Determining light suppression of mitochondrial respiration for three temperate marine macrophytes using the Kok method

Lina M. Rasmussonhttp://orcid.org/0000-0003-4297-0956 1  and Mats Björk 1
  • 1 Department of Ecology, Environment and Plant Sciences, Stockholm University, S-106 91 Stockholm, Sweden
Lina M. RasmussonORCID iD: http://orcid.org/0000-0003-4297-0956 and Mats Björk

Abstract

To properly calculate the carbon budgets of coastal marine habitats, potential fluctuations in oxygen consumption due to mitochondrial respiration must be taken into account. As mitochondrial respiration is sometimes inhibited in light, we used the Kok method to estimate whether such suppression occurs in the seagrasses Zostera marina and Ruppia maritima as well as in the macroalga Ulva intestinalis. For Z. marina and U. intestinalis, the respiration rate was clearly downregulated in light, a finding that might be important when determining the impact of respiration on estimated net primary productivity in these marine habitats.

  • Amthor, J.S. 2000. The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann. Bot. 86: 1–20.

    • Crossref
  • Atkin, O.K., J.R. Evans, M.C. Ball, H. Lambers and L.P. Thijs. 2000. Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. Plant Physiol. 122: 915–923.

    • Crossref
  • Barrón, C., C.M. Duarte, M. Frankignoulle and A. Vieira Borges. 2006. Organic carbon metabolism and carbonate dynamics in a Mediterranean seagrass (Posidonia oceanica) meadow. Estuaries Coasts 29: 417–425.

    • Crossref
  • Björk, M., F. Short, E. Mcleod and S. Beer. 2008. Managing seagrasses for resilience to climate change. IUCN, Gland, Switzerland. pp. 56.

  • Brooks, A. and G.D. Farquhar. 1985. Effect of temperature on the CO2/O2 specificity of ribulose-1,5-biphosphate carboxylase/oxygenase and the rate of respiration in the light-estimates from gas-exchange measurements on spinach. Planta 165: 397–406.

  • Bruhn, D., T.N. Mikkelsen, M. Herbst, W.L. Kutsch, M. Ball and K. Pilegaard. 2011. Estimating daytime ecosystem respiration from eddy-flux data. Biosystems 103: 309–313.

    • Crossref
  • Buapet, P., M. Gullström and M. Björk. 2013. 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.

    • Crossref
  • Budde, J.A. and D.D. Randall. 1990. Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner. Proc. Natl. Acad. Sci. USA 87: 673–676.

    • Crossref
  • Duarte, C.M., N. Marbà, E. Gacia, J.W. Fourqurean, J. Beggins, C. Barrón and E.T. Apostolaki. 2010. Seagrass community metabolism: assessing the carbon sink capacity of seagrass meadows. Global Biogeochem. Cycles 24, GB4032 24.

  • Gemel, J. and D.D. Randall. 1992. Light regulation of leaf mitochondrial pyruvate dehydrogenase complex. Role of photorespiratory carbon metabolism. Plant Physiol. 100: 908–914.

    • Crossref
    • PubMed
  • Green, E.P. and F.T. Short. 2003. World atlas of seagrasses. University of California Press, Los Angeles. pp. 310.

  • Hemminga, M.A. and C.M. Duarte. 2000. Seagrass ecology: an introduction. Cambridge University Press, Cambridge. pp. 298.

  • Hurry, V., A.U. Igamberdiev, O. Keerberg, T. Pärnik, O.K. Atkin, J. Zaragoza-Castells and P. Gardeström. 2005. Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. In: (H. Lambers and M. Ribas-Carbo, eds.) Plant respiration: from cell to ecosystem. Springer, Dordrecht. pp. 43–61.

  • Igamberdiev, A.U. and P. Gardeström. 2003. Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim. Biophys. Acta 1606: 117–125.

    • Crossref
    • PubMed
  • Kennedy, H. and M. Björk. 2009. Seagrass meadows. In: (D. d’A. Laffoley and G. Grimsditch, eds.) The management of natural coastal carbon sinks. IUCN, Gland. pp. 23–29.

  • Kennedy, H., J. Beggins, C.M. Duarte, J.W. Fourqurean, M. Holmer, N. Marbà and J.J Middelburg. 2010. Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochem. Cycles 24, GB4026.

  • Kok, B. 1948. A critical consideration of the quantum yield of Chlorella photosynthesis. Enzymology 13: 1–56.

  • Krömer, S. 1995. Respiration during photosynthesis. Ann. Rev. Plant Physiol. Plant Mol. Biol. 46: 45–70.

    • Crossref
  • Laisk, A.K. 1977. Kinetics of photosynthesis and photorespiration in C3 plants. Nauka, Moscow (in Russian).

  • Laisk, A.K. and F. Loreto. 1996. Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence. Plant Physiol. 110: 903–912.

    • Crossref
  • McCashin, B.G., E.A. Cossins and D.T. Canvin. 1988. Dark respiration during photosynthesis in wheat leaf slices. Plant Physiol. 87: 155–161.

    • Crossref
  • Middelburg, J.J., C.M. Duarte and J.-P. Gattuso. 2005. Respiration in coastal benthic communities. In: (P.A. del Giorgio and P.J. le B Williams, eds.) Respiration in aquatic ecosystems. Oxford University Press, New York. pp. 206–224.

  • Padmavathi, L. and A.S. Raghavendra. 2001. Importance of the cytochrome pathway of mitochondrial electron transport over the alternative pathway during the Kok effect in leaf discs of pea (Pisum sativum). Physiol. Plant 113: 430–434.

    • Crossref
  • Raghavendra, A.S., K. Padmasree and K. Saradadevi. 1994. Interdependence of photosynthesis and respiration in plant cells: interactions between chloroplasts and mitochondria. Plant Sci. 97: 1–14.

    • Crossref
  • Ribas-Carbo, M., J. Flexas, S.A. Robinson and G.G.B. Tcherkez. 2010. Essay 11.9: in vivo measurement of plant respiration. Plant Physiol. Online: http://5e.plantphys.net/article.php?id=480.

  • Ryan, M.G. 1991. Effects of climate change on respiration. Ecol. Appl. 1: 157–167.

    • Crossref
  • Shapiro, J.B., K.L. Griffin, J.D. Lewis and D.T. Tissue. 2004. Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature. New Phytol. 162: 377–386.

  • Sharp, R.E., M.A. Matthews and J.S. Boyer. 1984. Kok effect and the quantum yield of photosynthesis. Light partially inhibits dark respiration. Plant Physiol. 75: 95–101.

    • Crossref
  • Tcherkez, G., G. Cornic, R. Bligny, E. Gout and J. Ghashghaie. 2005. In vivo respiratory metabolism of illuminated leaves. Plant Physiol. 138: 1596–1606.

    • Crossref
  • Tcherkez, G., R. Bligny, E. Gout, A. Mahé, M. Hodges and G. Cornic. 2008. Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proc. Natl. Acad. Sci. USA 105: 797–802.

    • Crossref
  • Tcherkez, G., E. Boex-Fontvieille, A. Mahé and M. Hodges. 2012a. Respiratory carbon fluxes in leaves. Curr. Opin. Plant Biol. 15: 308–314.

    • Crossref
    • PubMed
  • Tcherkez, G., A. Mahé, F. Guérard, E.R.A. Boex-Fontvieille, E. Gout, M. Lamothe, M.M. Barbour and R. Bligny. 2012b. Short-term effects of CO2 and O2 on citrate metabolism in illuminated leaves. Plant Cell Environ. 35: 2208–2220.

    • Crossref
    • PubMed
  • Tovar-Méndez, A., J.A. Miernyk and D.D. Randall. 2003. Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur. J. Biochem. 270: 1043–1049.

    • Crossref
  • Villar, R., A.A. Held and J. Merino. 1994. Comparison of methods to estimate dark respiration in the light in leaves of two woody species. Plant Physiol. 105: 167–172.

    • Crossref
  • Yin, X., Z. Sun, P.C. Struik and J. Gu. 2011. Evaluating a new method to estimate the rate of leaf respiration in the light by analysis of combined gas exchange and chlorophyll fluorescence measurements. J. Exp. Bot. 62: 3489–3499.

    • Crossref
  • Zou, D., K. Gao, J. Xia, X. Zhang and S. Liu. 2007. Responses of dark respiration in the light to desiccation and temperature in the intertidal macroalga, Ulva lactuca (Chlorophyta) during emersion. Phycologia 46: 363–370.

  • Zou, D., K. Gao and J. Xia. 2011. Dark respiration in the light and in darkness of three marine macroalgal species grown under ambient and elevated CO2 concentrations. Acta Oceanol. Sin. 30: 1–7.

    • Crossref
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