Plant aquaporins on the move: Reversible phosphorylation, lateral motion and cycling

Current Opinion in Plant Biology

Volumn 22, Issue , 2014, Pages 101-107

  Verdoucq, Lionel ^a   Rodrigues, Olivier ^a   Martinière, Alexandre ^a   Luu, Doan Trung ^a   Maurel, Christophe ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN;

METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLANT CELL; TRANSPORT AT THE CELLULAR LEVEL;

AQUAPORINS; BIOLOGICAL TRANSPORT; PHOSPHORYLATION; PLANT CELLS;

EID: 84908391433     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.09.011     Document Type: Review

References (71)

1. Chaumont F., Tyerman S.D. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 2014, 164:1600-1618.
2. Li G., Santoni V., Maurel C. Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 2014, 1840:1574-1582.
3. Abascal F., Irisarri I., Zardoya R. Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 2014, 1840:1468-1481.
4. Hachez C., Besserer A., Chevalier A.S., Chaumont F. Insights into plant plasma membrane aquaporin trafficking. Trends Plant Sci 2013, 18:344-352.
5. Luu D.T., Maurel C. Aquaporin trafficking in plant cells: an emerging membrane-protein model. Traffic 2013, 14:629-635.
6. Soto G., Fox R., Ayub N., Alleva K., Guaimas F., Erijman E., Mazzella A., Amodeo G., Muschietti J. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J 2010, 64:1038-1047.
7. Wudick M.M., Luu D.T., Tournaire-Roux C., Sakamoto W., Maurel C. Vegetative and sperm cell-specific aquaporins of Arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol 2014, 164:1697-1706.
8. 2 permeability. Plant Cell 2008, 20:648-657.
9. Ferro M., Brugiere S., Salvi D., Seigneurin-Berny D., Court M., Moyet L., Ramus C., Miras S., Mellal M., Le Gall S., et al. AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 2010, 9:1063-1084.
10. Beebo A., Mathai J.C., Schoefs B., Spetea C. Assessment of the requirement for aquaporins in the thylakoid membrane of plant chloroplasts to sustain photosynthetic water oxidation. FEBS Lett 2013, 587:2083-2089.
11. 2 pore with physiological functions. Nature 2003, 425:734-737.
12. 2 transport facilitator. Plant J 2011, 67:795-804.
13. 2 transport by PIP2 aquaporins of barley. Plant Cell Physiol 2014, 55:251-257.
14. Secchi F., Zwieniecki M.A. The physiological response of Populus tremula x alba leaves to the down-regulation of PIP1 aquaporin gene expression under no water stress. Front Plant Sci 2013, 4:507.
15. 2 in vivo. Plant J 2006, 48:427-439.
16. 2 in living organisms. Biochim Biophys Acta 2014, 1840:1592-1595.
17. 2 diffusion pathway inside leaves. J Exp Bot 2009, 60:2235-2248.
18. Bienert G.P., Moller A.L., Kristiansen K.A., Schulz A., Moller I.M., Schjoerring J.K., Jahn T.P. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 2007, 282:1183-1192.
19. 2. Biochem J 2008, 414:53-61.
20. Bienert G.P., Heinen R.B., Berny M.C., Chaumont F. Maize plasma membrane aquaporin ZmPIP2;5, but not ZmPIP1;2, facilitates transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 2014, 1838:216-222.
21. Boursiac Y., Boudet J., Postaire O., Luu D.T., Tournaire-Roux C., Maurel C. Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J 2008, 56:207-218.
22. Hooijmaijers C., Rhee J.Y., Kwak K.J., Chung G.C., Horie T., Katsuhara M., Kang H. Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res 2012, 125:147-153.
23. di Pietro M., Vialaret J., Li G.W., Hem S., Prado K., Rossignol M., Maurel C., Santoni V. Coordinated post-translational responses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Mol Cell Proteomics 2013, 12:3886-3897.
24. Prak S., Hem S., Boudet J., Viennois G., Sommerer N., Rossignol M., Maurel C., Santoni V. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins. Role in sub-cellular trafficking of AtPIP2;1 in response to salt stress. Mol Cell Proteomics 2008, 7:1019-1030.
25. Zhou S., Hu W., Deng X., Ma Z., Chen L., Huang C., Wang C., Wang J., He Y., Yang G., et al. Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS ONE 2012, 7:e52439.
26. Belousov V.V., Fradkov A.F., Lukyanov K.A., Staroverov D.B., Shakhbazov K.S., Terskikh A.V., Lukyanov S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 2006, 3:281-286.
27. Miller E.W., Dickinson B.C., Chang C.J. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci U S A 2010, 107:15681-15686.
28. Vieceli Dalla Sega F., Zambonin L., Fiorentini D., Rizzo B., Caliceti C., Landi L., Hrelia S., Prata C. Specific aquaporins facilitate Nox-produced hydrogen peroxide transport through plasma membrane in leukaemia cells. Biochim Biophys Acta 2014, 1843:806-814.
29. Fetter K., Van Wilder V., Moshelion M., Chaumont F. Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 2004, 16:215-228.
30. Bienert G.P., Cavez D., Besserer A., Berny M.C., Gilis D., Rooman M., Chaumont F. A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem J 2012, 445:101-111.
31. Horie T., Kaneko T., Sugimoto G., Sasano S., Panda S.K., Shibasaka M., Katsuhara M. Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant Cell Physiol 2011, 52:663-675.
32. Mahdieh M., Mostajeran A., Horie T., Katsuhara M. Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant Cell Physiol 2008, 49:801-813.
33. Yaneff A., Sigaut L., Marquez M., Alleva K., Pietrasanta L.I., Amodeo G. Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci U S A 2014, 111:231-236.
34. Zelazny E., Borst J.W., Muylaert M., Batoko H., Hemminga M.A., Chaumont F. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci U S A 2007, 104:12359-12364.
35. Otto B., Uehlein N., Sdorra S., Fischer M., Ayaz M., Belastegui-Macadam X., Heckwolf M., Lachnit M., Pede N., Priem N., et al. Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 2010, 285:31253-31260.
36. Zelazny E., Miecielica U., Borst J.W., Hemminga M.A., Chaumont F. An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 2009, 57:346-355.
37. Sorieul M., Santoni V., Maurel C., Luu D.T. Mechanisms and effects of retention of over-expressed aquaporin AtPIP2;1 in the endoplasmic reticulum. Traffic 2011, 12:473-482.
38. + channel KAT1 to the plasma membrane. Plant Physiol 2006, 142:923-930.
39. Luu D.T., Martinière A., Sorieul M., Runions J., Maurel C. Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J 2012, 69:894-905.
40. Li X., Wang X., Yang Y., Li R., He Q., Fang X., Luu D.T., Maurel C., Lin J. Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 2011, 23:3780-3797.
41. Muday G.K., Peer W.A., Murphy A.S. Vesicular cycling mechanisms that control auxin transport polarity. Trends Plant Sci 2003, 8:301-304.
42. Li R., Liu P., Wan Y., Chen T., Wang Q., Mettbach U., Baluska F., Samaj J., Fang X., Lucas W.J., et al. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 2012, 24:2105-2122.
43. Gadeyne A., Sanchez-Rodriguez C., Vanneste S., Di Rubbo S., Zauber H., Vanneste K., Van Leene J., De Winne N., Eeckhout D., Persiau G., et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 2014, 156:691-704.
44. Demir F., Horntrich C., Blachutzik J.O., Scherzer S., Reinders Y., Kierszniowska S., Schulze W.X., Harms G.S., Hedrich R., Geiger D., et al. Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc Natl Acad Sci U S A 2013, 110:8296-8301.
45. Hao H., Fan L., Chen T., Li R., Li X., He Q., Botella M.A., Lin J. Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 2014, 26:1729-1745.
46. Sieber J.J., Willig K.I., Kutzner C., Gerding-Reimers C., Harke B., Donnert G., Rammner B., Eggeling C., Hell S.W., Grubmuller H., et al. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 2007, 317:1072-1076.
47. Bar-On D., Wolter S., van de Linde S., Heilemann M., Nudelman G., Nachliel E., Gutman M., Sauer M., Ashery U. Super-resolution imaging reveals the internal architecture of nano-sized syntaxin clusters. J Biol Chem 2012, 287:27158-27167.
48. Hachez C., Laloux T., Reinhardt H., Cavez D., Degand H., Grefen C., De Rycke R., Inzé D., Blatt M.R., Russinova E., et al. Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 2014, 26:3132-3147.
49. Besserer A., Burnotte E., Bienert G.P., Chevalier A.S., Errachid A., Grefen C., Blatt M.R., Chaumont F. Selective regulation of maize plasma membrane aquaporin trafficking and activity by the SNARE SYP121. Plant Cell 2012, 24:3463-3481.
50. Grefen C., Chen Z., Honsbein A., Donald N., Hills A., Blatt M.R. A novel motif essential for SNARE interaction with the K(+) channel KC1 and channel gating in Arabidopsis. Plant Cell 2010, 22:3076-3092.
51. + channel at the plasma membrane. Plant Cell 2006, 18:935-954.
52. Aimon S., Callan-Jones A., Berthaud A., Pinot M., Toombes G.E., Bassereau P. Membrane shape modulates transmembrane protein distribution. Dev Cell 2014, 28:212-218.
53. Quemeneur F., Sigurdsson J.K., Renner M., Atzberger P.J., Bassereau P., Lacoste D. Shape matters in protein mobility within membranes. Proc Natl Acad Sci U S A 2014, 111:5083-5087.
54. Santoni V., Verdoucq L., Sommerer N., Vinh J., Pflieger D., Maurel C. Methylation of aquaporins in plant plasma membrane. Biochem J 2006, 400:189-197.
55. Sahr T., Adam T., Fizames C., Maurel C.VS. O-carboxyl- and N-methyltransferases active on plant aquaporins. Plant Cell Physiol 2010, 51:2092-2104.
56. Lee H.K., Cho S.K., Son O., Xu Z., Hwang I., Kim W.T. Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 2009, 21:622-641.
57. Kline K.G., Barrett-Wilt G.A., Sussman M.R. In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci U S A 2010, 107:15986-15991.
58. Wu X.N., Sanchez Rodriguez C., Pertl-Obermeyer H., Obermeyer G., Schulze W.X. Sucrose-induced receptor kinase SIRK1 regulates a plasma membrane aquaporin in Arabidopsis. Mol Cell Proteomics 2013, 12:2856-2873.
59. Johansson I., Karlsson M., Shukla V.K., Chrispeels M.J., Larsson C., Kjellbom P. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 1998, 10:451-460.
60. Törnroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., Neutze R., Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 2006, 439:688-694.
61. Nyblom M., Frick A., Wang Y., Ekvall M., Hallgren K., Hedfalk K., Neutze R., Tajkhorshid E., Törnroth-Horsefield S. Structural and functional analysis of SoPIP2;1 mutants add insight into plant aquaporin gating. J Mol Biol 2009, 387:653-668.
62. Azad A.K., Katsuhara M., Sawa Y., Ishikawa T., Shibata H. Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation. Plant Cell Physiol 2008, 49:1196-1208.
63. Tong J., Briggs M.M., McIntosh T.J. Water permeability of aquaporin-4 channel depends on bilayer composition, thickness, and elasticity. Biophys J 2012, 103:1899-1908.
64. Tong J., Canty J.T., Briggs M.M., McIntosh T.J. The water permeability of lens aquaporin-0 depends on its lipid bilayer environment. Exp Eye Res 2013, 113:32-40.
65. Nuhse T.S., Stensballe A., Jensen O.N., Peck S.C. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 2004, 16:2394-2405.
66. Niittyla T., Fuglsang A.T., Palmgren M.G., Frommer W.B., Schulze W.X. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol Cell Proteomics 2007, 6:1711-1726.
67. Whiteman S.A., Nuhse T.S., Ashford D.A., Sanders D., Maathuis F.J. A proteomic and phosphoproteomic analysis of Oryza sativa plasma membrane and vacuolar membrane. Plant J 2008, 56:146-156.
68. Prado K., Boursiac Y., Tournaire-Roux C., Monneuse J.M., Postaire O., Da Ines O., Schaffner A.R., Hem S., Santoni V., Maurel C. Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell 2013, 25:1029-1039.
69. Jones A.M., Xuan Y., Xu M., Wang R.S., Ho C.H., Lalonde S., You C.H., Sardi M.I., Parsa S.A., Smith-Valle E., et al. Border control - a membrane-linked interactome of Arabidopsis. Science 2014, 344:711-716.
70. Shatil-Cohen A., Attia Z., Moshelion M. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA?. Plant J 2011, 67:72-80.
71. Peret B., Li G., Zhao J., Band L.R., Voss U., Postaire O., Luu D.T., Da Ines O., Casimiro I., Lucas M., et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 2012, 14:991-998.