DOI: 10.1104/pp.117.1.129. The Regulation of Photosynthetic Electron Transport during Nutrient Deprivation in<i>Chlamydomonas reinhardtii</i>1

The Regulation of Photosynthetic Electron Transport during Nutrient Deprivation inChlamydomonas reinhardtii1

10.1104/pp.117.1.129

Crossref journal-article

Oxford University Press (OUP)

Plant Physiology (286)

Abstract

AbstractThe light-saturated rate of photosynthetic O2 evolution in Chlamydomonas reinhardtii declined by approximately 75% on a per-cell basis after 4 d of P starvation or 1 d of S starvation. Quantitation of the partial reactions of photosynthetic electron transport demonstrated that the light-saturated rate of photosystem (PS) I activity was unaffected by P or S limitation, whereas light-saturated PSII activity was reduced by more than 50%. This decline in PSII activity correlated with a decline in both the maximal quantum efficiency of PSII and the accumulation of the secondary quinone electron acceptor of PSII nonreducing centers (PSII centers capable of performing a charge separation but unable to reduce the plastoquinone pool). In addition to a decline in the light-saturated rate of O2 evolution, there was reduced efficiency of excitation energy transfer to the reaction centers of PSII (because of dissipation of absorbed light energy as heat and because of a transition to state 2). These findings establish a common suite of alterations in photosynthetic electron transport that results in decreased linear electron flow when C. reinhardtii is limited for either P or S. It was interesting that the decline in the maximum quantum efficiency of PSII and the accumulation of the secondary quinone electron acceptor of PSII nonreducing centers were regulated specifically during S-limited growth by theSacI gene product, which was previously shown to be critical for the acclimation of C. reinhardtiito S limitation (J.P. Davies, F.H. Yildiz, and A.R. Grossman [1996] EMBO J 15: 2150–2159).

Bibliography

Wykoff, D. D., Davies, J. P., Melis, A., & Grossman, A. R. (1998). The Regulation of Photosynthetic Electron Transport during Nutrient Deprivation inChlamydomonas reinhardtii1. Plant Physiology, 117(1), 129â139.

Authors 4

Dennis D. Wykoff (first)
John P. Davies (additional)
Anastasios Melis (additional)
Arthur R. Grossman (additional)

References 56 Referenced 397

10.1016/S0005-2728(09)91014-3 / Biochim Biophys Acta / Protein phosphorylation in regulation of photosynthesis. by Allen (1992)
{'key': '2021050309534190000_R2', 'first-page': '77', 'article-title': 'Production and action of active oxygen species in photosynthetic tissues.', 'volume-title': 'Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants.', 'author': 'Asada', 'year': '1994'} / Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. / Production and action of active oxygen species in photosynthetic tissues. by Asada (1994)
10.1016/0168-9452(90)90162-H / Plant Sci / Physiology of starch storage in the monocellular alga Chlamydomonas reinhardtii. by Ball (1990)
{'key': '2021050309534190000_R4', 'first-page': '17', 'article-title': 'Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants.', 'volume-title': 'Ecophysiology of Photosynthesis.', 'author': 'Björkman', 'year': '1994'} / Ecophysiology of Photosynthesis. / Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. by Björkman (1994)
10.1104/pp.110.4.1405 / Plant Physiol / Possible role of Cbr, an algal early-light-induced protein, in nonphotochemical quenching of chlorophyll fluorescence. by Braun (1996)
{'key': '2021050309534190000_R6', 'first-page': '221', 'article-title': 'Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves.', 'volume': '13', 'author': 'Brooks', 'year': '1986', 'journal-title': 'Aust J Plant Physiol'} / Aust J Plant Physiol / Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves. by Brooks (1986)
10.1111/j.1432-1033.1992.tb16641.x / Eur J Biochem / Evidence for a selective destabilization of an integral membrane protein, the cytochrome b6/f complex, during gametogenesis in Chlamydomonas reinhardtii. by Bulte (1992)
10.1104/pp.90.2.765 / Plant Physiol / Inactive photosystem II complexes in leaves. by Chylla (1989)
10.1007/BF00018260 / Photosynth Res / Changes in the cyanobacterial photosynthetic apparatus in response to macronutrient deprivation. by Collier (1994)
10.1104/pp.55.2.183 / Plant Physiol / Partial reactions of photosynthesis in briefly sonicated Chlamydomonas. by Curtis (1975)
10.2307/3869674 / Plant Cell / Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. by Davies (1994)
10.1002/j.1460-2075.1996.tb00568.x / EMBO J / Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. by Davies (1996)
10.1007/BF00331273 / Mol Gen Genet / Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii. by de Hostos (1989)
10.1146/annurev.pp.43.060192.003123 / Annu Rev Plant Physiol Plant Mol Biol / Photoprotection and other responses of plants to high light stress. by Demmig-Adams (1992)
10.1104/pp.93.3.1219 / Plant Physiol / Carbon metabolism in spinach leaves as affected by leaf age and phosphorus and sulfur nutrition. by Dietz (1990)
10.1007/BF00049534 / Photosynth Res / Changes in photosystem II fluorescence in Chlamydomonas reinhardtii exposed to increasing levels of irradiance in relationship to the photosynthetic response to light. by Falk (1992)
10.1111/j.1399-3054.1992.tb05264.x / Physiol Plant / Recovery of photosynthesis and photosystem II fluorescence in Chlamydomonas reinhardtii after exposure to three levels of high light. by Falk (1992)
10.1016/S0021-9258(18)42512-4 / J Biol Chem / Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. by Ferreira (1992)
10.1016/S0304-4165(89)80016-9 / Biochim Biophys Acta / The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. by Genty (1989)
10.1007/BF00199689 / Planta / Stress-induced chlorosis and increase in D1-protein turnover precede photoinhibition in spinach suffering under magnesium/sulphur deficiency. by Godde (1994)
10.1007/BF00192543 / Planta / Photoinhibition and light-dependent turnover of the D1 reaction centre polypeptide of photosystem II are enhanced by mineral-stress conditions. by Godde (1994)
10.1073/pnas.54.6.1665 / Proc Natl Acad Sci USA / Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. by Gorman (1966)
10.1007/BF00033157 / Photosynth Res / Photosystem-II heterogeneity—the acceptor side. by Govindjee (1990)
10.1007/BF00030070 / Photosynth Res / The physiological significance of photosystem II heterogeneity in chloroplasts. by Guenther (1990)
10.1016/0005-2728(88)90125-9 / Biochim Biophys Acta / Photosystem stoichiometry and chlorophyll antenna size in Dunaliella salina (green algae). by Guenther (1988)
{'key': '2021050309534190000_R26'}
10.1111/j.1529-8817.1989.tb00251.x / J Phycol / Nitrogen limitation in Isochrysis galbana (haptophyceae). I. Photosynthetic energy conversion and growth efficiencies. by Herzig (1989)
10.1146/annurev.arplant.47.1.655 / Annu Rev Plant Physiol Plant Mol Biol / Regulation of light harvesting in green plants: indication by nonphotochemical quenching of chlorophyll fluorescence. by Horton (1996)
10.1007/BF02402263 / Biogeochemistry / Sulfur speciation and distribution in soils and above ground biomass of a boreal coniferous forest. by Houle (1992)
10.1111/j.1365-3040.1993.tb00500.x / Plant Cell Environ / In vivo photosynthetic electron transport does not limit photosynthetic capacity in phosphate-deficient sunflower and maize leaves. by Jacob (1993)
{'key': '2021050309534190000_R31'}
10.1104/pp.103.1.181 / Plant Physiol / Photosystem II reaction center damage and repair in Dunaliella salina (green alga). by Kim (1993)
10.1146/annurev.pp.42.060191.001525 / Annu Rev Plant Physiol Plant Mol Biol / Chlorophyll fluorescence and photosynthesis: the basics. by Krause (1991)
10.1007/0-306-48127-8_14 / Oxygeneic Photosynthesis: The Light Reactions. / Photosystem II heterogeneity. by Lavergne (1996)
10.1016/S0021-9258(18)92755-9 / J Biol Chem / Co-regulation of a gene homologous to early light-induced genes in higher plants and β-carotene biosynthesis in the alga Dunaliella bardawil. by Lers (1991)
10.1016/S0021-9258(19)36870-X / J Biol Chem / Cbr, an algal homolog of plant early light-induced proteins, is a putative zeaxanthin binding protein. by Levy (1993)
10.1080/00103628709367849 / Commun Soil Sci Plant Anal / Effect of sulfur additions on soil and the nutrition of wheat. by Mahler (1987)
10.1016/S0005-2728(05)80225-7 / Biochim Biophys Acta / Dynamics of photosynthetic membrane composition and function. by Melis (1991)
10.1104/pp.92.4.1196 / Plant Physiol / Activation of a reserve pool of photosystem II in Chlamydomonas reinhardtii counteracts photoinhibition. by Neale (1990)
10.2307/3870388 / Plant Cell / Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. by Niyogi (1997)
10.1007/BF00030069 / Photosynth Res / Inactive photosystem II centers. by Ort (1990)
10.1073/pnas.88.11.4791 / Proc Natl Acad Sci USA / Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. by Peltier (1991)
10.1093/jxb/45.7.919 / J Exp Bot / Photosynthesis and chlorophyll fluorescence in sunflower (Helianthus annuus L.) leaves as affected by phosphorus nutrition. by Plesnicar (1994)
10.1104/pp.111.3.839 / Plant Physiol / Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii. by Quisel (1996)
10.1007/BF00001529 / Biogeochemistry / Both nitrogen and phosphorus limit plant production on young Hawaiian lava flows. by Raich (1996)
10.1071/AR9931775 / Aust J Agric Res / Effects of placement of elemental S and sulfate on the growth of two rice varieties under flooded conditions. by Samosir (1993)
10.1007/BF00024185 / Photosynth Res / Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. by Schreiber (1986)
10.1016/0038-0717(91)90043-J / Soil Biol Biochem / Sulfur transformations and pool sizes in tropical forest soils. by Stanko-Golden (1991)
10.1111/j.0022-3646.1995.00897.x / J Phycol / Cytochrome f loss in astaxanthin-accumulating red cells of Haematococcus pluvialis (chlorophyceae): comparison of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polypeptides in red and green cells. by Tan (1995)
10.1007/BF00033156 / Photosynth Res / The use of chlorophyll fluorescence nomenclature in plant stress physiology. by van Kooten (1990)
10.1104/pp.44.11.1645 / Plant Physiol / Photoreduction of 2,6-dichlorophenolindophenol by diphenylcarbazide. A photosystem 2 reaction catalyzed by tris-washed chloroplasts and subchloroplast fragments. by Vernon (1969)
10.1080/01904169409364849 / J Plant Nutr / Effect of sulfur additions on the yield and elemental composition of canola and spring wheat. by Warman (1994)
{'key': '2021050309534190000_R53'}
10.1016/0005-2728(78)90137-8 / Biochim Biophys Acta / Duroquinol as an electron donor for chloroplast electron transfer reactions. by White (1978)
10.1104/pp.104.3.981 / Plant Physiol / Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. by Yildiz (1994)
10.1104/pp.112.2.669 / Plant Physiol / Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. by Yildiz (1996)

Dates

Type	When
Created	23 years ago (July 27, 2002, 1 a.m.)
Deposited	1 year, 7 months ago (Jan. 5, 2024, 8:04 a.m.)
Indexed	1 hour, 20 minutes ago (Aug. 23, 2025, 12:59 a.m.)
Issued	27 years, 3 months ago (May 1, 1998)
Published	27 years, 3 months ago (May 1, 1998)
Published Online	27 years, 3 months ago (May 1, 1998)
Published Print	27 years, 3 months ago (May 1, 1998)

Funders 0

None

BibTeX

@article{Wykoff_1998, title={The Regulation of Photosynthetic Electron Transport during Nutrient Deprivation inChlamydomonas reinhardtii1}, volume={117}, ISSN={0032-0889}, url={http://dx.doi.org/10.1104/pp.117.1.129}, DOI={10.1104/pp.117.1.129}, number={1}, journal={Plant Physiology}, publisher={Oxford University Press (OUP)}, author={Wykoff, Dennis D. and Davies, John P. and Melis, Anastasios and Grossman, Arthur R.}, year={1998}, month=may, pages={129–139} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        23
      ]
    ],
    "date-time": "2025-08-23T04:59:07Z",
    "timestamp": 1755925147187
  },
  "reference-count": 56,
  "publisher": "Oxford University Press (OUP)",
  "issue": "1",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1998,
            5,
            1
          ]
        ],
        "date-time": "1998-05-01T00:00:00Z",
        "timestamp": 893980800000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1998,
        5,
        1
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>The light-saturated rate of photosynthetic O2 evolution in Chlamydomonas reinhardtii declined by approximately 75% on a per-cell basis after 4 d of P starvation or 1 d of S starvation. Quantitation of the partial reactions of photosynthetic electron transport demonstrated that the light-saturated rate of photosystem (PS) I activity was unaffected by P or S limitation, whereas light-saturated PSII activity was reduced by more than 50%. This decline in PSII activity correlated with a decline in both the maximal quantum efficiency of PSII and the accumulation of the secondary quinone electron acceptor of PSII nonreducing centers (PSII centers capable of performing a charge separation but unable to reduce the plastoquinone pool). In addition to a decline in the light-saturated rate of O2 evolution, there was reduced efficiency of excitation energy transfer to the reaction centers of PSII (because of dissipation of absorbed light energy as heat and because of a transition to state 2). These findings establish a common suite of alterations in photosynthetic electron transport that results in decreased linear electron flow when C. reinhardtii is limited for either P or S. It was interesting that the decline in the maximum quantum efficiency of PSII and the accumulation of the secondary quinone electron acceptor of PSII nonreducing centers were regulated specifically during S-limited growth by theSacI gene product, which was previously shown to be critical for the acclimation of C. reinhardtiito S limitation (J.P. Davies, F.H. Yildiz, and A.R. Grossman [1996] EMBO J 15: 2150\u20132159).</jats:p>",
  "DOI": "10.1104/pp.117.1.129",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T05:00:20Z",
    "timestamp": 1027746020000
  },
  "page": "129-139",
  "source": "Crossref",
  "is-referenced-by-count": 397,
  "title": "The Regulation of Photosynthetic Electron Transport during Nutrient Deprivation in<i>Chlamydomonas reinhardtii</i>1",
  "prefix": "10.1093",
  "volume": "117",
  "author": [
    {
      "given": "Dennis D.",
      "family": "Wykoff",
      "sequence": "first",
      "affiliation": [
        {
          "name": "The Carnegie Institution of Washington, Department of Plant Biology, 260 Panama Street, Stanford, California 94305 (D.D.W., J.P.D., A.R.G.)"
        },
        {
          "name": "Department of Biological Sciences, Stanford University, Stanford, California 94305 (D.D.W.)"
        }
      ]
    },
    {
      "given": "John P.",
      "family": "Davies",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "The Carnegie Institution of Washington, Department of Plant Biology, 260 Panama Street, Stanford, California 94305 (D.D.W., J.P.D., A.R.G.)"
        }
      ]
    },
    {
      "given": "Anastasios",
      "family": "Melis",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Plant Biology, 411 Koshland Hall, University of California, Berkeley, California 94720 (A.M.)"
        }
      ]
    },
    {
      "given": "Arthur R.",
      "family": "Grossman",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "The Carnegie Institution of Washington, Department of Plant Biology, 260 Panama Street, Stanford, California 94305 (D.D.W., J.P.D., A.R.G.)"
        }
      ]
    }
  ],
  "member": "286",
  "published-online": {
    "date-parts": [
      [
        1998,
        5,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021050309534190000_R1",
      "doi-asserted-by": "crossref",
      "first-page": "275",
      "DOI": "10.1016/S0005-2728(09)91014-3",
      "article-title": "Protein phosphorylation in regulation of photosynthesis.",
      "volume": "1098",
      "author": "Allen",
      "year": "1992",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "2021050309534190000_R2",
      "first-page": "77",
      "article-title": "Production and action of active oxygen species in photosynthetic tissues.",
      "volume-title": "Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants.",
      "author": "Asada",
      "year": "1994"
    },
    {
      "key": "2021050309534190000_R3",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0168-9452(90)90162-H",
      "article-title": "Physiology of starch storage in the monocellular alga Chlamydomonas reinhardtii.",
      "volume": "66",
      "author": "Ball",
      "year": "1990",
      "journal-title": "Plant Sci"
    },
    {
      "key": "2021050309534190000_R4",
      "first-page": "17",
      "article-title": "Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants.",
      "volume-title": "Ecophysiology of Photosynthesis.",
      "author": "Bjo\u0308rkman",
      "year": "1994"
    },
    {
      "key": "2021050309534190000_R5",
      "doi-asserted-by": "crossref",
      "first-page": "1405",
      "DOI": "10.1104/pp.110.4.1405",
      "article-title": "Possible role of Cbr, an algal early-light-induced protein, in nonphotochemical quenching of chlorophyll fluorescence.",
      "volume": "110",
      "author": "Braun",
      "year": "1996",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R6",
      "first-page": "221",
      "article-title": "Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves.",
      "volume": "13",
      "author": "Brooks",
      "year": "1986",
      "journal-title": "Aust J Plant Physiol"
    },
    {
      "key": "2021050309534190000_R7",
      "doi-asserted-by": "crossref",
      "first-page": "327",
      "DOI": "10.1111/j.1432-1033.1992.tb16641.x",
      "article-title": "Evidence for a selective destabilization of an integral membrane protein, the cytochrome b6/f complex, during gametogenesis in Chlamydomonas reinhardtii.",
      "volume": "204",
      "author": "Bulte",
      "year": "1992",
      "journal-title": "Eur J Biochem"
    },
    {
      "key": "2021050309534190000_R8",
      "doi-asserted-by": "crossref",
      "first-page": "765",
      "DOI": "10.1104/pp.90.2.765",
      "article-title": "Inactive photosystem II complexes in leaves.",
      "volume": "90",
      "author": "Chylla",
      "year": "1989",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R9",
      "doi-asserted-by": "crossref",
      "first-page": "173",
      "DOI": "10.1007/BF00018260",
      "article-title": "Changes in the cyanobacterial photosynthetic apparatus in response to macronutrient deprivation.",
      "volume": "42",
      "author": "Collier",
      "year": "1994",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R10",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1104/pp.55.2.183",
      "article-title": "Partial reactions of photosynthesis in briefly sonicated Chlamydomonas.",
      "volume": "55",
      "author": "Curtis",
      "year": "1975",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R11",
      "doi-asserted-by": "crossref",
      "first-page": "53",
      "DOI": "10.2307/3869674",
      "article-title": "Mutants of Chlamydomonas with aberrant responses to sulfur deprivation.",
      "volume": "6",
      "author": "Davies",
      "year": "1994",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021050309534190000_R12",
      "doi-asserted-by": "crossref",
      "first-page": "2150",
      "DOI": "10.1002/j.1460-2075.1996.tb00568.x",
      "article-title": "Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation.",
      "volume": "15",
      "author": "Davies",
      "year": "1996",
      "journal-title": "EMBO J"
    },
    {
      "key": "2021050309534190000_R13",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1007/BF00331273",
      "article-title": "Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii.",
      "volume": "218",
      "author": "de Hostos",
      "year": "1989",
      "journal-title": "Mol Gen Genet"
    },
    {
      "key": "2021050309534190000_R14",
      "doi-asserted-by": "crossref",
      "first-page": "599",
      "DOI": "10.1146/annurev.pp.43.060192.003123",
      "article-title": "Photoprotection and other responses of plants to high light stress.",
      "volume": "43",
      "author": "Demmig-Adams",
      "year": "1992",
      "journal-title": "Annu Rev Plant Physiol Plant Mol Biol"
    },
    {
      "key": "2021050309534190000_R15",
      "doi-asserted-by": "crossref",
      "first-page": "1219",
      "DOI": "10.1104/pp.93.3.1219",
      "article-title": "Carbon metabolism in spinach leaves as affected by leaf age and phosphorus and sulfur nutrition.",
      "volume": "93",
      "author": "Dietz",
      "year": "1990",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R16",
      "doi-asserted-by": "crossref",
      "first-page": "31",
      "DOI": "10.1007/BF00049534",
      "article-title": "Changes in photosystem II fluorescence in Chlamydomonas reinhardtii exposed to increasing levels of irradiance in relationship to the photosynthetic response to light.",
      "volume": "31",
      "author": "Falk",
      "year": "1992",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R17",
      "doi-asserted-by": "crossref",
      "first-page": "61",
      "DOI": "10.1111/j.1399-3054.1992.tb05264.x",
      "article-title": "Recovery of photosynthesis and photosystem II fluorescence in Chlamydomonas reinhardtii after exposure to three levels of high light.",
      "volume": "85",
      "author": "Falk",
      "year": "1992",
      "journal-title": "Physiol Plant"
    },
    {
      "key": "2021050309534190000_R18",
      "doi-asserted-by": "crossref",
      "first-page": "7253",
      "DOI": "10.1016/S0021-9258(18)42512-4",
      "article-title": "Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death.",
      "volume": "267",
      "author": "Ferreira",
      "year": "1992",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021050309534190000_R19",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1016/S0304-4165(89)80016-9",
      "article-title": "The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.",
      "volume": "990",
      "author": "Genty",
      "year": "1989",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "2021050309534190000_R20",
      "doi-asserted-by": "crossref",
      "first-page": "291",
      "DOI": "10.1007/BF00199689",
      "article-title": "Stress-induced chlorosis and increase in D1-protein turnover precede photoinhibition in spinach suffering under magnesium/sulphur deficiency.",
      "volume": "195",
      "author": "Godde",
      "year": "1994",
      "journal-title": "Planta"
    },
    {
      "key": "2021050309534190000_R21",
      "doi-asserted-by": "crossref",
      "first-page": "290",
      "DOI": "10.1007/BF00192543",
      "article-title": "Photoinhibition and light-dependent turnover of the D1 reaction centre polypeptide of photosystem II are enhanced by mineral-stress conditions.",
      "volume": "193",
      "author": "Godde",
      "year": "1994",
      "journal-title": "Planta"
    },
    {
      "key": "2021050309534190000_R22",
      "doi-asserted-by": "crossref",
      "first-page": "1665",
      "DOI": "10.1073/pnas.54.6.1665",
      "article-title": "Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii.",
      "volume": "54",
      "author": "Gorman",
      "year": "1966",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021050309534190000_R23",
      "doi-asserted-by": "crossref",
      "first-page": "151",
      "DOI": "10.1007/BF00033157",
      "article-title": "Photosystem-II heterogeneity\u2014the acceptor side.",
      "volume": "25",
      "author": "Govindjee",
      "year": "1990",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R24",
      "doi-asserted-by": "crossref",
      "first-page": "105",
      "DOI": "10.1007/BF00030070",
      "article-title": "The physiological significance of photosystem II heterogeneity in chloroplasts.",
      "volume": "23",
      "author": "Guenther",
      "year": "1990",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R25",
      "doi-asserted-by": "crossref",
      "first-page": "108",
      "DOI": "10.1016/0005-2728(88)90125-9",
      "article-title": "Photosystem stoichiometry and chlorophyll antenna size in Dunaliella salina (green algae).",
      "volume": "934",
      "author": "Guenther",
      "year": "1988",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "2021050309534190000_R26"
    },
    {
      "key": "2021050309534190000_R27",
      "doi-asserted-by": "crossref",
      "first-page": "462",
      "DOI": "10.1111/j.1529-8817.1989.tb00251.x",
      "article-title": "Nitrogen limitation in Isochrysis galbana (haptophyceae). I. Photosynthetic energy conversion and growth efficiencies.",
      "volume": "25",
      "author": "Herzig",
      "year": "1989",
      "journal-title": "J Phycol"
    },
    {
      "key": "2021050309534190000_R28",
      "doi-asserted-by": "crossref",
      "first-page": "655",
      "DOI": "10.1146/annurev.arplant.47.1.655",
      "article-title": "Regulation of light harvesting in green plants: indication by nonphotochemical quenching of chlorophyll fluorescence.",
      "volume": "47",
      "author": "Horton",
      "year": "1996",
      "journal-title": "Annu Rev Plant Physiol Plant Mol Biol"
    },
    {
      "key": "2021050309534190000_R29",
      "doi-asserted-by": "crossref",
      "first-page": "63",
      "DOI": "10.1007/BF02402263",
      "article-title": "Sulfur speciation and distribution in soils and above ground biomass of a boreal coniferous forest.",
      "volume": "16",
      "author": "Houle",
      "year": "1992",
      "journal-title": "Biogeochemistry"
    },
    {
      "key": "2021050309534190000_R30",
      "doi-asserted-by": "crossref",
      "first-page": "785",
      "DOI": "10.1111/j.1365-3040.1993.tb00500.x",
      "article-title": "In vivo photosynthetic electron transport does not limit photosynthetic capacity in phosphate-deficient sunflower and maize leaves.",
      "volume": "16",
      "author": "Jacob",
      "year": "1993",
      "journal-title": "Plant Cell Environ"
    },
    {
      "key": "2021050309534190000_R31"
    },
    {
      "key": "2021050309534190000_R32",
      "doi-asserted-by": "crossref",
      "first-page": "181",
      "DOI": "10.1104/pp.103.1.181",
      "article-title": "Photosystem II reaction center damage and repair in Dunaliella salina (green alga).",
      "volume": "103",
      "author": "Kim",
      "year": "1993",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R33",
      "doi-asserted-by": "crossref",
      "first-page": "313",
      "DOI": "10.1146/annurev.pp.42.060191.001525",
      "article-title": "Chlorophyll fluorescence and photosynthesis: the basics.",
      "volume": "42",
      "author": "Krause",
      "year": "1991",
      "journal-title": "Annu Rev Plant Physiol Plant Mol Biol"
    },
    {
      "key": "2021050309534190000_R34",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1007/0-306-48127-8_14",
      "article-title": "Photosystem II heterogeneity.",
      "volume-title": "Oxygeneic Photosynthesis: The Light Reactions.",
      "author": "Lavergne",
      "year": "1996"
    },
    {
      "key": "2021050309534190000_R35",
      "doi-asserted-by": "crossref",
      "first-page": "13698",
      "DOI": "10.1016/S0021-9258(18)92755-9",
      "article-title": "Co-regulation of a gene homologous to early light-induced genes in higher plants and \u03b2-carotene biosynthesis in the alga Dunaliella bardawil.",
      "volume": "266",
      "author": "Lers",
      "year": "1991",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021050309534190000_R36",
      "doi-asserted-by": "crossref",
      "first-page": "20892",
      "DOI": "10.1016/S0021-9258(19)36870-X",
      "article-title": "Cbr, an algal homolog of plant early light-induced proteins, is a putative zeaxanthin binding protein.",
      "volume": "268",
      "author": "Levy",
      "year": "1993",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021050309534190000_R37",
      "doi-asserted-by": "crossref",
      "first-page": "653",
      "DOI": "10.1080/00103628709367849",
      "article-title": "Effect of sulfur additions on soil and the nutrition of wheat.",
      "volume": "18",
      "author": "Mahler",
      "year": "1987",
      "journal-title": "Commun Soil Sci Plant Anal"
    },
    {
      "key": "2021050309534190000_R38",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1016/S0005-2728(05)80225-7",
      "article-title": "Dynamics of photosynthetic membrane composition and function.",
      "volume": "1058",
      "author": "Melis",
      "year": "1991",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "2021050309534190000_R39",
      "doi-asserted-by": "crossref",
      "first-page": "1196",
      "DOI": "10.1104/pp.92.4.1196",
      "article-title": "Activation of a reserve pool of photosystem II in Chlamydomonas reinhardtii counteracts photoinhibition.",
      "volume": "92",
      "author": "Neale",
      "year": "1990",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R40",
      "doi-asserted-by": "crossref",
      "first-page": "1369",
      "DOI": "10.2307/3870388",
      "article-title": "Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching.",
      "volume": "9",
      "author": "Niyogi",
      "year": "1997",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021050309534190000_R41",
      "doi-asserted-by": "crossref",
      "first-page": "101",
      "DOI": "10.1007/BF00030069",
      "article-title": "Inactive photosystem II centers.",
      "volume": "23",
      "author": "Ort",
      "year": "1990",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R42",
      "doi-asserted-by": "crossref",
      "first-page": "4791",
      "DOI": "10.1073/pnas.88.11.4791",
      "article-title": "Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii.",
      "volume": "88",
      "author": "Peltier",
      "year": "1991",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021050309534190000_R43",
      "doi-asserted-by": "crossref",
      "first-page": "919",
      "DOI": "10.1093/jxb/45.7.919",
      "article-title": "Photosynthesis and chlorophyll fluorescence in sunflower (Helianthus annuus L.) leaves as affected by phosphorus nutrition.",
      "volume": "45",
      "author": "Plesnicar",
      "year": "1994",
      "journal-title": "J Exp Bot"
    },
    {
      "key": "2021050309534190000_R44",
      "doi-asserted-by": "crossref",
      "first-page": "839",
      "DOI": "10.1104/pp.111.3.839",
      "article-title": "Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii.",
      "volume": "111",
      "author": "Quisel",
      "year": "1996",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R45",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1007/BF00001529",
      "article-title": "Both nitrogen and phosphorus limit plant production on young Hawaiian lava flows.",
      "volume": "32",
      "author": "Raich",
      "year": "1996",
      "journal-title": "Biogeochemistry"
    },
    {
      "key": "2021050309534190000_R46",
      "doi-asserted-by": "crossref",
      "first-page": "1775",
      "DOI": "10.1071/AR9931775",
      "article-title": "Effects of placement of elemental S and sulfate on the growth of two rice varieties under flooded conditions.",
      "volume": "44",
      "author": "Samosir",
      "year": "1993",
      "journal-title": "Aust J Agric Res"
    },
    {
      "key": "2021050309534190000_R47",
      "doi-asserted-by": "crossref",
      "first-page": "51",
      "DOI": "10.1007/BF00024185",
      "article-title": "Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.",
      "volume": "10",
      "author": "Schreiber",
      "year": "1986",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R48",
      "doi-asserted-by": "crossref",
      "first-page": "1053",
      "DOI": "10.1016/0038-0717(91)90043-J",
      "article-title": "Sulfur transformations and pool sizes in tropical forest soils.",
      "volume": "23",
      "author": "Stanko-Golden",
      "year": "1991",
      "journal-title": "Soil Biol Biochem"
    },
    {
      "key": "2021050309534190000_R49",
      "doi-asserted-by": "crossref",
      "first-page": "897",
      "DOI": "10.1111/j.0022-3646.1995.00897.x",
      "article-title": "Cytochrome f loss in astaxanthin-accumulating red cells of Haematococcus pluvialis (chlorophyceae): comparison of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polypeptides in red and green cells.",
      "volume": "31",
      "author": "Tan",
      "year": "1995",
      "journal-title": "J Phycol"
    },
    {
      "key": "2021050309534190000_R50",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1007/BF00033156",
      "article-title": "The use of chlorophyll fluorescence nomenclature in plant stress physiology.",
      "volume": "25",
      "author": "van Kooten",
      "year": "1990",
      "journal-title": "Photosynth Res"
    },
    {
      "key": "2021050309534190000_R51",
      "doi-asserted-by": "crossref",
      "first-page": "1645",
      "DOI": "10.1104/pp.44.11.1645",
      "article-title": "Photoreduction of 2,6-dichlorophenolindophenol by diphenylcarbazide. A photosystem 2 reaction catalyzed by tris-washed chloroplasts and subchloroplast fragments.",
      "volume": "44",
      "author": "Vernon",
      "year": "1969",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R52",
      "doi-asserted-by": "crossref",
      "first-page": "1817",
      "DOI": "10.1080/01904169409364849",
      "article-title": "Effect of sulfur additions on the yield and elemental composition of canola and spring wheat.",
      "volume": "17",
      "author": "Warman",
      "year": "1994",
      "journal-title": "J Plant Nutr"
    },
    {
      "key": "2021050309534190000_R53"
    },
    {
      "key": "2021050309534190000_R54",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1016/0005-2728(78)90137-8",
      "article-title": "Duroquinol as an electron donor for chloroplast electron transfer reactions.",
      "volume": "502",
      "author": "White",
      "year": "1978",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "2021050309534190000_R55",
      "doi-asserted-by": "crossref",
      "first-page": "981",
      "DOI": "10.1104/pp.104.3.981",
      "article-title": "Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth.",
      "volume": "104",
      "author": "Yildiz",
      "year": "1994",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021050309534190000_R56",
      "doi-asserted-by": "crossref",
      "first-page": "669",
      "DOI": "10.1104/pp.112.2.669",
      "article-title": "Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii.",
      "volume": "112",
      "author": "Yildiz",
      "year": "1996",
      "journal-title": "Plant Physiol"
    }
  ],
  "container-title": "Plant Physiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://academic.oup.com/plphys/article-pdf/117/1/129/37213710/plphys_v117_1_129.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "http://academic.oup.com/plphys/article-pdf/117/1/129/37213710/plphys_v117_1_129.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        5
      ]
    ],
    "date-time": "2024-01-05T13:04:00Z",
    "timestamp": 1704459840000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://academic.oup.com/plphys/article/117/1/129/6098557"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        5,
        1
      ]
    ]
  },
  "references-count": 56,
  "journal-issue": {
    "issue": "1",
    "published-online": {
      "date-parts": [
        [
          1998,
          5,
          1
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          1998,
          5,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1104/pp.117.1.129",
  "relation": {},
  "ISSN": [
    "1532-2548",
    "0032-0889"
  ],
  "subject": [],
  "published-other": {
    "date-parts": [
      [
        1998,
        5,
        1
      ]
    ]
  },
  "published": {
    "date-parts": [
      [
        1998,
        5,
        1
      ]
    ]
  }
}