Nitrate reductase-dependent nitric oxide production is involved in microcystin-LR-induced oxidative stress in brassica rapa

Water, Air, and Soil Pollution

Volumn 223, Issue 7, 2012, Pages 4141-4152

  Chen, Jian ^a,b,c   Zhong, You Ming ^a,b,c   Zhang, Hai Qiang ^a,b,c,d   Shi, Zhi Qi ^a,b,c  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c State Key Laboratory Breeding Base   (China)

^d NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Brassica rapa; Microcystin LR; Nitrate reductase; Nitric oxide; Oxidative stress

Indexed keywords

ASCORBATE PEROXIDASE; BRASSICA RAPA; LIPID PEROXIDATION; MEMBRANE INTEGRITY; MICROCYSTIN-LR; NITRATE REDUCTASE; REACTIVE OXYGEN SPECIES; STRESS-INDUCED; SUPER OXIDE DISMUTASE; SUPEROXIDE ANION RADICALS; SYNTHASES;

HYDROGEN PEROXIDE; NITRIC OXIDE; OXYGEN; SODIUM COMPOUNDS;

OXIDATIVE STRESS;

ASCORBATE PEROXIDASE; CATALASE; ENZYME INHIBITOR; HYDROGEN PEROXIDE; MICROCYSTIN RR; N(G) METHYLARGININE; NITRATE REDUCTASE; NITRATE REDUCTASE INHIBITOR; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CONCENTRATION (COMPOSITION); HYDROGEN PEROXIDE; LEAFY VEGETABLE; LIPID; NITRATE; NITRIC OXIDE; PHYTOTOXICITY; SEEDLING; TOXIN;

ARTICLE; BRASSICA RAPA; CELL MEMBRANE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; EXPOSURE; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PHYTOTOXICITY; PLANT GROWTH; PLANT ROOT; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEEDLING; SHOOT; SIGNAL TRANSDUCTION;

BRASSICA RAPA;

EID: 84865497289     PISSN: 00496979     EISSN: 15732932     Source Type: Journal    
DOI: 10.1007/s11270-012-1180-y     Document Type: Article

References (59)

1. MB Ali P Vajpayee RD Tripathi UN Rai A Kumar, et al. 2000 Mercury bioaccumulation induces oxidative stress and toxicity to submerged macrophyte Potamogeton crispus L Bulletin of Environmental Contamination and Toxicology 65 573 582 10.1007/s001280000162 1:CAS:528:DC%2BD3cXotFamtbo%3D
2. K Apel H Hirt 2004 Reactive oxygen species: Metabolism, oxidative stress, and signal transduction Annual Review of Plant Biology 55 373 399 10.1146/annurev.arplant.55.031903.141701 1:CAS:528:DC%2BD2cXlvFeisL0%3D (Pubitemid 38940937)
3. M Arasimowicz J Floryszak-Wieczorek 2007 Nitric oxide as a bioactive signaling molecule in plant stress responses Plant Science 172 876 887 10.1016/j.plantsci.2007.02.005 1:CAS:528:DC%2BD2sXjvFals7c%3D (Pubitemid 46517737)
4. RF Beers Jr IW Sizer 1952 A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase Journal of Biological Chemistry 195 133 140 1:CAS:528:DyaG38Xjt12juw%3D%3D
5. A Besson-Bard A Pugin D Wendehenne 2008 New insights into nitric oxide signaling in plants Annual Review of Plant Biology 59 21 39 10.1146/annurev. arplant.59.032607.092830 1:CAS:528:DC%2BD1cXntFaqs7Y%3D (Pubitemid 351813022)
6. A Besson-Bard A Gravot P Richaud P Auroy C Duc, et al. 2009 Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake Plant Physiology 149 1302 1315 10.1104/pp.108.133348 1:CAS:528:DC%2BD1MXlsFCitbw%3D
7. MM Bradford 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Analytical Biochemistry 72 248 254 10.1016/0003-2697(76)90527-3 1:CAS:528:DyaE28XksVehtrY%3D
8. 2 synthesis The Plant Journal 45 113 122 10.1111/j.1365-313X.2005.02615.x 1:CAS:528:DC%2BD28XjvFOntw%3D%3D (Pubitemid 43373736)
9. J Chen L Song J Dai N Gan Z Liu 2004 Effects of microcystins on the growth and the activity of superoxide dismutase and peroxidase of rape (Brassica napus L.) and rice (Oryza sativa L.) Toxicon 43 393 400 10.1016/j.toxicon.2004. 01.011 1:CAS:528:DC%2BD2cXisFChu78%3D (Pubitemid 38402130)
10. J Chen S Shiyab FX Han DL Monts CA Waggoner, et al. 2009 Bioaccumulation and physiological effects of mercury in Pteris vittata and Nephrolepis exaltata Ecotoxicology 18 110 121 10.1007/s10646-008-0264-3 1:CAS:528: DC%2BD1MXhtlSltg%3D%3D
11. J Chen J Dai H Zhang C Wang G Zhou, et al. 2010 Bioaccumulation of microcystin and its oxidative stress in the apple (Malus pumila) Ecotoxicology 19 796 803 10.1007/s10646-009-0456-5 1:CAS:528:DC%2BC3cXjvVeju74%3D
12. J Chen FX Han F Wang HQ Zhang ZQ Shi 2012 Accumulation and phytotoxicity of microcystin-LR in rice (Oryza sativa) Ecotoxicology and Environmental Safety 76 193 199 10.1016/j.ecoenv.2011.09.022 1:CAS:528:DC%2BC3MXhsFegtbbJ
13. Corpas, F. J., Palma, J. M., Leterrier, M., del Río, L. A., & Barroso, J. B. (2009). Nitric oxide and abiotic stress in higher plants. In S. Hayat, M. Mori, J. Pichtel, & A. Ahmad (Eds.), Nitric oxide in plant physiology (pp. 51-63). Weinheim: Wiley-VCH GmbH & Co. KGaA.
14. JR Crush LR Briggs JM Sprosen SN Nichols 2008 Effect of irrigation with lake water containing microcystins on microcystin content and growth of ryegrass, clover, rape, and lettuce Environmental Toxicology 23 246 252 10.1002/tox.20331 1:CAS:528:DC%2BD1cXkt1Cmsbg%3D (Pubitemid 351458215)
15. MC de Pinto F Tomassi L de Gara 2002 Changes in the antioxidant systems as a part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells Plant Physiology 130 689 708
16. LA del Rio LM Sandalio FJ Corpas JM Palma JB Barroso 2006 Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling Plant Physiology 141 330 335 10.1104/pp.106.078204 (Pubitemid 43974523)
17. M Delledone 2005 NO news is good news for plants Current Opinion in Plant Biology 38 44 52
18. H Duan R Ma X Xu F Kong S Zhang, et al. 2009 Two-decade reconstruction of algal blooms in China's Lake Taihu Environmental Science & Technology 43 3522 3528 10.1021/es8031852 1:CAS:528:DC%2BD1MXktF2htL0%3D
19. J Foreman V Demidchik JH Bothwell P Mylona H Miedema, et al. 2003 Reactive oxygen species produced by NADPH oxidase regulate plant cell growth Nature 422 442 446 10.1038/nature01485 1:CAS:528:DC%2BD3sXitlGgtLg%3D (Pubitemid 36411398)
20. G Frahry P Schopfer 2001 NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay Planta 212 175 183 10.1007/s004250000376 1:CAS:528:DC%2BD3MXjs1Kktw%3D%3D (Pubitemid 32139873)
21. E Gas U Flores-Perez S Sauret-Gueto M Rodriguez-Concepcion 2009 Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism The Plant Cell 21 18 23 10.1105/tpc.108. 065243 1:CAS:528:DC%2BD1MXlsFCitr4%3D
22. CN Giannopolitis SK Ries 1977 Superoxide dismutases: I. Occurrence in higher plants Plant Physiology 59 309 314 10.1104/pp.59.2.309 1:CAS:528:DyaE2sXhtlKgtrs%3D
23. L Guo 2007 Doing battle with the green monster of Taihu Lake Science 317 1166 10.1126/science.317.5842.1166 1:CAS:528:DC%2BD2sXhtVWks77O
24. K Guo K Xia ZM Yang 2008 Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide Journal of Experimental Botany 59 3443 3452 10.1093/jxb/ern194 1:CAS:528:DC%2BD1cXhtFWit7vE
25. S Järvenpää C Lundberg-Niinistö L Spoof O Sjövall E Tyystjärvi, et al. 2007 Effects of microcystins on broccoli and mustard, and analysis of accumulated toxin by liquid chromatography-mass spectrometry Toxicon 49 865 874 10.1016/j.toxicon.2006.12.008 (Pubitemid 46590255)
26. J Jiang X Gu R Song X Wang L Yang 2011 Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara Journal of Hazardous Materials 190 188 196 10.1016/j.jhazmat.2011.03.023 1:CAS:528:DC%2BC3MXmtlWqtb4%3D
27. O Lamotte K Gould D Lecourieux A Sequeira-Legrand A Lebrun-Garcia, et al. 2004 Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein Plant Physiology 135 516 529 10.1104/pp.104.038968 1:CAS:528:DC%2BD2cXkt12msrY%3D (Pubitemid 38653696)
28. C Leigh MA Burford DT Roberts JW Udy 2010 Predicting the vulnerability of reservoirs to poor water quality and cyanobacterial blooms Water Research 44 4487 4496 10.1016/j.watres.2010.06.016 1:CAS:528:DC%2BC3cXpvVSnt7c%3D
29. M Martin MJR Colman DF Góez-Casati L Lamattina EJ Zabaleta 2009 Nitric oxide accumulation is required to protect against iron-mediated oxidative stress in frataxin-deficient Arabidopsis plants FEBS Letters 583 542 548 10.1016/j.febslet.2008.12.039 1:CAS:528:DC%2BD1MXhtlChs74%3D
30. C Máthé D Beyer F Erdodi Z Serfozo L Székvö lgyi, et al. 2009 Microcystin-LR induces abnormal root development by altering microtubule organization in tissue-cultured common reed (Phragmites australis) plantlets Aquatic Toxicology 92 122 130 10.1016/j.aquatox.2009.02.005
31. M M-Hamvas C Mathe E Molnar G Vasas I Grigorszky, et al. 2003 Microcystin-LR alters the growth, anthocyanin content and single-stranded DNase enzyme activities in Sinapis alba L seedlings Aquatic Toxicology 62 1 9 10.1016/S0166-445X(01)00273-9 1:CAS:528:DC%2BD38XotF2ju7o%3D (Pubitemid 36159005)
32. M M-Hamvas C Máthé G Vasas K Jámbrik M Papp, et al. 2011 Cylindrospermopsin and microcystin-LR alter the growth, development and peroxidase enzyme activity of white mustard (Sinapis alba L.) seedlings, a comparative analysis Acta Biologica Hungarica 61 35 48 10.1556/ABiol.61.2010. Suppl.5
33. R Mittler 2002 Oxidative stress, antioxidants and stress tolerance Trends in Plant Science 7 405 410 10.1016/S1360-1385(02)02312-9 1:CAS:528: DC%2BD38XntVWnu7Y%3D (Pubitemid 36726490)
34. R Mittler BA Zilinskas 1993 Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium Analytical Biochemistry 212 540 546 10.1006/abio.1993.1366 1:CAS:528:DyaK3sXlslKgsbg%3D (Pubitemid 23245109)
35. Y Nakano K Asada 1981 Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts Plant & Cell Physiology 22 867 880 1:CAS:528:DyaL3MXltFWqur0%3D
36. S Neill J Bright R Desikan J Hancock J Harrison, et al. 2008 Nitric oxide evolution and perception Journal of Experimental Botany 59 25 35 10.1093/jxb/erm218 1:CAS:528:DC%2BD1cXht1Sitbs%3D (Pubitemid 351598967)
37. E Ono HL Wong T Kawasaki M Hasegawa O Kodama K Shimamoto 2001 Essential role of the small GTPase Rac in disease resistance of rice Proceedings of the National Academy of Sciences of the United States of America 98 759 764 1:CAS:528:DC%2BD3MXnslKluw%3D%3D (Pubitemid 32105116)
38. M Orozco-Cardenas CA Ryan 1999 Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway Proceedings of the National Academy of Sciences of the United States of America 96 6553 6557 10.1073/pnas.96.11.6553 1:CAS:528:DyaK1MXksFKkur0%3D (Pubitemid 29256704)
39. HW Paerl NS Hall ES Calandrino 2011 Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change Science of the Total Environment 409 1739 1745 10.1016/j.scitotenv.2011.02.001 1:CAS:528:DC%2BC3MXjtFSmtrk%3D
40. S Pereira M Saker M Vale V Vasconcelos 2009 Comparison of sensitivity of grasses (Lolium perenne L. and Festuca rubra L.) and lettuce (Lactuca sativa L.) exposed to water contaminated with microcystins Bulletin of Environmental Contamination and Toxicology 83 81 84 10.1007/s00128-009-9763-z 1:CAS:528:DC%2BD1MXmslyhs70%3D
41. A Peuthert S Pflugmacher 2010 Influence of the cyanotoxin microcystin-LR on tocopherol in Alfalfa seedlings (Medicago sativa) Toxicon 56 411 417 10.1016/j.toxicon.2010.04.004 1:CAS:528:DC%2BC3cXotlSksLs%3D
42. A Peuthert S Chakrabarti S Pflugmacher 2007 Uptake of microcystins-LR and -LF (cyanobacterial toxins) in seedlings of several important agricultural plant species and the correlation with cellular damage (lipid peroxidation) Environmental Toxicology 22 436 442 10.1002/tox.20266 1:CAS:528: DC%2BD2sXotlCjs7g%3D (Pubitemid 47121924)
43. S Pflugmacher 2004 Promotion of oxidative stress in the aquatic macrophyte Ceratophyllum demersum during biotransformation of the cyanobacterial toxin microcystin-LR Aquatic Toxicology 70 169 178 10.1016/j.aquatox.2004.06. 010 1:CAS:528:DC%2BD2cXhtVSntbvM (Pubitemid 39506827)
44. S Pflugmacher K Jung L Lundvall S Neumann A Peuthert 2006 Effects of cyanobacterial toxins and cyanobacterial cell-free crude extract on germination of alfalfa (Medicago sativa) and induction of oxidative stress Environmental Toxicology and Chemistry 25 2381 2387 10.1897/05-615R.1 1:CAS:528: DC%2BD28XovVOrtrk%3D (Pubitemid 44763295)
45. S Pflugmacher M Aulhorn B Grimm 2007 Influence of a cyanobacterial crude extract containing microcystin-LR on the physiology and antioxidative defence systems of different spinach variants New Phytologist 175 482 489 10.1111/j.1469-8137.2007.02144.x 1:CAS:528:DC%2BD2sXpvFSqsLs%3D (Pubitemid 47083901)
46. S Pflugmacher J Hofmann B Hubner 2007 Effects on growth and physiological parameters in wheat (Triticum aestivum L.) grown in soil and irrigated with cyanobacterial toxin contaminated water Environmental Toxicology and Chemistry 26 2710 2716 10.1897/07-145.1 1:CAS:528:DC%2BD2sXhtlKktrfM (Pubitemid 350247126)
47. A Prieto A Campos A Cameán V Vasconcelos 2011 Effects on growth and oxidative stress status of rice plants (Oryza sativa) exposed to two extracts of toxin-producing cyanobacteria (Aphanizomenon ovalisporum and Microcystis aeruginosa) Ecotoxicology and Environmental Safety 74 1973 1980 10.1016/j.ecoenv.2011.06.009 1:CAS:528:DC%2BC3MXht1ehs7jM
48. Rio, L. A., Puppo, A., Bolwell, G. P., & Daudi, A. (2009). Reactive oxygen species in plant-pathogen interactions. In L. A. Rio & A. Puppo (Eds.), Reactive oxygen species in plant signaling, signaling and communication in plants (pp. 113-133). Berlin: Springer.
49. S Saqrane IE Ghazali Y Ouahid ME Hassni IE Hadrami, et al. 2007 Phytotoxic effects of cyanobacteria extract on the aquatic plant Lemna gibba: Microcystin accumulation, detoxication and oxidative stress induction Aquatic Toxicology 83 284 294 10.1016/j.aquatox.2007.05.004 1:CAS:528: DC%2BD2sXnsFKnsLg%3D (Pubitemid 47023012)
50. MA Torres JL Dangl JD Jones 2002 Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response Proceedings of the National Academy of Sciences of the United States of America 99 517 522 10.1073/pnas.012452499 1:CAS:528:DC%2BD38Xlt1CqsQ%3D%3D (Pubitemid 34060393)
51. YS Wang ZM Yang 2005 Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L Plant & Cell Physiology 46 1915 1923 10.1093/pcp/pci202 1:CAS:528:DC%2BD28XhsVOitQ%3D%3D (Pubitemid 43063799)
52. Z Wang B Xiao L Song X Wu J Zhang, et al. 2011 Effects of microcystin-LR, linear alkylbenzene sulfonate and their mixture on lettuce (Lactuca sativa L.) seeds and seedlings Ecotoxicology 20 803 814 10.1007/s10646-011-0632-2 1:CAS:528:DC%2BC3MXls1eqsrw%3D
53. M Welker H von Döhren 2006 Cyanobacterial peptides-Nature's own combinatorial biosynthesis FEMS Microbiology Reviews 30 530 563 10.1111/j.1574-6976.2006.00022.x 1:CAS:528:DC%2BD28Xms1Cqtbw%3D (Pubitemid 43855766)
54. W Woodbury AK Spencer MA Stahmann 1971 An improved procedure using ferricyanide for detecting catalase isoenzymes Analytical Biochemistry 44 301 305 10.1016/0003-2697(71)90375-7 1:CAS:528:DyaE38XktlWmtA%3D%3D
55. S Xie RD Pancost Y Wang H Yang PB Wignall, et al. 2010 Cyanobacterial blooms tied to volcanism during the 5 m.y. Permo-Triassic biotic crisis Geology 38 447 450 10.1130/G30769.1 1:CAS:528:DC%2BC3MXksFSisbY%3D
56. Y Yamamoto Y Kobayashi H Matsumoto 2001 Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots Plant Physiology 125 199 208 10.1104/pp.125.1.199 1:CAS:528:DC%2BD3MXjslymu7o%3D (Pubitemid 32116759)
57. A Zhang J Zhang J Zhang N Ye H Zhang, et al. 2010 Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves Plant & Cell Physiology 52 181 192 10.1093/pcp/pcq187
58. MG Zhao L Chen LL Zhang WH Zhang 2009 Nitric reductase-dependent NO production is involved in cold acclimation and freezing tolerance in Arabidopsis Plant Physiology 151 755 767 10.1104/pp.109.140996 1:CAS:528:DC%2BD1MXhtlSjsr7L
59. ZS Zhou SJ Wang ZM Yang 2008 Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants Chemosphere 70 1500 1509 10.1016/j.chemosphere.2007.08.028 1:CAS:528:DC%2BD1cXlvV2qsw%3D%3D