes. Plant Cell Physiol 55:122126–38
     [Google Scholar]
  127. 127. 
    Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ et al. 2004. A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:5645–53
     [Google Scholar]
  128. 128. 
    Schäfer N, Maierhofer T, Herrmann J, Jørgensen M-E, Lind C et al. 2018. A tandem amino acid residue motif in guard cell SLAC1 anion channel of grasses allows for the control of stomatal aperture by nitrate. Curr. Biol. 28:1370–79
     [Google Scholar]
  129. 129. 
    Schroeder JI, Hedrich R, Fernandez JM. 1984. Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312:5992361–62
     [Google Scholar]
  130. 130. 
    Schroeder JI, Keller BU 1992. Two types of anion channel currents in guard cells with distinct voltage regulation. PNAS 89:115025–29
     [Google Scholar]
  131. 131. 
    Schroeder JI, Ward JM, Gassmann W. 1994. Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annu. Rev. Biophys. Biomol. Struct. 23:441–71
     [Google Scholar]
  132. 132. 
    Schulze C, Sticht H, Meyerhoff P, Dietrich P. 2011. Differential contribution of EF-hands to the Ca2+-dependent activation in the plant two-pore channel TPC1. Plant J 68:3424–32
     [Google Scholar]
  133. 133. 
    Sharma T, Dreyer I, Riedelsberger J. 2013. The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Front. Plant Sci. 4:224
     [Google Scholar]
  134. 134. 
    Shih HW, Depew CL, Miller ND, Monshausen GB. 2015. The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana. Curr. Biol. 25:233119–25
     [Google Scholar]
  135. 135. 
    Sieben C, Mikosch M, Brandizzi F, Homann U. 2008. Interaction of the K+-channel KAT1 with the coat protein complex II coat component Sec24 depends on a di-acidic endoplasmic reticulum export motif. Plant J 56:6997–1006
     [Google Scholar]
  136. 136. 
    Singh SK, Chien CT, Chang IF. 2016. The Arabidopsis glutamate receptor-like gene GLR3.6 controls root development by repressing the Kip-related protein gene KRP4. J. Exp. Bot. 67:61853–69
     [Google Scholar]
  137. 137. 
    Sussman MR. 1992. Shaking Arabidopsis thaliana. Science 256:619
     [Google Scholar]
  138. 138. 
    Sutter J-U, Sieben C, Hartel A, Eisenach C, Thiel G, Blatt MR. 2007. Abscisic acid triggers the endocytosis of the Arabidopsis KAT1 K+ channel and its recycling to the plasma membrane. Curr. Biol. 17:161396–402
     [Google Scholar]
  139. 139. 
    Sutter J-U, Campanoni P, Tyrrell M, Blatt MR. 2006. Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18:4935–54
     [Google Scholar]
  140. 140. 
    Tang L, Zhang X, DeCaen P, Hasegawa K, He J et al. 2012. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486:7401130–34
     [Google Scholar]
  141. 141. 
    Tapken D, Anschütz U, Liu L-H, Huelsken T, Seebohm G et al. 2013. A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids. Sci. Signal. 6:ra47
     [Google Scholar]
  142. 142. 
    Tunc-Ozdemir M, Rato C, Brown E, Rogers S, Mooneyham A et al. 2013. Cyclic nucleotide gated channels 7 and 8 are essential for male reproductive fertility. PLOS ONE 8:2e55277
     [Google Scholar]
  143. 143. 
    Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR et al. 2013. A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 161:21010–20
     [Google Scholar]
  144. 144. 
    Vahisalu T, Kollist H, Wang Y-F, Nishimura N, Chan W-Y et al. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–91
     [Google Scholar]
  145. 145. 
    Vieira-Pires RS, Morais-Cabral JH. 2010. 310 helices in channels and other membrane proteins. J. Gen. Physiol. 136:6585–92
     [Google Scholar]
  146. 146. 
    Vincent TR, Avramova M, Canham J, Higgins P, Bilkey N et al. 2017. Interplay of plasma membrane and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding. Plant Cell 29:1460–79
     [Google Scholar]
  147. 147. 
    Vincill ED, Clarin AE, Molenda JN, Spalding EP. 2013. Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis. Plant Cell 25:41304–13
     [Google Scholar]
  148. 148. 
    Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K. 2006. Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J 48:2296–306
     [Google Scholar]
  149. 149. 
    von der Fecht-Bartenbach J, Bogner M, Krebs M, Stierhof Y-D, Schumacher K, Ludewig U. 2007. Function of the anion transporter AtCLC-d in the trans-Golgi network. Plant J 50:3466–74
     [Google Scholar]
  150. 150. 
    Wang C, Hu H, Qin X, Zeise B, Xu D et al. 2016. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell 28:2568–82
     [Google Scholar]
  151. 151. 
    Wang Y-F, Munemasa S, Nishimura N, Ren H-M, Robert N et al. 2013. Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. Plant Physiol 163:2578–90
     [Google Scholar]
  152. 152. 
    Wang Y, Wu W-H. 2013. Potassium transport and signaling in higher plants. Annu. Rev. Plant Biol. 64:451–76
     [Google Scholar]
  153. 153. 
    Ward JM, Mäser P, Schroeder JI. 2008. Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71:59–82
     [Google Scholar]
  154. 154. 
    Ward JM, Schroeder J. 1994. 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. Plant Cell 6:5669–83
     [Google Scholar]
  155. 155. 
    Wudick MM, Portes MT, Michard E, Rosas-Santiago P, Lizzio MA et al. 2018. CORNICHON sorting and regulation of GLR channels underlie pollen tube Ca2+ homeostasis. Science 360:6388533–36
     [Google Scholar]
  156. 156. 
    Yamamoto Y, Negi J, Wang C, Isogai Y, Schroeder JI, Iba K. 2016. The transmembrane region of guard cell SLAC1 channels perceives CO2 signals via an ABA-independent pathway in Arabidopsis. Plant Cell 28:2557–67
     [Google Scholar]
  157. 157. 
    Yoshida R, Mori IC, Kamizono N, Shichiri Y, Shimatani T et al. 2016. Glutamate functions in stomatal closure in Arabidopsis and fava bean. J. Plant Res. 129:139–49
     [Google Scholar]
  158. 158. 
    Yuan F, Yang H, Xue Y, Kong D, Ye R et al. 2014. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:7522367–71Identification of osmosensitive calcium-permeable cation channels.
     [Google Scholar]
  159. 159. 
    Yuen CCY, Christopher DA. 2013. The group IV-A cyclic nucleotide-gated channels, CNGC19 and CNGC20, localize to the vacuole membrane in Arabidopsis thaliana. AoB Plants 5:plt012
     [Google Scholar]
  160. 160. 
    Zhang B, Karnik R, Waghmare S, Donald N, Blatt MR. 2017. VAMP721 conformations unmask an extended motif for K+ channel binding and gating control. Plant Physiol 173:1536–51
     [Google Scholar]
  161. 161. 
    Zhang B, Wallmeroth N, Wang Y, Karnik R, Grefen C, Blatt MR. 2015. The Arabidopsis R-SNARE VAMP721 interacts with KAT1 and KC1 K+ channels to moderate K+ current at the plasma membrane. Plant Cell 27:61697–717
     [Google Scholar]
  162. 162. 
    Zhang H, Zhao F-G, Tang R-J, Yu Y, Song J et al. 2017. Two tonoplast MATE proteins function as turgor-regulating chloride channels in Arabidopsis. PNAS 114:10E2036–45
     [Google Scholar]
  163. 163. 
    Zhang J, Baetz U, Krugel U, Martinoia E, De Angeli A. 2013. Identification of a probable pore-forming domain in the multimeric vacuolar anion channel AtALMT9. Plant Physiol 163:2830–43
     [Google Scholar]
  164. 164. 
    Zhang J, Martinoia E, De Angeli A. 2014. Cytosolic nucleotides block and regulate the Arabidopsis vacuolar anion channel AtALMT9. J. Biol. Chem. 289:3725581–89
     [Google Scholar]
  165. 165. 
    Zhang J, Miao Y, Schroeder JI, Hauser F, Wang N et al. 2018. Identification of SLAC1 anion channel residues required for CO2/bicarbonate sensing and regulation of stomatal movements. PNAS 115:4411129–37
     [Google Scholar]
  166. 166. 
    Zhang S, Pan Y, Tian W, Dong M, Zhu H et al. 2017. Arabidopsis CNGC14 mediates calcium influx required for tip growth in root hairs. Mol. Plant 10:71004–6
     [Google Scholar]
  167. 167. 
    Zheng X, He K, Kleist T, Chen F, Luan S 2015. Anion channel SLAH3 functions in nitrate-dependent alleviation of ammonium toxicity in Arabidopsis. Plant Cell Environ 38:3474–86
     [Google Scholar]
  168. 168. 
    Zhou L, Lan W, Jiang Y, Fang W, Luan S. 2014. A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol. Plant 7:2369–76
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-081519-035925
Loading
Recent Advances in the Physiology of Ion Channels in Plants
Annual Review of Plant Biology 72, 463 (2021); https://doi.org/10.1146/annurev-arplant-081519-035925
/content/journals/10.1146/annurev-arplant-081519-035925
/content/journals/10.1146/annurev-arplant-081519-035925
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error