ROS and Regulation of Photosynthesis

  • Soumen Bhattacharjee


In plant, cell chloroplast is one of the prime locales for the formation of ROS and the origin of redox signal. Any redox imbalance in photosynthetic electron transport and photosynthetic carbon reduction cycle eventually causes generation of ROS in plants. An efficient antioxidative defense operates both at metabolic interface and at genetic level for processing ROS efficiently for the maintenance of redox homeostasis and ROS pool. The significance of antioxidative defense network in the maintenance of optimum photosynthetic rate has been revealed in many studies involving molecular genetics and proteomic approaches. Recent studies have confirmed that the internal redox state of some important components of Z-scheme electron carriers (plastoquinone, cytochrome b6f complex, etc.) affects chloroplast gene expression, hinting the significance of chloroplast redox signal in controlling photosynthesis. Additionally, through redox regulation, photosynthesis functions as sensors for environmental cues like excess photochemical energy. This in fact provides regulatory loop in which expression of photosynthetic genes is not only coupled with redox state of photosynthetic electron flow but also senses excess photochemical energy. So, keeping all these views under consideration, an effort has been made to describe the present concepts of the role of photosynthesis in the origin of oxidative stress and redox signaling.


Oxidative stress Photosynthesis Z-scheme regulation Photooxidative damage Redox signal 


  1. Alscher RG, Hess JL (1993) Antioxidants in higher plants. CRC Press, Boca RatonGoogle Scholar
  2. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefGoogle Scholar
  3. Baier M, Noctor G, Foyer CH, Dietz KJ (2000) Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol 124:823–832CrossRefGoogle Scholar
  4. Bartoli CG, Simontacchi M, Eduardo T, Beltrano J, Montaldi E, Pantarulo S (1999) Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 50:375–383CrossRefGoogle Scholar
  5. Bhattacharjee S (2012) An inductive pulse of hydrogen peroxide pretreatment restores redox homeostasis and mitigates oxidative membrane damage under extremes of temperature in two rice cultivars (Oryza sativa L., Cultivars Ratna and SR 26B). Plant Growth Regul 68:395–410CrossRefGoogle Scholar
  6. Bhattacharjee S (2014) Membrane lipid peroxidation and its conflict of interest: the two faces of oxidative stress. Curr Sci 107:1811–1823Google Scholar
  7. Bilger W, Björkman O (1994) Relationships among violaxanthin deepoxidation, thylakoid membrane conformation and non-photochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193:238–246CrossRefGoogle Scholar
  8. Bouvier F, d’Harlingue A, Hugueney P, Marin E, Marion-Poll A, Camara B (1996) Xanthophyll biosynthesis: cloning, expression, functional reconstitution and regulation of β-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum). J Biol Chem 271:28861–28867CrossRefGoogle Scholar
  9. Bratt CE, Arvidsson P-O, Carlsson M, Åkerlund H-E (1995) Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth Res 45:169–175CrossRefGoogle Scholar
  10. Bugos RC, Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci U S A 93:6320–6325CrossRefGoogle Scholar
  11. Bugos RC, Hieber AD, Yamamoto HY (1998) Xanthophyll-cycle enzymes are members of the lipocalin family, the first identified from plants. J Biol Chem 273:15321–15324CrossRefGoogle Scholar
  12. Della Penna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738CrossRefGoogle Scholar
  13. Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159CrossRefGoogle Scholar
  14. Dietz KJ, Horling F, Konig J, Baier M (2002) The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. J Exp Bot 53:1321–1329PubMedGoogle Scholar
  15. Foyer CH (1996) Oxygen metabolism and electron transport in photosynthesis. In: Scandalios J (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 587–621Google Scholar
  16. Foyer CH (1997) Oxygen metabolism and electron transport in photosynthesis. In: Scandalios J (ed) The molecular biology of free radical scavenging systems. Cold Spring Harbor Laboratory Press, New York, pp 587–621Google Scholar
  17. Foyer CH (2015) Redox homeostasis: opening up ascorbate transport. Nat Plants 1:14012CrossRefGoogle Scholar
  18. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefGoogle Scholar
  19. Foyer CH, Harbinson J (1999) Relationships between antioxidant metabolism and carotenoids in the regulation of photosynthesis. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The photochemistry of carotenoids. Kluwer Academic Publishers, Dordrecht, p 305Google Scholar
  20. Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364CrossRefGoogle Scholar
  21. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905CrossRefGoogle Scholar
  22. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100CrossRefGoogle Scholar
  23. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione associated mechanisms of acclimatory stress tolerance and signalling. Physiol Planta 100:241–254CrossRefGoogle Scholar
  24. Genty B, Harbinson J (1996) Regulation of light utilization for photosynthetic electron transport. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic Publishers, Dordrecht, pp 67–99Google Scholar
  25. Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Planta 99:197–209CrossRefGoogle Scholar
  26. Hager A, 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 192:581–589CrossRefGoogle Scholar
  27. Havaux M, Bonfils J-P, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol 124:273–284CrossRefGoogle Scholar
  28. Hideg É, Kalai T, Hideg K, Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37:11405–11411CrossRefGoogle Scholar
  29. Hideg E, Barta C, Kalai T, Vass M, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescence sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43:1154–1164CrossRefGoogle Scholar
  30. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230CrossRefGoogle Scholar
  31. Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154CrossRefGoogle Scholar
  32. Kanwischer M, Porfirova S, Bergmüller E, Dörmann P (2005) Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition, and oxidative stress. Plant Physiol 137:713–723CrossRefGoogle Scholar
  33. Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574CrossRefGoogle Scholar
  34. Krause GH (1994) Photoinhibition induced by low temperatures. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. Bios Scientific, Oxford, pp 331–342Google Scholar
  35. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564CrossRefGoogle Scholar
  36. Mehler AH (1951) Studies of reactions of illuminated chloroplasts. 10. Mechanics of reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77CrossRefGoogle Scholar
  37. Munekage YN, Genty B, Peltier G (2008) Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol 49:1688–1698CrossRefGoogle Scholar
  38. Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134CrossRefGoogle Scholar
  39. Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Björkman O (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosyn Res 67:139–145CrossRefGoogle Scholar
  40. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol 49:249–279CrossRefGoogle Scholar
  41. Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647Google Scholar
  42. Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 270:14919–14927Google Scholar
  43. Queval G, Hager J, Gakie’re B, Noctor G (2008) Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts. J Exp Bot 59:135–146CrossRefGoogle Scholar
  44. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051CrossRefGoogle Scholar
  45. Russell AW, Critchley C, Robinson SA, Franklin LA, Seaton GGR, Chow W-S, Anderson J, Osmond CB (1995) Photosystem II regulation and dynamics of the chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition. Plant Physiol 107:943–952CrossRefGoogle Scholar
  46. Santos M, Gousseau H, Lister C, Foyer C, Creissen G, Mullineaux P (1996) Cytosolic ascorbate peroxidase from Arabidopsis thaliana L. is encoded by a small multigene family. Planta 1981(1):64–69Google Scholar
  47. Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489CrossRefGoogle Scholar
  48. Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467CrossRefGoogle Scholar
  49. Tardy F, Havaux M (1997) Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim Biophys Acta 4 1330(2):179–193CrossRefGoogle Scholar
  50. Vass I, Aro EM (2008) Photoinhibition of photosynthetic electron transport. In: Renger G (ed) Primary processes of photosynthesis: basic principles and apparatus. Royal Society of Chemistry, Cambridge, pp 393–411Google Scholar
  51. Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:200–205CrossRefGoogle Scholar
  52. Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236CrossRefGoogle Scholar

Copyright information

© Springer Nature India Private Limited 2019

Authors and Affiliations

  • Soumen Bhattacharjee
    • 1
  1. 1.Department of BotanyUGC Centre For Advanced Study, The University of BurdwanBurdwanIndia

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