Differential regulation of vacuolar H +-ATPase and H +-PPase in Cucumis sativus roots by zinc and nickel

Plant Science

Volumn 180, Issue 3, 2011, Pages 531-539

  Kabała, Katarzyna ^a   Janicka Russak, Małgorzata ^a  

^a UNIVERSITY OF WROC AW   (Poland)

Author keywords

Heavy metal; Nickel; Proton pump; V ATPase; V PPase; Zinc

Indexed keywords

ADENOSINE TRIPHOSPHATE; INORGANIC PYROPHOSPHATASE; NICKEL; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYROPHOSPHATE; TRACE ELEMENT; VEGETABLE PROTEIN; ZINC;

ARTICLE; CUCUMBER; DRUG EFFECT; ENZYMOLOGY; HYDROLYSIS; METABOLISM; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATE; BIOLOGICAL TRANSPORT; CUCUMIS SATIVUS; DIPHOSPHATES; HYDROLYSIS; INORGANIC PYROPHOSPHATASE; MICRONUTRIENTS; NICKEL; PLANT PROTEINS; PLANT ROOTS; PROTONS; VACUOLAR PROTON-TRANSLOCATING ATPASES; ZINC;

CUCUMIS SATIVUS;

EID: 78651483070     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2010.11.013     Document Type: Article

References (73)

1. Broadley M.R., White P.J., Hammond J.P., Zelko I., Lux A. Zinc in plants. New Phytol. 2007, 173:677-702.
2. Rout G.R., Das P. Effect of metal toxicity on plant growth and metabolism. I. Zinc. Agronomie 2003, 23:3-11.
3. Cakmak I. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000, 146:185-205.
4. Seregin I.V., Kozhevnikowa A.D. Physiological role of nickel and its toxic effects on higher plants. Russ. J. Plant Physiol. 2006, 53:257-277.
5. Clemens S., Palmgren M.G., Krämer U. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 2002, 7:309-315.
6. Krämer U., Talke I.N., Hanikenne M. Transition metal transport. FEBS Lett. 2007, 581:2263-2272.
7. Martinoia E., Maeshima M., Neuhaus H.E. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 2007, 58:83-102.
8. Kobae Y., Uemura T., Sato M.H., Ohnishi M., Mimura T., Nakagawa T., Maeshima M. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol. 2004, 45:1749-1758.
9. + exchanger. EMBO J. 1999, 18:3973-3980.
10. + exchangers in plants. Plant Biol. 2006, 8:419-429.
11. Cipriano D.J., Wang Y., Bond S., Hinton A., Jefferies K.C., Qi J., Forgac M. Structure and regulation of the vacuolar ATPases. Biochim. Biophys. Acta 2008, 1777:599-604.
12. Domgall I., Venzke D., Lüttge U., Ratajczak R., Böttcher B. Three-dimensional map of a plant V-ATPase based on electron microscopy. J. Biol. Chem. 2002, 277:13115-13121.
13. Gaxiola R.A., Palmgren M.G., Schumacher K. Plant proton pumps. FEBS Lett. 2007, 581:2204-2214.
14. Krebs M., Beyhl D., Görlich E., Al-Rasheid K.A.S., Marten I., Stierhof Y.-D., Hedrich R., Schumacher K. Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3251-3256.
15. +-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol. 1995, 108:641-649.
16. Darley C.P., Davies J.M., Sanders D. Chill-induced changes in the activity and abundance of the vacuolar proton-pumping pyrophosphatase from mung bean hypocotyls. Plant Physiol. 1995, 109:659-665.
17. +-translocating pyrophosphatase by phosphate starvation of Brassica napus (rapeseed) suspension cell cultures. FEBS Lett. 2000, 486:155-158.
18. Kabała K., Janicka-Russak M., Burzyński M., Kłobus G. Comparison of heavy metal effect on the proton pumps of plasma membrane and tonoplast in cucumber root cells. J. Plant Physiol. 2008, 165:278-288.
19. +-coupled secondary transport in plant vacuoles. Methods Enzymol. 1987, 148:115-123.
20. Kabała K., Kłobus G. Characterization of the tonoplast proton pumps in Cucumis sativus L. root cells. Acta Physiol. Plant. 2001, 23:55-63.
21. Gallagher S.R., Leonard R.T. Effect of vanadate, molybdate and azide on membrane-associated ATPase and soluble phosphatase activities of corn roots. Plant Physiol. 1982, 70:1335-1340.
22. Maeshima M., Yoshida S. Purification and properties of vacuolar membrane proton-translocating inorganic pyrophosphatase from mung bean. J. Biol. Chem. 1989, 264:20068-20073.
23. Ames B.N. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 1966, 8:115-118.
24. +-ATPase during reformation of the central vacuole in germinating pumpkin seeds. Plant Physiol. 1994, 106:61-69.
25. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principles of protein dye binding. Anal. Biochem. 1976, 72:248-254.
26. Kabała K., Kłobus G. Modification of vacuolar proton pumps in cucumber roots under salt stress. J. Plant Physiol. 2008, 165:1830-1837.
27. Glaab J., Kaiser W.M. Increased nitrate reductase activity in leaf tissues after application of the fungicide Kresoxim-methyl. Planta 1999, 207:442-448.
28. Sairam R.K., Rao K.V., Srivastava G.C. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 2002, 163:1037-1046.
29. Colangelo E.P., Guerinot M.L. Put the metal on the petal: metal uptake and transport throughout plants. Curr. Opin. Plant Biol. 2006, 9:322-330.
30. Arrivaul S., Senger T., Krämer U. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J. 2006, 46:861-879.
31. Dräger D.B., Desbrosses-Fonrouge A.G., Krach C., Chardonnens A.N., Meyer R.C., Saumitou-Leprade P., Krämer U. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J. 2004, 39:425-439.
32. Korenkov V., Hirschi K., Crutchfield J.D., Wagner G.J. Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 2007, 226:1379-1387.
33. Yang X., Feng Y., He Z., Stoffella P.J. Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J. Trace Elem. Med. Biol. 2005, 18:339-353.
34. Persans M.W., Nieman K., Salt D.E. Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:9995-10000.
35. Ingle R.A., Fricker M.D., Smith J.A.C. Evidence for nickel/proton antiport activity at the tonoplast of the hyperaccumulator plant Alyssum lesbiacum. Plant Biol. 2008, 10:746-753.
36. Gries G., Wagner G.J. Association of nickel versus transport of cadmium and calcium in tonoplast vesicles of oat roots. Planta 1998, 204:390-396.
37. Chardonnens A.N., Koevoets P.L.M., van Zanten A., Schat H., Verkleij J.A.C. Properties of enhanced tonoplast zinc transport in naturally selected zinc tolerant Silene vulgaris. Plant Physiol. 1999, 120:779-785.
38. Siedlecka A., Krupa Z. Functions of enzymes in heavy metal treated plants. Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants 2002, 303-324. Kluwer Academic Publishers. M.N.V. Prasad, K. Strzałka (Eds.).
39. Devi S.R., Prasad M.N.V. Membrane lipid alterations in heavy metal exposed plants. Heavy Metal Stress in Plants. From Molecules to Ecosystems 1999, 99-116. Springer. M.N.V. Prasad, J. Hagemeyer (Eds.).
40. 2+-ATPase activity and fluidity of plasma membranes from rice, Oryza sativa (cv. Bahía) shoots. J. Exp. Bot. 1990, 41:457-462.
41. Ros R., Cooke D.T., Martinez-Cortina C., Picazo I. Nickel and cadmium-related changes in growth, plasma membrane lipid composition, ATPase hydrolytic activity and proton-pumping of rice (Oryza sativa L. cv. Bahía) shoots. J. Exp. Bot. 1992, 43:1475-1481.
42. Ros R., Morales A., Segura J., Picazo I. In vivo and in vitro effects of nickel and cadmium on the plasmalemma ATPase from rice (Oryza sativa L.) shoots and roots. Plant Sci. 1992, 83:1-6.
43. - uptake by cucumber seedlings. II. In vitro and in vivo effect of Cd, Cu, Pb and Ni on the plasmalemma ATPase and oxidoreductase from cucumber seedling roots. Acta Physiol. Plant. 1994, 16:297-302.
44. +-ATPase to heavy metal stress in Cucumis sativus roots. J. Exp. Bot. 2008, 59:3721-3728.
45. Kennedy C.D., Gonsalves F.A.N. The action of divalent Zn, Cd, Hg, Cu and Pb ions on the ATPase activity of plasma membrane fraction isolated from roots of Zea mays. Plant Soil 1989, 117:167-175.
46. +-ATPase by tonoplast glycolipids prepared from cultured rice (Oryza sativa L. var. Boro) cells. Plant Cell Physiol. 2001, 42:516-523.
47. Ahsan N., Renaut J., Komatsu S. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 2009, 9:2602-2621.
48. Becher M., Talke I.N., Krall L., Krämer U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 2004, 37:251-268.
49. Fukao Y., Ferjani A., Fujiwara M., Nishimori Y., Ohtsu I. Identification of zinc-responsive proteins in the roots of Arabidopsis thaliana using a highly improved method of two-dimensional electrophoresis. Plant Cell Physiol. 2009, 50:2234-2239.
50. Ingle R.A., Smith J.A.C., Sweetlove L.J. Responses to nickel in the proteome of hyperaccumulator plant Alyssum lesbiacum. BioMetals 2005, 18:627-641.
51. Weber M., Harada E., Vess C., Roepenack-Lahaye E.v., Clemens S. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 2004, 37:269-281.
52. Farinati S., DalCorso G., Bona E., Corbella M., Lampis S., Cecconi D., Polati R., Berta G., Vallini G., Furini A. Proteomic analysis of Arabidopsis halleri shoots in response to the heavy metals cadmium and zinc and rhizosphere microorganisms. Proteomics 2009, 9:4837-4850.
53. Schneider T., Schellenberg M., Meyer S., Keller F., Gehrig P., Riedel K., Lee Y., Eberl L., Martinoia E. Quantitative detection of changes in the leaf-mesophyll tonoplast proteome in dependency of a cadmium exposure of barley (Hordeum vulgare L.) plants. Proteomics 2009, 9:2668-2677.
54. Hong-Hermesdorf A., Brüx A., Grüber A., Grüber G., Schumacher K. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett. 2006, 580:932-939.
55. McCubbin A.G., Ritchie S.M., Swanson S.J., Gilroy S. The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of barley aleurone through regulation of vacuolar function. Plant J. 2004, 39:206-218.
56. Liu G.S., Chen S., Chen J., Wang X.C. Identification of the phosphorylation site of the V-ATPase subunit A in maize roots. Acta Bot. Sin. 2004, 46:428-435.
57. Klychnikov O.I., Li K.W., Lill H., de Boer A.H. The V-ATPase from etiolated barley (Hordeum vulgare L.) shoots is activated by blue light and interacts with 14-3-3 proteins. J. Exp. Bot. 2007, 58:1013-1023.
58. Dietz K.-J., Baier M., Krämer U. Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. Heavy Metal Stress in Plants. From Molecules to Ecosystems 1999, 73-97. Springer. M.N.V. Prasad, J. Hagemeyer (Eds.).
59. Chaoui A., Mazhoudi S., Ghorbal M.H., Ferjani E.E. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci. 1997, 127:139-147.
60. Li M., Hu C., Zhu Q., Chen L., Kong Z., Liu Z. Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 2006, 62:565-572.
61. Madhava Rao K.V., Sresty T.V. Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci. 2000, 157:113-128.
62. Prasad K.V.S.K., Paradha Saradhi P., Sharmila P. Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ. Exp. Bot. 1999, 42:1-10.
63. Singla-Pareek S.L., Yadav S.K., Pareek A., Reddy M.K., Sopory S.K. Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol. 2006, 140:613-623.
64. Ali M.B., Vajpayee P., Tripathi R.D., Rai U.N., Singh S.N., Singh S.P. Phytoremediation of lead, nickel, and copper by Salix acmophylla Boiss.: role of antioxidant enzymes and antioxidant substances. Bull. Environ. Contam. Toxicol. 2003, 70:462-469.
65. Baccouch S., Chaoui A., Ferjani E.E. Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots. Plant Physiol. Biochem. 1998, 36:689-694.
66. Freeman J.L., Persans M.W., Nieman K., Albrecht C., Peer W., Pickering I.J., Salt D.E. Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 2004, 16:2176-2191.
67. Gajewska E., Skłodowska M. Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. BioMetals 2007, 20:27-36.
68. Kessler A., Brand M.D. Quantitative determination of the regulation of oxidative phosphorylation by cadmium in potato tuber mitochondria. Eur. J. Biochem. 1994, 225:923-935.
69. Kuznetsova S.S., Azarkina N.V., Vygodina T.V., Siletsky S.A., Konstantinov A.A. Zinc ions as cytochrome c oxidase inhibitors: two sites of action. Biochemistry (Moscow) 2005, 70:160-170.
70. Tan Y.-F., O'Toole N., Taylor N.L., Millar A.H. Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol. 2010, 152:747-761.
71. +-pyrophosphatase in rye plants grown under conditions deficient in mineral nutrients. Plant Cell Physiol. 1998, 39:890-894.
72. Mustroph A., Albrecht G., Hajirezaei M., Grimm B., Biemelt S. Low levels of pyrophosphate in transgenic potato plants expressing E. coli pyrophosphatase lead to decreased vitality under oxygen deficiency. Ann. Bot. 2005, 96:717-726.
73. Dietz K.-J., Tavakoli N., Kluge C., Mimura T., Sharma S.S., Harris G.C., Chardonnens A.N., Golldack D. Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J. Exp. Bot. 2001, 52:1969-1980.