Viewing oxidative stress through the lens of oxidative signalling rather than damage

Biochemical Journal

Volumn 474, Issue 6, 2017, Pages 877-883

  Foyer, Christine H ^a   Ruban, Alexander V ^b   Noctor, Graham ^c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; REACTIVE OXYGEN METABOLITE; ADENOSINE TRIPHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PHOTOSYSTEM II;

CELL INTERACTION; COUPLING FACTOR; ELECTRON TRANSPORT; METABOLITE; NONPHOTOCHEMICAL QUENCHING; OXIDATIVE STRESS; PHOTOCHEMICAL QUENCHING; PHOTOINHIBITION; PHOTOSYSTEM II; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; AGONISTS; BIOSYNTHESIS; CHLOROPLAST; FLUORESCENCE; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHOTOTRANSDUCTION; PHYSIOLOGY; PLANT; RADIATION RESPONSE; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATE; CHLOROPHYLL; CHLOROPLASTS; FLUORESCENCE; LIGHT; LIGHT SIGNAL TRANSDUCTION; NADP; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS; REACTIVE OXYGEN SPECIES;

EID: 85016140584     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160814     Document Type: Review

References (53)

1. Jackson, M.J. (2008) Free radicals generated by contracting muscle: by-products of metabolism or key regulators of muscle function? Free Radic. Biol. Med. 44, 132-141 doi:10.1016/j.freeradbiomed.2007.06.003
2. Naviaux, R.K. (2012) Oxidative shielding or oxidative stress? J. Pharmacol. Exp. Ther. 342, 608-618 doi:10.1124/jpet.112.192120
3. Anderson, L.E. and Duggan, J.X. (1976) Light modulation of glucose 6-phosphate dehydrogenase. Partial characterisation of the light inactivation system and its effects on the properties of the chloroplastic and cytoplasmic forms of the enzyme. Plant Physiol. 58, 135-139 doi:10.1104/pp.58.2.135
4. Née, G., Zaffagnini, M., Trost, P. and Issakidis-Bourguet, E. (2009) Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: a new role for f-type thioredoxin. FEBS Lett. 583, 2827-2832 doi:10.1016/j.febslet.2009.07.035
5. Ahlfors, R., Macioszek, V., Rudd, J., Brosché, M., Schlichting, R., Scheel, D. et al. (2004) Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J. 40, 512-522 doi:10.1111/j.1365-313X.2004.02229.x
6. Overmyer, K., Brosché, M. and Kangasjärvi, J. (2003) Reactive oxygen species and the hormonal control of cell death. Trends Plant Sci. 8, 335-342 doi:10.1016/S1360-1385(03)00135-3
7. Bashandy, T., Guilleminot, J., Vernoux, T., Caparros-Ruiz, D., Ljung, K., Meyer, Y. et al. (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22, 376-391 doi:10.1105/tpc.109.071225
8. Achard, P., Renou, J.-P., Berthomé, R., Harberd, N.P. and Genschik, P. (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 18, 656-660 doi:10.1016/j.cub.2008.04.034
9. Zwack, P.J., De Clercq, I., Howton, T.C., Hallmark, H.T., Hurny, A., Keshishian, E.A. et al. (2016) Cytokinin response factor 6 represses cytokinin-associated genes during oxidative stress. Plant Physiol. 172, 1249-1258 doi:10.1104/pp.16.00415
10. Han, Y., Chaouch, S., Mhamdi, A., Queval, G., Zechmann, B. and Noctor, G. (2013) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid. Redox Signal. 18, 2106-2121 doi:10.1089/ars.2012.5052
11. Bigarella, C.L., Liang, R. and Ghaffari, S. (2014) Stem cells and the impact of ROS signalling. Development 141, 4206-4218 doi:10.1242/dev.107086
12. del Pozo, J.C. (2016) Reactive oxygen species: from harmful molecules to fine-tuning regulators of stem cell niche maintenance. PLoS Genet. 12, e1006251 doi:10.1371/journal.pgen.1006251
13. Considine, M.J., Diaz-Vivancos, P. Kerchev, P., Signorelli, S., Agudelo-Romero, P., Gibbs, D.J. et al. (2016) Learning to breathe: developmental phase transitions in oxygen status. Trends Plant Sci. doi: 10.1016/j.tplants.2016.11.013
14. Mohyeldin, A., Garzón-Muvdi, T. and Quiñones-Hinojosa, A. (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7, 150-161 doi:10.1016/j.stem.2010.07.007
15. Wagner, D., Przybyla, D., Op den Camp, R., Kim, C., Landgraf, F., Lee, K.P. et al. (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185 doi:10.1126/science.1103178
16. Chaouch, S., Queval, G., Vanderauwera, S., Mhamdi, A., Vandorpe, M., Langlois-Meurinne, M. et al. (2010) Peroxisomal H2O2 is coupled to biotic defense responses by ICS1 in a daylength-dependent manner. Plant Physiol. 153, 1692-1705 doi:10.1104/pp.110.153957
17. Li, S., Mhamdi, A., Trotta, A., Kangasjärvi, S. and Noctor, G. (2014) The protein phosphatase subunit PP2A-B'γ is required to suppress daylength-dependent pathogenesis responses triggered by intracellular oxidative stress. New Phytol. 202, 145-160 doi:10.1111/nph.12622
18. Waszczak, C., Kerchev, P.I., Mühlenbock, P., Hoeberichts, F.A., Van Der Kelen, K., Mhamdi, A. et al. (2016) SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. Plant Cell 28, 1844-1859 doi:10.1105/tpc.16. 00038
19. Mehler, A.H. (1951) Studies on reactions of illuminated chloroplasts. I. Mechanisms of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33, 65-77 doi:10.1016/0003-9861(51)90082-3
20. Asada, K., Kiso, K. and Yoshikawa, K. (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J. Biol. Chem. 249, 2175-2181 PMID:4362064
21. Foyer, C.H. and Noctor, G. (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875 doi:10.1105/tpc.105.033589
22. Foyer, C.H. and Noctor, G. (2016) Stress-triggered redox signalling: what's in pROSpect? Plant Cell Environ. 39, 951-964 doi:10.1111/pce.12621
23. Triantaphylidès, C. and Havaux, M. (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 14, 219-228 doi:10.1016/j.tplants.2009.01.008
24. Fischer, B.B., Hideg, É. and Krieger-Liszkay, A. (2013) Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid. Redox Signal. 18, 2145-2162 doi:10.1089/ars.2012.5124
25. Yamashita, A., Nijo, N., Pospíšil, P., Morita, N., Takenaka, D., Aminaka, R. et al. (2008) Quality control of photosystem II - reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress. J. Biol. Chem. 283, 28380-28391 doi:10.1074/jbc.M710465200
26. Allakhverdiev, S.I., Kreslavski, V.D., Klimov, V.V., Los, D.A., Carpentier, R. and Mohanty, P. (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosyn. Res. 98, 541-550 doi:10.1007/s11120-008-9331-0
27. 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 doi:10.1093/jxb/ers013
28. Barber, J. (1995) Molecular-basis of the vulnerability of photosystem-II to damage by light. Aust. J. Plant Physiol. 22, 201-208 doi:10.1071/PP9950201
29. Ohad, I., Kyle, D.J. and Arntzen, C.J. (1984) Membrane-protein damage and repair - removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J. Cell Biol. 99, 481-485 doi:10.1083/jcb.99.2.481
30. Powles, S.B. (1984) Photoinhibition of photosynthesis induced by visible-light. Annu. Rev. Plant Physiol. 35, 15-44 doi:10.1146/annurev.pp.35.060184.000311
31. Telfer, A., He, W.-Z. and Barber, J. (1990) Spectral resolution of more than one chlorophyll electron donor in the isolated photosystem-II reaction center complex. Biochim. Biophys. Acta, Bioenergetics 1017, 143-151 doi:10.1016/0005-2728(90)90145-T
32. De Las Rivas, J., Shipton, C.A., Ponticos, M. and Barber, J. (1993) Acceptor side mechanism of photoinduced proteolysis of the D1 protein in photosystem-II reaction centers. Biochemistry 32, 6944-6950 doi:10.1021/bi00078a019
33. Aro, E.-M., Virgin, I. and Andersson, B. (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta, Bioenergetics 1143, 113-134 doi:10.1016/0005-2728(93)90134-2
34. Demmig-Adams, B., Garab, G., Adams, III, W.W. and Govindgee (eds) (2014) Nonphotochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria, Advances in Photosynthesis and Respiration, vol. 40, Springer Netherlands
35. Ruban, A.V. (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol. 170, 1903-1916 doi:10.1104/pp.15.01935
36. Baker, N.R. and Horton, P. (1987) Physiological factors associated with fluorescence quenching during photoinhibition. In Topics in Photosynthesis, Photoinhibition (Arntzen, C.J., Kyle, D.J. and Osmond, C.B., eds.), vol. 9, pp. 145-168, Elsevier, Amsterdam
37. Krause, G.H. and Weis, E. (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313-349 doi:10.1146/annurev.pp.42.060191.001525
38. Demmig-Adams, B. and Adams, III, W.W. (1992) Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 599-626 doi:10.1146/annurev.pp.43.060192.003123
39. Jahns, P. and Holzwarth, A.R. (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim. Biophys. Acta, Bioenergetics 1817, 182-193 doi:10.1016/j.bbabio.2011.04.012
40. Adams, III, W.W., Demmig-Adams, B., Verhoeven, A.S. and Barker, D.H. (1995) 'Photoinhibition' during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Funct. Plant Physiol. 22, 261-276 doi:10.1071/PP9950261
41. Adams, III, W.W., Zarter, C.R., Mueh, K.E. and Demmig-Adams, B. (2008) Energy dissipation and photoinhibition: a continuum of photoprotection. In Photoprotection, Photoinhibition, Gene Regulation, and Environment (Demmig-Adams, B., Adams, III, W.W. and Mattoo A.K., eds.), pp. 49-64, Springer, The Netherlands
42. Demmig-Adams, B., Cohu, C.M., Muller, O. and Adams, III, W.W. (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth. Res. 113, 75-88 doi:10.1007/s11120-012-9761-6
43. Adams, III, W.W., Muller, O., Cohu, C.M. and Demmig-Adams, B. (2013) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth. Res. 117, 31-44 doi:10.1007/s11120-013-9849-7
44. Ruban, A.V. and Murchie, E.H. (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochim. Biophys. Acta, Bioenergetics 1817, 977-982 doi:10.1016/j.bbabio.2012.03.026
45. Ruban, A.V. and Belgio, E. (2014) The relationship between maximum tolerated light intensity and non-photochemical chlorophyll fluorescence quenching: chloroplast gains and losses. Philos. Trans. Roy. Soc. Lond. B, Biol. Sci. 369, 20130222 doi:10.1098/rstb.2013.0222
46. Oxborough, K. and Baker, N.R. (1997) Resolving chlorophyll a fluorescence of photosynthetic efficiency into photochemical components - calculation of qP and F0 v/F0 m without measuring Fo. Photosynth. Res. 54, 135-142 doi:10.1023/A:1005936823310
47. Ware, M.A., Belgio, E. and Ruban, A.V. (2015) Photoprotective capacity of nonphotochemical quenching in plants acclimated to different light intensities. Photosynth. Res. 126, 261-274 doi:10.1007/s11120-015-0102-4
48. Kromdijk, J., Głowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K. et al. (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857-861 doi:10.1126/science.aai8878
49. Creissen, G., Firmin, J., Fryer, M., Kular, B., Leyland, M., Reynolds, H. et al. (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco paradoxically causes increased oxidative stress. Plant Cell 11, 1277-1291 doi:10.1105/tpc.11.7.1277
50. Hackenberg, T., Juul, T., Auzina, A., Gwizdz, S., Małolepszy, A., Lehmann Nielsen, K. et al. (2013) Catalase and its regulator NO CATALASE ACTIVITY 1 (NCA1) promote autophagy-dependent cell death in Arabidopsis. Plant Cell 25, 4616-4626 doi:10.1105/tpc.113.117192
51. Johnston, E.J., Rylott, E.L., Beynon, E., Lorenz, A., Chechik, V. and Bruce, N.C. (2015) Monodehydroascorbate reductase mediates TNT toxicity in plants. Science 349, 1072-1075 doi:10.1126/science.aab3472
52. Noctor, G. (2015) Lighting the fuse on toxic TNT. An enzyme that helps control reactive oxidants sensitizes plants to TNT pollution. Science 349, 1052-1053 doi:10.1126/science.aad0941
53. Karki, S., Rizal, G. and Quick, W.P. (2013) Improvement of photosynthesis in rice (Oryza sativa L.) by inserting the C4 pathway. Rice 6, 28 doi:10.1186/1939-8433-6-28