ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)
"Biotechnologia Acta" v. 6, no. 3, 2013
https://doi.org/10.15407/biotech6.03.009
Р. 9-22, Bibliography 110, Ukrainian.
Universal Decimal classification: 57.023 581.1
THE TONOPLAST TRANSPORT SYSTEMS OF PLANT VACUOLES AND THEIR POTENTIAL APPLICATION IN BIOTECHNOLOGY
Institute of Food Biotechnology and Genomics of National Academy of Sciences of Ukraine, Kyiv
The pivotal role of plant vacuoles in plant survival was discussed in the review. Particularly, the providing of cellular turgor, accumulation of inorganic osmolytes and nutrients are the primary tasks of these cellular organelles. The main mechanisms of tonoplast transport systems were described. The known transport pathways of minerals, heavy metals, vitamins and other organic compounds were
classified and outlined. The main systems of membrane vacuolar transport were reviewed. The outline of the physiological functions and features of vacuolar membrane transport proteins were performed.
The physiological role of transport of minerals, nutrients and other compounds into vacuoles were discussed. This article reviews the main types of plant vacuoles and their functional role in plant cell. Current state and progress in vacuolar transport research was outlined. The examples of application for rinciples and mechanisms of vacuolar membrane transport in plant biotechnology were iven. The perspectives and approaches in plant and food biotechnology concerning transport and physiology of vacuoles are discussed.
Key words: vacuole, tonoplast, membrane transport, channels, transporters, biotechnology.
© Palladin Institute of Biochemistry of National Academy of Sciences of Ukraine, 2013
References
1. Neuhaus J. M., Martinoia E. Plant Vacuoles. eLS. 2011,
https://doi.org/10.1002/ 9780470015902.a0001675.pub2.
2. Isayenkov S., Isner J. C., Maathuis F. J. M. Vacuolar ion channels: Roles in plant nutrition and signaling. FEBS Lett. 2010, V.?584, P. 1982–1988.
3. Marty F. Plant vacuoles. Plant Cell. 1999, V. 11, Р. 587–600.
4. Maeshima M. Tonoplast transporters: Organization and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, V. 52, P. 469–497.
https://doi.org/10.1146/annurev.arplant.52.1.469
5. Sze H., Li X., Palmgren M. G. Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. Plant Cell. 1999, V. 11, P. 677–689.
6. Martinoia E., Massonneau A., Frangne N. Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol. 2000, V. 41, P. 1175–1186.
https://doi.org/10.1093/pcp/pcd059
7. Hedrich R., Barbier-Brygoo H., Felle H.?H. General mechanisms for solute transport across the tonoplast of plant vacuoles: a patch clamp survey of ion channels and proton pumps. Bot. Acta. 1988, V. 101, P. 7–13.
https://doi.org/10.1111/j.1438-8677.1988.tb00003.x
8. Maeshima M. Tonoplast transporters: Organization and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, V. 52, P. 469–497.
https://doi.org/10.1146/annurev.arplant.52.1.469https://doi.org/10.1146/annurev.arplant.52.1.469https://doi.org/10.1146/annurev.arplant.52.1.469
9. Jiang J., Phillips T., Hamm C. The protein storage vacuole: a unique compound organelle. J. Cell Biol. 2001, V. 155, P. 991–1002.
https://doi.org/10.1083/jcb.200107012
10. Barkla B. J., Pantoja O. Physiology of ion transport across the tonoplast of higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, V. 47, P. 159–184.
https://doi.org/10.1146/annurev.arplant.47.1.159
11. Hedrich R., Neher E. Cytoplasmic calcium regulates voltagedependent ion channels in plant vacuoles. Nature. 1987, V. 329, P. 833–836.
https://doi.org/10.1038/329833a0
12. Demidchik V., Maathuis F. J. M. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol. 2007, V.?175, P. 387–404.
https://doi.org/10.1111/j.1469-8137.2007.02128.x
13. Pantoja O., Dainty J., Blumwald E. Ion channels in vacuoles from halophytes and glycophytes. FEBS Lett. 1989, V. 255, P.?92–96.
https://doi.org//10.1016/0014-5793(89)81067-1
14. Fernie A. R., Martinoia E. Malate. Jack of all trades or master of a few? Phytochemistry. 2009, V. 70, P. 828–832.
https://doi.org/10.1016/j.phytochem.2009.04.023
15. Martinoia E., Maeshima M., Neuhaus H. E. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 2007, V. 58, P. 83–102.
https://doi.org/10.1093/jxb/erl183
16. Jaquinod M., Villiers F., Kieffer-Jaquinod S. A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics. 2007, V. 6, P. 394–412.
https://doi.org/10.1074/mcp.M600250-MCP200
17. Hafke J. B., Hafke Y., Smith J. A. Vacuolar malate uptake is mediated by an anion-selective inward rectifier. Plant J. 2003, V. 35, P. 116–128.
https://doi.org/10.1046/j.1365-313X.2003.01781.x
18. Kovermann P., Meyer S., Hoertensteiner S. The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J. 2007, V. 52, P. 1169–1180.
https://doi.org/10.1111/j.1365-313X.2007.03367.x
19. Liu J., Magalhaes J. V., Shaff J., Kochian L. V. Aluminium-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminium tolerance. Plant J. 2009, V. 57, P. 389–399.
https://doi.org/10.1111/j.1365-313X.2008.03696.x
20. Harada H., Kuromori T., Hirayama T. Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLCc, to variation in nitrate levels. J. Exp. Bot. 2004, V. 405, P. 2005–2014.
https://doi.org/10.1093/jxb/erh224
21. De Angeli A., Monachello D., Ephritikhine G. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature. 2006, V. 442, P.?939–942.
https://doi.org/10.1038/nature05013
22. Zifarelli G., Pusch M. Conversion of the 2Cl-/1H+ antiporter ClC-5 in a NO3–/H+ antiporter by a single point mutation. EMBO J. 2009, V. 28, P. 175–182.
https://doi.org/10.1038/emboj.2008.284
23. Nakamura A., Fukuda A., Sakai S., Tanaka Y. Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant Cell Physiol. 2006, V. 47, P. 32–42.
24. Lуpez-Rodriguez A., Trejo A., Coyne L. The product of the gene GEF1 of Saccharomyces cerevisiae transports Cl– across the plasma membrane. FEMS Yeast Res. 2007, V. 8, P. 1218–1229.
25. Kataoka T., Watanabe-Takahashi A., Hayashi N. Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell. 2004, V. 16, P. 2693–2704.
https://doi.org/10.1105/tpc.104.023960
26. Gobert A., Park G., Amtmann A. Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a nonselective ion transporter involved in germination and cation transport. J. Exp. Bot. 2006, V. 57, P. 791–800.
https://doi.org/10.1093/jxb/erj064
27. Malho R. Coding information in plant cells: the multiple roles of Ca2+ as a second messenger. Plant Biol. 1999, V. 1, P.?487–494.
https://doi.org/10.1111/j.1438-8677.1999.tb00774.x
28. Alexandre J., Lassalles J. P., Kado R. T. Opening of Ca2+ channels in isolated red beet root vacuole membrane by inositol 1,4,5-triphosphate. Nature. 1990, V. 343, P. 567–570.
https://doi.org/10.1038/343567a0
29. Allen G. J., Muir S. R., Sanders D. Release of Ca2+ from individual plant vacuoles by both Insp3 and cyclic ADP-ribose. Science. 1995, V. 268, P. 735–737.
https://doi.org/10.1126/science.7732384
30. Allen G. J., Sanders D. Vacuolar ion channels of higher plants. Adv. Bot. Res. 1997, V. 25, P. 217–252.
https://doi.org/10.1016/S0065-2296(08)60154-8
31. Pottosin I. I., Wherrett T., Shabala S. SV channels dominate the vacuolar Ca2+ release during intracellular signalling. FEBS Lett. 2009, V. 583, P. 921–926.
https://doi.org/10.1016/j.febslet.2009.02.009
32. Isaienkov S. V. Physiological and molecular aspects of plant salt stress. Tsitologiya i genetika. 2012, N 46, P. 50–71. (In Russian).
33. Peiter E., Maathuis F. J .M., Mills L. N. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature. 2005, V. 434, P. 404–408.
https://doi.org/10.1038/nature03381
34. Kurusu T., Yagala T., Miyao A. Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J. 2005, V. 42, P. 798–809.
https://doi.org/10.1111/j.1365-313X.2005.02415.x
35. Kadota Y., Furuichi T., Ogasawara Y. Identification of putative voltage-dependent Ca2+- permeable channels involved in cryptogein-induced Ca2+ transients and defense responses in tobacco BY-2 cells. Biochem. Biophys. Res. Comm. 2004, V. 317, P. 823–830.
https://doi.org/10.1016/j.bbrc.2004.03.114
36. Furuichi T., Cunningham K. W., Muto S. A putative two pore channel AtTPC1 mediates Ca2+ flux in Arabidopsis leaf cells. Plant Cell Physiol. 2001, V. 42, P. 900–905.
https://doi.org/10.1093/pcp/pce145
37. Allen G. J., Chu S. P., Schumacher K. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science. 2000, V. 289, P. 2338–2342.
https://doi.org/10.1126/science.289.5488.2338
38. Ranf S., Wunnenberg P., Lee J. Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J. 2008, V.?53, P. 287–299.
https://doi.org/10.1111/j.1365-313X.2007.03342.x
39. Beyhl D., Hurtensteiner S., Martinoia E. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J. 2009, V. 58, P. 715–723.
https://doi.org/10.1111/j.1365-313X.2009.03820.x
40. Demuro A., Parker I. Imaging single-channel calcium microdomains. Cell Calcium. 2006, V. 40, P. 413–422.
https://doi.org/10.1016/j.ceca.2006.08.006
41. Whiteman S. A., Serazetdinova L., Jones A. M. Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics. 2008, V. 8, P.?3536–3547.
https://doi.org/10.1002/pmic.200701104
42. Wang Y. J., Yu J. N., Chen T. Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat. J. Exp. Bot. 2005, V. 56, P. 3051–3060.
https://doi.org/10.1093/jxb/eri302
43. Ward J. M., Schroeder J. I. 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. 1994, V. 6, P. 669–683.
44. Gobert A., Isayenkov S., Voelker C. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in?K+ homeostasis. Proc. Natl. Acad.?Sci.?USA. 2007, V. 104, P.?10726–10731.
https://doi.org/10.1073/pnas.0702595104
45. Voelker C., Schmidt D., Mueller-Roeber B., Czempinski K. Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J. 2006, V. 48, P. 296–306.
https://doi.org/10.1111/j.1365-313X.2006.02868.x
46. Isayenkov S., Isner J. C., Maathuis F. J. M. Membrane localisation diversity of TPK channels and their physiological role. Plant Cell Signal. Behav. 2011, V. 6, P.?1201–1204.
47. Becker D., Geiger D., Dunkel M. AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner. Proc. Natl. Acad. Sci. USA. 2004, V. 101, P. 15621–15626.
https://doi.org/10.1073/pnas.0401502101
48. Dunkel M., Latz A., Schumacher K. Targeting of vacuolar membrane localized members of the TPK channel family. Mol. Plant. 2008, V. 1, P. 938–949.
https://doi.org/10.1093/mp/ssn064
49. Latz A., Becker D., Hekman M. et al. TPK1, a Ca2+-regulated Arabidopsis vacuole two-pore K+ channel is activated by 14-3-3 proteins. Plant J. 2007, V. 52, P. 449–459.
https://doi.org/10.1111/j.1365-313X.2007.03255.x
50. Hamamoto S., Marui J., Matsuoka K. et al. Characterization of a tobacco TPK-type K+ channel as a novel tonoplast K+ channel using yeast tonoplasts. J. Biol. Chem. 2008, V. 283, P. 1911–1920.
https://doi.org/10.1074/jbc.M708213200
51. Isayenkov S., Isner J. C., Maathuis F. J. M. Rice Two-Pore K+ Channels Are Expressed in Different Types of Vacuoles. Plant Cell. 2011, V. 23, P. 756–768.
https://doi.org/10.1105/tpc.110.081463
52. Blumwald E. Sodium transport and salt tolerance in plants. Curr. Opinion Cell Biol. 2000, V. 12, P. 431–434.
https://doi.org/10.1016/S0955-0674(00)00112-5
53. Apse M. P., Aharon G. S., Snedden W. A., Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science. 1999, V. 285, P. 1656–1658.
https://doi.org/10.1126/science.285.5431.1256
54. Xue Z. Y., Zhi D. Y., Xue G. P. Enhanced salt tolerance of transgenic wheat (Triticum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the ?eld and a reduced level of leaf Na+. Plant Sci. 2004, V. 167, P. 849–859.
https://doi.org/10.1016/j.plantsci.2004.05.034
55. Zhang H. X., Blumwald E. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotechnol. 2001, V. 19, P. 765–768.
https://doi.org/10.1038/90824
56. Li W. Y. F., Wong F. L., Tsai S. N. Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells. Plant Cell Environ. 2006, V. 29, P.?1122–1137.
https://doi.org/10.1111/j.1365-3040.2005.01487.x
57. Fukuda A., Nakamura A., Tanaka Y. Molecular cloning and expression of the Na+/H+ exchager gene in Oryza sativa. Biochim. Biophys. Acta. 1999, 1446,. P.?149–155.
https://doi.org/10.1016/S0167-4781(99)00065-2
58. Yokoi S., Bressan R. A., Hasegawa P. M. Salt Stress Tolerance of Plants. JIRCAS Working Report. 2002, P. 25–33.
59. Fukuda A., Nakamura A., Tagiri A. Function, intracellular localization and the importance of salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant?Cell?Physiol. 2004, V. 45, P. 146–159.
https://doi.org/10.1093/pcp/pch014
60. Chen Z. H., Pottosin I. I., Cuin T. A. Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol. 2007, V. 145, P.?1714–1725.
https://doi.org/10.1104/pp.107.110262
61. Yokoi S., Quintero F. J., Cubero B. et al. Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J. 2002, V. 30, P. 529–539.
https://doi.org/10.1046/j.1365-313X.2002.01309.x
62. Rodriguez-Rosales M. P., Jiang X., Galvez F. J. Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol. 2008, V. 179, P.?366–377.
https://doi.org/10.1111/j.1469-8137.2008.02461.x
63. Jiang X., Leidi E. O., Pardo J. M. How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal. Behav. 2010, V. 5, P. 792–795.
https://doi.org/10.4161/psb.5.7.11767
64. Hirschi К. D., Zhen R., Cunningham K. W. CAX1, an H+/Ca2+ antiporter from Arabidopsis. Proc. Natl. Acad. Sci. USA. 1996, V. 93, P. 8782–8786.
65. Shigaki T., Rees I., Nakhleh N., Hirschi K. D. Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J. Mol. Evol. 2006, V. 63, P.?815–825.
https://doi.org/10.1007/s00239-006-0048-4
66. Manohar M., Shigaki T., Hirschi K. D. Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biol. 2011, V. 4, P. 561–569.
https://doi.org/10.1111/j.1438-8677.2011.00466.x
67. Gunshin H., Mackenzie B., Berger U. V. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 1997, V. 388, P. 482–488.
https://doi.org/10.1038/41343
68. Belouchi A., Kwan T., Gros P. Cloning and characterization of the OsNRAMP family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant. Mol. Biol. 1997, V. 33, P. 1085–1092.
https://doi.org/10.1023/A:1005723304911
69. M?ser P., Thomine S., Schroeder J. I. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001, V. 126, P.?1646–1667.
https://doi.org/10.1104/pp.126.4.1646
70. Williams L. E., Pittman J. K, Hall J. L. Emerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta. 2000, V. 1465, P. 104–126.
https://doi.org/10.1016/S0005-2736(00)00133-4
71. Thomine S., Wang R., Ward J. M. Cadmium and iron transport by members of a plant transporter gene family in Arabidopsis with homology to NRAMP genes. Proc. Natl. Acad. Sci. USA. 2000, V. 97, P. 4991–4996.
https://doi.org/10.1073/pnas.97.9.4991
72. Thomine S., Leli?vre1 F., Debarbieux E. et al. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 2003, V. 34, P.?685–695.
https://doi.org/10.1046/j.1365-313X.2003.01760.x
73. Lanquar V., Lelievre F., Bolte S. et al. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 2005, V.?24, P. 4041–4051.
https://doi.org/10.1038/sj.emboj.7600864
74. Salt D. E., Wagner G. J. Cadmium transport across tonoplast of vesicles from oat roots — evidence for a Cd2+/H+ antiport activity. J.?Biol. Chem. 1993, V. 268, P.?12297–12302.
75. Shaul O., Hilgemann D. W., De Almeida-Engler J. et al. Cloning and characterization of a novel Mg/H exchanger. EMBO J. 1999, V. 18, P. 3973–3980.
https://doi.org/10.1093/emboj/18.14.3973
76. Van Der Zaal B. J., Neuteboom L. W., Pinas J. E. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 1999, V. 119, P.?1047–1055.
https://doi.org/10.1104/pp.119.3.1047
77. Kobae Y., Uemura T., Sato M. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell?Physiol. 2004, V. 45, P.?1749–1758.
https://doi.org/10.1093/pcp/pci015
78. Morel M., Crouzet J., Gravot A. et al. AtHMA3, a P1b-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. 2008, V. 149, P. 894–904.
https://doi.org/10.1104/pp.108.130294
79. Brinch-Pedersen H., Borg S., Tauris B., Holm?P. B. Molecular genetic approaches to increasing mineral availability and vitamin content of cereals. J. Cereal Sci. 2007, V.?46, P. 308–326.
https://doi.org/10.1016/j.jcs.2007.02.004
80. Bolte S., Lanquar V., Soler M. N. Distinct lytic vacuolar compartments are embedded inside the protein storage vacuole of dry and germinating Arabidopsis thaliana seeds. Plant Cell Physiol. 2011, V. 52, P. 1142–1152.
https://doi.org/10.1093/pcp/pcr065
81. Garcia-Molina A., Andrґes-Colґas N., Perea-Garcґia A. The intracellular Arabidopsis COPT5 transport protein is required for hotosynthetic electron transport under severe copper deficiency. Plant J. 2011, V. 65, P. 848–860.
https://doi.org/10.1111/j.1365-313X.2010.04472.x
82. Klaumann S., Nickolaus S. D., Furst S. H., Starck S. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol. 2011, V. 92, P. 393–404.
https://doi.org/10.1111/j.1469-8137.2011.03798.x
83. Fontes N., Ger?s H., Delrot S. Grape Berry Vacuole: A Complex and Heterogeneous Membrane System Specialized in the Accumulation of Solutes. Am. J. Enol. Vitic. 2011, P. 270–278.
https://doi.org/10.5344/ajev.2011.10125
84. Schulz A., Beyhl D., Marten I. Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J. 2011, V. 68, P.?129–136.
https://doi.org/10.1111/j.1365-313X.2011.04672.x
85. Etxeberria E., Pozueta-Romero J., Gonzalez P. In and out of the plant storage vacuole. Plant Sci. 2012, V. 190, P. 52–61.
https://doi.org/10.1016/j.plantsci.2012.03.010
86. Endler A., Meyer S., Schelbert S. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 2006, V. 141, P.?196–207.
https://doi.org/10.1104/pp.106.079533
87. Reinders A., Sivitz A. B., Starker C. G. Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant Mol. Biol. 2008, V. 68, P.?289–299.
https://doi.org/10.1007/s11103-008-9370-0
88. Martinoia E., Meyer S., De Angeli A., Nagy R. Vacuolar Transporters in Their Physiological Context . Annu. Rev. Plant Biol. 2012, V. 63, P. 183–213.
https://doi.org/10.1146/annurev-arplant-042811-105608
89. Aluri S., Buettner M. Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc. Natl. Acad. Sci. USA. 2007, V. 104, P. 2537–2542.
https://doi.org/10.1073/pnas.0610278104
90. Rea P. A., Li Z-S., Lu Y-P. From vacuolar GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, V. 49, P. 727–760.
https://doi.org//10.1146/annurev.arplant.49.1.727
91. Marinova K., Pourcel L., Weder B. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+- antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell. 2007, V. 19, P. 2023–2038.
https://doi.org/10.1105/tpc.106.046029
92. Klein M., Martinoia E., Hoffmann-Thoma G., Weissenbock G. A membrane-potential dependent ABC-like transportermediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J. 2000, V. 21, P. 289–304.
https://doi.org/10.1046/j.1365-313x.2000.00684.x
93. Liu G., Sґanchez-Fernґandez R., Li Z. S., Rea?P. A. Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J. Biol. Chem. 2001, V. 276, P. 8648–8656.
https://doi.org/10.1074/jbc.M009690200
94. Goodman C. D., Casati P., Walbot V. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell. 2004, V. 16, P.?1812–1826.
https://doi.org/10.1105/tpc.022574
95. Yazaki K., Shitan N., Sugiyama A., Takanashi K. Cell and molecular biology of ATP-binding cassette proteins in plants. Int. Rev. Cell Mol. Biol. 2009, V.?276, P. 263–299.
https://doi.org/10.1016/S1937-6448(09)76006-X
96. Song W.-Y., Park J., Mendoza-Coґzatl D. G. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl. Acad. Sci. USA. 2010, V. 107, P. 21187–21192.
https://doi.org/10.1073/pnas.1013964107
97. Shi J., Wang H., Schellin K. Embryospecific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotechnol. 2007, V.?25, P. 930–937.
https://doi.org/10.1038/nbt1322
98. Nagy R., Grob H., Weder B. The Arabidopsis ATP-binding cassette protein ATMRP5/ATABCC5 is a high-affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J. Biol. Chem. 2009, V. 284, P.?33614–33622.
https://doi.org/10.1074/jbc.M109.030247
99. Klein M., Geisler M., Suh S. J. Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J. 2004, V. 39, P. 219–236.
https://doi.org/10.1111/j.1365-313X.2004.02125.x
100. Raichaudhuri A., Peng M., Naponelli V. Plant vacuolar ATP-binding cassette transporters that translocate folates and antifolates in vitro and contribute to antifolate tolerance in vivo. J. Biol. Chem. 2009, V. 284, P. 8449–8460.
https://doi.org/10.1074/jbc.M808632200
101. Maurel C. Plant aquaporins: novel functions and regulation properties. FEBS Lett. 2007, V. 581, P. 2227–2236.
https://doi.org/10.1016/j.febslet.2007.03.021
102. Paris N., Stanley C. M., Jones R. L., Rogers?J. C. Plant cells contain two functionally distinct vacuolar compartments. Cell. 1996, V. 85, P. 563–572.
https://doi.org/10.1016/S0092-8674(00)81256-8
103. Gattolin S., Sorieul M., Frigerio L. Tonoplast intrinsic proteins and vacuolar identity. Biochem. Soc. Transact. 2010, V. 38, P. 769–773.
https://doi.org/10.1042/BST0380769
104. Frigerio L., Hinz G., Robinson D. G. Multiple vacuoles in plant cells: rule or exception? Traffic. 2008, V. 9, P. 1564–1570.
https://doi.org/10.1111/j.1600-0854.2008.00776.x
105. Park M., Kim S. J., Vitale A., Hwang I. Identification of the Protein Storage Vacuole and Protein Targeting to the Vacuole in Leaf Cells of Three Plant Species. Plant Physiol. 2004, V. 134, P.?625–639.
https://doi.org/10.1104/pp.103.030635
106. Jiang J., Phillips T., Hamm C. The protein storage vacuole: a unique compound organelle. J. Cell Biol. 2001, V. 155, P.?991–1002.
https://doi.org/10.1083/jcb.200107012
107. Martinez D. E., Costa M. L, Gomez F. M. Senescence-associated vacuoles are involved in the degradation of chloroplast proteins in tobacco leaves, Plant J. 2008, V. 56, P. 196–206.
https://doi.org/10.1111/j.1365-313X.2008.03585.x
108. Gaxiola R. A., Li J., Undurraga S. Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc. Natl. Acad. Sci. USA. 2001, V. 98, P. 11444–11249.
https://doi.org/10.1073/pnas.191389398
109. Palmgren M. G., Clemens S., Williams L. E. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 2010, V. 13, P. 464–473.
https://doi.org/10.1016/j.tplants.2008.06.005
110. Singh B. R., Gupta S. K., Azaizeh H. Safety of food crops on land contaminated with trace elements. J. Sci. Food Agric. 2011, V. 91, P. 1349–1366.
https://doi.org/10.1002/jsfa.4355