Advertisement

Journal of Plant Research

, Volume 131, Issue 2, pp 331–339 | Cite as

The responses of photosystem II and intracellular ATP production of Arabidopsis leaves to salt stress are affected by extracellular ATP

  • Qin-Zheng Hou
  • Kun Sun
  • Hui Zhang
  • Xue Su
  • Bao-Qiang Fan
  • Han-Qing Feng
Regular Paper

Abstract

Hypertonic salt stress with different concentrations of NaCl increased the levels of extracellular ATP of Arabidopsis leaves. And, hypertonic salt stress decreased the levels of F v /F m (the maximal efficiency of photosystem II), Φ PSII (the photosystem II operating efficiency), qP (photochemical quenching), and intracellular ATP (iATP) production. The treatment with β,γ-methyleneadenosine 5′-triphosphate (AMP-PCP), which can exclude extracellular ATP from its binding sites of extracellular ATP receptors, caused a further decrease in the levels of F v /F m , Φ PSII, qP, and iATP production of the salt-stressed Arabidopsis leaves, while the addition of exogenous ATP rescued the inhibitory effects of AMP-PCP on Φ PSII , qP, and iATP production under hypertonic salt stress. Under hypertonic salt stress, the values of F v /F m , Φ PSII , qP, and iATP production were lower in the dorn 13 mutant than in the wild-type plants. These results indicate that the responses of photosystem II and intracellular ATP production to salt stress could be affected by extracellular ATP.

Keywords

Extracellular ATP Hypertonic salt stress Intracellular ATP Photosystem II 

Notes

Acknowledgements

The authors thank the National Natural Science Foundation of China (Projects Nos. 31360044, 31560070 and 31260059) Key Project of Science and Technology Research of Chinese Ministry of Education (No. 211190), the Fundamental Research Funds for the Gansu Universities of Gansu Provincial Department of Finance, the University Scientific Research Project of Gansu Province (No. 2015A-007), and Youth Teacher Scientific Research Ability Promotion Plan Innovation Team Project of Northwest Normal University.

Supplementary material

10265_2017_990_MOESM1_ESM.docx (394 kb)
Supplementary material 1 (DOCX 394 KB)

References

  1. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA (2006) International union of pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58:281–341CrossRefPubMedPubMedCentralGoogle Scholar
  2. Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki NYK, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbagenes in synechocystis. Plant Physiol 130:1443CrossRefPubMedPubMedCentralGoogle Scholar
  3. Apostolova EL, Dobrikova AG, Ivanova PI, Petkanchin IB, Taneva SG (2006) Relationship between the organization of the ps ii super complex and the functions of the photosynthetic apparatus. J Photochem Photobiol B Biol 83:114–122CrossRefGoogle Scholar
  4. Bodin P, Burnstock G (2001) Purinergic signalling: ATP release. Neurochem Res 26:959–969CrossRefPubMedGoogle Scholar
  5. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 26:1024–1030CrossRefGoogle Scholar
  6. Boyum R, Guidotti G (1997) Glucose-dependent, cAMP-mediated ATP efflux from Saccharomyces cerevisiae. Microbiology 143:1901–1908CrossRefPubMedGoogle Scholar
  7. 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 17:3019–3034CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 60:436–448CrossRefPubMedGoogle Scholar
  9. 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 10:235–244CrossRefPubMedGoogle Scholar
  10. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science 343:290–294CrossRefPubMedGoogle Scholar
  11. Clark G, Wu M, Wat N, Onyirimba J, Pham T, Herz N, Ogoti J, Gomez D, Canales AA, Aranda G, Blzard M, Nyberg T, Terry A, Torres J, Wu J, Roux SJ (2010) 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):423–435CrossRefPubMedGoogle Scholar
  12. 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 58:903–913CrossRefPubMedGoogle Scholar
  13. Dichmann S, Idzko M, Zimpfer U, Hofmann C, Ferrari D, Luttmann W, Virchow CJD, Virgilio F, Norgauer J (2000) Adenosine triphosphate-induced oxygen radical production and CD11b up-regulation: Ca2+ mobilization and actin reorganization in human eosinophils. Blood 95:973–978PubMedGoogle Scholar
  14. Dutta AK, Okada Y, Sabirov RZ (2002) Regulation of an ATP-conductive large-conductance anion channel and swelling-induced ATP release by arachidonic acid. J Physiol 542:803–816CrossRefPubMedPubMedCentralGoogle Scholar
  15. Feng HQ, Jiao QS, Sun K, Jia LY, Tian WY (2015) Extracellular ATP affects chlorophyll fluorescence of kidney bean (Phaseolus vulgaris) leaves through Ca2+ and H2O2-dependent mechanism. Photosynthetica 2:201–206CrossRefGoogle Scholar
  16. Heil M (2009) Damaged-self recognition in plant herbivore defence. Trends Plant Sci 14:356–363CrossRefPubMedGoogle Scholar
  17. Heil M, Ibarra-Laclette E, Adame-Álvarez RM, Martínez O, Ramirez-Chávez E, Molina-Torres J, Herrera-Estrella L (2012) How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLoS ONE 7(2):e30537CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2 /H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831CrossRefPubMedPubMedCentralGoogle Scholar
  19. Huh GH, Damaz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659CrossRefPubMedGoogle Scholar
  20. Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends Plant Sci 16:614–623CrossRefPubMedGoogle Scholar
  21. Jouaville LS, Pinton P, Bastianutto C, Rutter GA, Rizzuto R (1999) Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc Natl Acad Sci USA 96:13807–13812CrossRefPubMedPubMedCentralGoogle Scholar
  22. Khakh BS, Burnstock G (2009) The double life of ATP. Sci Am 301:84–90, 92CrossRefPubMedPubMedCentralGoogle Scholar
  23. Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527–532CrossRefPubMedGoogle Scholar
  24. Kim SY, Sivaguru M, Stacey G (2006) Extracellular ATP in plants. Visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142:984–992CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kim SH, Yang SH, Kim TJ (2009) Hypertonic stress increased extracellular ATP levels and the expression of stress-responsive genes in Arabidopsis thaliana seedlings. Biosci Biotechnol Biochem 73:1252–1256CrossRefPubMedGoogle Scholar
  26. 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 64:785–795CrossRefPubMedGoogle Scholar
  27. Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lustig KD, Shiau AK, Brake AJ, Julius D (1993) Expression cloning of an ATP receptor from mouse neuroblastoma cells. Proc Natl Acad Sci 90:5113–5117CrossRefPubMedPubMedCentralGoogle Scholar
  29. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403CrossRefPubMedGoogle Scholar
  30. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  31. Moons A (2003) Ospdr 9, which encodes a pdr-type abc transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett 553:370–376CrossRefPubMedGoogle Scholar
  32. Parish RW, Weibel M (1980) Extracellular ATP, ecto-ATPase and calcium influx in Dictyostelium discoideum cells. FEBS Lett 118:263–266CrossRefPubMedGoogle Scholar
  33. Rieder B, Neuhaus HE (2011) Identification of an Arabidopsis plasma membrane-located ATP transporter important for anther development. Plant Cell 23:1932–1944CrossRefPubMedPubMedCentralGoogle Scholar
  34. Roy P, Niyogi K, Sengupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and pm-bound h+-atpase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci 168:583–591CrossRefGoogle Scholar
  35. Rutter GA, Burnett P, Rizzuto R, Brini M, Murgia M, Pozzan T, Tavaré JM, Denton RM (1996) Subcellular imaging of intramitochondrial Ca2+ with recombinant targeted aequorin: significance for the regulation of pyruvate dehydrogenase activity. Proc Natl Acad Sci 93:5489CrossRefPubMedPubMedCentralGoogle Scholar
  36. Silva G, Beierwaltes WH, Garvin JL (2006) Extracellular ATP stimulates no production in rat thick ascending limb. Hypertension 47:563CrossRefPubMedGoogle Scholar
  37. Snider JL, Oosterhuis DM, Skulman BW, Kawakami EM (2011) Mechanisms of reproductive thermotolerance in Gossypium hirsutum: the effect of genotype and exogenous calcium application. J Agron Crop Sci 197:228–236CrossRefGoogle Scholar
  38. Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii FR, Motamed N, Komatsu S (2010) Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Prot Sci 8:19CrossRefGoogle Scholar
  39. Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486CrossRefGoogle Scholar
  40. Sudhir PR, Pogoryelov D, Kovacs L, Garab G, Murthy SD (2005) The effects of salt stress on photosynthetic electron transport and thylakoid membrane proteins in the cyanobacterium Spirulina platensis. J Biochem Mol Biol 38:481–485PubMedGoogle Scholar
  41. Sun J, Zhang CL, Deng SR, Lu CF, Shen X, Zhou XY, Zheng XJ, Hu ZM, Chen SL (2012a) An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. Plant Cell Environ 35:893–916CrossRefPubMedGoogle Scholar
  42. Sun J, Zhang X, Deng SR, Zhang CL. Wang MJ, Ding MQ, Zhao R, Shen X, Zhou XY, Lu CF, Chen SL (2012b) Extracellular ATP signaling is mediated by H2O2 andcytosolic Ca2+ in the salt response of Populus euphratica cells. Plos One 7:e53136CrossRefPubMedPubMedCentralGoogle Scholar
  43. Tanaka K, Gilroy S, Jones AM, Stacey G (2010a) Extracellular ATP signaling in plants. Trends Cell Biol 20:601–608CrossRefPubMedPubMedCentralGoogle Scholar
  44. Tanaka K, Swanson SJ, Gilroy S, Stacey G (2010b) Extracellular nucleotides elicit cytosolic free calcium oscillations in Arabidopsis. Plant Physiol 154:705–719CrossRefPubMedPubMedCentralGoogle Scholar
  45. Tanaka K, Choi J, Cao YR, Stacey G (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front Plant Sci 5:446CrossRefPubMedPubMedCentralGoogle Scholar
  46. Thomas C, Rajagopal A, Windsor B, Dudler R, Lloyd A, Roux SJ (2000) A role for ectophosphatase in xenobiotic resistance. Plant Cell 12:519–533CrossRefPubMedPubMedCentralGoogle Scholar
  47. Yang S, Wang F, Guo F, Meng JJ, Li XG, Dong ST, Wan SB (2013) Exogenous calcium alleviates photoinhibition of PSII by improving the xanthophyll cycle in peanut (Arachis hypogaea) leaves during heat stress under high irradiance. Plos One 8:e71214CrossRefPubMedPubMedCentralGoogle Scholar
  48. Zheng CF, Jiang DJ, Liu FL, Dai TB, Cao WX (2009) Effects of salt and waterlogging stressesand their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  • Qin-Zheng Hou
    • 1
  • Kun Sun
    • 1
  • Hui Zhang
    • 1
  • Xue Su
    • 1
  • Bao-Qiang Fan
    • 1
  • Han-Qing Feng
    • 1
  1. 1.Department of Biology Science, College of Life SciencesNorthwest Normal UniversityLanzhouChina

Personalised recommendations