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Extracellular ATP: An Essential Apoplastic Messenger in Plants

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Progress in Botany Vol. 78

Part of the book series: Progress in Botany ((BOTANY,volume 78))

Abstract

Adenosine triphosphate (ATP) plays major roles in cell metabolism as an energy supplier and as a substrate for enzymatic reactions. While ATP is well known for its role as an intracellular energy carrier, recent studies have found that ATP exists not only in the cytoplasm, but also in the extracellular matrix. Cytoplasmic ATP can be secreted into the apoplast through wound leakage, secretory vesicles, or transporters in the plasma membrane. As a signaling molecule, extracellular ATP (eATP) regulates plant metabolism, growth and development, and responses to biotic and abiotic stimuli. eATP binds to receptors in the plasma membrane, where it triggers the generation of second messengers, including Ca2+, NO, and reactive oxygen species. These second messengers induce expression of a series of functional genes that promote changes in the cellular structure and physiological function of plant cells. Here, we discuss the progress in research on the function and signaling properties of this novel apoplastic messenger.

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References

  • Bodin P, Burnstock G (2001) Purinergic signalling: ATP release. Neurochem Res 26:959–969

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester K, Han M, Blanco-Portales R, Song W, Weide R, Guo L, van der Vossen E, Govers F (2013) The Arabidopsis lectin receptor kinase LecRK-1.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnol J 12:10–16

    Article  PubMed  Google Scholar 

  • Burnstock G (2006) Historical review: ATP as a neurotransmitter. Trends Pharmacol Sci 27:166–176

    Article  CAS  PubMed  Google Scholar 

  • Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483

    Article  CAS  PubMed  Google Scholar 

  • Burnstock G, Arnett T, Orriss I (2013) Purinergic signalling in the musculoskeletal system. Purinergic Signal 9:541–572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Tanaka K, Nguyen C, Stacey G (2014) Extracellular ATP is a central signaling molecule in plant stress responses. Curr Opin Plant Biol 20:82–87

    Article  CAS  PubMed  Google Scholar 

  • Cavaliere F, Donno C, Ambrosi N (2015) Purinergic signaling: a common pathway for neural and mesenchymal stem cell maintenance and differentiation. Front Cell Neurosci 9:211

    Article  PubMed  PubMed Central  Google Scholar 

  • Chivasa S, Slabas AR (2012) Plant extracellular ATP signalling: new insight from proteomics. Mol Biosyst 8:445–452

    Article  CAS  PubMed  Google Scholar 

  • Chivasa S, Ndimba B, Simon W, Robertson D, Yu X, Knox J, Bolwell P, Slabas A (2002) Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis 23:1754–1765

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chivasa S, Simon WJ, Murphy AM, Lindsey K, Carr J, Slabas A (2010) The effects of extracellular adenosine 5′-triphosphate on the tobacco proteome. Proteomics 10:235–244

    Article  CAS  PubMed  Google Scholar 

  • Chivasa S, Tome D, Hamilton J, Slabas A (2011) Proteomic analysis of extracellular ATP-regulated proteins identifies ATP synthase beta-subunit as a novel plant cell death regulator. Mol Cell Proteomics 10:M110.003905

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee S, Stacey G (2014a) Identification of a plant receptor for extracellular ATP. Science 343:290–294

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Tanaka K, Liang Y, Cao Y, Lee S, Stacey G (2014b) Extracellular ATP, a danger signal, is recognized by DORN1 in Arabidopsis. Biochem J 463:429–437

    Article  CAS  PubMed  Google Scholar 

  • Clark G, Roux SJ (2009) Extracellular nucleotides: ancient signaling molecules. Plant Sci 177:239–244

    Article  CAS  Google Scholar 

  • Clark G, Roux S (2011) Apyrases, extracellular ATP and the regulation of growth. Curr Opin Plant Biol 14:700–706

    Article  CAS  PubMed  Google Scholar 

  • Clark G, Torres J, Finlayson S, Guan X, Handley LJ, Kays J, Chen Z, Roux S (2010) Apyrase (NTPDase) and extracellular nucleotides regulate cotton fiber elongation in cultured ovules. Plant Physiol 152:1073–1083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crouzet J, Trombik T, Fraysse AS, Boutry M (2006) Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett 580:1123–1130

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Deng S, Sun J, Zhao R, Ding M, Zhang Y, Sun Y, Wang W, Tan Y, Liu D, Ma X, Hou P, Wang M, Lu C, Shen X, Chen S (2015) Populus euphratica APYRASE2 enhances cold tolerance by modulating vesicular trafficking and extracellular ATP in Arabidopsis plants. Plant Physiol 169:530–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drury AN, Szent-Györgyi A (1929) The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J Physiol 68:213–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etzler M, Kalsi G, Ewing N, Roberts N, Day R, Murphy J (1999) A nod factor binding lectin with apyrase activity from legume roots. Proc Natl Acad Sci U S A 96:5856–5861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari D, Vitiello L, Idzko M, la Sala A (2015) Purinergic signaling in atherosclerosis. Trends Mol Med 21:184–192

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fountain S, Cao L, Yound M, North R (2008) Permeation properties of a P2X receptor in the green algae Ostreococcus tauri. J Biol Chem 283:15122–15126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao L, Wang W, Chen C, Wang Y, Liu T, Li X, Shang Z (2012) Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein α subunit and reactive oxygen species. Mol Plant 5:852–864

    Article  CAS  PubMed  Google Scholar 

  • Idzko M, Ferrari D, Riegel A, Eltzschig H (2014) Extracellular nucleotide and nucleoside signaling in vascular and blood disease. Blood 124:1029–1037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennedy C (2015) ATP as a cotransmitter in the autonomic nervous system. Auton Neurosci 191:2–15

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Yang S, Kim T, Han J, Suh J (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  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lim M, Wu J, Yao J, Gallardo I, Dugger J, Webb L, Huang J, Salmi M, Song J, Clark G, Roux S (2014) Apyrase suppression raises extracellular ATP levels and induces gene expression and cell wall changes characteristic of stress responses. Plant Physiol 164:2054–2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Wu J, Clark G, Lundy S, Lim M, Arnold D, Chan J, Tang W, Muday G, Gardner G, Roux S (2012) Role for apyrases in polar auxin transport in Arabidopsis. Plant Physiol 160:1985–1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lüttge U, Schöch EV, 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 

  • McAlvin C, Stacey G (2005) Transgenic expression of the soybean apyrase in Lotus japonicus enhances nodulation. Plant Physiol 137:1456–1462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nejidat A, Itai C, Roth-Bejerano N (1983) Stomatal response to ATP mediated by phytochrome. Physiol Plant 57:367–370

    Article  CAS  Google Scholar 

  • Raghavendra A (1981) Energy supply for stomatal opening in epidermal strips of Commelina benghalensis. Plant Physiol 67:385–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:415–492

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riewe D, Grosman L, Fernie A, 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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Zhang C, Deng S, Lu C, Shen X, Zhou X, Zheng X, Hu Z, Chen S (2012a) An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphraticapce. Plant Cell Environ 35:893–916

    Article  PubMed  Google Scholar 

  • Sun J, Zhang X, Deng S, Zhang C, Wang M, Ding M, Zhao R, Shen X, Zhou X, Lu C, Chen S (2012b) Extracellular ATP signaling is mediated by H2O2 and cytosolic Ca2+ in the salt response of Populus euphratica cells. PLoS One 12, e53136

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Choi J, Cao Y, Gary S (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front Plant Sci 5, Article 446

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tonón C, Terrile MC, Iglesias MJ, Lamattina L, Casalongué 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  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 

  • Vanegas D, Clark G, Cannon A, Roux S, Chaturvedi P, McLamore E (2015) A self-referencing biosensor for real-time monitoring of physiological ATP transport in plant systems. Biosens Bioelectron 74:37–44

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Jia J, Wang Y, Wang W, Chen Y, Liu T, Shang Z (2014) Hyperpolization-activated Ca2+ channels in guard cell plasma membrane are involved in extracellular ATP-promoted stomatal opening in Vicia faba. J Plant Physiol 171:1241–1247

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Windsor B, Roux SJ, Lloyd A (2003) Multiherbicide tolerance conferred by AtPgp1 and apyrase in Arabidopsis: a novel mechanism of herbicide resistance. Nat Biotechnol 21:428–433

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Wu S, Wu J (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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S, Liu Y, Wu J (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  CAS  PubMed  Google Scholar 

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Acknowledgement

We thank National Natural Science Foundation of China (Grant No. 31370319) and the Natural Science Foundation of Hebei Province (Grant No. C2014205079) for supporting this work.

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Correspondence to Zhonglin Shang .

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Liu, T., Shang, Z. (2016). Extracellular ATP: An Essential Apoplastic Messenger in Plants. In: Cánovas, F., Lüttge, U., Matyssek, R. (eds) Progress in Botany Vol. 78. Progress in Botany, vol 78. Springer, Cham. https://doi.org/10.1007/124_2016_9

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