Polyamines in chemiosmosis in vivo: A cunning mechanism for the regulation of ATP synthesis during growth and stress

Frontiers in Plant Science

Volumn 5, Issue FEB, 2014, Pages

  Ioannidis, Nikolaos E ^a   Kotzabasis, Kiriakos ^a  

^a UNIVERSITY OF CRETE   (Greece)

Author keywords

ATP synthesis; Chloroplast; Photosynthesis; Polyamines; Proton motive force; Putrescine; Stress

Indexed keywords

EID: 84901036950     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00071     Document Type: Review

References (56)

1. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., et al. (2010a). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237-1249. doi: 10.1007/s00425-010-1130-0
2. Alcázar, R., Planas, J., Saxena, T., Zarza, X., Bortolotti, C., Cuevas, J., et al. (2010b). Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene. Plant Physiol. Biochem. 48, 547-552. doi: 10.1016/j.plaphy.2010.02.002
3. Alcázar, R., Marco, F., Cuevas, J. C., Patron, M., Ferrando, A., Carrasco, P., et al. (2006). Involvement of polyamines in plant response to abiotic stress. Biotechnol. Lett. 28, 1867-1876. doi: 10.1007/s10529-006-9179-3
4. Avenson, T. J., Cruz, J. A., Kanazawa, A., and Kramer, D. M. (2005). Regulating the proton budget of higher plant photosynthesis. Proc. Natl. Acad. Sci. U.S.A. 102, 9709-9713. doi: 10.1073/pnas.0503952102
5. Avenson, T. J., Cruz, J. A., and Kramer, D. M. (2004). Modulation of energy-dependent quenching of excitons in antennae of higher plants. Proc. Natl. Acad. Sci. U.S.A. 101, 5530-5535. doi: 10.1073/pnas.0401269101
6. Bagni, N., Ruiz-Carrasco, K., Franceschetti, M., Fornalè, S., Fornasiero, R. B., and Tassoni, A. (2006). Polyamine metabolism and biosynthetic gene expression in Arabidopsis thaliana under salt stress. Plant Physiol. Biochem. 44, 776-786. doi: 10.1016/j.plaphy.2006.10.011
7. Borrell, A., Culianez-Macia, F. A., Altabella, T., Besford, R. T., Flores, D., and Tiburcio, A. F. (1995). Arginine decarboxylase is localized in chloroplasts. Plant Physiol. 109, 771-776.
8. Capell, T., Bassie, L., and Christou, P. (2004). Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl. Acad. Sci. U.S.A. 101, 9909-9914. doi: 10.1073/pnas.0306974101
9. Cruz, J. A., Sacksteder, C., Kanazawa, A., and Kramer, D. M. (2001). Contribution of electric field Δψ to steady-state transthylakoid proton motive force in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by counterion fluxes. Biochemistry 40, 1226-1237. doi: 10.1021/bi0018741
10. Demetriou, G., Neonaki, C., Navakoudis, E., and Kotzabasis, K. (2007). Salt stress impact on the molecular structure und function of the photosynthetic apparatus-the protective role of polyamines. Biochim. Biophys. Acta 1767, 272-280. doi: 10.1016/j.bbabio.2007.02.020
11. Dromparis, P., and Michelakis, E. D. (2013). Mitochondria in vascular health and disease. Annu. Rev. Physiol. 75, 95-126. doi: 10.1146/annurev-physiol-030212-183804
12. Flores, H. E., and Galston, A. W. (1982). Polyamines and plant stress: activation of putrescine biosynthesis by osmotic shock. Science 217, 1259-1261. doi: 10.1126/science.217.4566.1259
13. Flores, H. E., and Galston, A. W. (1984). Osmotic stress-induced polyamine accumulation in cereal leaves. I. Physiological parameters of the response. Plant Physiol. 75, 102-109. doi: 10.1104/pp.75.1.102
14. Galston, A. W. (2001). Plant biology-retrospect and prospect. Curr. Sci. 80, 143-152.
15. Giersch, C., and Meyer, M. (1984). Effects of carboxylic ionophores and amines at low concentrations on phosphorylation rate, phosphorylation potential and proton motive force in chloroplasts. Bioelectrochem. Bioenerg. 12, 63-71. doi: 10.1016/0302-4598(84)85150-8
16. Guarino, L., and Cohen, S. S. (1979a). Mechanism of toxicity of putrescine in Anacystis nidulans. Proc. Natl. Acad. Sci. U.S.A. 76, 3660-3664. doi: 10.1073/pnas.76.8.3660
17. Guarino, L., and Cohen, S. S. (1979b). Uptake and accumulation of putrescine and its lethality in Anacystis nidulans. Proc. Natl. Acad. Sci. U.S.A. 76, 3184-3188. doi: 10.1073/pnas.76.7.3184
18. Hope, A. B. (2000). Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. Biochim. Biophys. Acta 1456, 5-26. doi: 10.1016/S0005-2728(99)00101-2
19. Hummel, I., Amrani, A. E., Gouesbet, G., Hennion, F., and Couée, I. (2004). Involvement of polyamines in the interacting effects of low temperature and mineral supply on Pringlea antiscorbutica (Kerguelen cabbage) seedlings. J. Exp. Bot. 55, 1125-1134. doi: 10.1093/jxb/erh126
20. Ioannidis, N. E., Cruz, J. A., Kotzabasis, K., and Kramer, D. M. (2012). Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS ONE 7:e29864. doi: 10.1371/journal.pone.0029864
21. Ioannidis, N. E., and Kotzabasis, K. (2007). Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim. Biophys. Acta 1767, 1372-1382. doi: 10.1007/s10545-008-1038-z
22. Ioannidis, N. E., Sfichi, L., and Kotzabasis, K. (2006). Putrescine stimulates chemiosmotic ATP synthesis. Biochim. Biophys. Acta 1757, 821-828. doi: 10.1016/j.bbabio.2006.05.034
23. Jänne, J., Pösö, H., and Raina, A. (1978). Polyamines in rapid growth and cancer. Biochim. Biophys. Acta 473, 241-293. doi: 10.1016/0304-419X(78)90015-X
24. Kasinathan, V., and Wingler, A. (2004). Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol. Plant. 121, 101-107. doi: 10.1111/j.0031-9317.2004.00309.x
25. Kotakis, C., Theodoropoulou, E., Tassis, K., Oustamanolakis, C., Ioannidis, N. E., and Kotzabasis, K. (2014). Putrescine, a fast-acting switch for tolerance against osmotic stress. J. Plant Physiol. 171, 48-51. doi: 10.1016/j.jplph.2013.09.015
26. Kramer, D. M., Avenson, T. J., and Edwards, G. E. (2004). Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci. 9, 349-357. doi: 10.1016/j.tplants.2004.05.001
27. Kramer, D. M., Cruz, J. A., and Kanazawa, A. (2003). Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 8, 27-32. doi: 10.1016/S1360-1385(02)00010-9.
28. Kramer, D. M., and Evans, J. R. (2011). The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155, 70-78. doi: 10.1104/pp.110.166652
29. Li, X.-P., Björkman, O., Shih, C., Grossman, A. R., Rosequist, M., Jansson, S., et al. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395. doi: 10.1038/35000131
30. Lütz, C., Navakoudis, E., Seidlitz, H. K., and Kotzabasis, K. (2005). Simulated solar irradiation with enhanced UV-B adjust plastid-and thylakoid-associated polyamine changes for UV-B protection. Biochim. Biophys. Acta 1710, 24-33. doi: 10.1016/j.bbabio.2005.09.001
31. Maiale, S., Sanchez, D. H., Guirda, A., Vidal, A., and Ruiz, O. (2004). Spermine accumulation under salt stress. J. Plant Physiol. 161, 35-42. doi: 10.1078/0176-1617-01167
32. Marco, F., Alcázar, R., Tiburcio, A. F., and Carrasco, P. (2011). Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS 15, 775-781. doi: 10.1089/omi.2011.0084
33. Mitchell, P. (1961). Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191, 144-148. doi: 10.1038/191144a0
34. Mitchell, P. (1978). Keilin's respiratory chain concept and its chemiosmotic consequences. Science 206, 1148-1159. doi: 10.1126/science.388618
35. Moschou, P. N., Paschalidis, K. A., and Roubelakis-Angelakis, K. A. (2008). Plant polyamine catabolism: The state of the art. Plant Signal. Behav. 3, 1061-1066. doi: 10.4161/psb.3.12.7172
36. Moschou, P. N., and Roubelakis-Angelakis, K. A. (2011). Characterization, assay, and substrate specificity of plant polyamine oxidases. Methods Mol. Biol. 720,183-194. doi: 10.1007/978-1-61779-034-8_11
37. Navakoudis, E., Lütz, C., Langebartels, C., Lütz-Meindl, U., and Kotzabasis, K. (2003). Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochim. Biophys. Acta 1621, 160-169. doi: 10.1016/S0304-4165(03)00056-4
38. Ort, D. R., Dilley, R. A., and Good N. E. (1976). Photophosphorylation as a function of illumination time. II. Effects of permeant buffers. Biochim. Biophys. Acta 449, 108-124. doi: 10.1016/0005-2728(76)90011-6
39. Pascal, A. A., Liu, Z., Broess, K., van Oort, B., van Amerongen, H., Wang, C., et al. (2005). Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436, 134-137. doi: 10.1038/nature03795
40. Paschalidis, K. A., and Roubelakis-Angelakis, K. A. (2005). Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant: correlations with age, cell division/expansion, and differentiation. Plant Physiol. 138, 142-152. doi: 10.1104/pp.104.055483
41. Pick, U., and Weiss M. (1988). The mechanism of stimulation of photophosphorylation by amines and by nigericin. Biochim. Biophys. Acta 934, 22-31. doi: 10.1016/0005-2728(88)90115-6
42. Richards, F. J., and Coleman, E. G. (1952). Occurrence of putrescine in potassium deficient barley. Nature 170, 460-461. doi: 10.1038/170460a0
43. Robinson, S. P., Downton, W. J. S., and Millhouse, J. A. (1983). Photosynthesis and ion content of leaves and isolated chloroplasts of salt-stressed spinach. Plant Physiol. 73, 238-242. doi: 10.1104/pp.73.2.238
44. Ruban, A. V., Berera, R., Ilioaia, C., van Stokkum, I. H., Kennis, J. T., Pascal, A. A., et al. (2007). Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575-578. doi: 10.1038/nature06262
45. Sacksteder, C. A., and Kramer, D. M. (2000). Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth. Res. 66, 145-158. doi: 10.1023/A:1010785912271
46. Schoenknecht, G., Hedfich, R., Junge, W., and Raschke, K. (1988). A voltage dependent chloride channel in the photosynthetic membrane of a higher plant. Nature 336, 589-592. doi: 10.1038/336589a0
47. Schuber, F. (1989). Influence of polyamines on membrane functions. Biochem. J. 260, 1-10.
48. Schuldiner, S., Rottenberg, H., and Avron M. (1972). Determination of ΔpH in chloroplasts. Fluorescent amines as a probe for the determination of ΔpH in chloroplasts. Eur. J. Biochem. 25, 64-70. doi: 10.1111/j.1432-1033.1972.tb01667.x
49. Sfakianaki, M., Sfichi, L., and Kotzabasis, K. (2006). The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature. J. Photochem. Photobiol. B Biol. 84, 181-188. doi: 10.1016/j.jphotobiol.2006.03.003
50. Sfichi, L., Ioannidis, N. E., and Kotzabasis, K. (2008). Fast and reversible response of thylakoid-associated polyamines during and after UV-B stress-a comparative study of the wild type and a mutant lacking chlorophyll b of unicellular green alga Scenedesmus obliquus. Planta 228, 341-353. doi: 10.1007/s00425-008-0741-1
51. Sigalat, C., Kouchkovsky, Y., Havaux, F., and Kouchkovsky, F. (1988). Shift from localized to delocalized protonic energy coupling in thylakoids by permeant amines. Biochim. Biophys. Acta 934, 375-388. doi: 10.1016/0005-2728(88)90095-3
52. Slater, E. C. (1987). The mechanism of the conservation of energy of biological oxidations. Eur. J. Biochem. 166, 489-504. doi: 10.1111/j.1432-1033.1987.tb13542.x
53. Takizawa, K., Cruz, J. A., Kanazawa, A., and Kramer, D. M. (2007). The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochim. Biophys. Acta 1767, 1233-1244. doi: 10.1016/j.bbabio.2007.07.006
54. Toninello, A., Di Lisa, F., Siliprandi, D., and Siliprandi, N. (1984). "Protective and restorative effects of spermine on the membrane potential of rat liver mitochondria, " in Advances in Polyamines in Biomedical Science, eds C. M. Caldarera and U. Bachrach (Bologna: CLUEB), 31-36.
55. Urano, K., Yoshiba, Y., Nanjo, T., Ito, T., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2004). Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem. Biophys. Res. Commun. 313, 369-375. doi: 10.1016/j.bbrc.2003.11.119
56. Williams, R. J. P. (1978). The history and the hypotheses concerning ATP-formation by energized protons. FEBS Lett. 85, 9-19. doi: 10.1016/0014-5793(78)81238-1