Effect of Chlamydomonas plastid terminal oxidase 1 expressed in tobacco on photosynthetic electron transfer

Plant Journal

Volumn 85, Issue 2, 2016, Pages 219-228

  Feilke, Kathleen ^a   Streb, Peter ^b   Cornic, Gabriel ^b   Perreau, François ^c   Kruk, Jerzy ^d   Krieger Liszkay, Anja ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INSTITUT JEAN PIERRE BOURGIN   (France)

^d JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Chlamydomonas reinhardtii PTOX1; Nicotiana tabacum; photooxidative stress; photosynthetic electron transport; plastid terminal oxidase; regulation

Indexed keywords

ALKALINITY; BIOCHEMISTRY; CARBON DIOXIDE; ELECTRONS; HIGH PRESSURE LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MEMBRANES; PLANTS (BOTANY); SAFETY VALVES; TOBACCO;

CHLAMYDOMONAS REINHARDTII; NICOTIANA TABACUM; PHOTO-OXIDATIVE STRESS; PHOTOSYNTHETIC ELECTRON TRANSPORT; REGULATION; TERMINAL OXIDASE;

ELECTRON TRANSPORT PROPERTIES;

OXIDOREDUCTASE;

CHLAMYDOMONAS; ELECTRON TRANSPORT; ENZYMOLOGY; GENETICS; METABOLISM; PHOTOSYNTHESIS; PLASTID; TOBACCO; TRANSGENIC PLANT;

CHLAMYDOMONAS; ELECTRON TRANSPORT; OXIDOREDUCTASES; PHOTOSYNTHESIS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; TOBACCO;

EID: 84955614367     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13101     Document Type: Article

References (50)

1. Ahmad, N., Michoux, F., and, Nixon, P.J., (2012) Investigating the production of foreign membrane proteins in tobacco chloroplasts: expression of an algal plastid terminal oxidase. PLoS ONE, 7, e41722.
2. Aluru, M.R., and, Rodermel, S.R., (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol. Plant. 120, 4-11.
3. Bailey, S., Melis, A., Mackey, K.R.M., Cardol, P., Finazzi, G., van Dijken, G., Berg, G.M., Arrigo, K., Shrager, J., and, Grossman, A., (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim. Biophys. Acta, 1777, 269-276.
4. Berthold, D.A., Andersson, M.E., and, Nordlund, P., (2000) New insight into the structure and function of the alternative oxidase. Biochim. Biophys. Acta, 1460, 241-254.
5. Carol, P., Stevenson, D., Bisanz, C., Breitenbach, J., Sandmann, G., Mache, R., Coupland, G., and, Kuntz, M., (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell, 11, 57-68.
6. + channel controls photosynthetic light utilization in plants. Science, 342, 114-118.
7. Díaz, M., de Haro, V., Muñoz, R., and, Quiles, M.J., (2007) Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. Plant, Cell Environ. 30, 1578-1585.
8. Ericsson, T., (1994) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil, 168-169, 205-214.
9. Feilke, K., Yu, Q., Beyer, P., Sétif, P., and, Krieger-Liszkay, A., (2014) In vitro analysis of the plastid terminal oxidase in photosynthetic electron transport. Biochim. Biophys. Acta, 1837, 1684-1690.
10. Foyer, C.H., Neukermans, J., Queval, G., Noctor, G., and, Harbinson, J., (2012) Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 63, 1637-1661.
11. Fu, A., Park, S., and, Rodermel, S., (2005) Sequences required for the activity of PTOX (IMMUTANS), a plastid terminal oxidase in vitro and in planta mutagenesis of iron-binding sites and a conserved sequence that corresponds to exon 8. J. Biol. Chem. 280, 42489-42496.
12. Hager, A., and, Holocher, K., (1994) Localization of the xanthophyll-cycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta, 192, 581-589.
13. 2 solubilization in leaves. Plant Physiol. 108, 1059-1066.
14. Heldt, H.W., Werdan, K., Milovancev, M., and, Geller, G., (1973) Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim. Biophys. Acta, 314, 224-241.
15. Hernández, J.A., Corpas, F.J., Gõmez, M., del Río, L.A., and, Sevilla, F., (1993) Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol. Plant. 89, 103-110.
16. Heyno, E., Gross, C.M., Laureau, C., Culcasi, M., Pietri, S., and, Krieger-Liszkay, A., (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J. Biol. Chem. 284, 31174-31180.
17. Hieber, A.D., Bugos, R.C., Verhoeven, A.S., and, Yamamoto, H.Y., (2002) Overexpression of violaxanthin de-epoxidase: properties of C-terminal deletions on activity and pH-dependent lipid binding. Planta, 214, 476-483.
18. Houille-Vernes, L., Rappaport, F., Wollman, F.A., Alric, J., and, Johnson, X., (2011) Plastid Terminal Oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc. Natl Acad. Sci. USA, 108, 20820-20825.
19. Ibáñez, H., Ballester, A., Muñoz, R., and, José Quiles, M., (2010) Chlororespiration and tolerance to drought, heat and high illumination. J. Plant Physiol. 167, 732-738.
20. Ivanov, A.G., Rosso, D., Savitch, L.V., Stachula, P., Rosembert, M., Oquist, G., Hurry, V., and, Hüner, N.P.A., (2012) Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth. Res. 113, 191-206.
21. Joët, T., Genty, B., Josse, E.M., Kuntz, M., Cournac, L., and, Peltier, G., (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J. Biol. Chem. 277, 31623-31630.
22. Joliot, P., and, Johnson, G.N., (2011) Regulation of cyclic and linear electron flow in higher plants. Proc. Natl Acad. Sci. USA, 108, 13317-13322.
23. Josse, E.-M., Alcaraz, J.-P., Labouré, A.-M., and, Kuntz, M., (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur. J. Biochem. 270, 3787-3794.
24. 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.
25. Krieger, A., Bolte, S., Dietz, K.-J., and, Ducruet, J.-M., (1998) Thermoluminescence studies on the facultative crassulacean-acid- metabolism plant Mesembryanthemum crystallinum L. Planta, 205, 587-594.
26. Krieger-Liszkay, A., (2005) Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337-346.
27. Kruk, J., and, Karpinski, S., (2006) An HPLC-based method of estimation of the total redox state of plastoquinone in chloroplasts, the size of the photochemically active plastoquinone-pool and its redox state in thylakoids of Arabidopsis. Biochim. Biophys. Acta, 1757, 1669-1675.
28. Kuntz, M., (2004) Plastid terminal oxidase and its biological significance. Planta, 218, 896-899.
29. Laureau, C., De Paepe, R., Latouche, G., Moreno-Chacõn, M., Finazzi, G., Kuntz, M., Cornic, G., and, Streb, P., (2013) Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant, Cell Environ. 36, 1296-1310.
30. Lennon, A.M., Prommeenate, P., and, Nixon, P.J., (2003) Location, expression and orientation of the putative chlororespiratory enzymes, ndh and immutans, in higher-plant plastids. Planta, 218, 254-260.
31. Munné-Bosch, S., and, Alegre, L., (2002) The function of tocopherols and tocotrienols in plants. Crit. Rev. Plant Sci. 21, 31-57.
32. Nambara, E., and, Marion-Poll, A., (2005) Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 56, 165-185.
33. Nawrocki, W.J., Tourasse, N.J., Taly, A., Rappaport, F., and, Wollman, F.-A., (2015) The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu. Rev. Plant Biol. 66, 49-74.
34. Nordby, H.E., and, Yelenosky, G., (1985) Change in citrus leaf lipids during freeze-thaw stress. Phytochemistry, 24, 1675-1679.
35. 2 diffusion. J. Exp. Bot. 57, 3195-3207.
36. Quiles, M.J., (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant, Cell Environ. 29, 1463-1470.
37. Roncel, M., and, Ortega, J.M., (2005) Afterglow thermoluminescence band as a possible early indicator of changes in the photosynthetic electron transport in leaves. Photosynth. Res. 84, 167-172.
38. Rosso, D., Ivanov, A.G., Fu, A., et al,. (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol. 142, 574-585.
39. Rumeau, D., Peltier, G., and, Cournac, L., (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant, Cell Environ. 30, 1041-1051.
40. Schönknecht, G., Hedrich, R., Junge, W., and, Raschke, K., (1988) A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant. Nature, 336, 589-592.
41. Shahbazi, M., Gilbert, M., Labouré, A.-M., and, Kuntz, M., (2007) Dual role of the plastid terminal oxidase in tomato. Plant Physiol. 145, 691-702.
42. Stepien, P., and, Johnson, G.N., (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol. 149, 1154-1165.
43. Streb, P., Feierabend, J., and, Bligny, R., (1997) Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants. Plant, Cell Environ. 20, 1030-1040.
44. Streb, P., Josse, E.-M., Gallouët, E., Baptist, F., Kuntz, M., and, Cornic, G., (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant, Cell Environ. 28, 1123-1135.
45. Szymańska, R., and, Kruk, J., (2010) Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant Cell Physiol. 51, 537-545.
46. Tester, M., and, Blatt, M.R., (1989) Direct measurement of k channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant Physiol. 91, 249-252.
47. Trouillard, M., Shahbazi, M., Moyet, L., Rappaport, F., and, Joliot, P.A., (2012) Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim. Biophys. Acta, 1817, 2140-2148.
48. Wetzel, C.M., Jiang, C.-Z., Meehan, L.J., Voytas, D.F., and, Rodermel, S.R., (1994) Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J. 6, 161-175.
49. Wu, D., Wright, D.A., Wetzel, C., Voytas, D.F., and, Rodermel, S., (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell, 11, 43-55.
50. Yu, Q., Feilke, K., Krieger-Liszkay, A., and, Beyer, P., (2014) Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim. Biophys. Acta, 1837, 1284-1292.