Abstract
We have isolated and characterized two nuclear mutations which affect plastoquinone accumulation in maize. The mutations, hcf103 and hcf114, modify the same genetic locus. Plants homozygous for either mutant allele exhibit reduced PS II electron transport activity, reduced variable chlorophyll fluorescence and reduced delayed fluorescence yield. In these ways, hcf103 and hcf114 resemble previously described PS II mutants which lack stably assembled PS II reaction center complexes. However, unlike most previously described PS II mutants, hcf103 and hcf114 possess stable membrane-associated PS II complexes. Plastoquinone (PQ-9), which performs a variety of redox functions essential to normal non-cyclic electron transport, is severely depleted in the mutants. The lack of PS II electron transport activity is attributed to the absence of PQ-9. This is the first report of mutants deficient in PQ which do not also suffer serious pleiotropic defects.
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Abbreviations
- PS II:
-
Photosystem II
- PQ:
-
plastoquinone
- QA and QB :
-
primary and secondary stable electron acceptors of PS II
- HPLC:
-
high pressure liquid chromatography
- LDS-PAGE:
-
lithium dodecyl sulfate polyacrylamide gel electrophoresis
- TLC:
-
thin layer chromatography
References
Allen JF, Bennett J, Steinback KE and Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291: 25–29
Amesz J (1973) The function of plastoquinone in photosynthetic electron transport. Biochim Biophys Acta 301: 35–51
Andréasson L-E and Vänngård T (1988) Electron transport in Photosystems I and II. Ann Rev Plant Physiol Plant Mol Biol 39: 379–411
Arnon DI (1949) Copper enzymes in isolated chloroplasts: Polyphenoxidase in Beta vulgaris. Plant Physiol 24: 1–15
Baker NR, Markwell JP and Thornber JP (1982) Photobiochem Photobiophys 5: 181–190
Bennett J, Steinback KE and Arntzen CJ (1980) Proc Natl Acad Sci 77: 5253–5257
Bishop NI (1959) The reactivity of a naturally occurring quinone (Q-255) in photochemical reactions of isolated chloroplasts. Proc Natl Acad Sci 45: 1696–1702
Bishop NI and Wong J (1971) Observations on Photosystem II mutant of Scenedesmus. Pigments and proteinaceous components of the chloroplasts. Biochim Biophys Acta 234: 433–445
Camm EL and Green B (1980) Fractionation of thylakoid membranes with the non-ionic detergent octyl-β-D glucopyranoside. Plant Phys 66: 428–432
Clayton RK (1970) Light and Living Matter, The Physical Part, Vol 1, p 87. McGraw Hill, New York
Cook WB (1988) Isolation and Characterization of Photosynthesis Mutants from a Robertson's Mutator Line of Maize (Zea mays). PhD Dissertation, University of Missouri, Columbia, Missouri
Crane FL, Widmer C, Lester RL and Hatefi Y (1959) Studies on the electron transport system. XV. Coenzyme Q and the succinoxidase activity of the electron transport particle. Biochim Biophys Acta 31: 476–489
Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1986) X-ray structure analysis of a membrane protein complex: Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomanas viridis. J Mol Biol 180: 385–398
Delepelaire P and Chua N-H (1979) Lithium dodecyl sulfate/polyacrylamide gel electrophoresis of thylakoid membranes at 4°C: Characterizations of two additional chlorophyll a-protein complexes. Proc Natl Acad Sci 76: 111–115
Delley RA (1964) Thin-layer chromatography of naturally occurring quinones and hydroquinones. Analytical Biochem 7: 240–246
Diner BA and Petrouleas V (1987) Light induced oxidation of the acceptor-side Fe(II) of Photosystem II be exogenous quinones acting through the QB binding site. II. Blockage by inhibitors and their effects on the Fe(III) EPR spectra. Biochim Biophys Acta 893: 138–148
Diner BA, Ries DF, Cohen BN and Metz JG (1988) COOH-terminal processing of polypeptide D1 of the Photosystem II reaction center of Scenedesmus obliquus is necessary for the assembly of the oxygen-evolving complex. J Biol Chem 263: 8972–8980
Epel BL and Levine RP (1971) Mutant strains of Chlamydomonas rienhardtii with lesions on the oxidizing side of Photosystem II. Biochem Biophys Acta 226: 154–160
Epel BL, Butler WL and Levine RP (1972) A spectroscopic analysis of low-fluorescent mutants of Chlamydomonas reinhardti blocked in their water-splitting oxygen evolving apparatus. Biochem Biophys Acta 275: 395–400
Goodwin and Mercer (1983) Terpenoid quinones and chromanols. In: Introduction to Plant Biochemistry, pp 48–462. Pergamon, Oxford
Horton P and Black MT (1980) Activation of adenosine 5′ triphosphate-induced quenching of chlorophyll fluorescence by reduced plastoquinone. FEBS Lett 119: 141–144
Itoh S, Tan X-S and Satoh K (1986) Interaction of the high-spin Fe atom in the Photosystem II reaction center with the quinones QA and QB in purified oxygen evolving PS II reaction center complex in PS II particles. FEBS Lett 205: 275–281
Janiskowska W, Michalski W and Kasprzyk Z (1976) Prenylquinones and alpha tocopherol in Calendula officinalis. Phytochem 15: 125–127
Jursinic PA (1986) Delayed luminescence: Current concepts and status. In: Govindjee, Amesz J and Fork DC (eds) Light Emission by Plant and Bacteria, pp 291–328. Academic Press, New York
Kofler M (1946) In: Festschrift Emil Christoph Barell, pp 199–212. Hofman-LaRoche, Basile
Krueger RG and Miles D (1981) Photosynthesis in tall fescue: III. Rates of electron transport in a polyploid series of tall fescue plants. Plant Physiol 68: 1110–1114
Lavorel J (1975) In: Govindjee (ed) Bioenergetics of Photosynthesis, pp 223–317. Academic Press, New York
Leto KJ, Bell E and McIntosh L (1985) Assembly of Photosystem II: Accelerated turnover of chloroplast-encoded polypeptides in a nuclear mutant lacking Photosystem II. In: Steinback KE, Bonitz S, Arntzen CJ and Bogorad L (eds) Molecular Biology of the Photosynthetic Aparatus, pp 39–45. Cold Spring Harbor Laboratory Press
Levine RP and Gorman DS (1966) Photosynthetic electron transport chains of Chlamydomonas reinhardtii: IV. Light induced absorbance changes in chloroplast fragments of the wild type and mutant strains. Plant Physiol 41: 1293–1300
Malkin S (1977) In: Barber J (ed) Primary Processes in Photosynthesis, pp 349–431. Elsevier, North-Holland Biomedical Press, Amsterdam
Maroc J and Garnier J (1979) Characterization of new strains of non-photosynthetic mutants of Chlamydomonas reinhardtii: II. Quinones and cytochromes b-559, b-563 and c-553 in twelve mutants having impaired Photosystem II function. Plant and Cell Physiol 20: 1029–1040
Mayfield SP, Rahire M, Frank G, Zuber H and Rochaix J-D (1987) Expression of the nuclear gene encoding the oxygen-evolving enhancer protein 2 is required for high levels of photosynthetic oxygen evolution in Chlamydomonas reinhardtii. PNAS 84: 749–753
McCauley SW and Melis A (1986) Quantitation of plastoquinone photoreduction in spinach chloroplasts. Photosynth Res 8: 3–16
McComb JC, Stein RR and Wraight CA (1990) Investigations on the influence of head group substitution and isoprene side chain length in the function of primary and secondary quinones of bacterial reaction centers. Biochem Biophys Acta 1015: 156–171
Metz JG and Miles D (1982) Use of a nuclear mutant of maize to identify components of Photosystem II. Biochem Biophys Acta 681: 95–102
Metz JG, Krueger RG and Miles D (1984) Chlorophyll-protein complexes of a Photosystem II mutant of maize. Plant Physiol 75: 238–241
Metz JG, Wong J and Bishop NI (1980) Changes in electrophoretic mobility of a chloroplast membrane polypeptide associated with the loss of the oxidizing side of Photosystem II in low fluorescent mutants of Scenedesmus. FEBS Lett 114: 61–66
Miles D (1980) Mutants of hgher plants: Maize. In: San Pietro A (ed) Methods in Enzymology, Photosynthesis, Part C, Vol 69, pp 3–23. Academic Press, New York
Miles D (1982) The use of mutations to probe photosynthesis in higher plants. In: Edelman M, Hallick RB and Chua N-H (eds) Methods in Chloroplast Molecular Biology, pp 75–107. Elsevier Press, Amsterdam
Mohanty N, Vass I and Demeter S (1989) Copper toxicity affects Photosystem II electron transport at the secondary quinone acceptor, QB. Plant Physiol 90: 175–179
Nanba O and Satoh K (1987) Isolation of Photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc. Natl Acad Sci USA 84: 109–112
Petrouleas V and Diner BA (1987) Light induced oxidation of the acceptor-side Fe(II) of Photosystem II by exogenous quinones acting through the QB binding site. I. Quinones, kinetics and pH dependence. Biochem Biophys Acta 893: 126–137
Robertson DS (1978) Characterization of a mutator system in maize. Mutation Res 51: 21–28
Rochaix J-D and Erickson J (1988) Function and assembly of Photosystem II: Genetic and molecular analysis. Trends in Biochemical Science 13: 56–59
Schulze-Siebert D and Shultz G (1987) Full automony in isoprenoid synthesis in spinach chloroplasts. Plant Physiol Biochem 25: 145–153
Schulze-Siebert D, Homeyer U, Soll J and Shultz G (1987) Synthesis of plastoquinone-9, α-tocopherol and phylloquinone (Vitamin K1) and its integration in chloroplast carbon metabolism of higher plants. In: Stumpf PK, Mudd JB and Nes WD (eds) The Metabolism, Structure and Function of Plant Lipids pp 29–36. Plenum, NY
Shultz G, Huchzermeyer Y, Keupke B and Bichel H (1976) On the intracellular site of biosynthesis of α-tocopherol in Hordeum vulgare. Physochem 15: 1383–1386
Smillie and Levine RP (1962) The photosynthetic electron transport chain of Chlamydomonas reinhardtii: II. Components of the triphosphate nucleotide-reductive pathway in wild type and mutant strains. J Biol Chem 238: 4058–4062
Somerville CR (1986) Analysis of photosynthesis with mutants of higher plants and algae. Ann Rev Plant Physiol 37: 467–507
Sunblad L-G (1988) Dark reduction of QA in intact barley leaves as an effect of lowered CO2 concentration monitored by chlorophyll a luminescence and chlorophyll a F0 dark fluorescence. Biochem Biophys Acta 936: 429–434
Threlfall DR (1982) Biosynthesis of biological important meroterpenoid quinones and chromanols. In: Wintermans JFGM and Kuipers (eds) Biochemistry and Metabolism of Plant Lipids. Elsevier, Oxford
Vass I, Mohanty N and Demeter S (1988) Photoinhibition of electron transport activity of Photosystem II in isolated thylakoids studied by thermoluminescence and delayed luminescence. Z Naturforsh 43c: 871–876
Warncke K and Dutton PL (1990) Resolution of in situ interaction energies between molecules and the reaction center QA site: Implications for electron transfer function. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 1, pp 157–160. Kluwer Academic Publishers, Dordrecht, the Netherlands
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Cook, W.B., Miles, D. Nuclear mutations affecting plastoquinone accumulation in maize. Photosynth Res 31, 99–111 (1992). https://doi.org/10.1007/BF00028787
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DOI: https://doi.org/10.1007/BF00028787