The calcium-dependent protein kinase CPK7 acts on root hydraulic conductivity

Plant Cell and Environment

Volumn 38, Issue 7, 2015, Pages 1312-1320

  Li, Guowei ^a,d   Boudsocq, Marie ^b,e   Hem, Sonia ^c   Vialaret, Jérôme ^c,f   Rossignol, Michel ^c   Maurel, Christophe ^a   Santoni, Véronique ^a  

^a CNRS   (France)

^b CEA SACLAY   (France)

^c Laboratoire de Biochimie Protéomique Clinique   (France)

^d SHANDONG PEANUT RESEARCH INSTITUTE   (China)

^e INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^f MONTPELLIER UNIVERSITY HOSPITAL   (France)

Author keywords

Aquaporin; CDPK; Phosphorylation; PIP; Quantitative proteomics; Root water transport

Indexed keywords

ANGIOSPERM; CALCIUM; ENZYME ACTIVITY; GENE EXPRESSION; GERM CELL; HYDRAULIC CONDUCTIVITY; PROTEOMICS;

ARABIDOPSIS;

AQUAPORIN; ARABIDOPSIS PROTEIN; CALCIUM-DEPENDENT PROTEIN KINASE; CPK7 PROTEIN, ARABIDOPSIS; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; WATER;

ARABIDOPSIS; ENZYMOLOGY; EVAPOTRANSPIRATION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLANT ROOT; PROTEOMICS; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

AQUAPORINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; MUTAGENESIS, INSERTIONAL; PHOSPHORYLATION; PLANT ROOTS; PLANT TRANSPIRATION; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; WATER;

EID: 84930354837     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12478     Document Type: Article

References (57)

1. Aasamaa K. & Sober A. (2005) Seasonal courses of maximum hydraulic conductance in shoots of six temperate deciduous tree species. Functional Plant Biology 32, 1077-1087.
2. Bagnasco S.M. (2012) Protein kinase C-alpha comes to the rescue of aquaporin-2. American Journal of Physiology-Renal Physiology 303, F35-F36.
3. Boudsocq M. & Sheen J. (2013) CDPKs in immune and stress signaling. Trends in Plant Science 18, 30-40.
4. 2+ sensor protein kinases. Nature 464, 418-422.
5. Boudsocq M., Droillard M.J., Regad L. & Lauriere C. (2012) Characterization of Arabidopsis calcium-dependent protein kinases: activated or not by calcium? Biochemical Journal 447, 291-299.
6. Boursiac Y., Chen S., Luu D.-T., Sorieul M., van den Dries N. & Maurel C. (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiology 139, 790-805.
7. Boursiac Y., Boudet J., Postaire O., Luu D.-T., Tournaire-Roux C. & Maurel C. (2008) Stimulus-induced down-regulation of root water transport involves reactive oxygen species cell signalling and plasma membrane intrinsic protein internalization. Plant Journal 56, 207-218.
8. Casado-Vela J., Muries B., Carvajal M., Iloro I., Elortza F. & Martinez-Ballesta M.C. (2010) Analysis of root plasma membrane aquaporins from Brassica oleracea: post-translational modifications, de novo sequencing and detection of isoforms by high resolution mass spectrometry. Journal of Proteome Research 9, 3479-3494.
9. Cheng S.H., Willmann M.R., Chen H.C. & Sheen J. (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiology 129, 469-485.
10. Curran A., Chang I.F., Chang C.L., Garg S., Miguel R.M., Barron Y.D., ... Harper J.F. (2011) Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Frontiers in Plant Science 2, 1-15.
11. Di Pietro M., Vialaret J., Li G.-W., Hem S., Prado K., Rossignol M., ... Santoni V. (2013) Coordinated post-translational responses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Molecular and Cellular Proteomics 12, 3886-3897.
12. Guenther J.F., Chanmanivone N., Galetovic M.P., Wallace I.S., Cobb J.A. & Roberts D.M. (2003) Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. The Plant Cell 15, 981-991.
13. Hrabak E.M., Chan C.W.M., Gribskov M., Harper J.F., Choi J.H., Halford N., ... Harmon A.C. (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology 132, 666-680.
14. Hu H.C., Wang Y.Y. & Tsay Y.F. (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant Journal 57, 264-278.
15. Javot H., Lauvergeat V., Santoni V., Martin F., Güclü J., Vinh J., ... Maurel C. (2003) Role for a single aquaporin isoform in root water uptake. The Plant Cell 15, 509-522.
16. Johanson U., Karlsson M., Johansson I., Gustavsson S., Sjövall S., Fraysse L., ... Kjellbom P. (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiology 126, 1-12.
17. Johansson I., Karlsson M., Shukla V.K., Chrispeels M.J., Larsson C. & Kjellbom P. (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. The Plant Cell 10, 451-459.
18. Kaldenhoff R., Ribas-Carbo M., Flexas J., Lovisolo C., Heckwolf M. & Uehlein N. (2008) Aquaporins and plant water balance. Plant, Cell and Environment 31, 658-666.
19. Kline K.G., Barrett-Wilt G.A. & Sussman M.R. (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proceedings of the National Academy of Sciences of the United States of America 36, 15986-15991.
20. + channel TPK1 by calcium dependent protein kinases (CDPKs). Molecular Plant 6, 1274-1289.
21. Lee H.K., Cho S.K., Son O., Xu Z., Hwang I. & Kim W.T. (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. The Plant Cell 21, 622-641.
22. Luan S. (2009) The CBL-CIPK network in plant calcium signaling. Trends in Plant Science 14, 37-42.
23. Ludwig A.A., Romeis T. & Jones J.D.G. (2004) CDPK-mediated signalling pathways: specificity and cross-talk. Journal of Experimental Botany 55, 181-188.
24. Maurel C. (2007) Plant aquaporins: novel functions and regulation properties. FEBS Letters 581, 2227-2236.
25. Maurel C., Kado R.T., Guern J. & Chrispeels M.J. (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporinα-TIP. EMBO Journal 14, 3028-3035.
26. 2+-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant Journal 63, 484-498.
27. Monneuse J.M., Sugano M., Becue T., Santoni V., Hem S. & Rossignol M. (2011) Towards the profiling of the Arabidopsis thaliana plasma membrane transportome by targeted proteomics. Proteomics 11, 1789-1797.
28. Nedvetsky P.I., Tabor V., Tamma G., Beulshausen S., Skroblin P., Kirschner A., ... Klussmann E. (2010) Reciprocal regulation of aquaporin-2 abundance and degradation by protein kinase A and p38-MAP kinase. Journal of the American Society of Nephrology 21, 1645-1656.
29. Niittylä T., Fuglsang A.T., Palmgren M.G., Frommer W.B. & Schulze W.X. (2007) Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Molecular and Cellular Proteomics 6, 1711-1726.
30. Otto B., Uehlein N., Sdorra S., Fischer M., Ayaz M., Belastegui-Macadam X., ... Kaldenhoff R. (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. Journal of Biological Chemistry 285, 31253-31260.
31. Patharkar O.R. & Cushman J.C. (2000) A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. Plant Journal 24, 679-691.
32. Peret B., Li G.W., Zhao J., Band L.R., Voss U., Postaire O., ... Bennett M.J. (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology 14, 991-998.
33. Postaire O., Tournaire-Roux C., Grondin A., Boursiac Y., Morillon R., Schäffner T. & Maurel C. (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiology 152, 1418-1430.
34. Prado K., Boursiac Y., Tournaire-Roux C., Monneuse J.M., Postaire O., Da Ines O., ... Maurel C. (2013) Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. The Plant Cell 25, 1029-1039.
35. Prak S., Hem S., Boudet J., Viennois J., Sommerer N., Rossignol R., ... Santoni V. (2008) 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. Molecular and Cellular Proteomics 7, 1019-1030.
36. Quigley F., Rosenberg J.M., Shachar-Hill Y. & Bohnert H.J. (2002) From genome to function: the Arabidopsis aquaporins. Genome Biology 3, 1-17.
37. Rodriguez Milla M.A., Uno Y., Chang I.F., Townsend J., Maher E.A., Quilici D. & Cushman J.C. (2006) A novel yeast two-hybrid approach to identify CDPK substrates: characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Letters 580, 904-911.
38. Sakakibara H., Kobayashi K., Deji A. & Sugiyama T. (1997) Partial characterization of the signaling pathway for the nitrate-dependent expression of genes for nitrogen-assimilatory enzymes using detached maize leaves. Plant and Cell Physiology 38, 837-843.
39. Santoni V., Vinh J., Pflieger D., Sommerer N. & Maurel C. (2003) A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochemical Journal 373, 289-296.
40. Santoni V., Verdoucq L., Sommerer N., Vinh J., Pflieger D. & Maurel C. (2006) Methylation of aquaporins in plant plasma membrane. Biochemical Journal 400, 189-197.
41. Schulz P., Herde M. & Romeis T. (2013) Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiology 163, 523-530.
42. Sjovall-Larsen S., Alexandersson E., Johansson I., Karlsson M., Johanson U. & Kjellbom P. (2006) Purification and characterization of two protein kinases acting on the aquaporin SoPIP2;1. Biochimica et Biophysica Acta 1758, 1157-1164.
43. Steudle E. & Peterson C.A. (1998) How does water get through roots? Journal of Experimental Botany 49, 775-788.
44. Stoscheck C.M. (1990) Quantitation of proteins. Methods in Enzymology 182, 50-68.
45. Sutka M., Li G.W., Boudet J., Boursiac Y., Doumas P. & Maurel C. (2011) Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions. Plant Physiology 155, 1264-1276.
46. Tornroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., ... Kjellbom P. (2006) Structural mechanism of plant aquaporin gating. Nature 439, 688-694.
47. Tournaire-Roux C., Sutka M., Javot H., Gout E., Gerbeau P., Luu D.-T., ... Maurel C. (2003) Gating of aquaporins by cytosolic pH regulates root water transport during anoxic stress. Nature 425, 393-397.
48. Uno Y.C., Milla M.A.R., Maher E. & Cushman J.C. (2009) Identification of proteins that interact with catalytically active calcium-dependent protein kinases from Arabidopsis. Molecular Genetics and Genomics 281, 375-390.
49. Van Wilder V., Miecielica U., Degand H., Derua R., Waelkens E. & Chaumont F. (2008) Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated. Plant and Cell Physiology 49, 1364-1377.
50. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. & Speleman F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, 1-10.
51. Vialaret J., Di Pietro M., Hem S., Maurel C., Rossignol M. & Santoni V. (2014) Phosphorylation dynamics of membrane proteins from Arabidopsis roots submitted to salt stress. Proteomics 14, 1058-1070.
52. Wiśniewski J.R., Zougman A., Nagaraj N. & Mann M. (2009) Universal sample preparation method for proteome analysis. Nature Methods 6, 359-362.
53. Wu X.N., Sanchez-Rodriguez C., Pertl-Obermeyer H., Obermeyer G. & Schulze W.X. (2013) Sucrose-induced receptor kinase SIRK1 regulates plasma membrane aquaporins in Arabidopsis. Molecular and Cellular Proteomics 12, 2856-2873.
54. Xu J., Tian Y.S., Peng R.H., Xiong A.S., Zhu B., Jin X.F., ... Yao Q.H. (2010) AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231, 1251-1260.
55. 2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367-371.
56. Zhu S.Y., Yu X.C., Wang X.J., Zhao R., Li Y., Fan R.C., ... Zhang D.P. (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. The Plant Cell 19, 3019-3036.
57. 2+-mediated stomatal regulation in response to drought stress. Plant Physiology 154, 1232-1243.