Long-term sulphur starvation of Arabidopsis thaliana modifies mitochondrial ultrastructure and activity and changes tissue energy and redox status

Journal of Plant Physiology

Volumn 171, Issue 7, 2014, Pages 549-558

  Ostaszewska, Monika ^a   Juszczuk, Izabela M ^a   Kołodziejek, Izabella ^a   Rychter, Anna M ^a  

^a UNIVERSITY OF WARSAW   (Poland)

Author keywords

Energy status; Mitochondria ultrastructure; Redox homeostasis; Respiration; Sulphur deficiency

Indexed keywords

SULFUR;

ARABIDOPSIS; ARTICLE; BREATHING; DRUG EFFECT; ELECTRON TRANSPORT; ENERGY METABOLISM; ENERGY STATUS; METABOLISM; MITOCHONDRIA ULTRASTRUCTURE; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGICAL STRESS; REDOX HOMEOSTASIS; SULPHUR DEFICIENCY; ULTRASTRUCTURE;

ENERGY STATUS; MITOCHONDRIA ULTRASTRUCTURE; REDOX HOMEOSTASIS; RESPIRATION; SULPHUR DEFICIENCY;

ARABIDOPSIS; ELECTRON TRANSPORT; ENERGY METABOLISM; MITOCHONDRIA; OXIDATION-REDUCTION; STRESS, PHYSIOLOGICAL; SULFUR;

EID: 84896264442     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2013.12.013     Document Type: Article

References (64)

1. Albury M.S., Elliott C., Moore A.L. Towards a structural elucidation of the alternative oxidase in plants. Physiol Plant 2009, 137(4):316-327.
2. Balk J., Pilon M. Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci 2011, 16:218-226.
3. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 1976, 72:248-254.
4. Buescher E., Achberger T., Amusan I., Giannini A., Ochsenfeld C., Rus A., et al. Natural genetic variation in selected populations of Arabidopsis thaliana is associated with ionomic differences. PLoS One 2010, 5(6):e11081.
5. Dudkina N.V., Heinemeyer J., Sunderhaus S., Boekema E.J., Braun H.P. Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends Plant Sci 2006, 11(5):232-240.
6. Florez-Sarasa I., Ostaszewska M., Galle A., Flexas J., Rychter A.M., Ribas-Carbó M. Changes of alternative oxidase activity, capacity and protein content in leaves of Cucumis sativus wild type and MSC16 mutant grown under different light intensities. Physiol Plant 2009, 137(4):419-426.
7. Gardeström P., Wigge B. Influence of photorespiration on ATP/ADP ratios in the chloroplasts, mitochondria, and cytosol, studied by rapid fractionation of barley (Hordeum vulgare) protoplasts. Plant Physiol 1988, 88(1):69-76.
8. Gostimskaya I.S., Grivennikova V.G., Zharova T.V., Bakeeva L.E., Vinogradov A.D. In situ assay of the intramitochondrial enzymes: use of alamethicin for permeabilization of mitochondria. Anal Biochem 2003, 313:46-52.
9. Grose J.H., Joss L., Velick S.F., Roth J.R. Evidence that feedback inhibition of NAD kinase controls responses to oxidative stress. Proc Natl Acad Sci USA 2006, 103(20):7601-7606.
10. Gutierres S., Sabar M., Lelandais C., Chetrit P., Diolez P., Degand H., et al. Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 1997, 94:3436-3441.
11. Hawkesford M.J., Buchner P., Hopkins L., Howarth J.R. The plant sulfate transporter family: specialized functions and integration with whole plant nutrition. Sulfur transport and assimilation in plants: regulation, interaction and signalling 2003, 1-10. Backhuys Publishers, Leiden. J.C. Davidian, D. Grill, L.J. DeKok, I. Stulen, M.J. Hawkesford, E. Schnug, H. Rennenberg (Eds.).
12. Hayashi M., Takahashi H., Tamura K., Huang J., Yu L.H., Kawai-Yamada M., et al. Enhanced dihydroflavonol-4-reductase activity and NAD homeostasis leading to cell death tolerance in transgenic rice. Proc Natl Acad Sci USA 2005, 102:7020-7025.
13. Hell R., Wirtz M. Molecular biology, biochemistry and cellular physiology of cysteine metabolism in Arabidopsis thaliana. Arabidopsis Book 2011, 9:e0154.
14. Hoefnagel M.H.N., Atkin O., Wiskich J.T. Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta 1998, 1366:235-255.
15. Johansson F.I., Michalecka A.M., Møller I.M., Rasmusson A.G. Oxidation and reduction of pyridine nucleotides in alamethicin-permeabilised plant mitochondria. Biochem J 2004, 380:193-202.
16. Juszczuk I.M., Ostaszewska M. Respiratory activity, energy and redox status in sulphur-deficient bean plants. Environ Exp Bot 2011, 74:245-254.
17. Juszczuk I.M., Rychter A.M. The changes in pyridine nucleotide levels in leaves and roots of bean plants (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 1997, 151:399-404.
18. Juszczuk I.M., Flexas J., Szal B., Dabrowska Z., Ribas-Carbo M., Rychter A.M. Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration and energy status of MSC16 cucumber (Cucumis sativus) mutant. Physiol Plant 2007, 131:527-541.
19. Kandlbinder A., Finkemeier I., Wormuth D., Hanitzsch M., Dietz K.J. The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 2004, 120(1):63-73.
20. Kunst A., Draeger B., Ziegenhorn J. Colorimertic methods with glucose oxidase and peroxidase. Methods in enzymatic analysis. Metabolites 1: carbohydrates 1985, vol. VI:178-185. Verlag Chemie, Weinheim. 3rd ed.
21. + réduits et oxydés dans les tissus foliaires et dans les plastes isolés de Spirodéle et de Blé. 2. Méthode d'analyse des nucléotides pyridiniques de tissus végétaux. Physiol Vég 1977, 15:63-93.
22. Lewandowska M., Sirko A. Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim Polon 2008, 55(3):457-471.
23. Lichtenthaler H.K. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in enzymology 1987, 350-382. Academic Press Inc., New York. L. Packer, R. Douce (Eds.).
24. Lin T.I., Sled V.D., Ohnishi T., Brennicke A., Grohmann L. Analysis of the iron-sulphur clusters within the complex I (NADH:ubiquinone oxidoreductase) isolated from potato tuber mitochondria. Eur J Biochem 1995, 230:1032-1036.
25. Logan D.C. The mitochondrial compartment. J Exp Bot 2006, 57(6):1225-1243.
26. López-Bucio J., Cruz-Ramírez A., Herrera-Estrella L. The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 2003, 6(3):280-287.
27. Ludin A. Use of firefly luciferase in ATP-related assays of biomass, enzymes, and metabolites. Method Enzymol 2000, 305:346-370.
28. Mikulska M., Bomsel J.L., Rychter A.M. The influence of phosphate deficiency on photosynthesis, respiration and adenine nucleotide pool in bean leaves. Photosynthetica 1998, 35(1):79-88.
29. Moore C.S., Cook-Johnson R.J., Rudhe C., Whelan J., Day D.A., Wiskich J.T., Soole K.L. Identification of AtNDI1, an internal non-phosphorylating NAD(P)H dehydrogenase in Arabidopsis mitochondria. Plant Physiol 2003, 133:1968-1978.
30. Nikiforova V.J., Freitag J., Kempa S., Adamik M., Hesse H., Hoefgen R. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 2003, 33:633-650.
31. Nikiforova V.J., Kopka J., Tolstikov V., Fiehn O., Hopkins L., Hawkesford M.J., et al. System rebalancing of metabolism in response to sulphur deprivation, as related by metabolome analysis of Arabidopsis plants. Plant Physiol 2005, 138:304-318.
32. Nishimura M., Douce R., Akazawa T. Isolation and characterization of metabolically competent mitochondria from spinach leaf protoplasts. Plant Physiol 1982, 69:916-920.
33. Noctor G., Queval G., Gakière B. NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. J Exp Bot 2006, 57(8):1603-1620.
34. Ohnishi T. Iron-sulfur clusters/semiquinones in complex I. Biochim Biophys Acta 1998, 1364:186-206.
35. Pacyna S., Schulz M., Scherer H.W. Influence of sulphur supply on glucose and ATP concentrations of inoculated broad beans (Vicia faba minor L.). Biol Fert Soils 2006, 42:324-329.
36. Pascal N., Douce R. Effect of iron deficiency on the respiration of sycamore (Acer pseudoplatanus L.) cells. Plant Physiol 1993, 103:1329-1338.
37. Prinzenberg A.E., Barbier H., Salt D.E., Stich B., Reymond M. Relationships between growth, growth response to nutrient supply, and ion content using a recombinant inbred line population in Arabidopsis. Plant Physiol 2010, 154(3):1361-1371.
38. Rasmusson A.G., Wallström S.V. Involvement of mitochondria in the control of plant cell NAD(P)H reduction levels. Biochem Soc Trans 2010, 38(2):661-666.
39. Rasmusson A.G., Geisler D.A., Møller I.M. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 2008, 8:47-60.
40. Rasmusson A.G., Fernie A.R., van Dongen J.T. Alternative oxidase: a defence against metabolic fluctuations?. Physiol Plant 2009, 137:371-382.
41. Rasmusson A.G., Soole K.L., Elthon T.E. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 2004, 55:23-39.
42. Ribas-Carbó M., Lennon A.M., Robinson S.A., Giles L., Berry J.A., Siedow J.N. The regulation of electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiol 1997, 113:903-911.
43. Ruiz J.M., Sánchez E., García P.C., López-Lefebre L.R., Rivero R.M., Romero L. Proline metabolism and NAD kinase activity in greenbean plants subjected to cold-shock. Phytochemistry 2002, 59(5):473-478.
44. Rychter A.M., Mikulska M. The relationship between phosphate status and cyanide-resistant respiration in bean roots. Physiol Plant 1990, 79(4):663-667.
45. 2 fixation of peas (Pisum sativum L.) and alfalfa (Medicago sativa L.) under S deficiency conditions. Biol Fert Soils 2008, 44:909-916.
46. Shi F., Li Y., Li Y., Wang X. Molecular properties, functions, and potential applications of NAD kinases. Acta Biochim Biophys Sin 2009, 352-361.
47. Shinmachi F., Buchner P., Stroud J.L., Parmar S., Zhao F.J., McGrath S.P., Hawkesford M.J. Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium, and molybdenum in wheat. Plant Physiol 2010, 153(1):327-336.
48. Suzuki N., Koussevitzky S., Mittler R., Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012, 35(2):259-270.
49. Szal B., Dabrowska Z., Malmberg G., Gardeström P., Rychter A.M. Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement. Planta 2008, 227:697-706.
50. Tewari R.K., Kumar P., Sharma P.N. Morphology and oxidative physiology of sulphur-deficient mulberry plants. Environ Exp Bot 2010, 68:301-308.
51. Trontin C., Tisné S., Bach L., Loudet O. What does Arabidopsis natural variation teach us (and does not teach us) about adaptation in plants?. Curr Opin Plant Biol 2011, 14(3):225-231.
52. Vernon L.P., Cardon S. Direct spectrophotometric measurement of photosystem I and photosystem II activities of photosynthetic membrane preparations from Cyanophora paradoxa, Phormidium laminosum, and spinach. Plant Physiol 1982, 70:442-445.
53. Vigani G. Discovering the role of mitochondria in the iron deficiency-induced metabolic responses of plants. J Plant Physiol 2012, 169(1):1-11.
54. Vigani G., Zocchi G. Effect of Fe deficiency on mitochondrial alternative NAD(P)H dehydrogenases in cucumber roots. J Plant Physiol 2010, 167:666-669.
55. Vigani G., Maffi D., Zocchi G. Iron availability affects the function of mitochondria in cucumber roots. New Phytol 2009, 182:127-136.
56. Wang S., Liang D., Li C., Hao Y., Ma F., Shu H. Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks. Plant Physiol Biochem 2012, 51:81-89.
57. Wanke M., Ciereszko I., Podbielkowska M., Rychter A.M. Response to phosphate deficiency in bean (Phaseolus vulgaris L.) roots. Respiratory metabolism, sugar localization and changes in ultrastructure of bean root cells. Ann Bot 1998, 82:809-819.
58. Wigge B., Gardeström P. The effects of different ionic conditions on the activity of cytochrome c-oxidase in purified plant mitochondria. Plant mitochondria 1987, 127-130. Plenum Press, New York. A.L. Moore, R.B. Beachy (Eds.).
59. Wulff-Zottele C., Gatzke N., Kopka J., Orellana A., Hoefgen R., Fisahn J., Hesse H. Photosynthesis and metabolism interact during acclimation of Arabidopsis thaliana to high irradiance and sulphur depletion. Plant Cell Environ 2010, 33:1974-1988.
60. Yi H., Galant A., Ravilious G.E., Preuss M.L., Jez J.M. Sensing sulphur conditions: simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol Plant 2010, 3:269-279.
61. Yoshimoto N., Inoue E., Watanabe-Takahashi A., Saito K., Takahashi H. Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 2007, 145(2):378-388.
62. Zhang J., Sun X., Zhang Z., Ni Y., Zhang Q., Liang X., et al. Metabolite profiling of Arabidopsis seedlings in response to exogenous sinalbin and sulfur deficiency. Phytochemistry 2011, 72(14-15):1767-1778.
63. Zhang S., Chen F., Peng S., Ma W., Korpelainen H., Li C. Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress. Proteomics 2010, 10(14):2661-2677.
64. Zuchi S., Cesco S., Varanini Z., Pinton R., Astolfi S. Sulphur deprivation limits Fe-deficiency responses in tomato plants. Planta 2009, 230:85-94.