Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation

European Journal of Phycology

Volumn 33, Issue 4, 1998, Pages 315-332

  Geider, Richard J ^a,e   Macintyre, Hugh L ^a,b   Graziano, Lisa M ^a,c   McKay, R Michael L ^a,d  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^c Sea Education Association   (United States)

^d BOWLING GREEN STATE UNIVERSITY   (United States)

^e THE LABORATORY   (United Kingdom)

Author keywords

Absorption coefficient; Accessory pigments; Chlorophyll; Dunaliella tertiolecta; Fluorescence quenching; Light harvesting complex; Quantum efficiency; Rubisco

Indexed keywords

CHLOROPHYCEAE; DUNALIELLA TERTIOLECTA;

EID: 0032426740     PISSN: 09670262     EISSN: None     Source Type: Journal    
DOI: 10.1017/S096702629800184X     Document Type: Article

References (84)

1. 2 to the activation sites. Plant Cell Physiol., 36: 425-433.
2. BABIN, M., MOREL, A., CLAUSTRE, H., BRICAUD, A., KOLBER, Z. & FALKOWSKI, P.G. (1996). Nitrogen- and irradiance-dependent variations of the maximum quantum yield of carbon fixation in eutrophic, mesotrophic and oligotrophic marine systems. Deep-Sea Res., 43: 1241-1272.
3. BEARDALL, J., ROBERTS, S. & MILLHOUSE, J. (1991). Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1,5-bisphosphate carboxylase/oxygenase in green microalgae. Can. J. Bot., 69: 1146-1150.
4. BEHRENFELD, M.J. & FALKOWSKI, P.G. (1997). Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr., 42: 1-20.
5. BERGES, J.A., CHARLEBOIS, D.O., MAUZERALL, D.C. & FALKOWSKI, P.G. (1996). Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol., 110: 689-696.
6. BERNER, T., DUBINSKY, Z. WYMAN, K. & FALKOWSKI, P.G. (1989). Photoadaptation and the "package" effect in Dunaliella tertiolecta (Chlorophyceae). J. Phycol., 25: 70-78.
7. BEVINGTON. P.R. (1969). Data Reduction and Error Analysis for the Physical Sciences. McGraw Hill, New York.
8. BIDIGARE, R.R., ONDRUSEK, M.E., MORROW, J.H. & KIEFER, D.A. (1990). In vivo absorption properties of algal pigments. Ocean Optics X. Proc. Soc. Photoopt. Instrum. Eng., 1302: 290-302.
9. BJÖRKMAN, O. (1981). Responses to different quantum flux densities. In: Physiological Plant Ecology. I. Responses to the Physical Environment (Lange, O.L., Nobel, P. S., Osmond, C.B. & Ziegler, H., editors), 57-107. Springer-Verlag, Heidelberg.
10. BLOCK, M.A., DORNE, A., JOYARD, J. & DOUCE, R. (1983 a). Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. I. Electrophoretic and immunochemical analysis. J. Biol. Chem., 258: 13273-13280.
11. BLOCK, M.A., DORNE, A., JOYARD, J. & DOUCE, R. (1983 b). Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical analysis. J. Biol. Chem., 258: 13281-13286.
12. BROOKS, A. (1986). Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of Calvin-cycle metabolites in spinach leaves. Aust. J. Plant Physiol., 13: 221-237.
13. CHALUP, M.S. & LAWS, E.A. (1990). A test of the assumptions and predictions of recent microalgal growth models with the marine phytoplankter Pavlova lutheri. Limnol. Oceanogr., 35: 583-596.
14. CLEVELAND, J.S., PERRY, M.J., KIEFER, D.A. & TALBOT, M.C. (1989). Maximal quantum yield of photosynthesis in the northwestern Sargasso Sea. J. Mar. Res., 47: 869-886.
15. CODISPOTI, L.A. (1989). Phosphorus vs. nitrogen limitation of new and export production. In Productivity of the Ocean: Present and Past (Berger, W.H., Smetacek, V.S. & Wefer, G., editors), 377-394. Wiley, New York.
16. COLEMAN, L.W., ROSEN, B.H. & SCHWARTZBACH, S.D. (1988 a). Environmental control of carbohydrate and lipid synthesis in Euglena. Plant Cell Physiol., 29: 423-432.
17. COLEMAN, L.W., ROSEN, B.H. & SCHWARTZBACH, S.D. (1988 b). Preferential loss of chloroplast proteins in nitrogen deficient Euglena. Plant Cell Physiol., 29: 1007-1014.
18. COLLIER, J.L. & GROSSMAN, A.R. (1992). Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PC 7942: not all bleaching is the same. J. Bacteriol., 174: 4718-4726.
19. CULLEN, J.J., YANG, X. & MACINTYRE, H.L. (1992). Nutrient limitation and marine photosynthesis. In Primary Productivity and Biogeochemical Cycles in the Sea (Falkoswki, P.G. & Woodhead, A.V., editors), 69-88. Plenum Press, New York.
20. DEMMIG-ADAMS, B. & ADAMS III, W.W. (1993). The xanthophyll cycle. In Carotenoids in Photosynthesis (Young, A. & Britton, G., editors), 206-251. Chapman and Hall, London.
21. 2 uptake in Arbutus unedo growing in Portugal. Planta, 177: 377-387.
22. DORTCH, Q., CLAYTON, J.R., THORESEN, S.S. & AHMED, S.I. (1984). Species differences in accumulation of nitrogen pools in phytoplankton. Mar. Biol., 81: 237-250.
23. DROOP, M.R., MICKELSON, M.J., SCOTT, J.M. & TURNER, M.F. (1982). Light and nutrient status of algal cells. J. Mar. Biol. Assoc. U.K., 62: 403-434.
24. EKMAN, P., LIGNELL, A. & PEDERSEN, M. (1989) Localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in Gracilaria secundata (Rhodophyta) and its role as a nitrogen storage pool. Bot. Mar. 32: 527-534.
25. ESCOUBAS J.-M., LOMAS, M., LA ROCHE, J. & FALKOWSKI, P.G. (1995). Light intensity regulation of CAB gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. U.S.A., 92: 10237-10241.
26. EVANS, J.R. (1996). Developmental constraints on photosynthesis: effects of light and nutrition. In Photosynthesis and the Environment (Baker, N.R., editor), 281-304. Kluwer Academic Publishers, The Netherlands.
27. FALKOWSKI, P.G., OWENS, T.G., LEY, A.C. & MAUZERALL, D.C. (1981). Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol., 68: 969-973.
28. FALKOWSKI, P.G., DUBINSKY, Z. & WYMAN, K. (1985). Growth-irradiance relationships in phytoplankton. Limnol Oceanogr., 30: 311-321.
29. FALKOWSKI, P.G., SUKENIK, A. & HERZIG, R. (1989). Nitrogen-limitation in Isochrysis galbana (Haptophyceae). II. Relative abundances of chloroplast proteins. J. Phycol., 25: 471-478.
30. FALKOWSKI, P.G., ZIEMANN, D., KOLBER, Z. & BIENFANG, P.K. (1991). Nutrient pumping and phytoplankton response in a subtropical mesoscale eddy. Nature, 352: 52-58.
31. FALKOWSKI, P.G., BARBER, R.T. & SMETACEK, V. (1998). Biogeochemical controls and feedbacks on ocean primary productivity. Science, 281: 200-206.
32. FISHER, T., SHURTZ-SWIRSKI, R., GEPSTEIN, S. & DUBINSKY, Z. (1987). Changes in levels of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in Tetraedron minimum (Chlorophyta) during light and shade adaptation. Plant Cell Physiol., 30: 221-228.
33. GARCIA-FERRIS, C. & MORENO, J. (1994). Oxidative modification and breakdown of ribulose-1,5-bisphosphate carboxylase/oxygenase in Euglena gracilis by nitrogen starvation. Planta, 193: 208-215.
34. GEIDER, R.J., LA ROCHE, J., GREENE, R.M. & OLAIZOLA, M. (1993). Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate and iron starvation. J. Phycol., 29: 755-766.
35. GEIDER, R.J., MACINTYRE, H.L. & KANA, T.M. (1998). A dynamic regulatory model of phytoplanktonic acclimation to light, nutrients and temperature. Limnol. Oceanogr., 43: 679-694.
36. GOLDMAN, J.C., MCCARTHY, J.J. & PEAVEY, D.G. (1979). Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature, 279: 210-215.
37. GREENE, R.M., GEIDER, R.J., KOLBER, Z. & FALKOWSKI, P.G. (1992). Iron-induced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiol., 100: 565-575.
38. HENLEY, W.J., LEVAVASSEUR, G., FRANKLIN, L.A., OSMOND, C.B. & RAMUS, J. (1991). Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta (Berl.), 184: 235-243.
39. HERMSMEIER, D., SCHULZ, R. & SENGER, H. (1994). Formation of light-harvesting complexes of photosystem II in Scenedesmus. I. Correlations between amounts of photosynthetic pigments, LHCPII messenger RNAs and LHCPII apoproteins during constitutional dark- and light-dependent LHCPII-gene expression. Planta (Berl.), 193: 398-405.
40. HERZIG, R. & FALKOWSKI, P.G. (1989). Nitrogen limitation in Isochrysis galbana (Haptophyceae). I. Photosynthetic energy conversion and growth efficiencies. J. Phycol., 25: 462-471.
41. HIPKIN, C.R. & SYRETT, P.J. (1977). Some effects of nitrogen-starvation on nitrogen and carbon metabolism in Ankistrodesmus braunii. Planta (Berl.), 133: 209-214.
42. HOLM-HANSEN, O. (1978) Chlorophyll a determination: improvements in methodology. Oikos, 30: 428-447.
43. JANSSON, S. (1994). The light-harvesting chlorophyll a/b-binding proteins. Biochim. Biophys. Acta, 1184: 1-20.
44. JENNINGS, R.C., GARLASCHI, F.M., FINZI, L. & ZUCCHELLI, G. (1996). Slow exciton trapping in photosystem II: a possible physiological role. Photosynth. Res., 47: 167-173.
45. -1 on marine Synechococcus WH7803. I. Growth, pigmentation, and cell composition. Deep-Sea Res., 34: 479-495.
46. KELLER, M.D., SELVIN, R.C., CLAUS, W. & GUILLAES, R.R.L. (1987). Media for the culture of oceanic ultraphytoplankton. J. Phycol., 23: 633-638.
47. KOLBER, Z., ZEHR, J. & FALKOWSKI, P.G. (1988). Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol., 88: 923-929.
48. KOST, H.-P., SENGER, M. & WANNER, G. (1984). Effect of nitrate and sulfate starvation on Porphyridium cruentum cells. Z. Planzenphysiol., 113: 231-249.
49. KROM, M.D., KRESS, N. & BRENNER, S. (1991). Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol. Oceanogr., 36: 424-432.
50. LACOSTE-ROYAL, G. & GIBBS, S.P. (1987). Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase in the pyrenoid and thylakoid region of the chloroplast of Chlamydomonas reinhardtii. Plant Physiol., 83: 602-606.
51. LANDRY, M.R., BARBER, R.T., BIDIGARE, R.R, CHAI, F., COALE, K.H., DAM, H.G., LEWIS, M.R., LINDLEY, S.T., MCCARTHY, J.J., ROMAN, M.R., STOECKER, D.K., VERITY, P.G. & WHITE, J.R. (1997). Iron and grazing constraints on primary production in the central equatorial Pacific: an EqPac synthesis. Limnol. Oceanogr., 42: 405-431.
52. LAPOINTE, B.E. & DUKE, C.S. (1984). Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light intensity and nitrogen availability. J. Phycol., 20: 488-495.
53. LARKUM, T. & HOWE, C.J. (1997). Molecular aspects of light-harvesting processes in algae. Adv. Bot. Res., 27: 257-330.
54. LA ROCHE, J., GEIDER, R .J., GRAZIANO, L.M., MURRAY, H. & LEWIS, K. (1993). Induction of specific proteins in eukaryotic algae grown under iron, phosphorus and nitrogen deficient conditions. J. Phycol., 29: 767-777.
55. LA ROCHE, J., MURRAY, H., ORELLANA, M. & NEWTON, J. (1995). Flavodoxin expression as an indicator of iron limitation in marine diatoms. J. Phycol., 31: 520-530.
56. LEWIS, M.R. & SMITH, J.C. (1983). A small volume, short-incubation-time method for measurement of photosynthesis as a function of irradiance. Mar. Ecol. Prog. Ser., 13: 99-102.
57. MARINO, A., NAKANO, H. & MAE, T. (1994). Responses of ribulose-1,5-bisphosphate carboxylase, cytochrome f, and sucrose synthesis enzymes in rice leaves to leaf nitrogen and their relationships to photosynthesis. Plant Physiol., 105: 173-179.
58. MANTOURA, R.F.C. & LLEWELLYN, C.A. (1983). The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high performance liquid chromatography. Anal. Chim. Acta, 151: 297-314.
59. MCCARTHY, J.J. (1981). The kinetics of nutrient utilization. Can. Bull. Fish. Aquat. Sci., 210: 211-233.
60. MCKAY, R.M.L. & GIBBS, S.P. (1989). Immunocytochemical localization of ribulose 1,5-bisphosphate carboxylase/oxygenase in light-limited and light-saturated cells of Chlorella pyrenoidosa. Protoplasma, 149: 31-37.
61. MCKAY, R.M.L., GIBBS, S.P. & VAUGHN, K.C. (1991). RuBisCo activase is present in the pyrenoid of green algae. Protoplasma, 162: 38-45.
62. MORTAIN-BERTRAND, A., BENNETT, J. & FALKOWSKI, P.G. (1990). Photoregulation of the light-harvesting chlorophyll protein complex associated with photosystem II in Dunaliella tertiolecta. Plant Physiol., 94: 304-311.
63. NELSON, N.B., PRÉZELIN, B.B. & BIDIGARE, R.R. (1993). Phytoplankton light absorption and the package effect in California coastal waters. Mar. Ecol. Prog. Ser., 94: 217-227.
64. OLAIZOLA, M. & YAMAMOTO, H.Y. (1994). Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). J. Phycol., 30: 606-612.
65. OSBORNE, B.A. & GEIDER, R.J. (1986). Effects of nitrate-nitrogen limitation on photosynthesis in the diatom Phaeodactylum tricornutum Bohlin (Bacillariophyceae). Plant Cell Environ., 9: 617-625.
66. PLUMLEY, F.G. & SCHMIDT, G.W. (1989). Nitrogen-dependent regulation of photosynthetic gene expression. Proc. Natl. Acad. Sci. U.S.A., 86: 2678-2682.
67. PRÉZELIN, B.B. (1982). Effects of light intensity on aging of the dinoflagellate Gonyaulax polyhedra. Mar. Biol., 69: 129-135.
68. PRÉZELIN, B.B. & MATLICK, H.A. (1983). Nutrient-dependent low-light adaptation in the dinoflagellate Gonyaulax polyhedra. Mar. Biol., 74: 141-150.
69. PROZUMENSHCHIKOVA, L.T., YADYKIN, A.A. & OSIPOVA, I.D. (1990). The effect of light and mineral feeding on photosynthetic enzyme activity and the content of pigments in the red algae Gracilaria verrucosa. J. Mar. Biol., 16: 44-47.
70. RHEE, G.-Y. (1973). A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. J. Phycol., 9: 495-506.
71. ROBERTS, J. (1997). Control of the supply line. Science, 278: 2073-2074.
72. SCIANDRA, A., GOSTAN, J., COLLOS, Y., DESCOLAS-GROS, C., LEBOULANGER, C., MARTIN-JEZEQUEL, V., DENIS, M., LEFEVRE, D., COPIN-MONTEGUT, C. & AVRIL, B. (1997). Growth-compensating phenomena in continuous cultures of Dunaliella tertiolecta limited simultaneously by light and nitrate. Limnol. Oceanogr. 42: 1325-1339.
73. SENFT, W.H. (1978). Dependence of light-saturated rates of algal photosynthesis on intracellular concentrations of phosphorus. Limnol. Oceanogr., 23: 709-718.
74. SHARKEY, T.D. (1990). Feedback limitation of photosynthesis and the physiological role of ribulose bisphosphate carboxylase carbamylation. Bot. Mag. Tokyo Special Issue, 2: 87-105.
75. SIEFERMANN-HARMS, D. & NINNEMANN, H. (1982). Pigment organization in the light-harvesting chlorophyll-a/b protein complex of lettuce chloroplasts: evidence obtained from protection of the chlorophylls against proton attack and from excitation energy tranfer. Photochem. Photobiol. 35: 719-731.
76. SOLORZANO, L. & SHARP, J.H. (1980). Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnol. Oceanogr., 25: 754-758.
77. SOSIK, H.M. & MITCHELL, B.G. (1991). Absorption, fluorescence, and quantum yield for growth in nitrogen-limited Dunaliella tertiolecta. Limnol. Oceanogr., 36: 910-921.
78. STITT, M. & SCHULTZ, D. (1994). Does Rubisco control the rate of photosynthesis and plant growth? An excercise in molecular ecophysiology. Plant Cell Environ., 17: 465-487.
79. SUKENIK, A., BENNETT, J. & FALKOWSKI, P.G. (1987). Light-saturated photosynthesis: limitation by electron transport or carbon-fixation? Biochim. Biophys. Acta, 891: 205-215.
80. SUKENIK, A., BENNETT, J. & FALKOWSKI, P.G. (1988). Changes in the abundance of individual apoproteins of light-harvesting chlorophyll a/b complexes of photosystem I and II with growth irradiance in the marine chlorophyte Dunaliella tertiolecta. Biochim. Biophys. Acta, 932: 206-215.
81. TING, C. S. & OWENS, T.G. (1994). The effects of excess irradiance on photosynthesis in the marine diatom Phaeodactylum tricornutum. Plant Physiol., 106: 763-770.
82. TURPIN, D.H., ELRIFI, I.R., BIRCH, D.G., WEGER, H.G. & HOLMES, J.J. (1988). Interactions between photosynthesis, respiration and nitrogen assimilation in microalgae. Can. J. Bot., 66: 2083-2097.
83. 18 column. J. Phycol., 28: 867-872.
84. YAMAMOTO, H.Y. & BASSI, R. (1996). Carotenoids: localization and function. In Oxygenic Photosynthesis: The Light Reactions (Ort, D. R. & Yocum, C. F., editors), 539-563. Kluwer Academic Press, The Netherlands.