StCDPK2 expression and activity reveal a highly responsive potato calcium-dependent protein kinase involved in light signalling

Planta

Volumn 233, Issue 3, 2011, Pages 593-609

  Giammaria, Verónica ^a   Grandellis, Carolina ^a   Bachmann, Sandra ^a   Gargantini, Pablo Rubén ^a,d   Feingold, Sergio Enrique ^b   Bryan, Glenn ^c   Ulloa, Rita María ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^d UNIVERSIDAD CATÓLICA DE CÓRDOBA   (Argentina)

Author keywords

Autophosphorylation; CDPK; Light; Phospholipids; Solanum tuberosum

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; CALCIUM PROTEIN KINASE; CALCIUM-DEPENDENT PROTEIN KINASE; ISOPROTEIN; PROTEIN KINASE; RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; POTATO; PROMOTER REGION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; UPREGULATION;

AMINO ACID SEQUENCE; CALCIUM; CALCIUM-BINDING PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; LIGHT; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; PROTEIN KINASES; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SOLANUM TUBEROSUM; UP-REGULATION;

SOLANUM TUBEROSUM;

EID: 79951947060     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1319-2     Document Type: Article

References (60)

1. Andronis C, Barak S, Knowles SM, Sugano S, Tobin EM (2008) The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol Plant 1: 58-67.
2. Arguello-Astorga G, Herrera-Estrella L (1998) Evolution of light-regulated plant promoters. Annu Rev Plant Physiol Plant Mol Biol 49: 525-555.
3. Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46: 356-366.
4. Bachmann M, Shiraishi N, Campbell WH, Yoo BC, Harmon AC, Huber SC (1996) Identification of the major regulatory phosphorylation site as Ser-543 in spinach leaf nitrate reductase and its phosphorylation by a calcium-dependent protein kinase in vitro. Plant Cell 8: 505-517.
5. Bonierbale MW, Plaisted RL, Pineda O, Tanksley SD (1994) QTL analysis of trichome-mediated insect resistance in potato. Theor Appl Genet 87: 973-987.
6. Chaudhuri S, Seal A, Gupta MD (1999) Autophosphorylation-dependent activation of a calcium-dependent protein kinase from groundnut. Plant Physiol 120: 859-866.
7. 2+. Plant Cell 20: 353-366.
8. 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 Physiol 129: 469-485.
9. Chico JM, Raíces M, Téllez-Iñón MT, Ulloa RM (2002) A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol 128: 256-270.
10. Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139: 1750-1761.
11. Dyson HJ, Wright PE (2005) Elucidation of the protein folding landscape by NMR. Methods Enzymol 394: 299-321.
12. Ellard-Ivey M, Hopkins RB, White TJ, Lomax TL (1999) Cloning, expression and N-terminal myristoylation of CpCPK1, a calcium-dependent protein kinase from zucchini (Cucurbita pepo L.). Plant Mol Biol 39: 199-208.
13. Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30: 235-238.
14. Farmer P, Choi J (1999) Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.). Biochim Biophys Acta 14: 6-17.
15. Feingold S, Lloyd J, Norero N, Bonierbale M, Lorenzen J (2005) Mapping and characterization of new EST-derived microsatellites for potato (Solanum tuberosum L.). Theor Appl Genet 111: 456-466.
16. Gargantini PR, Gonzalez-Rizzo S, Chinchilla D, Raices M, Giammaria V, Ulloa RM, Frugier F, Crespi MD (2006) A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. Plant J 48: 843-856.
17. Gargantini PR, Giammaria V, Grandellis C, Feingold SE, Maldonado S, Ulloa RM (2009) Genomic and functional characterization of StCDPK1. Plant Mol Biol 70: 153-172.
18. Gehring CA, Williams DA, Cody SH, Parish RW (1990) Phototropism and geotropism in maize coleoptiles are spatially correlated with increases in cytosolic free calcium. Nature 345: 528-530.
19. Gidoni D, Brosio P, Bond-Nutter D, Bedbrook J, Dunsmuir P (1989) Novel cis-acting elements in Petunia Cab gene promoters. Mol Gen Genet 215: 337-344.
20. Harada A, Shimazaki K (2007) Phototropins and blue light-dependent calcium signaling in higher plants. Photochem Photobiol 83: 102-111.
21. Harmon AC (2003) Calcium-regulated protein kinases of plants. Gravit Space Biol Bull 16: 83-90.
22. 2+ signal? Trends Plant Sci 5: 154-159.
23. Harper JF, Binder BM, Sussman MR (1993) Calcium and lipid regulation of an Arabidopsis protein kinase expressed in Escherichia coli. Biochemistry 32: 3282-3290.
24. 2+ signals through plant protein kinases. Annu Rev Plant Biol 55: 263-288.
25. Harris N, Spence J, Oparka KJ (1994) Immunocytochemistry for light and electron microscopy. In: Harris N, Oparka KJ (eds) Plant cell biology: a practical approach. IRL Press at Oxford University Press, Oxford, pp 157-176.
26. Hein I, McLean K, Chalhoub B, Bryan G (2007) Generation and screening of a BAC library from a diploid potato clone to unravel durable late blight resistance on linkage group IV. Int J Plant Genomics (article ID 51421).
27. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132: 666-680.
28. Ishida S, Yuasa T, Nakata M, Takahashi Y (2008) A tobacco calcium-dependent protein kinase, CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTH in response to gibberellins. Plant Cell 20: 3273-3288.
29. 2+-dependent protein kinase is important for substrate recognition. Plant Cell 22: 1592-1604.
30. Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269: 1863-1865.
31. Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2: 13-21.
32. Klimecka M, Muszyńska G (2007) Structure and functions of plant calcium-dependent protein kinases. Acta Biochim Pol 54: 219-233.
33. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080.
34. Kooijman EE, Tieleman DP, Testerink C, Munnik T, Rijkers DT, Burger KN, de Kruijff B (2007) An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. J Biol Chem 282: 11356-11364.
35. Kooijman EE, King KE, Gangoda M, Gericke A (2009) Ionization properties phosphatidylinositol polyphosphates in mixed model membranes. Biochemistry 48: 9360-9371.
36. Li A, Zhu YF, Tan XM, Wang X, Wei B, Guo HZ, Zhang ZL, Chen XB, Zhao GY, Kong XY, Jia JZ, Mao L (2008a) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66: 429-443.
37. Li A, Wang X, Leseberg CH, Jia J, Mao L (2008b) Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.). Plant Signal Behav 3: 654-656.
38. Lu S, Hrabak E (2002) An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum. Plant Physiol 12: 1008-1021.
39. Ludwig A, Romeis T, Jones J (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55: 181-188.
40. Martín ML, Busconi L (2000) Membrane localization of a rice calcium-dependent protein kinase (CDPK) is mediated by myristoylation and palmitoylation. Plant J 24: 429-435.
41. Monreal JA, López-Baena FJ, Vidal J, Echevarría C, García-Mauriño S (2010) Involvement of phospholipase D and phosphatidic acid in the light-dependent up-regulation of sorghum leaf phosphoenolpyruvate carboxylase-kinase. J Exp Bot 61: 2819-2827.
42. Munnik T, Testerink C (2009) Plant phospholipid signaling: "in a nutshell". J Lipid Res 50(Suppl): S260-S265.
43. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15: 473-497.
44. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321-4325.
45. Raices M, Gargantini PR, Chinchilla D, Crespi M, Tellez-Inon MT, Ulloa RM (2003) Regulation of CDPK isoforms during tuber development. Plant Mol Biol 52: 1011-1024.
46. Raíces M, Chico JM, Téllez-Iñón MT, Ulloa RM (2001) Molecular characterization of StCDPK1, a calcium-dependent protein kinase from Solanum tuberosum that is induced at the onset of tuber development. Plant Mol Biol 46: 591-601.
47. Romeis T, Piedras P, Jones JDG (2000) Resistance gene dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12: 803-815.
48. Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20: 5556-5567.
49. Saha P, Singh M (1995) Characterization of a winged bean (Psophocarpus tetragonolobus) protein kinase with calmodulin-like domain: regulation by autophosphorylation. Biochem J 305: 205-210.
50. Schaller GE, Harmon AC, Sussman MR (1992) Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat. Biochemistry 31: 1721-1727.
51. Schindler U, Cashmore AR (1990) Photoregulated gene expression may involve ubiquitous DNA binding proteins. EMBO J 9: 3415-3427.
52. Schlessinger A, Liu J, Rost B (2007) Natively unstructured loops differ from other loops. PLoS Comput Biol 3: e140.
53. Shapiro MB, Senapathy P (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15: 7155-7714.
54. Sutoh K, Yamauchi D (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant J 34: 635-645.
55. Szczegielniak J, Liwosz A, Jurkowski I, Loog M, Dobrowolska G, Ek P, Harmon AC, Muszyńska G (2000) Calcium-dependent protein kinase from maize seedlings activated by phospholipids. Eur J Biochem 267: 3818-3827.
56. Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, Harmon AC, Muszyńska G (2005) A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol 139: 1970-1983.
57. Ulloa RM, Raíces M, MacIntosh GC, Maldonado S, Téllez-Iñón MT (2002) Jasmonic acid affects plant morphology and calcium-dependent protein kinase expression and activity in Solanum tuberosum. Physiol Plant 115: 417-427.
58. van Os H, Andrzejewski S, Bakker E (2006) Construction of a 10, 000-marker ultra-dense genetic recombination map of potato: providing a framework for accelerated gene isolation and a genome wide physical map. Genetics 173: 1075-1087.
59. van Schooten B, Testerink C, Munnik T (2006) Signalling diacylglycerol pyrophosphate, a new phosphatidic acid metabolite. Biochim Biophys Acta 1761: 151-159.
60. Witte CP, Keinath N, Dubiella U, Demoulière R, Seal A, Romeis T (2010) Tobacco calcium-dependent protein kinases are differentially phosphorylated in vivo as part of a kinase cascade that regulates stress response. J Biol Chem 285: 9740-9748.