Phosphorylation of serine residues in the N-terminus modulates the activity of ACA8, a plasma membrane Ca 2+-ATPase of Arabidopsis thaliana

Journal of Experimental Botany

Volumn 63, Issue 3, 2012, Pages 1215-1224

  Giacometti, Sonia ^a   Marrano, Claudia Adriana ^a   Bonza, Maria Cristina ^a   Luoni, Laura ^a   Limonta, Margherita ^a   De Michelis, Maria Ida ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Arabidopsis thaliana; Ca 2+ ATPase; calcium dependent protein kinase; calmodulin; phosphorylation; plasma membrane

Indexed keywords

ACA8 PROTEIN, ARABIDOPSIS; ADENOSINE TRIPHOSPHATASE (CALCIUM); ARABIDOPSIS PROTEIN; CALMODULIN; SERINE;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM-TRANSPORTING ATPASES; CALMODULIN; CELL MEMBRANE; PHOSPHORYLATION; PLANTS, GENETICALLY MODIFIED; SERINE;

ARABIDOPSIS THALIANA; ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 84856836083     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err346     Document Type: Article

References (41)

1. Bækgaards L, Luoni L, De Michelis MI, Palmgren MG. 2006. The plant plasma membrane Ca2+ pump ACA8 contains overlapping as well as physically separated autoinhibitory and calmodulin-binding domains. Journal of Biological Chemistry 281, 1058-1065.
2. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJR, Slijper M, Menke FLH. 2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Molecular and Cellular Proteomics 6, 1198-1214.
3. Bonza MC, De Michelis MI. 2011. The plant Ca2+-ATPases repertoire: biochemical features and physiological functions. Plant Biology 13, 421-430.
4. Bonza MC, Luoni L. 2010. Plant and animal type 2B Ca2+-ATPases: evidence for a common auto-inhibitory mechanism. FEBS Letters 584, 4783-4788.
5. Bonza MC, Luoni L, De Michelis MI. 2004. Functional expression in yeast of an N-deleted form of At-ACA8, a plasma membrane Ca2+-ATPase of Arabidopsis thaliana, and characterization of a hyperactive mutant. Planta 218, 814-823.
6. Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI. 2000. At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiology 123, 1495-1505.
7. Boursiac Y, Harper JF. 2007. The origin and function of calmodulin regulated Ca2+ pumps in plants. Journal of Bioenergetic and Biomembranes 39, 409-414.
8. Chen Y, Hoehenwarter W, Weckwerth W. 2010. Comparative analysis of phytohormone-responsive phosphoproteins in Arabidopsis thaliana using TiO2-phosphopeptide enrichment and mass accuracy precursor alignment. The Plant Journal 63, 1-17.
9. Cheng S-H, Willmann MR, 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. Cunningham KW, Fink GR. 1994. Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+-ATPases. Journal of Cell Biology 124, 351-363.
11. Dammann C, Ichida A, Hong B, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF. 2003. Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiology 132, 1840-1848.
12. Das R, Pandey GK. 2010. Expressional analysis and role of calcium regulated kinases in abiotic stress signalling. Current Genomics 11, 2-13.
13. De Michelis MI, Carnelli A, Rasi-Caldogno F. 1993. The Ca2+ pump of the plasma membrane of Arabidopsis thaliana-characteristics and sensitivity to fluorescein derivatives. Botanica Acta 106, 20-25.
14. Dodd AN, Kudla J, Sanders D. 2010. The language of calcium signaling. Annual Review of Plant Biology 61, 593-620.
15. Enyedi A, Elwess NL, Filoteo AG, Verma AK, Paszty K, Penniston JT. 1997. Protein kinase C phosphorylates the 'a' forms of plasma membrane Ca2+ pump isoform 2 and 3 and prevents binding of calmodulin. Journal of Biological Chemistry 272, 27525-27528.
16. Enyedi A, Verma AK, Filoteo AG, Penniston JT. 1996. Protein kinase C activates the plasma membrane Ca2+ pump isoform 4b by phosphorylation of an inhibitory region downstream of the calmodulin-binding domain. Journal of Biological Chemistry 50, 32461-32467.
17. Fusca T, Bonza MC, Luoni L, Meneghelli S, Marrano CA, De Michelis MI. 2009. Single point mutations in the small cytoplasmic loop of ACA8, a plasma membrane Ca2+-ATPase of Arabidopsis thaliana, generate partially deregulated pumps. Journal of Biological Chemistry 284, 30881-30888.
18. Harper JF, Breton G, Harmon A. 2004. Decoding Ca2+ signals through plant protein kinases. Annual Review of Plant Biology 55, 263-288.
19. Harper JF, Huang J-F, Lloyd SJ. 1994. Genetic identification of an autoinhibitor in CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33, 7267-7277.
20. Hwang I, Sze H, Harper JF. 2000. A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proceedings of the National Academy of Sciences, USA 97, 6224-6229.
21. Jones AME, MacLean D, Studholme DJ, Sanz A, Andreasson E, Rathjen JP, Peck SC. 2009. Phosphoproteomic analysis of nuclei-enriched fractions from Arabidopsis thaliana. Journal of Proteomics 72, 439-451.
22. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
23. Luoni L, Bonza MC, De Michelis MI. 2006. Calmodulin/Ca2+-ATPase interaction at the Arabidopsis thaliana plasma membrane is dependent on calmodulin isoform showing isoform-specific Ca2+ dependencies. Physiologia Plantarum 126, 175-186.
24. Luoni L, Meneghelli S, Bonza MC, De Michelis MI. 2004. Auto-inhibition of Arabidopsis thaliana plasma membrane Ca2+-ATPase involves an interaction of the N-terminus with the small cytoplasmic loop. FEBS Letters 574, 20-24.
25. Malmström S, Akerlund HE, Askerlund P. 2000. Regulatory role of the N terminus of the vacuolar calcium-ATPase in cauliflower. Plant Physiology 122, 517-526.
26. McAinsh MR, Pittman JK. 2009. Shaping the calcium signature. New Phytologist 181, 275-294.
27. Meneghelli S, Fusca T, Luoni L, De Michelis MI. 2008. Dual mechanism of activation of plant plasma membrane Ca2+-ATPase by acidic phospholipids: evidence for a phospholipid binding site which overlaps the calmodulin-binding site. Molecular Membrane Biology 25, 539-546.
28. Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K. 2010. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiology 153, 1161-1174.
29. NiittyläT, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX. 2007. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Molecular and Cellular Proteomics 6, 1711-1726.
30. Nühse TS, Bottrill A, Jones AME, Peck SC. 2007. Quantitative phosphoproteomics analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. The Plant Journal 51, 931-940.
31. Nühse TS, Stensballe A, Jensen ON, Peck SC. 2004. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. The Plant Cell 16, 2394-2405.
32. Nühse TS, Stensballe A, Jensen ON, Peck SC. 2003. Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Molecular and Cellular Proteomics 2, 1234-1243.
33. Penniston JT, Enyedi A. 1998. Modulation of the plasma membrane Ca2+ pump. Journal of Membrane Biology 165, 101-109.
34. Pittman JK, Bonza MC, De Michelis MI. 2011. Ca2+ pumps and Ca2+ antiporters in plant development. In: Geisler M, Venema K, eds. Transporters and pumps in plant signalling. Berlin: Springer-Verlag, 133-161.
35. Rasi-Caldogno F, Carnelli A, De Michelis MI. 1993. Controlled proteolysis activates the plasma membrane Ca2+ pump of higher plants. Plant Physiology 103, 385-390.
36. Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossman J, Gruissem W, Baginsky S. 2009. Large scale Arabidopsis phosphoproteomic profiling reveals novel choloroplast kinase substrates and phosphorylation networks. Plant Physiology 150, 889-903.
37. Sanders D, Pelloux J, Brownlee C, Harper JF. 2002. Calcium at the crossroads of signaling. The Plant Cell 14, S401-S417.
38. Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y. 2008. Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Molecular Systems Biology 4, article 193.
39. Verma AK, Paszty K, Filoteo AG, Penniston JT, Enyedi A. 1999. Protein kinase C phosphorylates plasma membrane Ca2+ pump isoform 4a at its calmodulin binding domain. Journal of Biological Chemistry 1, 527-531.
40. Vitart V, Christodoulou J, Huang J-F, Chazin WJ, Harper JF. 2000. Intramolecular activation of a Ca2+-dependent protein kinase is disrupted by insertions in the tether that connects the calmodulin-like domain to the kinase. Biochemistry 39, 4004-4011.
41. Whiteman S, Serazetdinova L, Jones AME, Sanders D, Rathjen J, Peck SC, Maathuis FJM. 2008. Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics 8, 3536-3547.