Plasma Membrane H+-ATPase Regulation in the Center of Plant Physiology

Molecular Plant

Volumn 9, Issue 3, 2016, Pages 323-337

  Falhof, Janus ^a   Pedersen, Jesper Torbøl ^a   Fuglsang, Anja Thoe ^a   Palmgren, Michael ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

hormonal regulation; Key words blue light; pathogens; protein phosphorylation dephosphorylation; proton pump; stomata

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

CELL MEMBRANE; METABOLISM; MICROBIOLOGY; PLANT CELL; PLANT PHYSIOLOGY; PROTEIN PROCESSING; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; PLANT CELLS; PLANT PHYSIOLOGICAL PHENOMENA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTON-TRANSLOCATING ATPASES;

EID: 84960092790     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2015.11.002     Document Type: Review

References (105)

1. I. Appelhagen, N. Nordholt, T. Seidel, K. Spelt, R. Koes, F. Quattrochio, M. Sagasser, and B. Weisshaar TRANSPARENT TESTA 13 is a tonoplast P3A-ATPase required for vacuolar deposition of proanthocyanidins in Arabidopsis thaliana seeds Plant J. 82 2015 840 849
2. +-ATPase AHA10 proton pump is associated with citric acid accumulation in lemon juice sac cells Funct. Integr. Genomics 11 2011 551 563
3. M. Arango, F. Gévaudant, M. Oufattole, and M. Boutry The plasma membrane proton pump ATPase: The significance of gene subfamilies Planta 216 2003 355 365
4. +-ATPase with improved transport coupling efficiency identified by mutant selection in yeast Plant J. 10 1996 451 458
5. +-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system Plant J. 13 1998 661 671
6. I. Baxter, J. Tchieu, M.R. Sussman, M. Boutry, M.G. Palmgren, M. Gribskov, J.F. Harper, and K.B. Axelsen Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice Plant Physiol. 132 2003 618 628
7. +-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 102 2005 2649 2654
8. J.J. Benschop, S. Mohammed, M. O'Flaherty, A.J. Heck, M. Slijper, and F.L. Menke Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis Mol. Cell. Proteomics 6 2007 1198 1214
9. +-ATPase by acid stress: Antibodies as a tool to follow the phosphorylation status of the penultimate activating Thr Plant Signal. Behav. 5 2010 681 683
10. +-ATPase isoforms of Nicotiana tabacum are differentially regulated by phosphorylation of their penultimate threonine Plant J. 62 2010 291 301
11. +-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa Ann. Bot. 115 2015 481 494
12. K. Caesar, K. Elgass, Z. Chen, P. Huppenberger, J. Witthöft, F. Schleifenbaum, M.R. Blatt, C. Oecking, and K. Harter A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana Plant J. 66 2011 528 540
13. Y. Chen, W. Hoehenwarter, and W. Weckwerth Comparative analysis of phytohormone-responsive phosphoproteins in Arabidopsis thaliana using TiO2-phosphopeptide enrichment and mass accuracy precursor alignment Plant J. 63 2010 1 17
14. +-ATPase are involved in the regulation of magnesium-mediated increases in aluminum-induced citrate exudation in broad bean (Vicia faba L) Plant Cell Physiol. 56 2015 1144 1153
15. D. Chevalier, E.R. Morris, and J.C. Walker 14-3-3 and FHA domains mediate phosphoprotein interactions Annu. Rev. Plant Biol. 60 2009 67 91
16. G. Duby, and M. Boutry The plant plasma membrane proton pump ATPase: A highly regulated P-type ATPase with multiple physiological roles Pflugers Arch. 457 2009 645 655
17. +-ATPase C-terminal region J. Biol. Chem. 284 2009 4213 4221
18. R.C. Edgar MUSCLE: Multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797
19. K. Ekberg, M.G. Palmgren, B. Veierskov, and M.J. Buch-Pedersen A novel mechanism of P-type ATPase autoinhibition involving both termini of the protein J. Biol. Chem. 285 2010 7344 7350
20. R.J. Ferl 14-3-3 proteins: Regulation of signal-induced events Physiol. Plant 120 2004 173 178
21. 947 J. Biol. Chem. 274 1999 36774 36780
22. +-ATPase: Involvement of a region promoting phosphorylation-independent interaction in addition to the phosphorylation-dependent C-terminal end J. Biol. Chem. 278 2003 42266 42272
23. +-ATPase C-terminus in the same region as 14-3-3 protein Physiol. Plant 1238 2006 334 340
24. +-ATPase by preventing interaction with 14-3-3 protein Plant Cell. 19 2007 1617 1634
25. A.T. Fuglsang, A. Kristensen, T.A. Cuin, W.X. Schulze, J. Persson, K.H. Thuesen, C.K. Ytting, C.B. Oehlenschlæger, K. Mahmood, T.E. Sondergaard, and et al. Receptor kinase-mediated control of primary active proton pumping at the plasma membrane Plant J. 80 2014 951 964
26. +-ATPase alters plant development and increases salt tolerance Plant Physiol. 144 2007 1763 1776
27. +-ATPase) of Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 86 1989 1234 1238
28. M. Haruta, and M.R. Sussman The effect of a genetically reduced plasma membrane protonmotive force on vegetative growth of Arabidopsis Plant Physiol. 158 2012 1158 1171
29. M. Haruta, H.L. Burch, R.B. Nelson, G. Barrett-Wilt, K.G. Kline, S.B. Mohsi, J.C. Young, M.S. Otegui, and M.R. Sussman Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity J. Biol. Chem. 285 2010 17918 17929
30. M. Haruta, G. Sabat, K. Stecker, B.B. Minkoff, and M.R. Sussman A peptide hormone and its receptor protein kinase regulate plant cell expansion Science 343 2014 408 411
31. +-ATPase Plant Cell Physiol. 51 2010 1186 1196
32. +-ATPase in stomatal guard cells Plant Cell Physiol. 52 2011 1238 1248
33. +-ATPase in Arabidopsis thaliana Plant Cell Physiol. 55 2014 845 853
34. H.M. Hubberten, D. Sieh, D. Zöller, R. Hoefgen, and F. Krajinski Medicago truncatula Mtha1-2 mutants loose metabolic responses to mycorrhizal colonization Plant Signal. Behav. 10 2015 e989025
35. +-ATPase Plant Cell. 9 1997 1805 1814
36. M. Janicka-Russak, K. Kabała, A. Wdowikowska, and G. Kłobus Modification of plasma membrane proton pumps in cucumber roots as an adaptation mechanism to salt stress J. Plant Physiol. 170 2013 915 922
37. D.T. Jones, W.R. Taylor, and J.M. Thornton The rapid generation of mutation data matrices from protein sequences Computer Appl. Biosciences 8 1992 275 282
38. M.G. Kim, L. da Cunha, A.J. McFall, Y. Belkhadir, S. DebRoy, J.L. Dangl, and D. Mackey Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis Cell 121 2005 749 759
39. +-ATPase by phosphorylation of the C-terminus in stomatal guard cells EMBO J. 18 1999 5548 5558
40. +-ATPase Int. Rev. Cell. Mol. Biol. 289 2011 89 115
41. T. Kinoshita, M. Doi, N. Suetsugu, T. Kagawa, M. Wada, and K. Shimazaki Phot1 and phot2 mediate blue light regulation of stomatal opening Nature 414 2001 656 660
42. +-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis Plant Cell. 26 2014 1808 1817
43. +-ATPase, and BAK1 Plant Cell. 27 2015 1718 1729
44. 2 plays important roles in cell elongation and shoot gravitropism in Arabidopsis Plant Cell. 15 2003 1990 2002
45. +-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis Plant Cell. 27 2015 2042 2056
46. +-ATPases to regulate stomatal apertures during pathogen attack PLoS Biol. 7 2009 e1000139
47. J. Liu, J.M. Elmore, Z.J. Lin, and G. Coaker A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor Cell Host Microbe 9 2011 137 146
48. F.J. Maathuis, V. Filatov, P. Herzyk, G.C. Krijger, K.B. Axelsen, S. Chen, B.J. Green, Y. Li, K.L. Madagan, R. Sánchez-Fernández, and et al. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress Plant J. 35 2003 675 692
49. E. Marrè Fusicoccin: A tool in plant physiology Annu. Rev. Plant Physiol. 30 1979 273 288
50. +-ATPase expressed in yeast is activated by phosphorylation at its penultimate residue and binding of 14-3-3 regulatory proteins in the absence of fusicoccin J. Biol. Chem. 275 2000 17762 17770
51. M. Melotto, W. Underwood, J. Koczan, K. Nomura, and S.Y. He Plant stomata function in innate immunity against bacterial invasion Cell 126 2006 969 980
52. +-ATPase prevents abscisic acid-mediated stomatal closure EMBO J. 26 2007 3216 3226
53. J.-M. Monneuse, M. Sugano, T. Becue, V. Santoni, S. Hem, and M. Rossignol Towards the profiling of the Arabidopsis thaliana plasma membrane transportome by targeted proteomics Proteomics 11 2011 1789 1797
54. +-ATPase ion pumps Nat. Rev. Mol. Cell. Biol. 12 2011 60 70
55. T.T. Nguyen, J.D. Volkening, C.M. Rose, M. Venkateshwaran, M.S. Westphall, J.J. Coon, J.M. Ané, and M.R. Sussman Potential regulatory phosphorylation sites in a Medicago truncatula plasma membrane proton pump implicated during early symbiotic signaling in roots FEBS Lett. 589 2015 2186 2193
56. T. Niittylä, A.T. Fuglsang, M.G. Palmgren, W.B. Frommer, and W.X. Schulze Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis Mol. Cell. Proteomics 6 2007 1711 1726
57. T.S. Nühse, A.R. Bottrill, A.M. Jones, and S.C. Peck Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses Plant J. 51 2007 931 940
58. +-ATPase containing a penultimate threonine in the bryophyte Plant Signal. Behav. 7 2012 979 982
59. +-ATPase in the liverwort Marchantia polymorpha Plant Physiol. 159 2012 826 834
60. +-ATPase is protected by fusicoccin-induced 14-3-3 binding Plant Physiol. 118 1998 551 555
61. +-ATPase by combining X-ray crystallography and electron cryomicroscopy Mol. Cell. 25 2007 427 440
62. +-ATPase activity Physiol. Plant. 83 1991 314 323
63. +-ATPases: Powerhouses for nutrient uptake Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 2001 817 845
64. M.G. Palmgren, and M. Sommarin Lysophosphatidylcholine stimulates ATP dependent proton accumulation in isolated oat root plasma membrane vesicles Plant Physiol. 90 1989 1009 1014
65. +-ATPase J. Biol. Chem. 266 1991 20470 20475
66. +-ATPase gene from the plant Arabidopsis thaliana J. Biol. Chem. 264 1989 8557 8562
67. +-ATPase Plant Physiol. 93 1990 1654 1658
68. B.P. Pedersen, M.J. Buch-Pedersen, J.P. Morth, M.G. Palmgren, and P. Nissen Crystal structure of the plasma membrane proton pump Nature 450 2007 1111 1114
69. C.N. Pedersen, K.B. Axelsen, J.F. Harper, and M.G. Palmgren Evolution of plant P-type ATPases Front. Plant Sci. 3 2012 31
70. + pump: Stabilization of the phosphoenzyme intermediate contributes to post-translational pump activation J. Biol. Chem. 290 2015 20396 20406
71. + ATPases J. Proteomics 108 2014 17 29
72. +-ATPase activates the enzyme with no requirement for regulatory 14-3-3 proteins J. Biol. Chem. 286 2011 18474 18482
73. +, and anions J. Exp. Bot. 66 2015 813 825
74. F. Portillo, and R. Serrano Dissection of the functional domains of the yeast proton-pumping ATPase by directed mutagenesis EMBO J. 7 1988 1793 1798
75. L.R. Poulsen, R.L. López-Marqués, P.R. Pedas, S.C. McDowell, E. Brown, R. Kunze, J.F. Harper, T.G. Pomorski, and M. Palmgren A phospholipid uptake system in the model plant Arabidopsis thaliana Nat. Commun. 6 2015 7649
76. D.L. Rayle, and R.E. Cleland The acid growth theory of auxin induced cell elongation is alive and well Plant Physiol. 99 1992 1271 1274
77. +-ATPase in homologous and heterologous environments J. Biol. Chem. 287 2012 4904 4913
78. M. Salehin, R. Bagchi, and M. Estelle SCFTIR1/AFB-based auxin perception: Mechanism and role in plant growth and development Plant Cell. 27 2015 9 19
79. +-ATPase Plant Physiol. 138 2005 287 296
80. +-ATPase Plant Physiol. 136 2004 2475 2482
81. A.K. Spartz, S.H. Lee, J.P. Wenger, N. Gonzalez, H. Itoh, D. Inzé, W.A. Peer, A.S. Murphy, P.J. Overvoorde, and W.M. Gray The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion Plant J. 70 2012 978 990
82. +-ATPases to promote cell expansion in Arabidopsis Plant Cell. 26 2014 2129 2142
83. +-ATPase creates a binding site for the regulatory 14-3-3 protein Plant Cell. 11 1999 2379 2391
84. +-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis Plant Physiol. 159 2012 632 641
85. A. Takemiya, T. Kinoshita, M. Asanuma, and K. Shimazaki Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba Proc. Natl. Acad. Sci. USA 103 2006 13549 13554
86. A. Takemiya, N. Sugiyama, H. Fujimoto, T. Tsutsumi, S. Yamauchi, A. Hiyama, Y. Tada, J.M. Christie, and K. Shimazaki Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening Nat. Commun. 4 2013 2094
87. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: Molecular evolutionary genetics analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729
88. +-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin Plant Cell Environ. 32 2009 465 475
89. +-ATPase J. Biol. Chem. 270 1995 19659 19667
90. + P-ATPase on the tonoplast determines vacuolar pH and flower colour Nat. Cell Biol. 10 2008 1456 1462
91. M. Wang, Y. Wang, J. Sun, M. Ding, S. Deng, P. Hou, X. Ma, Y. Zhang, F. Wang, G. Sa, and et al. Overexpression of PeHA1 enhances hydrogen peroxide signaling in salt-stressed Arabidopsis Plant Physiol. Biochem. 71 2013 37 48
92. +-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula Plant Cell. 26 2014 1818 1830
93. +-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth Proc. Natl. Acad. Sci. USA 111 2014 533 538
94. X. Wang, Y. Cai, H. Wang, Y. Zeng, X. Zhuang, B. Li, and L. Jiang Trans-Golgi network-located AP1 gamma adaptins mediate dileucine motif-directed vacuolar targeting in Arabidopsis Plant Cell. 26 2014 4102 4118
95. S.J. Wi, S.Y. Seo, K. Cho, M.H. Nam, and K.Y. Park Lysophosphatidylcholine enhances susceptibility in signaling pathway against pathogen infection through biphasic production of reactive oxygen species and ethylene in tobacco plants Phytochemistry 104 2014 48 59
96. +-ATPase by lysophospholipids depends on the autoinhibitory N-A nd C-terminal domains J. Biol. Chem. 290 2015 16281 16291
97. J. Witthöft, K. Caesar, K. Elgass, P. Huppenberger, J. Kilian, F. Schleifenbaum, C. Oecking, and K. Harter The activation of the Arabidopsis P-ATPase 1 by the brassinosteroid receptor BRI1 is independent of threonine 948 phosphorylation Plant Signal. Behav. 6 2011 1063 1066
98. M. Würtele, C. Jelich-Ottmann, A. Wittinghofer, and C. Oecking Structural view of a fungal toxin acting on a 14-3-3 regulatory complex EMBO J. 22 2003 987 994
99. X.F. Xin, and S.Y. He Pseudomonas syringae pv. tomato DC3000: A model pathogen for probing disease susceptibility and hormone signaling in plants Annu. Rev. Phytopathol. 51 2013 473 498
100. +-ATPase in jasmonate-induced ion fluxes and stomatal closure in Arabidopsis thaliana Plant J. 83 2015 638 649
101. +-ATPase through interaction with the PKS5 kinase Plant Cell. 22 2010 1313 1332
102. E. Zeiger The biology of stomatal guard cells Annu. Rev. Plant Physiol. 34 1983 441 475
103. H. Zhang, B. Han, T. Wang, S. Chen, H. Li, Y. Zhang, and S. Dai Mechanisms of plant salt response: Insights from proteomics J. Proteome Res. 11 2012 49 67
104. Z. Zhou, Y. Wu, Y. Yang, M. Du, X. Zhang, Y. Guo, C. Li, and J.M. Zhou An Arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatal invasion Plant Cell. 27 2015 2032 2041
105. +-ATPase is involved in methyl jasmonate-induced root hair formation in lettuce (Lactuca sativa L.) seedlings Plant Cell Rep. 34 2015 1025 1036