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Protoplasma

, Volume 256, Issue 5, pp 1375–1383 | Cite as

Impact of antimycin A and myxothiazol on cadmium-induced superoxide, hydrogen peroxide, and nitric oxide generation in barley root tip

  • Veronika Zelinová
  • Loriana Demecsová
  • Ladislav TamásEmail author
Original Article

Abstract

In order to gain more insight into the involvement of mitochondrial complex III in the Cd-induced stress, we studied the effect of complex III inhibitors, antimycin A (AA), and myxothiazol (MYXO), on the Cd-induced ROS and NO generation in the barley root tip. Short-term exposure of barley roots to either MYXO or AA provoked a dose-dependent increase in both H2O2 and NO formation. In contrast to H2O2 generation, an enhanced superoxide formation in the transition zone of the root was a characteristic feature of AA-treated roots. MYXO and AA co-treatment had an additive effect on the amount of both H2O2 and NO formed in roots. On the other hand, AA-induced superoxide formation was markedly reversed in roots co-treated with MYXO. Both AA and MYXO exacerbated the Cd-mediated H2O2 or NO generation in the root tip. On the contrary, while AA also exacerbated the Cd-induced superoxide generation, MYXO dose-dependently attenuated it. These data provide strong evidence that ROS generation, a very early symptom of Cd toxicity in roots, is originated in mitochondria. Cd, similarly to AA, generates superoxide by blocking the mitochondrial electron transport chain (ETC) at complex III. In turn, the site of Cd-induced NO generation is not associated with complex III, but ROS formed in mitochondria at this third complex of ETC are probably responsible for enhanced NO generation in barley root under Cd stress.

Keywords

Barley Cadmium Hydrogen peroxide Mitochondrion Nitric oxide Superoxide 

Notes

Acknowledgements

The authors would also like to thank the anonymous reviewers for their helpful criticisms, which improved the manuscript.

Funding information

This work was supported by the Grant Agency VEGA, project No. 2/0039/16.

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Alber NA, Sivanesan H, Vanlerberghe GC (2017) The occurrence and control of nitric oxide generation by the plant mitochondrial electron transport chain. Plant Cell Environ 40:1074–1085CrossRefPubMedGoogle Scholar
  2. Alemayehu A, Zelinová V, Bočová B, Huttová J, Mistrík I, Tamás L (2015) Enhanced nitric oxide generation in root transition zone during the early stage of cadmium stress is required for maintaining root growth in barley. Plant Soil 390:213–222CrossRefGoogle Scholar
  3. Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, Pereira E, Ahmad I, Tuteja R, Tuteja N (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple and associated enzymes. Protoplasma 251:1265–1283CrossRefPubMedGoogle Scholar
  4. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Deckert J, Rucińska-Sobkowiak R, Gzyl J, Pawlak-Sprada S, Abramowski D, Jelonek T, Gwóźdź EA (2012) Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiol Biochem 58:124–134CrossRefPubMedGoogle Scholar
  5. Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou J-P, Pugin A, Wendehenne D (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 Physiol 149:1302–1315CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bi YH, Chen WL, Zhang WN, Zhou Q, Yun LJ, Xing D (2009) 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 101:629–643CrossRefPubMedGoogle Scholar
  7. Castro-Guerrero NA, Rodríguez-Zavala JS, Marín- Hernández A, Rodríguez-Enríquez S, Moreno-Sánchez R (2008) Enhanced alternative oxidase and antioxidant enzymes under Cd2+ stress in Euglena. J Bioenerg Biomembr 40:227–235CrossRefPubMedGoogle Scholar
  8. Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003a) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793CrossRefPubMedGoogle Scholar
  9. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003b) Production of reactive oxygen species by mitochondria. Central role of complex III. J Biol Chem 278:36027–36031CrossRefPubMedGoogle Scholar
  10. Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940CrossRefPubMedPubMedCentralGoogle Scholar
  11. De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanita di Toppi L, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fancy NN, Bahlmann A-K, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472CrossRefPubMedGoogle Scholar
  13. Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46CrossRefGoogle Scholar
  14. Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261CrossRefPubMedGoogle Scholar
  15. Gupta KJ, Igamberdiev AU (2016) Reactive nitrogen species in mitochondria and their implications in plant energy status and hypoxic stress tolerance. Front Plant Sci 7:369PubMedPubMedCentralGoogle Scholar
  16. Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168CrossRefPubMedGoogle Scholar
  17. Han D, Williams E, Cadenas E (2001) Mitochondrial respiratory chain-dependent generation of superoxde anion and its release into the intermembrane space. Biochem J 353:411–416CrossRefPubMedPubMedCentralGoogle Scholar
  18. Han FX, Banin A, Su Y, Monts DL, Plodinec MJ, Kingery WL, Triplett GE (2002) Industrial age anthropogenic inputs of heavy metals into the pedosphere. Naturwissenschaften 89:497–504CrossRefPubMedGoogle Scholar
  19. Han D, Antunes F, Canali R, Rettori D, Cadenas E (2003) Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 278:5557–5563CrossRefPubMedGoogle Scholar
  20. He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140CrossRefPubMedGoogle Scholar
  21. Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol 179:687–699CrossRefPubMedGoogle Scholar
  22. Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923CrossRefPubMedGoogle Scholar
  23. Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plant 138:393–404CrossRefPubMedGoogle Scholar
  24. Jones RD, Hancock JT, Morice AH (2000) NADPH oxidase: a universal oxygen sensor? Free Rad Biol Med 29:416–424CrossRefPubMedGoogle Scholar
  25. Keunen E, Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2013) Alternative respiration as a primary defence during cadmium-induced mitochondrial oxidative challenge in Arabidopsis thaliana. Environ Exp Bot 91:63–73CrossRefGoogle Scholar
  26. Khan MA, Khan S, Khan A, Alam M (2017) Soil contamination with cadmium, consequences and remediation using organic amendments. Sci Total Environ 601-602:1591–1605CrossRefPubMedGoogle Scholar
  27. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE (2009) Mitochondria and reactive oxygen species. Free Rad Biol Med 47:333–343CrossRefPubMedGoogle Scholar
  28. Kozlov AV, Staniek K, Nohl H (1999) Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett 454:127–130CrossRefPubMedGoogle Scholar
  29. Liptáková Ľ, Bočová B, Huttová J, Mistrík I, Tamás L (2012) Superoxide production induced by short-term exposure of barley roots to cadmium, auxin, alloxan and sodium dodecyl sulfate. Plant Cell Rep 31:2189–2197CrossRefPubMedGoogle Scholar
  30. Lum HK, Butt YKC, Lo SCL (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide 6:205–213CrossRefPubMedGoogle Scholar
  31. Mahawar L, Kumar R, Shekhawat GS (2018) Evaluation of heme oxygenase 1 (HO 1) in cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzymes in two to four leaf stage seedlings of Vigna radiata. Protoplasma 255:527–545CrossRefPubMedGoogle Scholar
  32. Mahmood T, Gupta KJ, Kaiser WM (2009) Cadmium stress stimulates nitric oxide production by wheat roots. Pak J Bot 41:1285–1290Google Scholar
  33. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15CrossRefPubMedGoogle Scholar
  34. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276CrossRefPubMedPubMedCentralGoogle Scholar
  35. Miccadei S, Floridi A (1993) Sites of inhibition of mitochondrial electron transport by cadmium. Chemico-Biol Interac 89:159–167CrossRefGoogle Scholar
  36. Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591CrossRefPubMedGoogle Scholar
  37. Muller F, Crofts AR, Kramer DM (2002) Multiple Q-cycle bypass reactions at the Q0 site of the cytochrome bc1 complex. Biochemistry 41:7866–7874CrossRefPubMedGoogle Scholar
  38. Muller FL, Liu Y, Van Remmen H (2004) Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279:49064–49073CrossRefPubMedGoogle Scholar
  39. Nohl H, Staniek K, Kozlov AV (2005) The existence and significance of a mitochondrial nitrite reductase. Redox Rep 10:281–286CrossRefPubMedGoogle Scholar
  40. Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ortega-Villasante C, Hernández LE, Rellán-Álvarez R, Del Campo FF, Carpena-Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176:96–107CrossRefPubMedGoogle Scholar
  42. Poderoso JJ, Lisdero C, Schöpfer F, Riobó N, Carreras MC, Cadenas E, Boveris A (1999) The regulation of mitochondrial oxygen uptake by redox reactions involving nitric oxide and ubiquinol. J Biol Chem 274:37709–37716CrossRefPubMedGoogle Scholar
  43. Raha S, McEachern GE, Myint AT, Robinson BH (2000) Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase. Free Rad Biol Med 29:170–180CrossRefPubMedGoogle Scholar
  44. Ranieri A, Castagna A, Scebba F, Careri M, Zagnoni I, Predieri G, Pagliari M, Sanita di Toppi L (2005) Oxidative stress and phytochelatin characterisation in bread wheat exposed to cadmium excess. Plant Physiol Biochem 43:45–54CrossRefPubMedGoogle Scholar
  45. Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126CrossRefPubMedGoogle Scholar
  46. Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in Populus canescens roots. Plant Physiol Biochem 40:577–584CrossRefGoogle Scholar
  47. Smiri M, Chaoui A, Rouhier N, Kamel C, Gelhaye E, Jacquot J-P, El Ferjani E (2010) Cadmium induced mitochondrial redox changes in germinating pea seed. Biometals 23:973–984CrossRefPubMedGoogle Scholar
  48. Srivastava RK, Rajpoot R, Pandey P, Rani A, Dubey RS (2018) Cadmium alters mitochondrial membrane potential, inhibits electron transport chain activity and induces callose deposition in rice seedlings. J Plant Growth Regul 37:335–344CrossRefGoogle Scholar
  49. Starkov AA, Fiskum G (2001) Myxothiazol induces H2O2 production from mitochondrial respiratory chain. Biochem Biophys Res Commun 281:645–650CrossRefPubMedGoogle Scholar
  50. Tamás L, Mistrík I, Zelinová V (2016) Cadmium activates both diphenyleneiodonium- and rotenone-sensitive superoxide production in barley root tips. Planta 244:1277–1287CrossRefPubMedGoogle Scholar
  51. Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals 26:255–269CrossRefPubMedGoogle Scholar
  52. Wang Y, Fang J, Leonard SS, Rao KMK (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Rad Biol Med 36:1434–1443CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Botany, Plant Science and Biodiversity CentreSlovak Academy of SciencesBratislavaSlovak Republic

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