Vacuolar chloride fluxes impact ion content and distribution during early salinity stress

Plant Physiology

Volumn 172, Issue 2, 2016, Pages 1167-1181

  Baetz, Ulrike ^a   Eisenach, Cornelia ^a   Tohge, Takayuki ^b   Martinoia, Enrico ^a   De Angeli, Alexis ^c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALMT9 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CHLORIDE; CHLORIDE CHANNEL; ION; SODIUM; SODIUM CHLORIDE;

ARABIDOPSIS; CELL VACUOLE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; ION TRANSPORT; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS; PLANT ROOT; PLANT STOMA; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALINITY; SHOOT; TRANSGENIC PLANT; XYLEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLORIDE CHANNELS; CHLORIDES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; ION TRANSPORT; IONS; MUTATION; PLANT ROOTS; PLANT SHOOTS; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALINITY; SODIUM; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; VACUOLES; XYLEM;

EID: 84989300029     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00183     Document Type: Article

References (96)

1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11: 36-42
2. Arrivault S, Senger T, Krämer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46: 861-879
3. Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse JM, Gambale F, Thomine S, Wege S (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu Rev Plant Biol 62: 25-51
4. Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24: 1127-1142
5. Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23: 224-239
6. Baud S, Wuillème S, Lemoine R, Kronenberger J, Caboche M, Lepiniec L, Rochat C (2005) The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J 43: 824-836
7. Britto DT, Ruth TJ, Lapi S, Kronzucker HJ (2004) Cellular and whole-plant chloride dynamics in barley: insights into chloride-nitrogen interactions and salinity responses. Planta 218: 615-622
8. Brumós J, Talón M, Bouhlal R, Colmenero-Flores JM (2010) Cl- homeostasis in includer and excluder citrus rootstocks: transport mechanisms and identification of candidate genes. Plant Cell Environ 33: 2012-2027
9. Cataldo D, Maroon L, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissues by nitration of salicylic acid. Commun Soil Sci Plant Anal 6: 71-80
10. Chen CZ, Lv XF, Li JY, Yi HY, Gong JM (2012) Arabidopsis NRT1.5 is another essential component in the regulation of nitrate reallocation and stress tolerance. Plant Physiol 159: 1582-1590
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
12. Colcombet J, Lelièvre F, Thomine S, Barbier-Brygoo H, Frachisse JM (2005) Distinct pH regulation of slow and rapid anion channels at the plasma membrane of Arabidopsis thaliana hypocotyl cells. J Exp Bot 56: 1897-1903
13. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15: 1196-1200
14. Craig Plett D, Møller IS (2010) Na(+) transport in glycophytic plants: what we know and would like to know. Plant Cell Environ 33: 612-626
15. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469
16. Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30: 497-507
17. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442: 939-942
18. De Angeli A, Zhang J, Meyer S, Martinoia E (2013) AtALMT9 is a malateactivated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat Commun 4: 1804
19. De Rybel B, van den Berg W, Lokerse A, Liao CY, van Mourik H, Möller B, Peris CL, Weijers D (2011) A versatile set of ligation-independent cloning vectors for functional studies in plants. Plant Physiol 156: 1292-1299
20. Frachisse JM, Colcombet J, Guern J, Barbier-Brygoo H (2000) Characterization of a nitrate-permeable channel able to mediate sustained anion efflux in hypocotyl cells from Arabidopsis thaliana. Plant J 21: 361-371
21. Geelen D, Lurin C, Bouchez D, Frachisse JM, Lelièvre F, Courtial B, Barbier-Brygoo H, Maurel C (2000) Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. Plant J 21: 259-267
22. Geilfus CM, Mithöfer A, Ludwig-Müller J, Zörb C, Muehling KH (2015) Chloride-inducible transient apoplastic alkalinizations induce stomata closure by controlling abscisic acid distribution between leaf apoplast and guard cells in salt-stressed Vicia faba. New Phytol 208: 803-816
23. Genc Y, Oldach K, Taylor J, Lyons GH (2016) Uncoupling of sodium and chloride to assist breeding for salinity tolerance in crops. New Phytol 210: 145-156
24. Gilliham M, Tester M (2005) The regulation of anion loading to the maize root xylem. Plant Physiol 137: 819-828
25. Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20: 1203-1207
26. Hall D, Evans AR, Newbury HJ, Pritchard J (2006) Functional analysis of CHX21: a putative sodium transporter in Arabidopsis. J Exp Bot 57: 1201-1210
27. Henderson SW, Baumann U, Blackmore DH, Walker AR, Walker RR, Gilliham M (2014) Shoot chloride exclusion and salt tolerance in grapevine is associated with differential ion transporter expression in roots. BMC Plant Biol 14: 273
28. Henderson SW, Wege S, Qiu J, Blackmore DH, Walker AR, Tyerman SD, Walker RR, Gilliham M (2015) Grapevine and Arabidopsis cationchloride cotransporters localize to the Golgi and trans-Golgi network and indirectly influence long-distance ion transport and plant salt tolerance. Plant Physiol 169: 2215-2229
29. Huang CX, Van Steveninck RF (1989) Maintenance of low cl concentrations in mesophyll cells of leaf blades of barley seedlings exposed to salt stress. Plant Physiol 90: 1440-1443
30. Hurth MA, Suh SJ, Kretzschmar T, Geis T, Bregante M, Gambale F, Martinoia E, Neuhaus HE (2005) Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. Plant Physiol 137: 901-910
31. James RA, Munns R, von Caemmerer S, Trejo C, Miller C, Condon TA (2006) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl- in salt-affected barley and durum wheat. Plant Cell Environ 29: 2185-2197
32. Jiang X, Leidi EO, Pardo JM (2010) How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal Behav 5: 792-795
33. Jossier M, Kroniewicz L, Dalmas F, Le Thiec D, Ephritikhine G, Thomine S, Barbier-Brygoo H, Vavasseur A, Filleur S, Leonhardt N (2010) The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant J 64: 563-576
34. Karley AJ, Leigh RA, Sanders D (2000a) Differential ion accumulation and ion fluxes in the mesophyll and epidermis of barley. Plant Physiol 122: 835-844
35. Karley AJ, Leigh RA, Sanders D (2000b) Where do all the ions go? The cellular basis of differential ion accumulation in leaf cells. Trends Plant Sci 5: 465-470
36. Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Bréhaut V, Miller A, Daniel-Vedele F, Sakakibara H, Krapp A (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24: 245-258
37. Kovermann P, Meyer S, Hörtensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52: 1169-1180
38. Krebs M, Beyhl D, Görlich E, Al-Rasheid KA, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107: 3251-3256
39. Läuchli A, James RA, Huang CX, McCully M, Munns R (2008) Cellspecific localization of Na+ in roots of durum wheat and possible control points for salt exclusion. Plant Cell Environ 31: 1565-1574
40. 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. Proc Natl Acad Sci USA 106: 21419-21424
41. Leidi EO, Barragán V, Rubio L, El-Hamdaoui A, Ruiz MT, Cubero B, Fernández JA, Bressan RA, Hasegawa PM, Quintero FJ, et al (2010) The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J 61: 495-506
42. Lelandais-Brière C, Jovanovic M, Torres GA, Perrin Y, Lemoine R, Corre-Menguy F, Hartmann C (2007) Disruption of AtOCT1, an organic cation transporter gene, affects root development and carnitine-related responses in Arabidopsis. Plant J 51: 154-164
43. Léran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, et al (2014) A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19: 5-9
44. Li B, Byrt CS, Qiu J, Baumann U, Hrmova M, Evrard A, Johnson AA, Birnbaum KD, Mayo GM, Jha D, et al (2016) Identification of a stelarlocalised transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiol 170: 1014-1029
45. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323
46. Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, et al (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22: 1633-1646
47. Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277: 5360-5368
48. Lim CW, Kim JH, Baek W, Kim BS, Lee SC (2012) Functional roles of the protein phosphatase 2C, AtAIP1, in abscisic acid signaling and sugar tolerance in Arabidopsis. Plant Sci 187: 83-88
49. 2+-ATPase of Arabidopsis thaliana. Plant Mol Biol 84: 387-397
50. Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22: 1005-1013
51. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2004) dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J 37: 720-729
52. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellindeactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56: 613-626
53. Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58: 83-102
54. Martinoia E, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Annu Rev Plant Biol 63: 183-213
55. Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N, et al (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531: 157-161
56. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25: 295-303
57. Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B, Gambale F, Martinoia E (2011) Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J 67: 247-257
58. Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21: 2163-2178
59. Møller IS, Tester M (2007) Salinity tolerance of Arabidopsis: a good model for cereals? Trends Plant Sci 12: 534-540
60. Monachello D, Allot M, Oliva S, Krapp A, Daniel-Vedele F, Barbier-Brygoo H, Ephritikhine G (2009) Two anion transporters AtClCa and AtClCe fulfil interconnecting but not redundant roles in nitrate assimilation pathways. New Phytol 183: 88-94
61. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25: 239-250
62. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681
63. Munns R, Wallace PA, Teakle NL, Colmer TD (2010) Measuring soluble ion concentrations (Na(+), K(+), Cl(-)) in salt-treated plants. Methods Mol Biol 639: 371-382
64. Nagy R, Grob H, Weder B, Green P, Klein M, Frelet-Barrand A, Schjoerring JK, Brearley C, Martinoia E (2009) The Arabidopsis ATPbinding cassette protein AtMRP5/AtABCC5 is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J Biol Chem 284: 33614-33622
65. Nakamura RL, McKendree WL Jr, Hirsch RE, Sedbrook JC, Gaber RF, Sussman MR (1995) Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiol 109: 371-374
66. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207: 123-131
67. Nguyen CT, Agorio A, Jossier M, Depré S, Thomine S, Filleur S (2016) Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol 57: 764-775
68. Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H (2007) ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res 35: D863-D869
69. Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61: 1205-1213
70. Peng JS, Gong JM (2014) Vacuolar sequestration capacity and longdistance metal transport in plants. Front Plant Sci 5: 19
71. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18: 2368-2379
72. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45
73. Pommerrenig B, Popko J, Heilmann M, Schulmeister S, Dietel K, Schmitt B, Stadler R, Feussner I, Sauer N (2013) SUCROSE TRANSPORTER 5 supplies Arabidopsis embryos with biotin and affects triacylglycerol accumulation. Plant J 73: 392-404
74. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140
75. Rubio S, Rodrigues A, Saez A, Dizon MB, Galle A, Kim TH, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150: 1345-1355
76. Shapira O, Khadka S, Israeli Y, Shani U, Schwartz A (2009) Functional anatomy controls ion distribution in banana leaves: significance of Na+ seclusion at the leaf margins. Plant Cell Environ 32: 476-485
77. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97: 6896-6901
78. Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants. Plant Cell 14: 465-477
79. Sibole JV, Cabot C, Poschenrieder C, Barceló J (2003) Efficient leaf ion partitioning, an overriding condition for abscisic acid-controlled stomatal and leaf growth responses to NaCl salinization in two legumes. J Exp Bot 54: 2111-2119
80. Storey R, Schachtman DP, Thomas MR (2003) Root structure and cellular chloride, sodium and potassium distribution in salinized grapevines. Plant Cell Environ 26: 789-800
81. Strohm AK, Vaughn LM, Masson PH (2015) Natural variation in the expression of ORGANIC CATION TRANSPORTER 1 affects root length responses to cadaverine in Arabidopsis. J Exp Bot 66: 853-862
82. Sunarpi HT, Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44: 928-938
83. Taochy C, Gaillard I, Ipotesi E, Oomen R, Leonhardt N, Zimmermann S, Peltier JB, Szponarski W, Simonneau T, Sentenac H, et al (2015) The Arabidopsis root stele transporter NPF2.3 contributes to nitrate translocation to shoots under salt stress. Plant J 83: 466-479
84. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK (2011) Additive effects of Na+ and Cl- ions on barley growth under salinity stress. J Exp Bot 62: 2189-2203
85. Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl- ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61: 4449-4459
86. Teakle NL, Tyerman SD (2010) Mechanisms of Cl(-) transport contributing to salt tolerance. Plant Cell Environ 33: 566-589
87. Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A, Makam SN, Lee OR, Richards EL, Murphy AS, Sato F, et al (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17: 2922-2939
88. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot (Lond) 91: 503-527
89. Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, et al (2010) Perturbation of indole-3-butyric acid homeostasis by the UDPglucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22: 2660-2679
90. Wege S, De Angeli A, Droillard MJ, Kroniewicz L, Merlot S, Cornu D, Gambale F, Martinoia E, Barbier-Brygoo H, Thomine S, et al (2014) Phosphorylation of the vacuolar anion exchanger AtCLCa is required for the stomatal response to abscisic acid. Sci Signal 7: ra65
91. Wege S, Jossier M, Filleur S, Thomine S, Barbier-Brygoo H, Gambale F, De Angeli A (2010) The proline 160 in the selectivity filter of the Arabidopsis NO(3)(-)/H(+) exchanger AtCLCa is essential for nitrate accumulation in planta. Plant J 63: 861-869
92. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, et al (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27: 581-590
93. Yang KY, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98: 741-746
94. Yu Y, Assmann SM (2016) The effect of NaCl on stomatal opening in Arabidopsis wild type and agb1 heterotrimeric G-protein mutant plants. Plant Signal Behav 11: e1085275, doi: 10.1080/15592324.2015.1085275
95. Zhang J, Baetz U, Krügel U, Martinoia E, De Angeli A (2013) Identification of a probable pore-forming domain in the multimeric vacuolar anion channel AtALMT9. Plant Physiol 163: 830-843
96. + influx in Vicia guard cells. J Plant Physiol 168: 903-910