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Naunyn-Schmiedeberg's Archives of Pharmacology

, Volume 388, Issue 2, pp 119–132 | Cite as

Clues to the functions of plant NDPK isoforms

  • Sonia Dorion
  • Jean Rivoal
Review

Abstract

This review describes the five nucleoside diphosphate kinase (NDPK) genes found in both model plants Arabidopsis thaliana (thale cress) and Oryza sativa L. (rice). Phylogenetic and sequence analyses of these genes allow the definition of four types of NDPK isoforms with different predicted subcellular localization. These predictions are supported by experimental evidence for most NDPK types. Data mining also provides evidence for the existence of a novel NDPK type putatively localized in the endoplasmic reticulum. Phylogenic analyses indicate that plant types I, II, and III belong to the previously identified Nme group I whereas type IV belongs to Nme group II. Additional analysis of the literature offers clues supporting the idea that the various plant NDPK types have different functions. Hence, cytosolic type I NDPKs are involved in metabolism, growth, and stress responses. Type II NDPKs are localized in the chloroplast and mainly involved in photosynthetic development and oxidative stress management. Type III NDPKs have dual targeting to the mitochondria and the chloroplast and are principally involved in energy metabolism. The subcellular localization and precise function of the novel type IV NDPKs, however, will require further investigations.

Keywords

Plant Nucleoside diphosphate kinase Isoform Stress Metabolism Growth and development 

Abbreviations

AK

Adenylate kinase

ANT

Adenine nucleotide translocator

ER

Endoplasmic reticulum

GFP

Green fluorescent protein

IM

Inner membrane

IMS

Intermembrane space

NDP

Nucleoside diphosphate

NDPK

Nucleoside diphosphate kinase

NTP

Nucleoside triphosphate

PCD

Programmed cell death

ROS

Reactive oxygen species

Notes

Acknowledgments

This work was supported by a Discovery Grant from the National Science and Engineering Research Council of Canada (NSERC) and a grant from the Projet de Recherche en Équipe from the Fonds de Recherche du Québec - Nature et technologies (FRQ-NT).

References

  1. Bernard MA, Ray NB, Olcott MC, Hendricks SP, Mathews CK (2000) Metabolic functions of microbial nucleoside diphosphate kinases. J Bioenerg Biomembr 32:259–267PubMedGoogle Scholar
  2. Boissan M, Dabernat S, Peuchant E, Schlattner U, Lascu I, Lacombe ML (2009) The mammalian Nm23/NDPK family: from metastasis control to cilia movement. Mol Cell Biochem 329:51–62PubMedGoogle Scholar
  3. Bölter B, Sharma R, Soll J (2007) Localisation of Arabidopsis NDPK2−revisited. Planta 226:1059–1065PubMedGoogle Scholar
  4. Bosnar MH, Bago R, Cetković H (2009) Subcellular localization of Nm23/NDPK A and B isoforms: a reflection of their biological function. Mol Cell Biochem 329:63–71. doi: 10.1007/s11010-009-0107-4 PubMedGoogle Scholar
  5. Bovet L, Meylan-Bettex M, Eggman T, Martinoia E, Siegenthaler PA (1999) CDP phosphotransferase activity in spinach intact chloroplasts: possible involvement of nucleoside diphosphate kinase II. Plant Physiol Biochem 37:645–652Google Scholar
  6. Cao T, Srivastava S, Rahman MH, Kav NNV, Hotte N, Deyholos MK, Strelkov SE (2008) Proteome-level changes in the roots of Brassica napus as a result of Plasmodiophora brassicae infection. Plant Sci 174:97–115Google Scholar
  7. Chen JH, Tian L, Xu HF, Tian DG, Luo YM, Ren CM, Yang LM, Shi JS (2012) Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis. Plant Omics 5:194–199Google Scholar
  8. Cho SM, Shin SH, Kim KS, Kim YC, Eun MY, Cho BH (2004) Enhanced expression of a gene encoding a nucleoside diphosphate kinase 1 (OsNDPK1) in rice plants upon infection with bacterial pathogens. Mol Cells 18:390–395PubMedGoogle Scholar
  9. Choi G, Yi H, Lee J, Kwon YK, Soh MS, Shin B, Luka Z, Hahn TR, Song PS (1999) Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401:610–613PubMedGoogle Scholar
  10. Choi G, Kim JI, Hong SW, Shin B, Choi G, Blakeslee JJ, Murphy AS, Seo YW, Kim K, Koh EJ, Song PS, Lee H (2005) A possible role for NDPK2 in the regulation of auxin-mediated responses for plant growth and development. Plant Cell Physiol 46:1246–1254. doi: 10.1093/pcp/pci133 PubMedGoogle Scholar
  11. Dancer J, Veith R, Feil R, Komor E, Stitt M (1990) Independent changes of inorganic pyrophosphate and the ATP/ADP or UTP/UDP ratios in plant cell suspension cultures. Plant Sci 66:59–63Google Scholar
  12. Dar HH, Chakraborti PK (2010) Intermolecular phosphotransfer is crucial for efficient catalytic activity of nucleoside diphosphate kinase. Biochem J 430:539–549. doi: 10.1042/BJ20100026 PubMedGoogle Scholar
  13. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469. doi: 10.1093/nar/gkn180 PubMedCentralPubMedGoogle Scholar
  14. Desvignes T, Pontarotti P, Fauvel C, Bobe J (2009) Nme protein family evolutionary history, a vertebrate perspective. BMC Evol Biol 9:256. doi: 10.1186/1471-2148-9-256 PubMedCentralPubMedGoogle Scholar
  15. Desvignes T, Pontarotti P, Bobe J (2010) Nme gene family evolutionary history reveals pre-metazoan origins and high conservation between humans and the sea anemone, Nematostella vectensis. PLoS One 5:e15506. doi: 10.1371/journal.pone.0015506 PubMedCentralPubMedGoogle Scholar
  16. Dorion S, Dumas F, Rivoal J (2006a) Autophosphorylation of Solanum chacoense cytosolic nucleoside diphosphate kinase on Ser117. J Exp Bot 57:4079–4088PubMedGoogle Scholar
  17. Dorion S, Matton DP, Rivoal J (2006b) Characterization of a cytosolic nucleoside diphosphate kinase associated with cell division and growth in potato. Planta 224:108–124PubMedGoogle Scholar
  18. Edlund B (1971) Purification of a nucleoside diphosphate kinase from pea seed and phosphorylation of the enzyme with adenosine (P32) triphosphate. Acta Chem Scand 25:1370–1376PubMedGoogle Scholar
  19. Escobar Galvis ML, Hakansson G, Alexciev K, Knorpp C (1999) Cloning and characterisation of a pea mitochondrial NDPK. Biochimie 81:1089–1096PubMedGoogle Scholar
  20. Escobar Galvis ML, Marttila S, Hakansson G, Forsberg J, Knorpp C (2001) Heat stress response in pea involves interaction of mitochondrial nucleoside diphosphate kinase with a novel 86-kilodalton protein. Plant Physiol 126:69–77PubMedCentralPubMedGoogle Scholar
  21. Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T (2013) The proteome response of Hordeum spontaneum to salinity stress. Cereal Res Commun 41:78–87Google Scholar
  22. Finan PM, White IR, Findlay JBC, Millner PA (1992) Identification of nucleoside diphosphate kinase from pea microsomal membranes. Biochem Soc Trans 20:10SPubMedGoogle Scholar
  23. Fukamatsu Y, Yabe N, Hasunuma K (2003) Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982–989PubMedGoogle Scholar
  24. Guo G, Lv D, Yan X, Subburaj S, Ge P, Li X, Hu Y, Yan Y (2012) Proteome characterization of developing grains in bread wheat cultivars (Triticum aestivum L.). BMC Plant Biol 12:147. doi: 10.1186/1471-2229-12-147 PubMedCentralPubMedGoogle Scholar
  25. Hajheidari M, Abdollahian-Noghabi M, Askari H, Heidari M, Sadeghian SY, Ober ES, Salekdeh GH (2005) Proteome analysis of sugar beet leaves under drought stress. Proteomics 5:950–960. doi: 10.1002/pmic.200401101 PubMedGoogle Scholar
  26. Hammargren J, Salinas T, Marechal-Drouard L, Knorpp C (2007a) The pea mitochondrial nucleoside diphosphate kinase cleaves DNA and RNA. FEBS Lett 581:3507–3511. doi: 10.1016/j.febslet.2007.06.062 Google Scholar
  27. Hammargren J, Sundström J, Johansson M, Bergman P, Knorpp C (2007b) On the phylogeny, expression and targeting of plant nucleoside diphosphate kinases. Physiol Plant 129:79–89Google Scholar
  28. Hammargren J, Rosenquist S, Jansson C, Knorpp C (2008) A novel connection between nucleotide and carbohydrate metabolism in mitochondria: sugar regulation of the Arabidopsis nucleoside diphosphate kinase 3a gene. Plant Cell Rep 27:529–534. doi: 10.1007/s00299-007-0486-5 PubMedGoogle Scholar
  29. Hanton SL, Matheson LA, Brandizzi F (2006) Seeking a way out: export of proteins from the plant endoplasmic reticulum. Trends Plant Sci 11:335–343PubMedGoogle Scholar
  30. Harris N, Taylor JE, Roberts JA (1994) Isolation of a mRNA encoding a nucleoside diphosphate kinase from tomato that is up-regulated by wounding. Plant Mol Biol 25:739–742PubMedGoogle Scholar
  31. Hooks MA, Shearer GC, Roberts JKM (1994) Nucleotide availability in maize (Zea mays L.) root tips (estimation of free and protein-bound nucleotides using 31P-Nuclear Magnetic Resonance and a novel protein ligand binding assay). Plant Physiol 104:581–589PubMedCentralPubMedGoogle Scholar
  32. Hsu T (2011) NME genes in epithelial morphogenesis. Naunyn-Schmiedeberg's Arch Pharmacol 384:363–372Google Scholar
  33. Hu XL, Lu MH, Li CH, Liu TX, Wang W, Wu JY, Tai FJ, Li X, Zhang J (2011) Differential expression of proteins in maize roots in response to abscisic acid and drought. Acta Physiol Plant 33:2437–2446Google Scholar
  34. Hughes J (2013) Phytochrome cytoplasmic signaling. Annu Rev Plant Biol 64:377–402. doi: 10.1146/annurev-arplant-050312-120045 PubMedGoogle Scholar
  35. Hutton JL, Knight CD, Millner PA (1998) The Physcomitrella patens GPα1 homologue is located at protonemal cell junctions. J Exp Bot 49:1113–1118Google Scholar
  36. Igamberdiev AU, Kleczkowski LA (2001) Implications of adenylate kinase-governed equilibrium of adenylates on contents of free magnesium in plant cells and compartments. Biochem J 360:225–231PubMedCentralPubMedGoogle Scholar
  37. Ishikawa T, Morimoto Y, Madhusudhan R, Sawa Y, Shibata H, Yabuta Y, Nishizawa A, Shigeoka S (2005) Acclimation to diverse environmental stresses caused by a suppression of cytosolic ascorbate peroxidase in tobacco BY-2 cells. Plant Cell Physiol 46:1264–1271PubMedGoogle Scholar
  38. Jacoby RP, Millar AH, Taylor NL (2013) Investigating the role of respiration in plant salinity tolerance by analyzing mitochondrial proteomes from wheat and a salinity-tolerant Amphiploid (wheat x Lophopyrum elongatum). J Proteome Res 12:4807–4829. doi: 10.1021/pr400504a PubMedGoogle Scholar
  39. Jaedicke K, Rosler J, Gans T, Hughes J (2011) Bellis perennis: a useful tool for protein localization studies. Planta 234:759–768. doi: 10.1007/s00425-011-1443-7 PubMedGoogle Scholar
  40. Johansson M, Mackenzie-Hose A, Andersson I, Knorpp C (2004) Structure and mutational analysis of a plant mitochondrial nucleoside diphosphate kinase. Identification of residues involved in serine phosphorylation and oligomerization. Plant Physiol 136:3034–3042PubMedCentralPubMedGoogle Scholar
  41. Johansson M, Hammargren J, Uppsall E, MacKenzie A, Knorpp C (2008) The activities of nucleoside diphosphate kinase and adenylate kinase are influenced by their interaction. Plant Sci 174:192–199Google Scholar
  42. Ju CL, Chang C (2012) Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane. Aob Plants 2012:031Google Scholar
  43. Kangasjarvi S, Neukermans J, Li SC, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636PubMedGoogle Scholar
  44. Kav NNV, Srivastava S, Goonewardene L, Blade SF (2004) Proteome-level changes in the roots of Pisum sativum in response to salinity. Ann Appl Biol 145:217–230Google Scholar
  45. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905PubMedCentralPubMedGoogle Scholar
  46. Kihara A, Saburi W, Wakuta S, Kim MH, Hamada S, Ito H, Imai R, Matsui H (2011) Physiological and biochemical characterization of three nucleoside diphosphate kinase isozymes from rice (Oryza sativa L.). Biosci Biotech Biochem 75:1740–1745Google Scholar
  47. Kim YH, Lim S, Yang KS, Kim C, Kwon SY, Lee HS, Wang X, Zhou Z, Ma D, Yun DJ, Kwak SS (2009) Expression of Arabidopsis NDPK2 increases antioxidant enzyme activities and enhances tolerance to multiple environmental stresses in transgenic sweetpotato plants. Mol Breeding 24:233–244Google Scholar
  48. Kim YH, Kim MD, Choi YI, Park SC, Yun DJ, Noh EW, Lee HS, Kwak SS (2011) Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance. Plant Biotechnol J 9:334–347PubMedGoogle Scholar
  49. Knorpp C, Johansson M, Baird AM (2003) Plant mitochondrial nucleoside diphosphate kinase is attached to the membrane through interaction with the adenine nucleotide translocator. FEBS Lett 555:363–366PubMedGoogle Scholar
  50. Kottapalli KR, Rakwal R, Shibato J, Burow G, Tissue D, Burke J, Puppala N, Burow M, Payton P (2009) Physiology and proteomics of the water-deficit stress response in three contrasting peanut genotypes. Plant, Cell Environ 32:380–407. doi: 10.1111/j.1365-3040.2009.01933.x Google Scholar
  51. Lambeth DO, Mehus JG, Ivey MA, Milavetz BI (1997) Characterization and cloning of a nucleoside-diphosphate kinase targeted to matrix of mitochondria in pigeon. J Biol Chem 272:24604–24611PubMedGoogle Scholar
  52. Lascu I, Gonin P (2000) The catalytic mechanism of nucleoside diphosphate kinases. J Bioenerg Biomembr 32:237–246PubMedGoogle Scholar
  53. Lee DG, Ahsan N, Lee SH, Kang KY, Lee JJ, Lee BH (2007) An approach to identify cold-induced low-abundant proteins in rice leaf. C R Biol 330:215–225. doi: 10.1016/j.crvi.2007.01.001 PubMedGoogle Scholar
  54. Li Y, Zhang Z, Nie Y, Zhang L, Wang Z (2012) Proteomic analysis of salicylic acid-induced resistance to Magnaporthe oryzae in susceptible and resistant rice. Proteomics 12:2340–2354. doi: 10.1002/pmic.201200054 PubMedGoogle Scholar
  55. Liao M, Li Y, Wang Z (2009) Identification of elicitor-responsive proteins in rice leaves by a proteomic approach. Proteomics 9:2809–2819. doi: 10.1002/pmic.200800192 PubMedGoogle Scholar
  56. Lin SK, Chang MC, Tsai YG, Lur HS (2005) Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression. Proteomics 5:21:40–2156. doi: 10.1002/pmic.200401105 Google Scholar
  57. Liu YD, Ren DT, Pike S, Pallardy S, Gassmann W, Zhang SQ (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51:941–954PubMedGoogle Scholar
  58. Lubeck J, Soll J (1995) Nucleoside diphosphate kinase from pea chloroplasts: purification, cDNA cloning and import into chloroplasts. Planta 196:668–673PubMedGoogle Scholar
  59. Marino N, Nakayama J, Collins J, Steeg P (2012) Insights into the biology and prevention of tumor metastasis provided by the Nm23 metastasis suppressor gene. Cancer Metastasis Rev 31:593–603PubMedGoogle Scholar
  60. Martinez-Esteso MJ, Selles-Marchart S, Lijavetzky D, Pedreno MA, Bru-Martinez R (2011) A DIGE-based quantitative proteomic analysis of grape berry flesh development and ripening reveals key events in sugar and organic acid metabolism. J Exp Bot 62:2521––2569. doi: 10.1093/jxb/erq434 PubMedGoogle Scholar
  61. McFarlane HE, Doring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol. doi: 10.1146/annurev-arplan PubMedGoogle Scholar
  62. McIntosh S, Watson L, Bundock P, Crawford A, White J, Cordeiro G, Barbary D, Rooke L, Henry R (2007) SAGE of the developing wheat caryopsis. Plant Biotechnol J 5:69––83. doi: 10.1111/j.1467-7652.2006.00218 PubMedGoogle Scholar
  63. Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: simple ligand, complex regulation. Curr Opin Plant Biol 16:554–560. doi: 10.1016/j.pbi.2013.08.001 PubMedGoogle Scholar
  64. Milon L, Meyer P, Chiadmi M, Munier A, Johansson M, Karlsson A, Lascu I, Capeau J, Janin J, Lacombe ML (2000) The human nm23-H4 gene product is a mitochondrial nucleoside diphosphate kinase. J Biol Chem 275:14264–14272PubMedGoogle Scholar
  65. Mlejnek P, Dolezel P, Prochazka S (2003) Intracellular phosphorylation of benzyladenosine is related to apoptosis induction in tobacco BY-2 cells. Plant, Cell Environ 26:1723–1735Google Scholar
  66. Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci U S A 100:358–363PubMedCentralPubMedGoogle Scholar
  67. Nomura T, Fukui T, Ichikawa A (1991) Purification and characterization of nucleoside diphosphate kinase from spinach leaves. Biochim Biophys Acta 1077:47–55PubMedGoogle Scholar
  68. Nomura T, Yatsunami K, Honda A, Sugimoto Y, Fukui T, Zhang J, Yamamoto J, Ichikawa A (1992) The amino acid sequence of nucleoside diphosphate kinase I from spinach leaves, as deduced from the cDNA sequence. Arch Biochem Biophys 297:42–45PubMedGoogle Scholar
  69. Novikova GV, Moshkov IE, Smith AR, Kulaeva ON, Hall MA (1999) The effect of ethylene and cytokinin on guanosine 5'-triphosphate binding and protein phosphorylation in leaves of Arabidopsis thaliana. Planta 208:239–246PubMedGoogle Scholar
  70. Novikova GV, Moshkov IE, Smith AR, Hall MA (2003) Nucleoside diphosphate kinase is a possible component of the ethylene signal transduction pathway. Biochemistry (Mosc ) 68:1342–1348Google Scholar
  71. Ovecka M, Takac T, Komis G, Vadovic P, Bekesova S, Doskocilova A, Smekalova V, Luptovciak I, Samajova O, Schweighofer A, Meskiene I, Jonak C, Krenek P, Lichtscheidl I, Skultety L, Hirt H, Samaj J (2014) Salt-induced subcellular kinase relocation and seeding susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis. J Exp Bot In press. DOI eru115 [pii]; 10.1093/jxb/eru115
  72. Pan L, Kawai M, Yano A, Uchimiya H (2000) Nucleoside diphosphate kinase required for coleoptile elongation in rice. Plant Physiol 122:447–452PubMedCentralPubMedGoogle Scholar
  73. Parks REJ, Agarwal RP (1973) Nucleoside diphosphokinases. Enzymes 8:307–334Google Scholar
  74. Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 5:114–133. doi: 10.1074/mcp.M500180-MCP200 PubMedGoogle Scholar
  75. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide-a central hub for information flow in plant cells. Aob Plants 2012:pls014PubMedCentralPubMedGoogle Scholar
  76. Reiter WD, Vanzin GF (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Mol Biol 47:95–113PubMedGoogle Scholar
  77. Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber AP, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150:125–143. doi: 10.1104/pp.109.137703 PubMedCentralPubMedGoogle Scholar
  78. Reuveni M, Dupont FM (2001) Manganese enhances the phosphorylation of membrane-associated proteins isolated from barley roots. J Plant Physiol 158:699–708Google Scholar
  79. Ricardo CP, Martins I, Francisco R, Sergeant K, Pinheiro C, Campos A, Renaut J, Fevereiro P (2011) Proteins associated with cork formation in Quercus suber L. stem tissues. J Proteomics 74:1266–1278. doi: 10.1016/j.jprot.2011.02.003 PubMedGoogle Scholar
  80. Roberts JKM, Aubert S, Gout E, Bligny R, Douce R (1997) Cooperation and competition between adenylate kinase, nucleoside diphosphokinase, electron transport, and ATP synthase in plant mitochondria studied by 31P-Nuclear Magnetic Resonance. Plant Physiol 113:191–199PubMedCentralPubMedGoogle Scholar
  81. Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J (2002) Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2:1131–1145. doi: 10.1002/1615-9861 PubMedGoogle Scholar
  82. Schlattner U, Tokarska-Schlattner M, Ramirez S, Tyurina YY, Amoscato AA, Mohammadyani D, Huang Z, Jiang J, Yanamala N, Seffouh A, Boissan M, Epand RF, Epand RM, Klein-Seetharaman J, Lacombe ML, Kagan VE (2013) Dual function of mitochondrial Nm23-H4 protein in phosphotransfer and intermembrane lipid transfer: a cardiolipin-dependent switch. J Biol Chem 288:111–121. doi: 10.1074/jbc.M112.408633 PubMedCentralPubMedGoogle Scholar
  83. Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7:277–284PubMedGoogle Scholar
  84. Sharma R, Soll J, Bölter B (2007) Import and localisation of nucleoside diphosphate kinase 2 in chloroplasts. J Plant Res 120:451–456. doi: 10.1007/s10265-007-0071-6 PubMedGoogle Scholar
  85. Shin DH, In JG, Lim YP, Hasunuma K, Choi KS (2004) Molecular cloning and characterization of nucleoside diphosphate (NDP) kinases from Chinese cabbage (Brassica campestris). Mol Cells 17:86–94PubMedGoogle Scholar
  86. Spetea C, Lundin B (2012) Evidence for nucleotide-dependent processes in the thylakoid lumen of plant chloroplasts—an update. FEBS Lett 586:2946–2954. doi: 10.1016/j.febslet.2012.07.005 PubMedGoogle Scholar
  87. Spetea C, Hundal T, Lohmann F, Andersson B (1999) GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the photosystem II D1 protein. Proc Natl Acad Sci U S A 96:6547–6552PubMedCentralPubMedGoogle Scholar
  88. Spetea C, Keren N, Hundal T, Doan JM, Ohad I, Andersson B (2000) GTP enhances the degradation of the photosystem II D1 protein irrespective of its conformational heterogeneity at the Q(B) site. J Biol Chem 275:7205–7211PubMedGoogle Scholar
  89. Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B (2004) Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proc Natl Acad Sci U S A 101:1409–1414PubMedCentralPubMedGoogle Scholar
  90. Steeg PS, Zollo M, Wieland T (2011) A critical evaluation of biochemical activities reported for the nucleoside diphosphate kinase/Nm23/Awd family proteins: opportunities and missteps in understanding their biological functions. Naunyn Schmiedebergs Arch Pharmacol 384:331–339. doi: 10.1007/s00210-011-0651-9 PubMedGoogle Scholar
  91. Struglics A, Hakansson G (1999) Purification of a serine and histidine phosphorylated mitochondrial nucleoside diphosphate kinase from Pisum sativum. Eur J Biochem 262:765–773PubMedGoogle Scholar
  92. Sweetlove LJ, Mowday B, Hebestreit HF, Leaver CJ, Millar AH (2001) Nucleoside diphosphate kinase III is localized to the inter-membrane space in plant mitochondria. FEBS Lett 508:272–276PubMedGoogle Scholar
  93. Tanaka N, Ogura T, Noguchi T, Hirano H, Yabe N, Hasunuma K (1998) Phytochrome-mediated light signals are transduced to nucleoside diphosphate kinase in Pisum sativum L. cv. Alaska. J Photochem Photobiol, B 45:113–121Google Scholar
  94. Tang L, Kim MD, Yang KS, Kwon SY, Kim SH, Kim JS, Yun DJ, Kwak SS, Lee HS (2008) Enhanced tolerance of transgenic potato plants overexpressing nucleoside diphosphate kinase 2 against multiple environmental stresses. Transgenic Res 17:705–715. doi: 10.1007/s11248-007-9155-2 PubMedGoogle Scholar
  95. Thuswaldner S, Lagerstedt JO, Rojas-Stutz M, Bouhidel K, Der C, Leborgne-Castel N, Mishra A, Marty F, Schoefs B, Adamska I, Persson BL, Spetea C (2007) Identification, expression, and functional analyses of a thylakoid ATP/ADP carrier from Arabidopsis. J Biol Chem 282:8848–8859. doi: 10.1074/jbc.M609130200 PubMedGoogle Scholar
  96. Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281. doi: 10.1104/pp.010999 PubMedCentralPubMedGoogle Scholar
  97. Tognetti VB, Muhlenbock P, Van Breusegem F (2012) Stress homeostasis—the redox and auxin perspective. Plant, Cell Environ 35:321–333Google Scholar
  98. Tokarska-Schlattner M, Boissan M, Munier A, Borot C, Mailleau C, Speer O, Schlattner U, Lacombe ML (2008) The nucleoside diphosphate kinase D (NM23-H4) binds the inner mitochondrial membrane with high affinity to cardiolipin and couples nucleotide transfer with respiration. J Biol Chem 283:26198–26207. doi: 10.1074/jbc.M803132200 PubMedCentralPubMedGoogle Scholar
  99. Um MO, Park TI, Kim YJ, Seo HY, Kim JG, Kwon SY, Kwak SS, Yun DJ, Yun SJ (2007) Particle bombardment-mediated transformation of barley with an Arabidopsis NDPK2 cDNA. Plant Biotechnol Rep 1:71–77Google Scholar
  100. Valenti D, Vacca RA, De Pinto MC, De GL, Marra E, Passarella S (2007) In the early phase of programmed cell death in Tobacco Bright Yellow 2 cells the mitochondrial adenine nucleotide translocator, adenylate kinase and nucleoside diphosphate kinase are impaired in a reactive oxygen species-dependent manner. Biochim Biophys Acta 1767:66–78. doi: 10.1016/j.bbabio.2006.11.004 PubMedGoogle Scholar
  101. Verslues PE, Batelli G, Grillo S, Agius F, Kim YS, Zhu J, Agarwal M, Katiyar-Agarwal S, Zhu JK (2007a) Interaction of SOS2 with NDPK2 and catalases reveals a point of connection between salt stress and H2O2 signaling in Arabidopsis. Mol Cell Biol 27:7771–7780Google Scholar
  102. Verslues PE, Kim YS, Zhu JK (2007b) Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate:glyoxylate aminotransferase mutant. Plant Mol Biol 64:205–217. doi: 10.1007/s11103-007-9145-z PubMedGoogle Scholar
  103. Vitale A, Denecke J (1999) The endoplasmic reticulum-gateway of the secretory pathway. Plant Cell 11:615–628PubMedCentralPubMedGoogle Scholar
  104. White IR, Finan PM, Millner PA (1993) Nucleoside diphosphate kinase associated with Pisum sativum microsomal membranes: apparent binding of GTP-gamma-S at nM concentrations. J Plant Physiol 142:191–196Google Scholar
  105. Yang LM, Lamppa GK (1996) Rapid purification of a chloroplast nucleoside diphosphate kinase using CoA-affinity chromatography. Biochim Biophys Acta 1294:99–102PubMedGoogle Scholar
  106. Yang KA, Moon H, Kim G, Lim CJ, Hong JC, Lim CO, Yun DJ (2003) NDP kinase 2 regulates expression of antioxidant genes in Arabidopsis. P Jpn Acad B-Phys Biol Sci 79:86–91Google Scholar
  107. Yang PF, Li XJ, Liang Y, Jing YX, Shen SH, Kuang TY (2006) Proteomic analysis of the response of Liangyoupeijiu (super high-yield hybrid rice) seedlings to cold stress. J Int Plant Biol 48:945–951Google Scholar
  108. Zhang J, Fukui T, Ichikawa A (1995) A third type of nucleoside diphosphate kinase from spinach leaves: purification, characterization and amino-acid sequence. Biochim Biophys Acta 1248:19–26Google Scholar
  109. Zimmermann S, Baumann A, Jaekel K, Marbach I, Engelberg D, Frohnmeyer H (1999) UV-responsive genes of arabidopsis revealed by similarity to the Gcn4- mediated UV response in yeast. J Biol Chem 274:17017–17024PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.IRBVUniversité de MontréalMontréalCanada

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