, Volume 53, Issue 2, pp 201–206 | Cite as

Extracellular ATP affects chlorophyll fluorescence of kidney bean (Phaseolus vulgaris) leaves through Ca2+ and H2O2-dependent mechanism

  • H. -Q. Feng
  • Q. -S. Jiao
  • K. Sun
  • L. -Y. Jia
  • W. -Y. Tian
Original Papers


Extracellular ATP (eATP) has been considered as an important extracellular compound to mediate several physiological processes in plant cells. We investigated the effects of eATP on chlorophyll (Chl) fluorescence characteristics of kidney bean (Phaseolus vulgaris) leaves. Treatment with exogenous ATP at 1 mM showed no significant effect on the maximal photochemical efficiency of PSII. However, the treatment significantly enhanced the values of the PSII operating efficiency (ΦPSII), rate of photosynthetic electron transport through PSII (ETR), and photochemical quenching (qP), while the values of the nonphotochemical quenching (qN) and quantum yield of regulated energy dissipation of PSII (YNPQ) significantly decreased. Our observations indicated that eATP stimulated the PSII photochemistry in kidney bean leaves. Similarly, the treatment with exogenous Ca2+ or H2O2 at 1 mM caused also the significant increase in ΦPSII, qP, and ETR and the significant decrease in qN and YNPQ. LaCl3 (an inhibitor of Ca2+ channels) and dimethylthiourea (a scavenger of H2O2) abolished the effects of exogenous ATP. The results suggest that the role of eATP in enhancing the PSII photochemistry could be related to a Ca2+ or H2O2 signaling pathway.

Additional key words

photosynthesis reactive oxygen species signaling molecules 





extracellular ATP


the rate of photosynthetic electron transport through PSII


the maximal photochemical efficiency of PSII


the nonphotochemical quenching


the photochemical quenching


reactive oxygen species


the quantum yield of nonregulated energy dissipation of PSII


the quantum yield of regulated energy dissipation of PSII


the PSII operating efficiency


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  1. Baker N.R., Harbinson J., Kramer D.M.: Determining the limitations and regulation of photosynthetic energy transduction in leaves. — Plant Cell Environ. 30: 1107–1125, 2007.CrossRefPubMedGoogle Scholar
  2. Boyum R, Guidotti G.: Glucose-dependent, cAMP-mediated ATP efflux from Saccharomyces cerevisiae. — Microbiology 143: 1901–1908, 1997.CrossRefPubMedGoogle Scholar
  3. Chivasa S., Murphy A.M., Hamilton J.M. et al.: Extracellular ATP is a regulator of pathogen defence in plants. — Plant J. 60: 436–448, 2009.CrossRefPubMedGoogle Scholar
  4. Chivasa S., Simon W.J., Murphy A.M. et al.: The effects of extracellular adenosine 5′-triphosphate on the tobacco proteome. — Proteomics 10: 235–244, 2010.CrossRefPubMedGoogle Scholar
  5. Choi J., Tanaka K., Cao Y. et al.: Identification of a plant receptor for extracellular ATP. — Science 343: 290–294, 2014.CrossRefPubMedGoogle Scholar
  6. Costa A., Drago I., Behera S. et al.: H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2+-dependent scavenging system. — Plant J. 62: 760–772, 2010.CrossRefPubMedCentralPubMedGoogle Scholar
  7. Dat J., Vandenabeele S., Vranová E. et al.: Dual action of the active oxygen species during plant stress responses. — Cell Mol. Life Sci. 57: 779–795, 2000.CrossRefPubMedGoogle Scholar
  8. Demidchik V., Nichols C., Oliynyk M. et al.: Is ATP a signaling agent in plants? — Plant Physiol. 133: 456–461, 2003.CrossRefPubMedCentralPubMedGoogle Scholar
  9. Demidchik V., Shang Z.L., Shin R. et al.: Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. — Plant J. 58: 903–913, 2009.CrossRefPubMedGoogle Scholar
  10. Demidchik V., Shabala S.N., Davies J.M.: Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. — Plant J. 49: 377–386, 2007.CrossRefPubMedGoogle Scholar
  11. Demmig-Adams B., Adams W.W., Barker D.H. et al.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. — Physiol. Plantarum 98: 253–264, 1996.CrossRefGoogle Scholar
  12. Dichmann S., Idzko M., Zimpfer U. et al.: Adenosine triphosphate-induced oxygen radical production and CD11b up-regulation: Ca2+ mobilization and actin reorganization in human eosinophils. — Blood 95: 973–978, 2000.PubMedGoogle Scholar
  13. Donnini S., Guidi L., Degl’Innocenti E. et al.: Image changes in chlorophyll fluorescence of cucumber leaves in response to iron deficiency and resupply. — J. Plant Nutr. Soil Sc. 176: 734–742, 2013.Google Scholar
  14. Foresi N.P., Laxalt A.M., Tonón C.V. et al.: Extracellular ATP induces nitric oxide production in tomato cell suspensions. — Plant Physiol. 145: 589–592, 2007.CrossRefPubMedCentralPubMedGoogle Scholar
  15. Hepler P. K.: Calcium: A regulator of growth and development. — Plant Cell 17: 2142–2155, 2005.CrossRefPubMedCentralPubMedGoogle Scholar
  16. Jeter C.R., Tang W., Henaff E. et al.: Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. — Plant Cell 16: 2652–2664, 2004.CrossRefPubMedCentralPubMedGoogle Scholar
  17. Joseph S.M., Buchakjian M.R., Dubyak G.R.: Colocalization of ATP release sites and ecto-ATPase activity at the extra-cellular surface of human astrocytes. — J. Biol. Chem. 278: 23331–23342, 2003.CrossRefPubMedGoogle Scholar
  18. Kärkönen A, Koutaniemi S.: Lignin biosynthesis studies in plant tissue cultures. — J. Integr. Plant Biol. 52: 176–185, 2010.CrossRefPubMedGoogle Scholar
  19. Kim S.Y., Sivaguru M., Stacey G.: Extracellular ATP in plants. Visualization, localization, and analysis of physiological significance in growth and signaling. — Plant Physiol. 142: 984–992, 2006.CrossRefPubMedCentralPubMedGoogle Scholar
  20. Lim M.H., Wu J., Yao J. et al.: Apyrase suppression raises extracellular ATP levels and induces gene expression and cell wall changes characteristic of stress responses. — Plant Physiol. 164: 2054–2067, 2014.CrossRefPubMedCentralPubMedGoogle Scholar
  21. Maxwell K., Johnson G. N.: Chlorophyll fluorescence: a practical guide. — J. Exp. Bot. 51: 659–668, 2000.CrossRefPubMedGoogle Scholar
  22. Parish R.W., Weibel M.: Extracellular ATP, ecto-ATPase and calcium influx in Dictyostelium discoideum cells. — FEBS Lett. 118: 263–266, 1980.CrossRefPubMedGoogle Scholar
  23. Petroutsos D., Buscha A., Janßena I. et al.: The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. — Plant Cell 23: 2950–2963, 2011.CrossRefPubMedCentralPubMedGoogle Scholar
  24. Rentel M.C., Knight M.R.: Oxidative stress-induced calcium signaling in Arabidopsis. — Plant Physiol. 135: 1471–1479, 2004.CrossRefPubMedCentralPubMedGoogle Scholar
  25. Riewe D., Grosman L., Fernie A.R. et al.: A cell wall-bound adenosine nucleosidase is involved in the salvage of extracellular ATP in Solanum tuberosum. — Plant Cell Physiol. 49: 1572–1579, 2008.CrossRefPubMedGoogle Scholar
  26. Song C.J., Steinebrunner I., Wang X. et al.: Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. — Plant Physiol. 140: 1222–1232, 2006.CrossRefPubMedCentralPubMedGoogle Scholar
  27. Staxen I., Pical C., Montgomery L.T. et al.: Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. — P. Natl. Acad. Sci. USA 96: 1779–1784, 1999.CrossRefGoogle Scholar
  28. Sun J., Zhang C.L., Deng S.R. et al.: An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. — Plant Cell Environ. 35: 893–916, 2012.CrossRefPubMedGoogle Scholar
  29. Takeda S., Gapper C., Kaya H. et al.: Local positive feedback regulation determines cell shape in root hair cells. — Science 319: 1241–1244, 2008.CrossRefPubMedGoogle Scholar
  30. Tanaka K., Gilroy S., Jones A.M. et al.: Extracellular ATP signaling in plants. — Trends Cell Biol. 20: 601–608, 2010a.CrossRefPubMedGoogle Scholar
  31. Tanaka K., Swanson S.J., Gilroy S. et al.: Extracellular nucleotides elicit cytosolic free calcium oscillations in Arabidopsis. — Plant Physiol. 154: 705–719, 2010b.CrossRefPubMedCentralPubMedGoogle Scholar
  32. Thomas C., Rajagopal A., Windsor B. et al.: A role for ectophosphatase in xenobiotic resistance. — Plant Cell 12: 519–533, 2000.CrossRefPubMedCentralPubMedGoogle Scholar
  33. Wang W.H., Chen J., Liu T.W. et al.: Regulation of the calciumsensing receptor in both stomatal movement and photosynthetic electron transport is crucial for water use efficiency and drought tolerance in Arabidopsis. — J. Exp. Bot. 65: 223–234, 2014.CrossRefPubMedCentralPubMedGoogle Scholar
  34. Yegutkin G.G., Mikhailov A., Samburski S.S. et al.: The detection of micromolar pericellular ATP pool on lymphocyte surface by using lymphoid ecto-adenylate kinase as intrinsic ATP sensor. — Mol. Biol. Cell 17: 3378–3385, 2006.CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2015

Authors and Affiliations

  • H. -Q. Feng
    • 1
  • Q. -S. Jiao
    • 1
  • K. Sun
    • 1
  • L. -Y. Jia
    • 1
  • W. -Y. Tian
    • 1
  1. 1.College of Life ScienceNorthwest Normal UniversityLanzhouChina

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