Abstract
To investigate the effects of potassium on photosynthetic activity in the green alga Ulva pertusa, we enzymatically isolated protoplasts from thallus samples. Photochemical quenching showed that protoplasts were capable of electron transport by photosystem II (PS II) during illumination. This quenching was dependent on external pH, with a reduced electron transport rate at pH >6.8 and less ability to use HCO −3 under alkaline conditions. In the presence of external Na+, K+ enhanced PS II quantum yield, indicating a functional role for K+ during photosynthesis. That yield was enhanced in a [K+]-dependent manner, with maximum activity at 100 mM. However, potassium alone did not maintain photochemical activity, and its addition supported photosynthetic O2 evolution only in the presence of Na+. A deficiency of K+ led to the production of superoxide anions. Because of that generation, activities of superoxide dismutase and ascorbate peroxidase, two key enzymes involved in scavenging reactive oxygen species in the water–water cycle, also increased during such stress. These results strongly suggest that a series of ROS-scavenging systems are initiated in Ulva chloroplasts in response to K+ deficiency and that enzyme activities might protect algal cell photosynthesis.
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References
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Asada K (1999) The water-water cycle in chloroplast: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Axelson L, Mercado JM, Figuerosa FL (2000) Utilization of HCO3- at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35:53–59
Badger BMR, 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 355:1433–1446
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–281
Beer S, Israel A (1986) Photosynthetic Ulva sp. III. O2 effects, carboxylase activities, and the CO2 incorporation pattern. Plant Physiol 81:937–938
Beer S, Israel A (1990) Photosynthetic Ulva fasciata III. pH, carbonic anhydrase and inorganic carbon conversions in the unstirred layer. Plant Cell Environ 13:555–560
Blum DE, Elzenga JTM, Linnemeyer PA, van Volkenburgh E (1992) Stimulation of growth and ion uptake in bean leaves by red and blue light. Plant Physiol 100:1968–1975
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72:248–255
Burkhardt S, Amoroso G, Riebessell U, Sültemeyer D (2001) CO2 and HCO -3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46:1378–1391
Chen X, Gao K (2004) Photosynthetic utilization of inorganic carbon and its regulation in the marine diatom Skeletonema costatum. Funct Plant Biol 31:1027–1033
Chen X, Qiu CE, Shao JZ (2006) Evidence for K+-dependent HCO -3 utilization in the marine diatom Phaeodactylum tricornutum. Plant Physiol 141:731–736
Choi S, Jeong SJ, Jeong WJ, Kwon SY, Chow WS, Park YI (2002) Chloroplast Cu/Zn-superoxide dismutase is a highly sensitive site in cucumber leaves chilled in the light. Planta 216:315–324
Colman B (1984) The effect of temperature and oxygen on the CO2 compensation point of the marine alga Ulva lactuca. Plant Cell Environ 7:619–621
Darehshouri A, Lütz-Meindl U (2010) H2O2 localization in the green alga Micrasterias after salt and osmotic stress by TEM-coupled electron energy loss spectroscopy. Protoplasma 236:49–56
Dromgoole FI (1978) The effect of pH and inorganic carbon on photosynthesis and dark respiration of Carpophyllum (Fucales, Phaeophyceae). Aquat Bot 4:11–22
Elstner EF, Heupel A (1976) Oxygen activation by isolated chloroplasts from Euglena gracilis. Isolation and properties of a fluorescent compound that catalyzes monovalent oxygen reduction. Arch Biochem Biophys 173:614–622
Escassi L, Escassi L, Aguilera J, Figueroa FL, Fernández JA (2002) Potassium drives daily reversible thallus enlargement in the marine red alga Porphyra leucosticte (Rhodophyta). Planta 214:759–766
Espie GS, Kandasamy RA (1992) Na+-independent HCO -3 transport and accumulation in the cyanobacterium Synechococcus UTEX625. Plant Physiol 98:560–568
Friedlander M (2007) Advances in cultivation of Gelidiales. J Appl Phycol 20:451–456
Genty B, Briantais JM, Barker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Goh C-H, Tatsuo O, Shimazaki K (1995) Properties of proton pumping in response to blue light and fuscicoccin in guard cell protoplasts isolated from adaxial epidermis of Vicia leaves. Plant Physiol 109:187–194
Goh C-H, Schreiber U, Hedrich R (1999) New approach of monitoring changes in chlorophyll a fluorescence of single guard cells and protoplasts in response to physiological stimuli. Plant Cell Environ 22:1057–1070
James RA, Munns R, von Caemmerer S, Trejo C, Miller C, Condon TA (2006) Photosynthetic capacity is related to the cellular and subcellular portioning of Na+, K+ and Cl- in salt-affected barley and durum wheat. Plant Cell Environ 29:2185–2197
Kaplan A, Schwartz R, Lieman-Hurwitz J, Reinhold L (2006) Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol 97:851–855
Lu C, Vonshak A (2002) Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol Plant 114:405–413
Lüning K (1992) Day and night kinetics of growth rate in green, brown and red seaweeds. J Phycol 28:794–803
Lüning K, Titlyanov EA, Titlyanov TV (1997) Diurnal and circadian periodicity of mitosis and growth in marine macroalgae. III. The red alga Porphyra umbilicalis. Eur J Phycol 32:167–173
Maberly SG (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449
Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom, Phaeodactylum tricornutum. Plant Cell Environ 24:611–620
McNeil DL (1976) The basis of osmotic pressure maintenance during expansion growth in Helianthus annuus hypocotyls. Austr J Plant Physiol 3:311–324
Menendez M, Martnez 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 Expt Mar Biol Ecol 256:123–136
Naidoo G, Kift J (2006) Responses of the saltmarsh rush Juncus kraussii to salinity and waterlogging. Aquat Bot 84:217–225
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Pogoryelov D, Sudhir P-R, Kovács L, Gombos Z, Brown I, Garab G (2003) Sodium dependency of the photosynthetic electron transport in the alkaliphilic cyanobacterium Arthrospira platensis. J Bioenerg Biomembranes 35:427–437
Popelková H, Yocum H (2007) Current status of the role of Cl- ion in the oxygen-evolving complex. Photosynth Res 93:111–121
Ramani B, Reeck T, Debez A, Stelzer R, Huchzermeyer B, Schmidt A, Papenbrock J (2006) Aster tripolium L. and Sesuvium portulacastrum L.: two halophytes, two strategies to survive in saline habitats. Plant Physiol Biochem 44:395–408
Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27:85–183
Rees TAV (1984) Sodium dependent photosynthetic oxygen evolution in a marine diatom. J Expt Bot 35:332–337
Rotatore C, Colman B, Kuzuma M (1995) The active uptake of carbon dioxide by the marine diatoms Phaeodactylum tricornutum and Cyclotella sp. Plant Cell Environ 18:913–918
Sawada S, Sato M, Kasai A, Yaochi D, Kameya Y, Matsumoto I (2003) Analysis of the feed-forward effects of sink activity on the photosynthetic source-sink balance in single-rooted sweet potato leaves. I. Activation of RUBPcase through the development of sinks. Plant Cell Environ 44:190–197
Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a noninstructive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis: ecological studies. Springer Publishers, Berlin, pp 49–70
Schreiber U, Quayle P, Schmidt S, Escher BI, Mueller JE (2007) Methodology and evaluation of a highly sensitive algae toxicity test based on multiwell chlorophyll fluorescence imaging. Biosens Bioelectron 22:2554–2563
Stevenson TT, Cleland RE (1981) Osmoregulation in the Avena coleoptile in relation to auxin and growth. Plant Physiol 67:749–753
van Thor JJ, Jeanjean R, Havaux M, Sjollema KA, Joset F, Hellingwerf KJ, Matthijs HC (2000) Salt shock-inducible photosystem I cyclic electron transfer in Synechocystis PCC6803 relies on binding of ferredoxin:NADP(+) reductase to the thylakoid membranes via its CpcD phycobilisome-linker homologous N-terminal domain. Biochim Biophys Acta 1457:129–144
van Volkenburgh E, Cleland RE (1990) Light-stimulated cell expansion in bean (Phaseolus vulgaris L.) leaves. I. Growth can occur without photosynthesis. Planta 182:72–76
Xia J, Li Y, Zou D (2004) Effects of salinity stress on PS II in Ulva lactuca as probed by chlorophyll fluorescence measurements. Aquat Bot 80:129–137
Yamazaki J-Y, Suzuki T, Maruta E, Kamimura Y (2005) The stoichiometry and antenna size of the two photosystems in marine green algae, Bryopsis maxima and Ulva pertusa, in relation to the light environment of their natural habitat. J Expt Bot 56:1517–1523
Zhao J, Brand J (1989) Sequential Events in the photoinhibition of Synechocystis under sodium stress. Plant Physiol 91:91–100
Acknowledgments
We thank Young-Jae Eu and Ho-Seung Kim (Busan National University, South Korea) for providing the IMAGING-PAM Chlorophyll Fluorometer and for pigment analysis. This research was supported by grants from the Ministry of Maritime Affairs and Fisheries of the Korean Government as parts of the “Greenhouse Gas Removal by Seaweed” project (E10600107A060000120) to C.-H.G. and in part by University of Incheon Research Grant (2005) to T.H.
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An erratum to this article is available at http://dx.doi.org/10.1007/s12374-013-0908-6.
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Goh, CH., Oh, SJ., Jun, SS. et al. External K+ Deficiency Inhibits Photosynthetic Activity Through Superoxide Anion Production in Protoplasts Isolated from the Thallus of Ulva pertusa . J. Plant Biol. 53, 155–164 (2010). https://doi.org/10.1007/s12374-010-9101-3
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DOI: https://doi.org/10.1007/s12374-010-9101-3