Abstract
Clonal tissue of the marine chlorophyte macroalga, Ulva rotundata Blid., was transferred from 100 to 1700 μmol photons · m−2 · s−1 under limiting (1.5 μM NH +4 maximum, N/P=2) and sufficient (15 μM NH +4 maximum, N/P=20) nitrogen supply at 18° C and 11 h light-13 h darkness daily. Photoinhibition was assayed by light-response curves (photosynthetic O2 exchange), and chlorophyll fluorescence at 77 K and room temperature. Daily surface-area growth rate (μSA) in N-sufficient plants increased sixfold over 3 d and was sustained at that level. During this period, respiration (R d) doubled and light-saturated net photosynthesis capacity (P m) increased by nearly 50%, indicating acclimation to high light. Quantum yield (ϕ) decreased by 25% on the first day, but recovered completely within one week. The ratio of variable to maximum fluorescence (F v/F m) also decreased markedly on the first day, because of an increase in initial fluorescence (F o) and a decrease in F m, and partially recovered over several days. Under the added stress of N deficiency, μSA accelerated fivefold over 4 d, despite chronic photoinhibition, then declined along with tissue-N. Respiration doubled, but P m decreased by 50% over one week, indicating inability to acclimate to high light. Both ϕ and F v/F m decreased markedly on the first day and did not significantly recover. Changes in F o, F m and xanthophyll-cycle components indicate concurrent photodamage to photosystem II (PSII) and photoprotection by thermal deexcitation in the antenna pigments. Increasing μSA coincided with photoinhibition of PSII. Insufficient diel-carbon balance because of elevated R d and declining P m and tissue-N, rather than photochemical damage per se, was the apparent proximate cause of decelerating growth rate and subsequent tissue degeneration under N deficiency in U. rotundata.
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Abbreviations
- Chl:
-
chlorophyll
- Fo, Fm, Fv :
-
in the sequence given, initial, maximum and variable chlorophyll fluorescence
- PFD:
-
photon flux density
- Pm :
-
photosynthesis rate at light saturation
- PSI, PSII:
-
photosystems I, II, respectively
- Rd :
-
dark-respiration rate
- RT:
-
room temperature
- ϕ :
-
quantum yield of photosynthetic O2 evolution
- μSA :
-
daily surface-area specific growth rate
References
Adams, W.W., III, Osmond, C.B., Sharkey, T.D. (1987a) Responses of two CAM species to different irradiances during growth and susceptibility to photoinhibition by high light. Plant Physiol. 83, 213–218
Adams, W.W., III, Smith, S.D., Osmond, C.B. (1987b) Photoinhibition of the CAM succulent Opuntia basilaris growing in Death Valley: evidence from 77 K fluorescence and quantum yield. Oecologia 71, 221–228
Adams, W.W., III, Demmig-Adams, B., Winter, K., Schreiber, U. (1990). The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77 K, as an indicator of the photon yield of photosynthesis. Planta 180, 166–174
Anderson, J.M., Osmond, C.B. (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Topics in Photosynthesis, vol. 9: Photoinhibition, pp. 1–38, Kyle, D.J., Osmond, C.B., Arntzen, C.J., eds. Elsevier, Amsterdam
Baker, N.R., Horton, P. (1987) Chlorophyll fluorescence quenching during photoinhibition. In: Topics in Photosynthesis, vol. 9: Photoinhibition, pp. 145–168, Kyle, D.J., Osmond, C.B., Arntzen, C.J., eds. Elsevier, Amsterdam
Björkman, O. (1981) Responses to different quantum flux densities. In: Encyclopedia of Plant Physiology, vol. 12A: Physiological plant ecology I, Responses to the physical environment, pp. 57–107, Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H., eds. Springer, Berlin Heidelberg New York
Björkman, O. (1987) Low-temperature chlorophyll fluorescence in leaves and its relationship to photon yield of photosynthesis in photoinhibition. In: Topics in photosynthesis, vol. 9: Photoinhibition, pp. 123–144, Kyle, D.J., Osmond, C.B., Arntzen, C.J., eds. Elsevier, Amsterdam
Björkman, O., Demmig, B. (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504
Böse, S., Herbert, S.K., Fork, D.C. (1988) Fluorescence characteristics of photoinhibition and recovery in a sun and a shade species of the red algal genus Porphyra. Plant Physiol. 86, 946–950
Britz, S.J., Briggs, W.R. (1976) Circadian rhythms of chloroplast orientation and photosynthetic capacity in Ulva. Plant Physiol. 58, 22–27
Butler, W.L., Kitajima, M. (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim. Biophys. Acta 376, 116–125
Chow, W.S., Osmond, C.B., Huang, L.K. (1989) Photosystem II function and herbicide binding sites during photoinhibition of spinach chloroplasts in-vivo and in-vitro. Photosynth. Res. 21, 17–26
Demmig, B., Björkman, O. (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171, 171–184
Demmig-Adams, B. (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1–24
Ferrar, P.J., Osmond, C.B. (1986) Nitrogen supply as a factor influencing photoinhibition and photosynthetic acclimation after transfer of shade-grown Solanum dulcamara to bright light. Planta 168, 563–570
Greer, D.H., Berry, J.A., Björkman, O. (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168, 253–260
Guillard, R.R.L., Ryther, J.H. (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229–239
Harbinson, J., Genty, B., Baker, N.R. (1989) Relationship between the quantum efficiencies of photosystems I and II in pea leaves. Plant Physiol. 90, 1029–1034
Henley, W.J. (1990) Uncoupling of various measures of growth in Ulva rotundata (Chlorophyta) following a large decrease in irradiance. J. Phycol. 26, 206–207
Henley, W.J., Ramus, J. (1989a) Time course of physiological response of Ulva rotundata to growth irradiance transitions. Mar. Ecol. Prog. Ser. 54, 171–177
Henley, W.J., Ramus, J. (1989b) Optimization of pigment content and the limits of photoacclimation for Ulva rotundata. Mar. Biol. 103, 267–274
Herbert, S.K., Waaland, J.R. (1988) Photoinhibition of photosynthesis in a sun and a shade species of the red algal genus Porphyra. Mar. Biol. 97, 1–7
Krause, G.H. (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 74, 566–574
Krause, G.H., Cornic, G. (1987) CO2 and O2 interactions in photoinhibition. In: Topics in photosynthesis, vol. 9: Photoinhibition, pp. 169–196, Kyle, D.J., Osmond, C.B., Arntzen, C.J., eds. Elsevier, Amsterdam
Lapointe, B.E., Tenore, K.R., Dawes, C.J. (1984) Interactions between light and temperature on the physiological ecology of Gracilaria tikvahiae (Gigartinales: Rhodophyta). I. Growth, photosynthesis and respiration. Mar. Biol. 80, 161–170
Levavasseur, G. (1986) Plasticite de l'appareil pigmentaire des grandes algues marines. Regulations en fonction de leur environment. These Doctorat d'Etat, Université P. et M. Curie, Paris VI, France
Lüning, K., Dring, M.J. (1985) Action spectra and spectral quantum yield of photosynthesis in marine macroalgae with thin and thick thalli. Mar. Biol. 87, 119–129
Masle, J., Farquhar, G.D., Gifford, R.M. (1990) Growth and carbon economy of wheat seedlings as affected by soil resistance to penetration and ambient partial pressure of CO2. Aust. J. Plant Physiol. 17, 465–487
Nultsch, W., Pfau, J., Rüffer, U. (1981) Do correlations exist between chromatophore arrangement and photosynthetic activity in seaweeds? Mar. Biol. 62, 111–117
Ögren, E., Öquist, G. (1984) Photoinhibition of photosynthesis in Lemna gibba as induced by the interaction of light and temperature. II. Chlorophyll fluorescence at 77 K. Physiol. Plant. 62, 193–200
Ohad, I., Kyle, D.J., Arntzen, C.J. (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilo-dalton polypeptides in chloroplast membranes. J. Cell Biol. 99, 481–485
Osmond, C.B. (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim. Biophys. Acta 639, 77–98
Osmond, C.B. (1987) Photosynthesis and the carbon economy of plants. New Phytol. 106, Suppl., 161–175
Powles, S.B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35, 15–44
Prézelin, B.B., Samuelsson, G., Matlick, H.A. (1986) Photosystem II photoinhibition and altered kinetics of photosynthesis during nutrient-dependent high-light photoadaptation in Gonyaulax polyedra. Mar. Biol. 93, 1–12
Ramus, J. (1983) A physiological test of the theory of complementary chromatic adaptation. II. Brown, green and red seaweeds. J. Phycol. 19, 173–178
Raven, J.A. (1984) A cost-benefit analysis of photon absorption by photosynthetic unicells. New Phytol. 98, 593–625
Samuelsson, G., Lönneborg, A., Gustafsson, P., Öquist, G. (1987) The susceptibility of photosynthesis to photoinhibition and the capacity of recovery in high and low light grown cyanobacteria, Anacystic nidulans. Plant Physiol. 83, 438–441
Schreiber, U., Schliwa, U., Bilger, W. (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10, 51–62
Seemann, J.R., Sharkey, T.D., Wang, J., Osmond, C.B. (1987) Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol. 84, 796–802
Steemann Nielsen, E. (1962) Inactivation of the photochemical mechanism in photosynthesis as a means to protect the cells against too high light intensities. Physiol. Plant. 15, 161–171
Terashima, I., Huang, L-K., Osmond, C.B. (1989) Effects of leaf chilling on thylakoid functions, measured at room temperature in Cucumis sativus L. and Oryza sativa L. Plant Cell Physiol. 30, 841–850
Thayer, S.S., Björkman, O. (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth. Res. 23, 331–343
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We wish to thank Jud Kenworthy, National Marine Fisheries Service, Beaufort, N.C., USA for performing the C/N analysis, and Olle Björkman and Susan Thayer, Carnegie Institution of Washington, Stanford, Cal., USA for the analysis of xanthophylls. This research was supported by National Science Foundation (NSF) grant OCE-8812157 to C.B.O. and J.R. Support for G.L. was provided by a NSF-CNRS (Centre National de la Recherche Scientifique) exchange fellowship.
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Henley, W.J., Levavasseur, G., Franklin, L.A. et al. Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta 184, 235–243 (1991). https://doi.org/10.1007/BF00197952
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DOI: https://doi.org/10.1007/BF00197952