Skip to main content
SpringerLink
Log in
Book cover

Progress in Botany pp 119–144Cite as

Nucleotides and Nucleosides: Transport, Metabolism, and Signaling Function of Extracellular ATP

  • Chapter
  • First Online:

Part of the book series: Progress in Botany ((BOTANY,volume 75))

Abstract

The focus of this work is to summarize the current knowledge related to transport of nucleotides and nucleosides in and outside of cells, including the vacuole, and functions and metabolism of extracellular ATP (eATP). Thereby mechanisms on how nucleotides and their derivatives can leave cells and how their export is stimulated are described. Furthermore, effects exerted by eATP are listed including the corresponding downstream signaling events. The signal molecule eATP is removed from the extracellular space by the hydrolytic activity of several degrading enzymes like E-NTPDases, phosphatases, 5′ nucleotidases, and nucleoside hydrolases. The final reaction products of these enzymes, nucleosides and nucleobases, are then reimported into the cells to supply the corresponding cytosolic pools. The family of equilibrative nucleoside transporters (ENTs), responsible for nucleoside reimport into the cells, is presented in more detail. Finally, plant ENT family members residing at the plasma membrane or the tonoplast are compared with human and yeast homologs at the biochemical and physiological level.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abeijon C, Yanagisawa K, Mandon EC, Hausler A, Moremen K, Hirschberg CB, Robbins PW (1993) Guanosine diphosphatase is required for protein and sphingolipid glycosylation in the Golgi lumen of Saccharomyces cerevisiae. J Cell Biol 122:307–323

    Article  PubMed  CAS  Google Scholar 

  • Abel S, Blume B, Glund K (1990) Evidence for RNA-oligonucleotides in plant vacuoles isolated from cultured tomato cells. Plant Physiol 94:1163–1171

    Article  PubMed  CAS  Google Scholar 

  • Abraham EH, Prat AG, Gerweck L, Seneveratne T, Arceci RJ, Kramer R, Guidotti G, Cantiello HF (1993) The multidrug resistance (mdr1) gene product functions as an ATP channel. Proc Natl Acad Sci USA 90:312–316

    Article  PubMed  CAS  Google Scholar 

  • Albacete A, Ghanem ME, Martinez-Andujar C, Acosta M, Sanchez-Bravo J, Martinez V, Lutts S, Dodd IC, Perez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131

    Article  PubMed  CAS  Google Scholar 

  • Allen M, Qin W, Moreau F, Moffatt B (2002) Adenine phosphoribosyltransferase isoforms of Arabidopsis and their potential contributions to adenine and cytokinin metabolism. Physiol Plant 115:56–68

    Article  PubMed  CAS  Google Scholar 

  • Baldwin SA, Beal PR, Yao SY, King AE, Cass CE, Young JC (2003) The equilibrative nucleoside transporter family, SLC29. Pflugers Arch 447:735–743

    PubMed  Google Scholar 

  • Baldwin SA, Yao SY, Hyde RJ, Ng AM, Foppolo S, Barnes K, Ritzel MW, Cass CE, Young JD (2005) Functional characterization of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes. J Biol Chem 280:15880–15887

    Article  PubMed  CAS  Google Scholar 

  • Beck HE (1996) Regulation of shoot/root ratio from roots in Urtica dioica: opinion. Plant Soil 185:3–12

    Article  CAS  Google Scholar 

  • Bernard C, Traub M, Kunz HH, Hach S, Trentmann O, Möhlmann T (2011) Equilibrative nucleoside transporter 1 (ENT1) is critical for pollen germination and vegetative growth in Arabidopsis. J Exp Bot 62:4627–4637

    Article  PubMed  CAS  Google Scholar 

  • Blatt MR (1987) Electrical characteristics of stomatal guard cells: the contribution of ATP-dependent, “Electrogenic” transport revealed by current–voltage and difference-current–voltage analysis. J Membr Biol 98:257–274

    Article  CAS  Google Scholar 

  • Borisjuk L, Rolletschek H, Walenta S, Panitz R, Wobus U, Weber H (2003) Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. Plant J 36:318–329

    Article  PubMed  CAS  Google Scholar 

  • Bürkle L, Cedzich A, Dopke C, Stransky H, Okumoto S, Gillissen B, Kuhn C, Frommer WB (2003) Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis. Plant J 34:13–26

    Article  PubMed  Google Scholar 

  • Burnstock G (2009) Purinergic signalling: past, present and future. Braz J Med Biol Res 42:3–8

    Article  PubMed  CAS  Google Scholar 

  • Cedzich A, Stransky H, Schulz B, Frommer WB (2008) Characterization of cytokinin and adenine transport in Arabidopsis cell cultures. Plant Physiol 148:1857–1867

    Article  PubMed  CAS  Google Scholar 

  • Chen CM, Kristopeit SM (1981) Metabolism of cytokinin: dephosphorylation of cytokinin ribonucleotides by 5′-nucleotidases from wheat germ cytosol. Plant Physiol 67:494–498

    Article  PubMed  CAS  Google Scholar 

  • Chen KL, Xu MX, Li GY, Liang H, Xia ZL, Liu X, Zhang JS, Zhang AM, Wang DW (2006) Identification of AtENT3 as the main transporter for uridine uptake in Arabidopsis roots. Cell Res 16:377–388

    Article  PubMed  CAS  Google Scholar 

  • Chiu TY, Christiansen K, Moreno I, Lao J, Loque D, Orellana A, Heazlewood JL, Clark G, Roux SJ (2012) AtAPY1 and AtAPY2 function as Golgi localized nucleoside diphosphatases in Arabidopsis thaliana. Plant Cell Physiol 53:1913–1925

    Article  PubMed  CAS  Google Scholar 

  • Chivasa S, Ndimba BK, Simon WJ, Lindsey K, Slabas AR (2005) Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 17:3019–3034

    Article  PubMed  CAS  Google Scholar 

  • Chivasa S, Murphy AM, Hamilton JM, Lindsey K, Carr JP, Slabas AR (2009) Extracellular ATP is a regulator of pathogen defence in plants. Plant J 60:436–448

    Article  PubMed  CAS  Google Scholar 

  • Choi DS, Cascini MG, Mailliard W, Young H, Paredes P, McMahon T, Diamond I, Bonci A, Messing RO (2004) The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference. Nat Neurosci 7:855–861

    Article  PubMed  CAS  Google Scholar 

  • Clark G, Torres J, Finlayson S, Guan X, Handley C, Lee J, Kays JE, Chen ZJ, Roux SJ (2010a) Apyrase (nucleoside triphosphate-diphosphohydrolase) and extracellular nucleotides regulate cotton fiber elongation in cultured ovules. Plant Physiol 152:1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Clark G, Wu M, Wat N, Onyirimba J, Pham T, Herz N, Ogoti J, Gomez D, Canales AA, Aranda G, Blizard M, Nyberg T, Terry A, Torres J, Wu J, Roux SJ (2010b) Both the stimulation and inhibition of root hair growth induced by extracellular nucleotides in Arabidopsis are mediated by nitric oxide and reactive oxygen species. Plant Mol Biol 74:423–435

    Article  PubMed  CAS  Google Scholar 

  • Clark G, Fraley D, Steinebrunner I, Cervantes A, Onyirimba J, Liu A, Torres J, Tang W, Kim J, Roux SJ (2011) Extracellular nucleotides and apyrases regulate stomatal aperture in Arabidopsis. Plant Physiol 156:1740–1753

    Article  PubMed  CAS  Google Scholar 

  • Cornelius S, Traub M, Bernard C, Salzig C, Lang P, Möhlmann T (2012) Nucleoside transport across the plasma membrane mediated by equilibrative nucleoside transporter 3 influences metabolism of Arabidopsis seedlings. Plant Biol 14:696–705

    Article  CAS  Google Scholar 

  • Crawford CR, Patel DH, Naeve C, Belt JA (1998) Cloning of the human equilibrative, nitrobenzylmercaptopurine riboside (NBMPR)-insensitive nucleoside transporter ei by functional expression in a transport-deficient cell line. J Biol Chem 273:5288–5293

    Article  PubMed  CAS  Google Scholar 

  • Dark A, Demidchik V, Richards SL, Shabala S, Davies JM (2011) Release of extracellular purines from plant roots and effect on ion fluxes. Plant Signal Behav 6:1855–1857

    Article  PubMed  CAS  Google Scholar 

  • Day R, McAlvin C, Loh J, Denny R, Wood T, Young N, Stacey G (2000) Differential expression of two soybean apyrases, one of which is an early nodulin. Mol Plant Microbe Interact 13:1053–1070

    Article  PubMed  CAS  Google Scholar 

  • Demidchik V, Nichols C, Oliynyk M, Dark A, Glover BJ, Davies JM (2003) Is ATP a signaling agent in plants? Plant Physiol 133:456–461

    Article  PubMed  CAS  Google Scholar 

  • Demidchik V, Shang Z, Shin R, Thompson E, Rubio L, Laohavisit A, Mortimer JC, Chivasa S, Slabas AR, Glover BJ, Schachtman DP, Shabala SN, Davies JM (2009) Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. Plant J 58:903–913

    Article  PubMed  CAS  Google Scholar 

  • Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652

    Article  PubMed  CAS  Google Scholar 

  • Dunkley TP, Hester S, Shadforth IP, Runions J, Weimar T, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci USA 103:6518–6523

    Article  PubMed  CAS  Google Scholar 

  • Foresi NP, Laxalt AM, Tonon CV, Casalongue CA, Lamattina L (2007) Extracellular ATP induces nitric oxide production in tomato cell suspensions. Plant Physiol 145:589–592

    Article  PubMed  CAS  Google Scholar 

  • Fountain SJ, Cao L, Young MT, North RA (2008) Permeation properties of a P2X receptor in the green algae Ostreococcus tauri. J Biol Chem 283:15122–15126

    Article  PubMed  CAS  Google Scholar 

  • Gookin TE, Kim J, Assmann SM (2008) Whole proteome identification of plant candidate G-protein coupled receptors in Arabidopsis, rice, and poplar: computational prediction and in-vivo protein coupling. Genome Biol 9:R120

    Article  PubMed  Google Scholar 

  • Griffiths M, Beaumont N, Yao SY, Sundaram M, Boumah CE, Davies A, Kwong FY, Coe I, Cass CE, Young JD, Baldwin SA (1997) Cloning of a human nucleoside transporter implicated in the cellular uptake of adenosine and chemotherapeutic drugs. Nat Med 3:89–93

    Article  PubMed  CAS  Google Scholar 

  • Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179

    Article  PubMed  CAS  Google Scholar 

  • Hao LH, Wang WX, Chen C, Wang YF, Liu T, Li X, Shang ZL (2012) Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein alpha subunit and reactive oxygen species. Mol Plant 5:852–864

    Article  PubMed  CAS  Google Scholar 

  • Hatsugai N, Perez Koldenkova V, Imamura H, Noji H, Nagai T (2012) Changes in cytosolic ATP levels and intracellular morphology during bacteria-induced hypersensitive cell death as revealed by real-time fluorescence microscopy imaging. Plant Cell Physiol 53:1768–1775

    Article  PubMed  CAS  Google Scholar 

  • Hillwig MS, Contento AL, Meyer A, Ebany D, Bassham DC, MacIntosh GC (2011) RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. Proc Natl Acad Sci USA 108:1093–1098

    Article  PubMed  CAS  Google Scholar 

  • Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946

    Article  PubMed  CAS  Google Scholar 

  • Hirose N, Makita N, Yamaya T, Sakakibara H (2005) Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiol 138:196–206

    Article  PubMed  CAS  Google Scholar 

  • Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83

    Article  PubMed  CAS  Google Scholar 

  • Hsu CL, Lin W, Seshasayee D, Chen YH, Ding X, Lin Z, Suto E, Huang Z, Lee WP, Park H, Xu M, Sun M, Rangell L, Lutman JL, Ulufatu S, Stefanich E, Chalouni C, Sagolla M, Diehl L, Fielder P, Dean B, Balazs M, Martin F (2012) Equilibrative nucleoside transporter 3 deficiency perturbs lysosome function and macrophage homeostasis. Science 335:89–92

    Article  PubMed  CAS  Google Scholar 

  • Jaffe MJ (1973) The role of ATP in mechanically stimulated rapid closure of the Venus’s flytrap. Plant Physiol 51:17–18

    Article  PubMed  CAS  Google Scholar 

  • Jeter CR, Tang W, Henaff E, Butterfield T, Roux SJ (2004) Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. Plant Cell 16:2652–2664

    Article  PubMed  CAS  Google Scholar 

  • Jung B, Flörchinger M, Kunz HH, Traub M, Wartenberg R, Jeblick W, Neuhaus HE, Möhlmann T (2009) Uridine-ribohydrolase is a key regulator in the uridine degradation pathway of Arabidopsis. Plant Cell 21:876–891

    Article  PubMed  CAS  Google Scholar 

  • Jung B, Hoffmann C, Möhlmann T (2011) Arabidopsis nucleoside hydrolases involved in intracellular and extracellular degradation of purines. Plant J 65:703–711

    Article  PubMed  CAS  Google Scholar 

  • Kieber JJ (2002) Cytokinins. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Physiologists, Rockville, MD. Online publication. DOI/11.1199/tab.0018. http://aspb.org/publications/arabidopsis/

  • Kim SY, Sivaguru M, Stacey G (2006) Extracellular ATP in plants. Visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142:984–992

    Article  PubMed  CAS  Google Scholar 

  • Kim SH, Yang SH, Kim TJ, Han JS, Suh JW (2009) Hypertonic stress increased extracellular ATP levels and the expression of stress-responsive genes in Arabidopsis thaliana seedlings. Biosci Biotechnol Biochem 73:1252–1256

    Article  PubMed  CAS  Google Scholar 

  • King AE, Ackley MA, Cass CE, Young JD, Baldwin SA (2006) Nucleoside transporters: from scavengers to novel therapeutic targets. Trends Pharmacol Sci 27:416–425

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg M (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 1778:1978–2021

    Article  PubMed  CAS  Google Scholar 

  • Knowles AF (2011) The GDA1_CD39 superfamily: NTPDases with diverse functions. Purinergic Signal 7:21–45

    Article  PubMed  CAS  Google Scholar 

  • Krebs M, Held K, Binder A, Hashimoto K, Den Herder G, Parniske M, Kudla J, Schumacher K (2012) FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics. Plant J 69:181–192

    Article  PubMed  CAS  Google Scholar 

  • Kukulski F, Lévesque SA, Lavoie EG, Lecka J, Bigonnesse F, Knowles AF, Robson SC, Kirley TL, Sévigny J (2005) Comparative hydrolysis of P2 receptor agonists by NTPDases 1, 2, 3 and 8. Purinergic Signal 1:193–204

    Article  PubMed  CAS  Google Scholar 

  • Lai Y, Tse CM, Unadkat JD (2004) Mitochondrial expression of the human equilibrative nucleoside transporter 1 (hENT1) results in enhanced mitochondrial toxicity of antiviral drugs. J Biol Chem 279:4490–4497

    Article  PubMed  CAS  Google Scholar 

  • Leroch M, Neuhaus HE, Kirchberger S, Zimmermann S, Melzer M, Gerhold J, Tjaden J (2008) Identification of a novel adenine nucleotide transporter in the endoplasmic reticulum of Arabidopsis. Plant Cell 20:438–451

    Article  PubMed  CAS  Google Scholar 

  • Lew R, Dearnaley J (2000) Extracellular nucleotide effects on the electrical properties of growing Arabidopsis thaliana root hairs. Plant Sci 153:1–6

    Article  CAS  Google Scholar 

  • Li G, Liu K, Baldwin SA, Wang D (2003) Equilibrative nucleoside transporters of Arabidopsis thaliana: cDNA cloning, expression pattern and analysis of transport activities. J Biol Chem 278:35732–35742

    Article  PubMed  CAS  Google Scholar 

  • Li G, Wang D (2000) Cloning and in vitro expression of the cDNA encoding a putative nucleoside transporter from Arabidopsis thaliana. Plant Sci 157:23–32

    Article  PubMed  CAS  Google Scholar 

  • Liang C, Tian J, Lam HM, Lim BL, Yan X, Liao H (2010) Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152:854–865

    Article  PubMed  CAS  Google Scholar 

  • Lu SP, Lin SJ (2011) Phosphate-responsive signaling pathway is a novel component of NAD+ metabolism in Saccharomyces cerevisiae. J Biol Chem 286:14271–14281

    Article  PubMed  CAS  Google Scholar 

  • Lüttge U, Schoch E, Ball E (1974) Can externally applied ATP supply energy to active ion uptake mechanisms of intact plant cells? Aust J Plant Physiol 1:211–220

    Article  Google Scholar 

  • Mani RS, Hammond JR, Marjan JM, Graham KA, Young JD, Baldwin SA, Cass CE (1998) Demonstration of equilibrative nucleoside transporters (hENT1 and hENT2) in nuclear envelopes of cultured human choriocarcinoma (BeWo) cells by functional reconstitution in proteoliposomes. J Biol Chem 273:30818–30825

    Article  PubMed  CAS  Google Scholar 

  • Mansfield TA, Schultes NP, Mourad GS (2009) AtAzg1 and AtAzg2 comprise a novel family of purine transporters in Arabidopsis. FEBS Lett 583:481–486

    Article  PubMed  CAS  Google Scholar 

  • Marechal R, Mackey JR, Lai R, Demetter P, Peeters M, Polus M, Cass CE, Young J, Salmon I, Deviere J, Van Laethem JL (2009) Human equilibrative nucleoside transporter 1 and human concentrative nucleoside transporter 3 predict survival after adjuvant gemcitabine therapy in resected pancreatic adenocarcinoma. Clin Cancer Res 15:2913–2919

    Article  PubMed  CAS  Google Scholar 

  • Meyerhof O (1945) The origin of the reaction of Harden and Young in cell-free alcoholic fermentation. J Biol Chem 157:105–119

    CAS  Google Scholar 

  • Moffatt B, Pethe C, Laloue M (1991) Metabolism of benzyladenine is impaired in a mutant of Arabidopsis thaliana lacking adenine phosphoribosyltransferase activity. Plant Physiol 95:900–908

    Article  PubMed  CAS  Google Scholar 

  • Möhlmann T, Mezher Z, Schwerdtfeger G, Neuhaus HE (2001) Characterisation of a concentrative type of adenosine transporter from Arabidopsis thaliana (ENT1, At). FEBS Lett 509:370–374

    Article  PubMed  Google Scholar 

  • Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, Batth TS, Smith-Moritz AM, Morrison S, McInerney P, Hadi MZ, Auer M, Mukhopadhyay A, Petzold CJ, Scheller HV, Loque D, Heazlewood JL (2012) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol 159:12–26

    Article  PubMed  CAS  Google Scholar 

  • Phillips DA, Joseph CM, Hirsch PR (1997) Occurrence of flavonoids and nucleosides in agricultural soils. Appl Environ Microbiol 63:4573–4577

    PubMed  CAS  Google Scholar 

  • Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413–492

    PubMed  CAS  Google Scholar 

  • Reichler SA, Torres J, Rivera AL, Cintolesi VA, Clark G, Roux SJ (2009) Intersection of two signalling pathways: extracellular nucleotides regulate pollen germination and pollen tube growth via nitric oxide. J Exp Bot 60:2129–2138

    Article  PubMed  CAS  Google Scholar 

  • Rieder B, Neuhaus HE (2011) Identification of an Arabidopsis plasma membrane-located ATP transporter important for anther development. Plant Cell 23:1932–1944

    Article  PubMed  CAS  Google Scholar 

  • Riegler H, Geserick C, Zrenner R (2011) Arabidopsis thaliana nucleosidase mutants provide new insights into nucleoside degradation. New Phytol 191:349–359

    Article  PubMed  CAS  Google Scholar 

  • Riewe D, Grosman L, Fernie AR, Wucke C, Geigenberger P (2008) The potato-specific apyrase is apoplastically localized and has influence on gene expression, growth and development. Plant Physiol 147:1092–1109

    Article  PubMed  CAS  Google Scholar 

  • Roux SJ, Steinebrunner I (2007) Extracellular ATP: an unexpected role as signaler in plants. Trends Plant Sci 12:522–527

    Article  PubMed  CAS  Google Scholar 

  • Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, Yamamoto A, Moriyama Y (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105:5683–5686

    Article  PubMed  CAS  Google Scholar 

  • Schiller M, Massalski C, Kurth T, Steinebrunner I (2012) The Arabidopsis apyrase AtAPY1 is localized in the Golgi instead of the extracellular space. BMC Plant Biol 12:123

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Su YH, Kunze R, Warner S, Hewitt M, Slocum RD, Ludewig U, Frommer WB, Desimone M (2004) UPS1 and UPS2 from Arabidopsis mediate high affinity transport of uracil and 5-fluorouracil. J Biol Chem 279:44817–44824

    Article  PubMed  CAS  Google Scholar 

  • Song C, Steinebrunner I, Wang X, Stout SC, Roux SJ (2006) Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis thaliana. Plant Physiol 140:1222–1232

    Article  PubMed  CAS  Google Scholar 

  • Srobarova A, da Silva JA, Kogan G, Ritieni A, Santini A (2009) Beauvericin decreases cell viability of wheat. Chem Biodivers 6:1208–1215

    Article  PubMed  CAS  Google Scholar 

  • Steinebrunner I, Wu J, Sun Y, Corbett A, Roux SJ (2003) Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol 131:1638–1647

    Article  PubMed  CAS  Google Scholar 

  • Sueldo DJ, Foresi NP, Casalongue CA, Lamattina L, Laxalt AM (2010) Phosphatidic acid formation is required for extracellular ATP-mediated nitric oxide production in suspension-cultured tomato cells. New Phytol 185:909–916

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Hirose N, Wang X, Wen P, Xue L, Sakakibara H, Zuo J (2005) Arabidopsis SOI33/AtENT8 gene encodes a putative equilibrative nucleoside transporter that is involved in cytokinin transport in planta. J Integr Plant Biol 47:588–603

    Article  CAS  Google Scholar 

  • Sun J, Zhang CL, Deng SR, Lu CF, Shen X, Zhou XY, Zheng XJ, Hu ZM, Chen SL (2012) An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. Plant Cell Environ 35:893–916

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Toyoda K, Hirakawa Y, Morishita K, Kato T, Inagaki Y, Ichinose Y, Shiraishi T (2006) Localization and responsiveness of a cowpea apyrase VsNTPase1 to phytopathogenic microorganisms. J Gen Plant Pathol 72:143–151

    Article  CAS  Google Scholar 

  • Tanaka K, Gilroy S, Jones AM, Stacey G (2010a) Extracellular ATP signaling in plants. Trends Cell Biol 20:601–608

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Swanson SJ, Gilroy S, Stacey G (2010b) Extracellular nucleotides elicit cytosolic free calcium oscillations in Arabidopsis. Plant Physiol 154:705–719

    Article  PubMed  CAS  Google Scholar 

  • Tang W (2004) Effects of extracellular ATP and ADP on growth and development of Arabidopsis seedlings. PhD thesis, The University of Texas at Austin, Austin

    Google Scholar 

  • Tang W, Brady SR, Sun Y, Muday GK, Roux S (2003) Extracellular ATP inhibits root gravitropism at concentrations that inhibit polar auxin transport. Plant Physiol 131:147–154

    Article  PubMed  CAS  Google Scholar 

  • Thomas C, Sun Y, Naus K, Lloyd A, Roux S (1999) Apyrase functions in plant phosphate nutrition and mobilizes phosphate from extracellular ATP. Plant Physiol 119:543–551

    Article  PubMed  CAS  Google Scholar 

  • Thomas C, Rajagopal A, Windsor B, Dudler R, Lloyd A, Roux S (2000) A role for ecto-phosphatase in xenobiotic resistance. Plant Cell 12:519–533

    PubMed  CAS  Google Scholar 

  • Tonon C, Cecilia Terrile M, Jose Iglesias M, Lamattina L, Casalongue C (2010) Extracellular ATP, nitric oxide and superoxide act coordinately to regulate hypocotyl growth in etiolated Arabidopsis seedlings. J Plant Physiol 167:540–546

    Article  PubMed  CAS  Google Scholar 

  • Torres J, Rivera A, Clark G, Roux SJ (2008) Participation of extracellular nucleotides in the wound response of Dasycladus vermicularis and Acetabularia acetabulum (Dasycladales, Chlorophyta). J Phycol 44:1504–1511

    Article  CAS  Google Scholar 

  • Traub M, Flörchinger M, Piecuch J, Kunz HH, Weise-Steinmetz A, Deitmer JW, Ekkehard NH, Möhlmann T (2007) The fluorouridine insensitive 1 (fur1) mutant is defective in equilibrative nucleoside transporter 3 (ENT3), and thus represents an important pyrimidine nucleoside uptake system in Arabidopsis thaliana. Plant J 49:855–864

    Article  PubMed  CAS  Google Scholar 

  • Udvardy J, Farkas GL (1973) ATP stimulates the formation of nucleases in excised Avena leaves. Z Pflanzenphysiol 69:394–401

    Article  CAS  Google Scholar 

  • Vickers MF, Yao SYM, Baldwin SA, Young JD, Cass CE (2000) Nucleoside transporter proteins of Saccharomyces cerevisiae. J Biol Chem 275:25931–25939

    Article  PubMed  CAS  Google Scholar 

  • Visser F, Zhang J, Raborn RT, Baldwin SA, Young JD, Cass CE (2005) Residue 33 of human equilibrative nucleoside transporter 2 is a functionally important component of both the dipyridamole and nucleoside binding sites. Mol Pharmacol 67:1291–1298

    Article  PubMed  CAS  Google Scholar 

  • von Schwartzenberg K, Kruse S, Reski R, Moffatt B, Laloue M (1998) Cloning and characterization of an adenine kinase from Physcomitrella involved in cytokinin metabolism. Plant J 13:249–257

    Article  Google Scholar 

  • Weerasinghe RR, Swanson SJ, Okada SF, Garrett MB, Kim SY, Stacey G, Boucher RC, Gilroy S, Jones AM (2009) Touch induces ATP release in Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. FEBS Lett 583:2521–2526

    Article  PubMed  CAS  Google Scholar 

  • Wolf C, Hennig M, Romanovicz D, Steinebrunner I (2007) Developmental defects and seedling lethality in apyrase AtAPY1 and AtAPY2 double knockout mutants. Plant Mol Biol 64:657–672

    Article  PubMed  CAS  Google Scholar 

  • Wormit A, Traub M, Flörchinger M, Neuhaus HE, Möhlmann T (2004) Characterization of three novel members of the Arabidopsis thaliana equilibrative nucleoside transporter (ENT) family. Biochem J 383:19–26

    Article  PubMed  CAS  Google Scholar 

  • Wu K, King J (1994) Biochemical and genetic characterization of 5-fluoro-2′deoxyuridine-resistant mutants of Arabidopsis thaliana. Planta 194:117–122

    Article  CAS  Google Scholar 

  • Wu SJ, Wu JY (2008) Extracellular ATP-induced NO production and its dependence on membrane Ca2+ flux in Salvia miltiorrhiza hairy roots. J Exp Bot 59:4007–4016

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Steinebrunner I, Sun Y, Butterfield T, Torres J, Arnold D, Gonzalez A, Jacob F, Reichler S, Roux SJ (2007) Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiol 144:961–975

    Article  PubMed  CAS  Google Scholar 

  • Wu SJ, Liu YS, Wu JY (2008) The signaling role of extracellular ATP and its dependence on Ca2+ flux in elicitation of Salvia miltiorrhiza hairy root cultures. Plant Cell Physiol 49:617–624

    Article  PubMed  CAS  Google Scholar 

  • Wu S, Peiffer M, Luthe DS, Felton GW (2012) ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLoS One 7:e41947

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Visser F, King KM, Baldwin SA, Young JD, Cass CE (2007) The role of nucleoside transporters in cancer chemotherapy with nucleoside drugs. Cancer Metastasis Rev 26:85–110

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Phillips GJ, Li Q, Yeung ES (2008) Imaging localized astrocyte ATP release with firefly luciferase beads attached to the cell surface. Anal Chem 80:9316–9325

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann H, Beaudoin AR, Bollen M, Goding JW, Guidotti G, Kirley TL, Robson SC, Sano K (2000) Proposed nomenclature for two novel nucleotide hydrolyzing enzyme families expressed on the cell surface. In: Vanduffel L, Lemmens R (eds) Ecto-ATPases and related ectonucleotidases. Shaker Publishing BV, Maastricht, pp 1–8

    Google Scholar 

  • Zimmermann H, Zebisch M, Sträter N (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8:437–502

    Article  PubMed  CAS  Google Scholar 

  • Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol 57:805–836

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

Scientific network meetings in 2010–2012 funded by a grant (STE 1455/4-1 to T.M. and I.S.) from the German Research Foundation (DFG) contributed to the content of this article. Work in E.N.’s laboratory is funded by the Deutsche Forschungsgemeinschaft (Reinhard-Kosselleck-Grant).

Author information

Authors and Affiliations

  1. Pflanzenphysiologie, Fachbereich Biologie, Universität Kaiserslautern, Erwin-Schrödinger-Straße, 3049, 67663, Kaiserslautern, Germany

    Torsten Möhlmann & Ekkehard Neuhaus

  2. Department of Biology, Technische Universität Dresden, Helmholtzstr. 10, Dresden, 01069, Germany

    Iris Steinebrunner

Authors
  1. Torsten Möhlmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iris Steinebrunner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ekkehard Neuhaus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Torsten Möhlmann .

Editor information

Editors and Affiliations

  1. Darmstadt, Germany

    Ulrich Lüttge

  2. Universität Bielefeld FB Geobotanik, Bielefeld, Germany

    Wolfram Beyschlag

  3. MS330/Department of Biochemistry, University of Nevada, Reno, Nevada, USA

    John Cushman

Gene and Protein Identifiers

Gene and Protein Identifiers

AtAPY1 (At3g04080), AtAPY2 (At5g18280), AtPGP1 (At2g36910), AtGPA1 (At2g26300), AtrbohD (AF055357), GDA1 (856669), GhAPY1 (GU385147), GhAPY2 (GU385148), human E-NTPDase 1 (NC_000010.10), human E-NTPDase 2, human E-NTPDase 3, human E-NTPDase 8, LOX2 (L23968), OtP2X (Ot07g02160), PAL1 (NM129260), PM-ANT1 (At5g56450), PvPAP3 (D2D4J4 UniProtKB), StAPY3 (EU125183), VsNTPase1 (Q5NT85 UniProtKB), hENT1 (AAC51103), hENT2 (AAC39526), hENT3 (AF326987), AtENT1 (At1g70330), AtENT3 (At4g05120), AtENT6 (At4g05110), OsENT2 (Os07g37100), FUN26 (AAC04935).

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Möhlmann, T., Steinebrunner, I., Neuhaus, E. (2014). Nucleotides and Nucleosides: Transport, Metabolism, and Signaling Function of Extracellular ATP. In: Lüttge, U., Beyschlag, W., Cushman, J. (eds) Progress in Botany. Progress in Botany, vol 75. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-38797-5_4

Download citation

Publish with us

Policies and ethics

Search

Navigation