Skip to main content
SpringerLink
Log in

Molecular Mechanism of Plant Recognition of Extracellular ATP

  • Chapter
  • First Online:
Protein Reviews

Part of the book series: Advances in Experimental Medicine and Biology ((PROTRE,volume 1051))

Abstract

Adenosine 5′-triphosphate (ATP), a ubiquitously dispersed biomolecule, is not only a major source of biochemical energy for living cells, but also acts as a critical signaling molecule through inter-cellular communication. Recent studies have clearly shown that extracellular ATP is involved in various physiological processes in plants, including root growth, stomata movement, pollen tube development, gravitropism, and abiotic/biotic stress responses. The first plant purinergic receptor for extracellular ATP, DORN1 (the founding member of the P2K family of purinergic receptors), was identified in Arabidopsis thaliana by a forward genetic screen. DORN1 consists of an extracellular lectin domain, transmembrane domain, and serine/threonine kinase, intracellular domain. The predicted structure of the DORN1 extracellular domain revealed putative key ATP binding residues but an apparent lack of sugar binding. In this chapter, we summarize recent studies on the molecular mechanism of plant recognition of extracellular ATP with specific reference to the role of DORN1.

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

Access this chapter

Log in via an institution

Institutional subscriptions

Abbreviations

ACS6:

1-aminocyclopropane-1-carboxylic acid synthase 6

ADP:

Adenosine 5′-diphosphate

ADPβS:

Adenosine 5′-[β-thio]diphosphate

AMP:

Adenosine 5′-monophosphate

AMP-PCP:

Adenosine 5′-[beta,gamma]-methylenetriphosphate

ATP:

Adenosine 5′-triphosphate

ATPγS:

Adenosine 5′-[γ-thio]triphosphate

BEA:

Beauvericin

Bz-ATP:

Benzoylbenzoyl- adenosine 5′-triphosphate

2me-ATP:

2-Methylthio-adenosine 5′-triphosphate

CBD:

cellulose binding domain

CTP:

Cytidine 5′-triphosphate

CW-PM:

Cell wall-plasma membrane

DAMP:

Damage-associated molecular pattern

DORN1:

Does not respond to nucleotide 1

ECM:

Extracellular matrix

EGTA:

Ethylene-bis(oxyethylenenitrilo)tetraacetic acid

EMS:

Ethyl methanesulfonate

ERFs:

Ethylene response factors

GTP:

Guanosine 5′-triphosphate

IPI-O:

In planta induced-O

ITP:

Inosine 5′-triphosphate

LecRK:

Lectin receptor kinase

LOX2:

Lipoxygenase 2

MAPK:

mitogen-activated protein kinase

MEKK1:

Mitogen-activated protein kinase kinase kinase 1

NADPH:

nicotinamide adenine dinucleotide phosphate

NO:

Nitrogen oxide

P2K:

kinase family of purinergic receptors

PA:

phosphatidic acid

PAL1:

Phe-ammonia lyase 1

PK19:

serine/threonine protein kinase 19

PPADS:

pyridoxalphosphate-6-azophenyl-2′,4′-disulfonic acid

RBOHC:

Respiratory burst oxidase homolog protein C

RBOHD:

Respiratory burst oxidase homolog protein D

RBOHF:

Respiratory burst oxidase homolog protein F

RD:

Arginine-aspartate

RGD:

Arginine-gylcine-aspartic acid

RGE:

Arginine-gylcine-glutamic acid

RLKs:

Receptor-like kinases

ROS:

Reactive oxygen species

TTP:

Thymidine 5′-triphosphat

UDP:

Uridine 5′-diphosphate

References

  • Abbracchio MP, Ceruti S (2006) Roles of P2 receptors in glial cells: focus on astrocytes. Purinergic Signal 2(4):595–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barre A, Hervé C, Lescure B, Rougé P (2002) Lectin Receptor Kinases in Plants. Crit Rev Plant Sci 21(4):379–399

    Article  CAS  Google Scholar 

  • Bernard C, Traub M, Kunz HH, Hach S, Trentmann O, Mohlmann T (2011) Equilibrative nucleoside transporter 1 (ENT1) is critical for pollen germination and vegetative growth in Arabidopsis. J Exp Bot 62(13):4627–4637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bodin P, Burnstock G (2001a) Purinergic signalling: ATP release. Neurochem Res 26(8–9):959–969

    Article  CAS  PubMed  Google Scholar 

  • Bodin P, Burnstock G (2001b) Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J Cardiovasc Pharmacol 38(6):900–908

    Article  CAS  PubMed  Google Scholar 

  • Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC (2006) Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 112(2):358–404

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester K, Govers F (2009) Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J Exp Bot 60(15):4383–4396

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, Canut H, Govers F (2011) The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog 7(3):e1001327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouwmeester K, Han M, Blanco-Portales R, Song W, Weide R, Guo LY, van der Vossen EA, Govers F (2014) The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnol J 12(1):10–16

    Article  CAS  PubMed  Google Scholar 

  • Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24(3):509–581

    CAS  PubMed  Google Scholar 

  • Burnstock G (2001) Purine-mediated signalling in pain and visceral perception. Trends Pharmacol Sci 22(4):182–188

    Article  CAS  PubMed  Google Scholar 

  • Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64(12):1471–1483

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Tanaka K, Nguyen CT, 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 

  • Chen KM, GL W, Wang YH, Tian CT, Samaj J, Baluska F, Lin JX (2008) The block of intracellular calcium release affects the pollen tube development of Picea wilsonii by changing the deposition of cell wall components. Protoplasma 233(1–2):39–49

    Article  CAS  PubMed  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(11):3019–3034

    Article  CAS  PubMed  PubMed Central  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(3):436–448

    Article  CAS  PubMed  Google Scholar 

  • Chivasa S, Simon WJ, Murphy AM, Lindsey K, Carr JP, Slabas AR (2010) The effects of extracellular adenosine 5′-triphosphate on the tobacco proteome. Proteomics 10(2):235–244

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Tanaka K, Liang Y, Cao Y, Lee SY, Stacey G (2014a) Extracellular ATP, a danger signal, is recognized by DORN1 in Arabidopsis. Biochem J 463(3):429–437

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014b) Identification of a plant receptor for extracellular ATP. Science 343(6168):290–294

    Article  CAS  PubMed  Google Scholar 

  • Clark G, Roux SJ (2011) Apyrases, extracellular ATP and the regulation of growth. Curr Opin Plant Biol 14(6):700–706

    Article  CAS  PubMed  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(2):1073–1083

    Article  CAS  PubMed  PubMed Central  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(4–5):423–435

    Article  CAS  PubMed  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(4):1740–1753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dardick C, Ronald P (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog 2(1):e2

    Article  PubMed  PubMed Central  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(11):1855–1857

    Article  CAS  PubMed  PubMed Central  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(2):456–461

    Article  CAS  PubMed  PubMed Central  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(6):903–913

    Article  CAS  PubMed  Google Scholar 

  • Deng K, Wang Q, Zeng J, Guo X, Zhao X, Tang D, Liu X (2009) A Lectin receptor kinase positively regulates ABA response during seed germination and is involved in salt and osmotic stress response. J Plant Biol 52(6):493

    Article  CAS  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(1):530–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erb L, Liu J, Ockerhausen J, Kong Q, Garrad RC, Griffin K, Neal C, Krugh B, Santiago-Perez LI, Gonzalez FA, Gresham HD, Turner JT, Weisman GA (2001) An RGD sequence in the P2Y(2) receptor interacts with alpha(V)beta(3) integrins and is required for G(o)-mediated signal transduction. J Cell Biol 153(3):491–501

    Article  CAS  PubMed  PubMed Central  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(3):589–592

    Article  CAS  PubMed  PubMed Central  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(22):15122–15126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouget A, Senchou V, Govers F, Sanson A, Barre A, Rouge P, Pont-Lezica R, Canut H (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140(1):81–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Govindarajulu M, Kim SY, Libault M, Berg RH, Tanaka K, Stacey G, Taylor CG (2009) GS52 ecto-apyrase plays a critical role during soybean nodulation. Plant Physiol 149(2):994–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanley PJ, Musset B, Renigunta V, Limberg SH, Dalpke AH, Sus R, Heeg KM, Preisig-Muller R, Daut J (2004) Extracellular ATP induces oscillations of intracellular Ca2+ and membrane potential and promotes transcription of IL-6 in macrophages. Proc Natl Acad Sci U S A 101(25):9479–9484

    Article  CAS  PubMed  PubMed Central  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(4):852–864

    Article  CAS  PubMed  Google Scholar 

  • Hardham AR, Takemoto D, White RG (2008) Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8:63

    Article  PubMed  PubMed Central  Google Scholar 

  • Herve C, Serres J, Dabos P, Canut H, Barre A, Rouge P, Lescure B (1999) Characterization of the Arabidopsis lecRK-a genes: members of a superfamily encoding putative receptors with an extracellular domain homologous to legume lectins. Plant Mol Biol 39(4):671–682

    Article  CAS  PubMed  Google Scholar 

  • Jaffe MJ (1973) The role of ATP in mechanically stimulated rapid closure of the venus’s flytrap. Plant Physiol 51(1):17–18

    Article  CAS  PubMed  PubMed Central  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(10):2652–2664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson LN, Noble ME, Owen DJ (1996) Active and inactive protein kinases: structural basis for regulation. Cell 85(2):149–158

    Article  CAS  PubMed  Google Scholar 

  • Kamizyo A, Tanaka N (1982) Studies on the generative nuclear division III. Effect of exogenous ATP on the generative nuclear division in Lilium longiflorum. Cytologia 47:195–205

    Article  CAS  Google Scholar 

  • Khakh BS, Burnstock G (2009) The double life of ATP. Sci Am 301(6):84–90, 92

    Article  CAS  PubMed  PubMed Central  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(3):984–992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knight H, Knight MR (1995) Recombinant aequorin methods for intracellular calcium measurement in plants. Methods Cell Biol 49:201–216

    Article  CAS  PubMed  Google Scholar 

  • Knowles JR (1980) Enzyme-catalyzed phosphoryl transfer reactions. Annu Rev Biochem 49:877–919

    Article  CAS  PubMed  Google Scholar 

  • Lazarowski ER, Boucher RC, Harden TK (2003) Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol 64(4):785–795

    Article  CAS  PubMed  Google Scholar 

  • Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150(1):12–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li Z, Chakraborty S, Xu G (2016) X-ray crystallographic studies of the extracellular domain of the first plant ATP receptor, DORN1, and the orthologous protein from Camelina sativa. Acta Crystallogr F Struct Biol Commun 72(Pt 10):782–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim MH, Wu J, Yao J, Gallardo IF, Dugger JW, Webb LJ, Huang J, Salmi ML, Song J, Clark G, Roux SJ (2014) Apyrase suppression raises extracellular ATP levels and induces gene expression and cell wall changes characteristic of stress responses. Plant Physiol 164(4):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 GK, Gardner G, Roux SJ (2012) Role for apyrases in polar auxin transport in Arabidopsis. Plant Physiol 160(4):1985–1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lustig KD, Shiau AK, Brake AJ, Julius D (1993) Expression cloning of an ATP receptor from mouse neuroblastoma cells. Proc Natl Acad Sci U S A 90(11):5113–5117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McPhail LC, Waite KA, Regier DS, Nixon JB, Qualliotine-Mann D, Zhang WX, Wallin R, Sergeant S (1999) A novel protein kinase target for the lipid second messenger phosphatidic acid. Biochim Biophys Acta 1439(2):277–290

    Article  CAS  PubMed  Google Scholar 

  • Navarro-Gochicoa MT, Camut S, Timmers AC, Niebel A, Herve C, Boutet E, Bono JJ, Imberty A, Cullimore JV (2003) Characterization of four lectin-like receptor kinases expressed in roots of Medicago truncatula. Structure, location, regulation of expression, and potential role in the symbiosis with Sinorhizobium meliloti. Plant Physiol 133(4):1893–1910

    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(3):367–370

    Article  CAS  Google Scholar 

  • Nguyen CT, Tanaka K, Cao Y, Cho SH, Xu D, Stacey G (2016) Computational analysis of the ligand binding Site of the extracellular ATP Receptor, DORN1. PLoS One 11(9):e0161894

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishiguchi M, Yoshida K, Sumizono T, Tazaki K (2002) A receptor-like protein kinase with a lectin-like domain from lombardy poplar: gene expression in response to wounding and characterization of phosphorylation activity. Mol Gen Genomics 267(4):506–514

    Article  CAS  Google Scholar 

  • Park J, Gu Y, Lee Y, Yang Z, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134(1):129–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson TS, Camden JM, Wang Y, Seye CI, Wood WG, Sun GY, Erb L, Petris MJ, Weisman GA (2010) P2Y2 nucleotide receptor-mediated responses in brain cells. Mol Neurobiol 41(2–3):356–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puchalowicz K, Tarnowski M, Baranowska-Bosiacka I, Chlubek D, Dziedziejko V (2014) P2X and P2Y receptors-role in the pathophysiology of the nervous system. Int J Mol Sci 15(12):23672–23704

    Article  PubMed  PubMed Central  Google Scholar 

  • Raghavendra AS (1981) Energy supply for stomatal opening in epidermal strips of Commelina benghalensis. Plant Physiol 67(2):385–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50(3):413–492

    CAS  PubMed  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(7):2129–2138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riewe D, Grosman L, Fernie AR, Zauber H, Wucke C, Geigenberger P (2008) A cell wall-bound adenosine nucleosidase is involved in the salvage of extracellular ATP in Solanum tuberosum. Plant Cell Physiol 49(10):1572–1579

    Article  CAS  PubMed  Google Scholar 

  • Riou C, Hervé C, Pacquit V, Dabos P, Lescure B (2002) Expression of an Arabidopsis lectin kinase receptor gene, lecRK-a1, is induced during senescence, wounding and in response to oligogalacturonic acids. Plant Physiol Biochem 40(5):431–438

    Article  CAS  Google Scholar 

  • Roberts NJ, Morieri G, Kalsi G, Rose A, Stiller J, Edwards A, Xie F, Gresshoff PM, Oldroyd GE, Downie JA, Etzler ME (2013) Rhizobial and mycorrhizal symbioses in Lotus japonicus require lectin nucleotide phosphohydrolase, which acts upstream of calcium signaling. Plant Physiol 161(1):556–567

    Article  CAS  PubMed  Google Scholar 

  • Rose PW, Bi C, Bluhm WF, Christie CH, Dimitropoulos D, Dutta S, Green RK, Goodsell DS, Prlic A, Quesada M, Quinn GB, Ramos AG, Westbrook JD, Young J, Zardecki C, Berman HM, Bourne PE (2013) The RCSB Protein Data Bank: new resources for research and education. Nucleic Acids Res 41(D1):D475–D482

    Article  CAS  PubMed  Google Scholar 

  • Roux SJ, Steinebrunner I (2007) Extracellular ATP: an unexpected role as a signaler in plants. Trends Plant Sci 12(11):522–527

    Article  CAS  PubMed  Google Scholar 

  • Roux SJ, Song C, Jeter C (2006) Regulation of plant growth and development by extracellular nucleotides. In: Communication in plants. Springer, Berlin/Heidelberg, pp 221–234

    Chapter  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 U S A 105(15):5683–5686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senchou V, Weide R, Carrasco A, Bouyssou H, Pont-Lezica R, Govers F, Canut H (2004) High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif. Cell Mol Life Sci 61(4):502–509

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Harada N, Nakazawa H, Yamashita T (2005) Involvement of the nitric oxide-cyclic GMP pathway and neuronal nitric oxide synthase in ATP-induced Ca2+ signalling in cochlear inner hair cells. Eur J Neurosci 21(11):2912–2922

    Article  PubMed  Google Scholar 

  • Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001(113):re22

    CAS  PubMed  Google Scholar 

  • Song CJ, Steinebrunner I, Wang X, Stout SC, Roux SJ (2006) Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiol 140(4):1222–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srobarova A, da Silva JA, Kogan G, Ritieni A, Santini A (2009) Beauvericin decreases cell viability of wheat. Chem Biodivers 6(8):1208–1215

    Article  CAS  PubMed  Google Scholar 

  • Steinebrunner I, Wu J, Sun Y, Corbett A, Roux SJ (2003) Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol 131(4):1638–1647

    Article  CAS  PubMed  PubMed Central  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(4):909–916

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Zhang CL, Deng SR, CF L, Shen X, Zhou XY, Zheng XJ, ZM H, Chen SL (2012a) An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. Plant Cell Environ 35(5):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 H(2)O(2) and cytosolic Ca(2)(+) in the salt response of Populus euphratica cells. PLoS One 7(12):e53136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Gilroy S, Jones AM, Stacey G (2010a) Extracellular ATP signaling in plants. Trends Cell Biol 20(10):601–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Swanson SJ, Gilroy S, Stacey G (2010b) Extracellular nucleotides elicit cytosolic free calcium oscillations in Arabidopsis. Plant Physiol 154(2):705–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka K, Nguyen CT, Libault M, Cheng J, Stacey G (2011) Enzymatic activity of the soybean ecto-apyrase GS52 is essential for stimulation of nodulation. Plant Physiol 155(4):1988–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang W, Brady SR, Sun Y, Muday GK, Roux SJ (2003) Extracellular ATP inhibits root gravitropism at concentrations that inhibit polar auxin transport. Plant Physiol 131(1):147–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrile MC, Tonon CV, Iglesias MJ, Lamattina L, Casalongue CA (2010) Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings. Plant Signal Behav 5(6):698–701

    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(2):543–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas C, Rajagopal A, Windsor B, Dudler R, Lloyd A, Roux SJ (2000) A role for ectophosphatase in xenobiotic resistance. Plant Cell 12(4):519–533

    Article  CAS  PubMed  PubMed Central  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(7):540–546

    Article  CAS  PubMed  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)(1). J Phycol 44(6):1504–1511

    Article  CAS  PubMed  Google Scholar 

  • Udvardy J, Farkas GL (1973) ATP stimulates the formation of nucleases in excised Avena leaves. Z Pflanzenphysiol 69(5):394–401

    Article  CAS  Google Scholar 

  • Vaid N, Macovei A, Tuteja N (2013) Knights in action: lectin receptor-like kinases in plant development and stress responses. Mol Plant 6(5):1405–1418

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Jia J, Wang Y, Wang W, Chen Y, Liu T, Shang Z (2014) Hyperpolization-activated Ca(2+) channels in guard cell plasma membrane are involved in extracellular ATP-promoted stomatal opening in Vicia faba. J Plant Physiol 171(14):1241–1247

    Article  CAS  PubMed  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(15):2521–2526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson RE (1975) Cytoplasmic streaming in Chara: a cell model activated by ATP and inhibited by cytochalasin B. J Cell Sci 17(3):655–668

    CAS  PubMed  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(14):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 SJ (2007) Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiol 144(2):961–975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu SJ, Liu YS, JY W (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(4):617–624

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Wang B, Farris B, Clark G, Roux SJ (2015) Modulation of root skewing in arabidopsis by apyrases and extracellular ATP. Plant Cell Physiol 56(11):2197–2206

    CAS  PubMed  Google Scholar 

  • Zhou J, Fan C, Liu K, Jing Y (2015) Extracellular ATP is involved in the initiation of pollen germination and tube growth in Picea meyeri. Trees 29(2):563–574

    Article  CAS  Google Scholar 

Download references

Acknowledgement

We thank Dr. Katalin Tóth and Dr. Daewon Kim (University of Missouri, USA) for valuable comments on the manuscript. This work was supported by the Next-Generation BioGreen 21 Program, Systems and Synthetic Agrobiotech Center, Rural Development Administration, Republic of Korea (grant no. PJ01116604). This work was also supported by The National Institute of General Medical Science of the National Institutes of Health (grant no. RO1GM 121445 to GS). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Authors and Affiliations

  1. Divisions of Plant Science and Biochemistry, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA

    Sung-Hwan Cho, Cuong The Nguyen, Jeongmin Choi & Gary Stacey

  2. Department of Plant Sciences, University of Cambridge, Downing street, Cambridge, CB2 3EA, UK

    Jeongmin Choi

Authors
  1. Sung-Hwan Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cuong The Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeongmin Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gary Stacey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gary Stacey .

Editor information

Editors and Affiliations

  1. Biochem and Mol Biol, Baylor College of Medicine, Houston, Texas, USA

    M. Zouhair Atassi

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Cho, SH., Nguyen, C.T., Choi, J., Stacey, G. (2017). Molecular Mechanism of Plant Recognition of Extracellular ATP. In: Atassi, M. (eds) Protein Reviews. Advances in Experimental Medicine and Biology(), vol 1051. Springer, Singapore. https://doi.org/10.1007/5584_2017_110

Download citation

Publish with us

Policies and ethics

Search

Navigation