Extracellular ATP Signaling Is Mediated by H2O2 and Cytosolic Ca2+ in the Salt Response of Populus euphratica Cells

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Sun, Jian ^a,b   Zhang, Xuan ^a   Deng, Shurong ^a   Zhang, Chunlan ^a   Wang, Meijuan ^a   Ding, Mingquan ^a   Zhao, Rui ^a   Shen, Xin ^a   Zhou, Xiaoyang ^a   Lu, Cunfu ^a   Chen, Shaoliang ^a  

^a BEIJING FORESTRY UNIVERSITY   (China)

^b JIANGSU NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; GLUCOSE; HEXOKINASE; HYDROGEN PEROXIDE; POTASSIUM ION; PURINERGIC P2 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; REACTIVE OXYGEN METABOLITE; SODIUM CHLORIDE; SODIUM ION; SURAMIN;

ARTICLE; CALCIUM CELL LEVEL; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL STRESS; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; GENE EXPRESSION; HOMEOSTASIS; MICROELECTRODE; NONHUMAN; PLANT CELL; PLANT GENE; POPULUS; POPULUS EUPHRATICA; PROTON SODIUM EXCHANGE; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALT STRESS; SALT TOLERANCE; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ADENOSINE TRIPHOSPHATE; ANTIOXIDANTS; CALCIUM; CELL SURVIVAL; CELLS, CULTURED; CYTOSOL; EXTRACELLULAR SPACE; HYDROGEN PEROXIDE; PLANT CELLS; POPULUS; SALT-TOLERANCE; SIGNAL TRANSDUCTION; SODIUM CHLORIDE;

POPULUS EUPHRATICA;

EID: 84871689815     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053136     Document Type: Article

References (57)

1. Zhang F, Wang Y, Yang YL, Wu H, Wang D, et al. (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30: 775-785.
2. Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H, (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53: 554-565.
3. Tracy FE, Gilliham M, Dodd AN, Webb AAR, Tester M, (2008) NaCl-induced changes in cytosolic free Ca2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ 31: 1063-1073.
4. Sun J, Wang M, Ding M, Deng S, Liu M, et al. (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33: 943-958.
5. Sun J, Li L, Liu M, Wang M, Ding M, et al. (2010) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tiss Organ Cult 103: 205-215.
6. Zhu JK, (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6: 1-5.
7. Martínez-Atienza J, Jiang XY, Garciadeblas B, Mendoza I, Zhu JK, et al. (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143: 1001-1012.
8. Tang RJ, Liu H, Bao Y, Lv QD, Yang L, et al. (2010) The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol Biol 74: 367-380.
9. Shi H, Ishitani M, Kim C, Zhu JK, (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. PNAS USA 97: 6896-6901.
10. Shi H, Quintero FJ, Pardo JM, Zhu JK, (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long distance Na+ transport in plants. Plant Cell 14: 465-477.
11. Wu Y, Ding N, Zhao X, Zhao M, Chang Z, et al. (2007) Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Mol Biol 65: 1-11.
12. Sun J, Chen S, Dai S, Wang R, Li N, et al. (2009) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar sepecies. Plant Physiol 149: 1141-1153.
13. Fraile-Escanciano A, Kamisugi Y, Cuming AC, Rodriguez-Navarro A, Benito B, (2010) The SOS1 transporter of Physcomitrella patens mediates sodium efflux in planta. New Phytol 188: 750-761.
14. Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, et al. (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279: 207-215.
15. Batelli G, Verslues PE, Agius F, Qiu Q, Fujii H, et al. (2007) SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Mol Cell Biol 27: 7781-7790.
16. Demidchik V, Shabala S, Davies J, (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J 49: 377-386.
17. Zhu JK, (2001) Plant salt tolerance. Trends Plant Sci 6: 66-71.
18. Munns R, Tester M, (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-81.
19. Shabala S, Cuin TA, (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133: 651-669.
20. Roux SJ, Steinebrunner I, (2007) Extracellular ATP: an unexpected role as a signaler in plants. Trends Plant Sci 12: 522-527.
21. Tanaka K, Gilroy S, Jones AM, Stacey G, (2010) Extracellular ATP signaling in plants. Trends Cell Biol 20: 601-608.
22. Clark G, Torres J, Finlayson S, Guan X, Handley C, et al. (2010) Apyrase (NTPDase) and extracellular nucleotides regulate cotton fiber elongation in cultured ovules. Plant Physiol 152: 1073-1083.
23. 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.
24. Reichler SA, Torres J, Rivera AL, Cintolesi VA, Clark G, et al. (2009) Intersection of two signalling pathways: extracellular nucleotides regulate pollen germination and pollen tube growth via nitric oxide. J Exp Bot 60: 2129-2138.
25. Clark G, Fraley D, Steinebrunner I, Cervantes A, Onyirimba J, et al. (2011) Extracellular nucleotides and apyrases regulate stomatal aperture in Arabidopsis. Plant Physiol 156: 1740-1753.
26. Hao LH, Wang WX, Chen C, Wang YF, Liu T, et al. (2012) Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein α subunit and reactive oxygen species. Mol Plant 5: 852-864.
27. 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: 147-154.
28. Lew RR, Dearnaley JDW, (2000) Extracellular nucleotide effects on the electrical properties of growing Arabidopsis thaliana root hairs. Plant Sci 153: 1-6.
29. 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.
30. Chivasa S, Ndimba B, Simon W, Lindsey K, Slabas A, (2005) Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 17: 3019-3034.
31. Song CJ, Steinebrunner I, Wang XZ, Stout SC, Roux SJ, (2006) Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiol 140: 1222-1232.
32. Chivasa S, Murphy AM, Hamilton JM, Lindsey K, Carr JP, et al. (2009) Extracellular ATP is a regulator of pathogen defence in plants. Plant J 60: 436-448.
33. Demidchik V, Nichols C, Oliynyk M, Dark A, Glover BJ, et al. (2003) Is ATP a signaling agent in plants? Plant Physiol 133: 456-461.
34. 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.
35. Demidchik V, Shang Z, Shin R, Thompson E, Rubio L, et al. (2009) Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. Plant J 58: 903-913.
36. Clark G, Roux SJ, (2009) Extracellular nucleotides: ancient signaling molecules. Plant Sci 177: 239-244.
37. Kim SH, Yang SH, Kim TJ, Han JS, Suh JW, (2009) Hypertonic stress increased extracellular ATP levels and the expression of stress-responsible genes in Arabidopsis thaliana seedlings. Biosci Biotech Biochem 73: 1252-1256.
38. Silva P, Facanha AR, Tavares RM, Geros H, (2009) Role of tonoplast proton pumps and Na+/H+ antiport system in salt tolerance of Populus euphratica Oliv. J Plant Growth Regul 29: 23-34.
39. Konrad KR, Hedrich R, (2008) The use of voltage-sensitive dyes to monitor signal-induced changes in membrane potential-ABA triggered membrane depolarization in guard cells. Plant J 55: 161-173.
40. Oh DH, Leidi E, Zhang Q, Hwang S, Li Y, et al. (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151: 210-222.
41. Sun J, Zhang C, Deng S, Lu C, Shen X, et al. (2012) An ATP signaling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica. Plant Cell Environ 35: 893-916.
42. Jiang M, Zhang J, (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53: 2401-2410.
43. Wang R, Chen S, Zhou X, Shen X, Deng L, et al. (2008) Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol 28: 947-957.
44. Bradford M, (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
45. Wang R, Chen S, Deng L, Fritz E, Hüttermann A, et al. (2007) Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees 21: 581-591.
46. Desikan R, A-H-Mackerness S, Hancock JT, Neill SJ, (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172.
47. Vranová E, Inzé D, Breusegem F, (2002) Signal transduction during oxidative stress. J Exp Bot 53: 1227-1236.
48. Shabala SN, Newman IA, (2000) Salinity effects on the activity of plasma membrane H+ and Ca2+ transporters in bean leaf mesophyll: masking role of the cell wall. Ann Bot 85: 681-686.
49. Sun J, Dai S, Wang R, Chen S, Li N, et al. (2009) Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiol 29: 1175-1186.
50. Pottosin I, Wherrett T, Shabala S, (2009) SV channels dominate the vacuolar Ca2+ release during intracellular signalling. FEBS Let 583: 921-926.
51. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, et al. (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt stressed barley. Plant Physiol 145: 1714-1725.
52. Yamazaki T, Kawamura Y, Minami A, Uemura M, (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20: 3389-3404.
53. Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, et al. (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20: 337 4-3388.
54. Sueldo DJ, Foresi NP, Casalongue CA, Lamattina L, Laxalt AM, (2010) Phosphatidic acid formation is required for extracellular ATP-mediated nitric oxide production is suspension-cultured tomato cells. New Phytol 185: 909-916.
55. Yu L, Nie J, Cao C, Jin Y, Yan M, et al. (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188: 762-773.
56. Zhang A, Jiang M, Zhang J, Tan M, Hu X, (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 141: 475-487.
57. Tanaka K, Swanson SJ, Gilroy S, Stacey G, (2010) Extracellular nucleotides elicit cytosolic free calcium oscillations in Arabidopsis. Plant Physiol 154: 705-719.