Skip to main content
SpringerLink
Log in

The role of O2 as an electron acceptor alternative to CO2 in photosynthesis of the common marine angiosperm Zostera marina L.

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

This study investigates the role of O2 as an electron acceptor alternative to CO2 in photosynthesis of the common marine angiosperm Zostera marina L. Electron transport rates (ETRs) and non-photochemical quenching (NPQ) of Z. marina were measured under saturating irradiance in synthetic seawater containing 2.2 mM DIC and no DIC with different O2 levels (air-equilibrated levels, 3 % of air equilibrium and restored air-equilibrated levels). Lowering O2 did not affect ETR when DIC was provided, while it caused a decrease in ETR and an increase in NPQ in DIC-free media, indicating that O2 acted as an alternative electron acceptor under low DIC. The ETR and NPQ as a function of irradiance were subsequently assessed in synthetic seawater containing (1) 2.2 mM DIC, air-equilibrated O2; (2) saturating CO2, no O2; and (3) no DIC, air-equilibrated O2. These treatments were combined with glycolaldehyde pre-incubation. Glycolaldehyde caused a marked decrease in ETR in DIC-free medium, indicating significant electron flow supported by photorespiration. Combining glycolaldehyde with O2 depletion completely suppressed ETR suggesting the operation of the Mehler reaction, a possibility supported by the photosynthesis-dependent superoxide production. However, no notable effect of suppressing the Mehler reaction on NPQ was observed. It is concluded that during DIC-limiting conditions, such as those frequently occurring in the habitats of Z. marina, captured light energy exceeds what is utilised for the assimilation of available carbon, and photorespiration is a major alternative electron acceptor, while the contribution of the Mehler reaction is minor.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abel KM, Drew EA (1989) Carbon metabolism. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, pp 760–796

    Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Avenson TJ, Cruz JA, Kanazawa A, Kramer DM (2005) Regulating the proton budget of higher plant photosynthesis. Proc Natl Acad Sci USA 102:9709–9713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc Lond B Biol Sci 355:1433–1445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beer S (1989) Photosynthesis and photorespiration in marine angiosperms. Aquat Bot 34:153–166

    Article  CAS  Google Scholar 

  • Beer S, Björk M (2000) Measuring rates of photosynthesis of two tropical seagrasses by pulse amplitude modulated (PAM) fluorometry. Aquat Bot 66:69–76

    Article  CAS  Google Scholar 

  • Beer S, Rehnberg J (1997) The acquisition of inorganic carbon by the seagrass Zostera marina. Aquat Bot 56:277–283

    Article  CAS  Google Scholar 

  • Beer S, Wetzel RG (1982) Photosynthetic carbon fixation pathways in Zostera marina and 3 Florida seagrasses. Aquat Bot 13:141–146

    Article  CAS  Google Scholar 

  • Beer S, Vilenkin B, Weil A, Veste M, Susel L, Eshel A (1998) Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry. Mar Ecol Prog Ser 174:293–300

    Article  CAS  Google Scholar 

  • Beer S, Björk M, Hellblom F, Axelsson L (2002) Inorganic carbon utilisation in marine angiosperms (seagrasses). Funct Plant Biol 29:349–354

    Article  CAS  Google Scholar 

  • Beer S, Axelsson L, Björk M (2006) Modes of photosynthetic bicarbonate utilisation in seagrasses, and their possible roles in adaptations to specific habitats. Biol Mar Medit 13:3–7

    Google Scholar 

  • Black CC, Burris JE, Everson RG (1976) The influence of oxygen concentration on photosynthesis in marine plants. Aust J Plant Physiol 3:81–86

    Article  CAS  Google Scholar 

  • Buapet P, Rasmusson LM, Gullström M, Björk M (2013a) Photorespiration and carbon limitation determine productivity in temperate seagrasses. PLoS ONE 8(12):e83804. doi:10.1371/journal.pone.0083804

    Article  PubMed  PubMed Central  Google Scholar 

  • Buapet P, Gullström M, Björk M (2013b) Photosynthetic activity of seagrasses and macroalgae in temperate shallow waters can alter seawater pH and total inorganic carbon content at the scale of a coastal embayment. Mar Freshw Res 64:1040–1048

    Article  CAS  Google Scholar 

  • Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807:912–918

    Article  CAS  PubMed  Google Scholar 

  • Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–816

    Article  CAS  PubMed  Google Scholar 

  • Downton WJS, Bishop DG, Larkum AWD, Osmond CB (1976) Oxygen inhibition of photosynthetic oxygen evolution in marine plants. Aust J Plant Physiol 3:73–79

    Article  Google Scholar 

  • Driever SM, Baker NR (2011) The water–water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted. Plant Cell Environ 34:837–846

    Article  CAS  PubMed  Google Scholar 

  • Frankignoulle M, Distèche A (1984) CO2 chemistry in the water column above Posidonia seagrass bed and related air-sea exchanges. Oceanol Acta 7:209–219

    CAS  Google Scholar 

  • Frost-Christensen H, Sand-Jensen K (1992) The quantum efficiency of photosynthesis in macroalgae and submerged angiosperms. Oecologia 91:377–384

    Article  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114

    Article  CAS  PubMed  Google Scholar 

  • Heber U (2002) Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res 73:223–231

    Article  CAS  PubMed  Google Scholar 

  • Hellblom F, Beer S, Björk M, Axelsson L (2001) A buffer sensitive inorganic carbon utilisation system in Zostera marina. Aquat Bot 69:55–62

    Article  CAS  Google Scholar 

  • Heyno E, Gross CM, Laureau C, Culcasi M, Pietri S, Krieger-Liszkay A (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J Biol Chem 284:31174–31180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu YT, Lee TM (2010) Photosynthetic electron transport mediates the light-controlled up-regulation of expression of methionine sulfoxide reductase A and B from marine macroalga Ulva fasciata. J Phycol 46:112–122

    Article  CAS  Google Scholar 

  • Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci USA 99:12789–12794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer DM, Evans J (2011) Update: the importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci 8:27–32

    Article  CAS  PubMed  Google Scholar 

  • Laisk A, Edwards E (1998) Oxygen and electron flow in C4 photosynthesis: Mehler reaction, photorespiration and CO2 concentration in the bundle sheath. Planta 205:632–645

    Article  CAS  Google Scholar 

  • Laisk A, Eichelmann H, Oja V (2015) Oxidation of plastohydroquinone by photosystem II and by dioxygen in leaves. Biochim Biophys Acta 1847:565–575

    Article  CAS  PubMed  Google Scholar 

  • Laureau C, De Paepe R, Latouche G, Moreno-Chacón M, Finazzi G, Kuntz M, Cornic G, 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

    Article  CAS  PubMed  Google Scholar 

  • Lovelock CE, Winter K (1996) Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical tree species. Planta 198:580–587

    Article  CAS  Google Scholar 

  • Makino A, Miyake C, Yokota A (2002) Physiological functions of the water–water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves. Plant Cell Physiol 43:1017–1026

    Article  CAS  PubMed  Google Scholar 

  • Mass T, Genin A, Shavit U, Grinstein M, Tchernov D (2010) Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water. Proc Natl Acad Sci USA 107:2527–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Hüner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967

    Article  CAS  PubMed  Google Scholar 

  • Mehler AH (1957) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77

    Article  Google Scholar 

  • Menéndez M, Martinez M, Comin FA (2001) A comparative study of the effect of pH and inorganic carbon resources on the photosynthesis of three floating macroalgae species of a Mediterranean coastal lagoon. J Exp Mar Biol Ecol 256:123–136

    Article  PubMed  Google Scholar 

  • Middelboe AL, Hansen PJ (2007) High pH in shallow-water macroalgal habitats. Mar Ecol Prog Ser 338:107–117

    Article  CAS  Google Scholar 

  • Munekage Y, Hashimoto M, Miyaka C, Tomizawa KI, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in wheat leaves: A predominant role for photorespiration? Ann Bot 89:841–850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ochieng CA, Short FT, Walker D (2010) Photosynthetic and morphological responses of eelgrass (Zostera marina L.) to a gradient of light conditions. J Exp Mar Biol Ecol 382:117–124

    Article  CAS  Google Scholar 

  • Oja V, Eichelmann H, Laisk A (2011) The size of the lumenal proton pool in leaves during induction and steady-state photosynthesis. Photosynth Res 110:73–88

    Article  CAS  PubMed  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  CAS  PubMed  Google Scholar 

  • Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46:1351–1362

    Article  CAS  Google Scholar 

  • Panigrahi PK, Biswal UC (1979) Aging of chloroplasts in vitro II. Changes in absorption spectra and DCPIP Hill reaction. Plant Cell Physiol 20:781–787

    CAS  Google Scholar 

  • Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Proctor MCF, Smirnoff N (2011) Ecophysiology of photosynthesis in bryophytes: major roles for oxygen photoreduction and non-photochemical quenching? Physiol Plant 141:130–140

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Larkum AWD (2007) Are there ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations? Photosynth Res 94:31–42

    Article  CAS  PubMed  Google Scholar 

  • Roach T, Na CS, Krieger-Liszkay A (2015) High light-induced hydrogen peroxide production in Chlamydomonas reinhardtii is increased by high CO2 availability. Plant J 81:759–766

    Article  CAS  PubMed  Google Scholar 

  • Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368

    Article  CAS  PubMed  Google Scholar 

  • Saderne V, Fietzek P, Herman PMJ (2013) Extreme variations of pCO2 and pH in a macrophyte meadow of the Baltic Sea in summer: evidence of the effect of photosynthesis and local upwelling. PLoS ONE 8(4):e62689. doi:10.1371/journal.pone.0062689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanisms of nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293

    Article  CAS  PubMed  Google Scholar 

  • Semesi IS, Beer S, Björk M (2009) Seagrass photosynthesis controls rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow. Mar Ecol Prog Ser 382:41–47

    Article  CAS  Google Scholar 

  • Shirao M, Kuroki S, Kaneko K, Kinjo Y, Tsuyama M, Förster B, Takahashi S, Badger MR (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54:1152–1163

    Article  CAS  PubMed  Google Scholar 

  • Siebke K, Ghannoum O, Conroy JP, Badger MR, von Caemmerer S (2003) Photosynthetic oxygen exchange in C4 grasses: the role of oxygen as electron acceptor. Plant Cell Environ 26:1963–1972

    Article  CAS  Google Scholar 

  • Silva J, Santos R (2004) Can chlorophyll fluorescence be used to estimate photosynthetic production in the seagrass Zostera noltii? J Exp Mar Biol Ecol 307:207–216

    Article  CAS  Google Scholar 

  • Silva J, Sharon Y, Santos R, Beer S (2009) Measuring seagrass photosynthesis: methods and applications. Aquat Biol 7:127–141

    Article  Google Scholar 

  • Silva J, Barrote I, Costa MM, Albano S, Santos R (2013) Physiological responses of Zostera marina and Cymodocea nodosa to light-limitation stress. PLoS ONE 8(11):e81058. doi:10.1371/journal.pone.0081058

    Article  PubMed  PubMed Central  Google Scholar 

  • Stepien P, Johnson GN (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touchette BW, Burkholder JM (2000) Overview of the physiological ecology of carbon metabolism in seagrasses. J Exp Mar Biol Ecol 250:169–205

    Article  CAS  PubMed  Google Scholar 

  • Trouillard M, Shahbazi M, Moyet L, Rappaport F, Joliot P, Kuntz M, Finazzi G (2012) Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim Biophys Acta 1817:2140–2148

    Article  CAS  PubMed  Google Scholar 

  • Unsworth RKF, Collier CJ, Henderson GM, McKenzie LJ (2012) Tropical seagrass meadows modify seawater carbon chemistry: implications for coral reefs impacted by ocean acidification. Environ Res Lett 7:024026

    Article  Google Scholar 

  • Waring J, Klenell M, Bechtold U, Underwood GJC, Baker NR (2010) Light-induced responses of oxygen photoreduction, reactive oxygen species production and scavenging in two diatom species. J Phycol 46:1206–1217

    Article  Google Scholar 

  • Wiese C, Shi LB, Heber U (1998) Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation. Physiol Plant 102:437–446

    Article  CAS  Google Scholar 

  • Yu Q, Feilke K, Krieger-Liszkay A, Beyer P (2014) Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim Biophys 1837:1284–1292

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Martin Gullström and Maria Asplund for help collecting plant material. The authors also acknowledge the Kristineberg Marine Research Station at the Sven Lovén Centre for Marine Sciences for providing research facilities. This study was supported by funding to support internationalization and scientific renewal at the Lovén Centre from the Royal Swedish Academy of Sciences.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai, 90112, Songkhla, Thailand

    Pimchanok Buapet

  2. Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, SE-106 91, Sweden

    Mats Björk

Authors
  1. Pimchanok Buapet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mats Björk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pimchanok Buapet.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buapet, P., Björk, M. The role of O2 as an electron acceptor alternative to CO2 in photosynthesis of the common marine angiosperm Zostera marina L.. Photosynth Res 129, 59–69 (2016). https://doi.org/10.1007/s11120-016-0268-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-016-0268-4

Keywords

Search

Navigation