Selenite activates the alternative oxidase pathway and alters primary metabolism in Brassica napus roots: Evidence of a mitochondrial stress response

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Dimkovikj, Aleksandar ^a   Van Hoewyk, Doug ^a  

^a Department of Public Health   (United States)

Author keywords

Glutathione; Mitochondrial superoxide; Selenium; TCA cycle; glutamyl cyclotransferase

Indexed keywords

BRASSICA NAPUS;

ACONITATE HYDRATASE; ALTERNATIVE OXIDASE; GLUTATHIONE; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; SELENIOUS ACID; SUPEROXIDE; VEGETABLE PROTEIN;

CELL RESPIRATION; ENZYMOLOGY; METABOLISM; MITOCHONDRION; PENTOSE PHOSPHATE CYCLE; PHYSIOLOGICAL STRESS; PLANT ROOT; RAPESEED;

ACONITATE HYDRATASE; BRASSICA NAPUS; CELL RESPIRATION; GLUTATHIONE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDOREDUCTASES; PENTOSE PHOSPHATE PATHWAY; PLANT PROTEINS; PLANT ROOTS; SELENIOUS ACID; STRESS, PHYSIOLOGICAL; SUPEROXIDES;

EID: 84908456000     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0259-6     Document Type: Article

References (54)

1. Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004, 55:373-399. 10.1146/annurev.arplant.55.031903.141701, 15377225.
2. Sweetlove L, Heazlewood J, Herald V, Holtzapffel R, Day D, Leaver C, Millar A. The impact of oxidative stress on Arabidopsis mitochondria. Plant J 2002, 32:891-904. 10.1046/j.1365-313X.2002.01474.x, 12492832.
3. Verniquet F, Gaillard J, Neuburger M, Douce R. Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J 1991, 276:643-648. 1648348.
4. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN. Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 2006, 141:357-366. 10.1104/pp.106.079129, 16760488.
5. Lehmann M, Schwarzländer M, Obata T, Sirikantaramas S, Burow M, Olsen CE, Tohge T, Fricker MD, Møller BL, Fernie AR. The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol Plant 2009, 2:390-406. 10.1093/mp/ssn080, 19825624.
6. Møller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Annu Rev Plant Physiol Plant Mol Biol 2007, 58:459-481. 10.1146/annurev.arplant.58.032806.103946.
7. Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A. Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 2011, 12:6894-6918. 10.3390/ijms12106894, 22072926.
8. Jacoby RP, Taylor NL, Millar AH. The role of mitochondrial respiration in salinity tolerance. Trends Plant Sci 2011, 16:614-623. 10.1016/j.tplants.2011.08.002, 21903446.
9. Bi Y, Chen W, Zhang W, Zhou Q, Yun L, Xing D. Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium-induced cell death in Arabidopsis thaliana. Biol Cell 2009, 101:629-643. 10.1042/BC20090015, 19453296.
10. Morgan MJ, Lehmann M, Schwarzländer M, Baxter CJ, Sienkiewicz-Porzucek A, Williams TC, Schauer N, Fernie AR, Fricker MD, Ratcliffe RG. Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol 2008, 147:101-114. 10.1104/pp.107.113613, 18337490.
11. Gupta KJ, Shah JK, Brotman Y, Jahnke K, Willmitzer L, Kaiser WM, Bauwe H, Igamberdiev AU. Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J Exp Bot 2012, 63:1773-1784. 10.1093/jxb/ers053, 22371326.
12. Cvetkovska M, Vanlerberghe GC. Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 2012, 195:32-39. 10.1111/j.1469-8137.2012.04166.x, 22537177.
13. Watanabe CK, Hachiya T, Terashima I, Noguchi K. The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defence systems in Arabidopsis thaliana leaves. Plant Cell Environ 2008, 31:1190-1202. 10.1111/j.1365-3040.2008.01834.x, 18507803.
14. Vanlerberghe GC. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 2013, 14:6805-6847. 10.3390/ijms14046805, 23531539.
15. Rayman MP. The importance of selenium to human health. Lancet 2000, 356:233-241. 10.1016/S0140-6736(00)02490-9, 10963212.
16. Kikkert J, Berkelaar E. Plant Uptake and Translocation of Inorganic and Organic Forms of Selenium. Arch Environ Contam Toxicol 2013, 65:458-465. 10.1007/s00244-013-9926-0, 23793939.
17. El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian J-C. Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 2007, 143:1231-1241. 10.1104/pp.106.091462, 17208959.
18. Zhu YG, Pilon-Smits EA, Zhao FJ, Williams PN, Meharg AA. Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 2009, 14:436-442. 10.1016/j.tplants.2009.06.006, 19665422.
19. Sabbagh M, Van Hoewyk D. Malformed selenoproteins are removed by the ubiquitin-proteasome pathway in Stanleya pinnata. Plant Cell Physiol 2012, 53:555-564. 10.1093/pcp/pcs015, 22323770.
20. Van Hoewyk D. A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Ann Bot 2013, 112:965-972. 10.1093/aob/mct163, 23904445.
21. Ng BH, Anderson JW. Light-dependent incorporation of selenite and sulphite into selenocysteine and cysteine by isolated pea chloroplasts. Phytochemistry 1979, 18:573-580. 10.1016/S0031-9422(00)84263-6.
22. Chen JJ, Boylan LM, Wu CK, Spallholz JE. Oxidation of glutathione and superoxide generation by inorganic and organic selenium compounds. Biofactors 2007, 31:55-66. 10.1002/biof.5520310106, 18806309.
23. Wallenberg M, Misra S, Wasik AM, Marzano C, Björnstedt M, Gandin V, Fernandes AP. Selenium induces a multi-targeted cell death process in addition to ROS formation. J Cell Mol Med 2014, 18:671-784. 10.1111/jcmm.12214, 24400844.
24. Zechmann B, Mauch F, Sticher L, Müller M. Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 2008, 59:4017-4027. 10.1093/jxb/ern243, 18977750.
25. Robinson KM, Janes MS, Beckman JS. The selective detection of mitochondrial superoxide by live cell imaging. Nat Protoc 2008, 3:941-947. 10.1038/nprot.2008.56, 18536642.
26. Li Z, Xing D. Mechanistic study of mitochondria-dependent programmed cell death induced by aluminium phytotoxicity using fluorescence techniques. J Exp Bot 2011, 62:331-343. 10.1093/jxb/erq279, 20937730.
27. Tarrago L, Laugier E, Rey P. Protein-repairing methionine sulfoxide reductases in photosynthetic organisms: gene organization, reduction mechanisms, and physiological roles. Mol Plant 2009, 2:202-217. 10.1093/mp/ssn067, 19825608.
28. Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. Protein degradation - an alternative respiratory substrate for stressed plants. Trends Plant Sci 2011, 16:489-498. 21684795.
29. Vanlerberghe GC, Day DA, Wiskich JT, Vanlerberghe AE, McIntosh L. Alternative oxidase activity in tobacco leaf mitochondria (dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation). Plant Physiol 1995, 109:353-361. 12228600.
30. Koprivova A, Mugford ST, Kopriva S. Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 2010, 29:1157-1167. 10.1007/s00299-010-0902-0, 20669021.
31. Paulose B, Chhikara S, Coomey J, Jung H-I, Vatamaniuk O, Dhankher OP. A γ-Glutamyl Cyclotransferase Protects Arabidopsis Plants from Heavy Metal Toxicity by Recycling Glutamate to Maintain Glutathione Homeostasis. Plant Cell 2013, 25:4580-4595. 10.1105/tpc.113.111815, 24214398.
32. Zhou X, Yuan Y, Yang Y, Rutzke M, Thannhauser TW, Kochian LV, Li L. Involvement of a broccoli COQ5 methyltransferase in the production of volatile selenium compounds. Plant Physiol 2009, 151:528-540. 10.1104/pp.109.142521, 19656903.
33. Bergamini C, Moruzzi N, Sblendido A, Lenaz G, Fato R. A water soluble CoQ10 formulation improves intracellular distribution and promotes mitochondrial respiration in cultured cells. PLoS One 2012, 7:e33712. 10.1371/journal.pone.0033712, 22432044.
34. Sharma SS, Dietz KJ. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 2006, 57:711-726. 10.1093/jxb/erj073, 16473893.
35. Grant K, Carey NM, Mendoza M, Schulze J, Pilon M, Pilon-Smits EA, van Hoewyk D. Adenosine 5'-phosphosulfate reductase (APR2) mutation in Arabidopsis implicates glutathione deficiency in selenate toxicity. Biochem J 2011, 438:325-335. 10.1042/BJ20110025, 21585336.
36. Van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EA. Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 2008, 132:236-253. 18251864.
37. Nikiforova V, Bielecka M, Gakiere B, Krueger S, Rinder J, Kempa S, Morcuende R, Scheible W-R, Hesse H, Hoefgen R. Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino Acids 2006, 30:173-183. 10.1007/s00726-005-0251-4, 16552493.
38. Fontaine JX, Terce-Laforgue T, Armengaud P, Clement G, Renou JP, Pelletier S, Catterou M, Azzopardi M, Gibon Y, Lea PJ, Hirel B, Dubois F. Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell 2012, 24:4044-4065. 10.1105/tpc.112.103689, 23054470.
39. Van Aken O, Zhang B, Carrie C, Uggalla V, Paynter E, Giraud E, Whelan J. Defining the mitochondrial stress response in Arabidopsis thaliana. Mol Plant 2009, 2:1310-1324. 10.1093/mp/ssp053, 19995732.
40. Palmieri L, Picault N, Arrigoni R, Besin E, Palmieri F, Hodges M. Molecular identification of three Arabidopsis thaliana mitochondrial dicarboxylate carrier isoforms: organ distribution, bacterial expression, reconstitution into liposomes and functional characterization. Biochem J 2008, 410:621-629. 10.1042/BJ20070867, 18039180.
41. Pilon-Smits EA, Quinn CF, Tapken W, Malagoli M, Schiavon M. Physiological functions of beneficial elements. Curr Opin Plant Biol 2009, 12:267-274. 10.1016/j.pbi.2009.04.009, 19477676.
42. Couée I, Sulmon C, Gouesbet G, El Amrani A. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 2006, 57:449-459. 10.1093/jxb/erj027, 16397003.
43. Hauschild R, von Schaewen A. Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato. Plant Physiol 2003, 133:47-62. 10.1104/pp.103.025676, 12970474.
44. Pena LB, Zawoznik MS, Tomaro ML, Gallego SM. Heavy metals effects on proteolytic system in sunflower leaves. Chemosphere 2008, 72:741-746. 10.1016/j.chemosphere.2008.03.024, 18462779.
45. Huang Q, Wang H, Perry SW, Figueiredo-Pereira ME. Negative regulation of 26S proteasome stability via calpain-mediated cleavage of Rpn10 subunit upon mitochondrial dysfunction in neurons. J Biol Chem 2013, 288:12161-12174. 10.1074/jbc.M113.464552, 23508964.
46. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH. Glutathione in plants: an integrated overview. Plant Cell Environ 2012, 35:454-484. 10.1111/j.1365-3040.2011.02400.x, 21777251.
47. Łabanowska M, Filek M, Kościelniak J, Kurdziel M, Kuliś E, Hartikainen H. The effects of short-term selenium stress on Polish and Finnish wheat seedlings-EPR, enzymatic and fluorescence studies. J Plant Physiol 2012, 169:275-284. 10.1016/j.jplph.2011.10.012, 22153751.
48. Inostroza-Blancheteau C, Reyes-Díaz M, Alberdi M, Godoy K, Rojas-Lillo Y, Cartes P, de la Luz Mora M. Influence of selenite on selenium uptake, differential antioxidant performance and gene expression of sulfate transporters in wheat genotypes. Plant Soil 2013, 369:47-59. 10.1007/s11104-012-1492-0.
49. Cartes P, Gianfreda L, Mora ML. Uptake of selenium and its antioxidant activity in ryegrass when applied as selenate and selenite forms. Plant Soil 2005, 276:359-367. 10.1007/s11104-005-5691-9.
50. Dutilleul C, Lelarge C, Prioul J-L, De Paepe R, Foyer CH, Noctor G. Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiol 2005, 139:64-78. 10.1104/pp.105.066399, 16126851.
51. White PJ, Bowen HC, Marshall B, Broadley MR. Extraordinary high leaf selenium to sulfur ratios define " Se-accumulator" plants. Ann Bot 2007, 100:111-118. 10.1093/aob/mcm084, 17525099.
52. Xu J, Zhu Y, Ge Q, Li Y, Sun J, Zhang Y, Liu X. Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. New Phytol 2012, 196:125-138. 10.1111/j.1469-8137.2012.04236.x, 22809437.
53. Jacoby RP, Millar AH, Taylor NL. Investigating the role of respiration in plant salinity tolerance by analyzing mitochondrial proteomes from wheat and a salinity-tolerant Amphiploid (wheat x Lophopyrum elongatum). J Proteome Res 2013, 12:4807-4829. 10.1021/pr400504a, 23895732.
54. Yang P, Fu H, Walker J, Papa CM, Smalle J, Ju YM, Vierstra RD. Purification of the Arabidopsis 26 S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms. J Biol Chem 2004, 279:6401-6413. 10.1074/jbc.M311977200, 14623884.