Am. J. Bot.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (7)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lebkuecher, J. G
Right arrow Articles by Minton, D. A
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lebkuecher, J. G
Right arrow Articles by Minton, D. A
Agricola
Right arrow Articles by Lebkuecher, J. G
Right arrow Articles by Minton, D. A
(American Journal of Botany. 1999;86:1087-1092.)
© 1999 Botanical Society of America, Inc.

Development of photosystem-II activity during irradiance of etiolated Helianthus (Asteraceae) seedlings1

Jefferson G Lebkuecher2, Kurt A Haldeman, Christine E Harris, Sonia L Holz, Sary A Joudah and Darcy A Minton

Department of Biology, Austin Peay State University, Clarksville, Tennessee 37044

Received for publication February 25, 1998. Accepted for publication December 21, 1998.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Light-induced development of photosystem (PS)-II activity was followed during irradiance of etiolated Helianthus annuus (sunflower) cotyledons using chlorophyll a fluorescence. Cotyledons from seedlings grown in continuous darkness for 6 d were exposed to 100 µmol photons·m-2·s-1 for time periods of 1, 3, 6, and 12 h. Associated with increased time of irradiance exposure were significant: (1) increases in concentration of PS II, (2) increases in quantum efficiency of PS II, (3) decreases in the ratio of PS-II quinoneB (QB)-nonreducing centers to total PS-II centers (PS-II QB-nonreducing centers + PS-II QB-reducing centers), and (4) decreases in the ratio of slow PS-II QB-reducing centers to total PS-II QB-reducing centers (fast PS-II QB-reducing centers + slow PS-II QB-reducing centers). The results support the hypotheses that development of PS II involves assembly of complexes which initially cannot reduce QB and that heterogeneous aspects of PS-II pools during chloroplast maturation may represent different developmental states.

Key Words: Asteraceae • chlorophyll a fluorescence; etioplast • Helianthus • photosystem-II development; photosystem-II heterogeneity; quinoneB


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
During germination of angiosperm seeds in darkness, proplastids develop into pale-yellow etioplasts, which lack the structural components and organization necessary for photosynthesis (Leech, 1984 ). Conversion of etioplasts to chloroplasts occurs when the shoot emerges from the soil and is exposed to light. Coordination of several phytochrome-mediated events is required for this conversion (Hendricks and Van der Woude, 1993 ) and includes transformation of prolamellar bodies into thylakoids (Gunning and Steer, 1975 ), photoreduction of protochlorophyllide to chlorophyllide and subsequent addition of the polyisoprene-phytyl moiety to yield chlorophyll (Klein, Katz, and Neeman, 1977 ; Castelfranco and Beale, 1983 ), and synthesis of the four major protein complexes of the thylakoid membranes: photosystem (PS) II, PS I, cytochrome-B6f complex, and ATP synthase (Ono, Kajikawa, and Inoue, 1986 ; Mullet, 1988 ).

PS II consists of ~22 polypeptides, the synthesis of which requires phytochrome-mediated expression of nuclear and chloroplast genomes (Kawaguchi et al., 1992 ; Pakrasi and Vermaas, 1992 ). The polypeptides, pigments, and prosthetic components that comprise PS II are assembled into the light-harvesting complexes of PS II (LHC II), the oxygen-evolving complex, and the PS-II core (Hansson and Wydrzynski, 1990 ; Melis, 1991 ). Several aspects of heterogeneity within populations of PS II have been observed and during chloroplast development may represent different stages of PS-II construction (Guenther, Nemson, and Melis, 1990 ).

One aspect of PS-II heterogeneity is the size of LHC II, known as {alpha}, ß heterogeneity (Melis, 1985 ). PS IIß contains the inner complement of LHC II (LHC-II inner) of ~130 chlorophyll (chl) molecules. PS II{alpha} has the same components as PS IIß plus the peripheral component of LHC II (LHC-II peripheral) for a total of 210 or more chl molecules (Guenther, Nemson, and Melis, 1990 ). Larsson, Anderson, and Anderson (1987) and Ghirardi and Melis (1988) suggested that PS IIß is a precursor to PS II{alpha}. Guenther, Nemson, and Melis (1990) provided evidence that this developmental sequence occurs during the synthesis of PS II in Chlamydomonas reinhardtii.

Other aspects of PS-II heterogeneity involve the process of electron transport from quinoneA (QA), the first stable electron acceptor of PS II, to quinoneB (QB), the second stable electron acceptor of PS II (Lavergne, 1982 ). Approximately 20–25% of healthy, mature chloroplasts do not transfer electrons from QA to QB (Black, Brearley, and Horton, 1986 ; Graan and Ort, 1986 ; Guenther, Nemson, and Melis, 1988 ; Cao and Govindjee, 1990 ). QB-nonreducing centers may constitute a developmental and/or repair state of PS II in which electron transfer between QA-1 and QB has yet to be established (Guenther and Melis, 1990 ). This hypothesis is supported by increased concentrations of QB-nonreducing centers following environmental stresses that affect PS II (Godde and Hefer, 1994 ; Klinkovsky and Naus, 1994 ; Lebkuecher, 1997 ) and decreasing ratios of QB-nonreducing centers to total PS II during chloroplast maturation in Chlamydomonas reinhardtii (Guenther, Nemson, and Melis, 1990 ). Another aspect of heterogeneity is evident among QB-reducing centers relative to the rate of electron transfer between QA-1 and QB. This heterogeneity is referred to as fast QB-reducing center, slow QB-reducing center heterogeneity (Govindjee, 1995 ; Strasser, Srivastava, and Govindjee, 1995 ) and may reflect differences in the efficiency of the oxygen-evolving complex.

Environmental controls that regulate the synthesis and activities of chloroplast components vary among photoautotrophs (Mullet, 1988 ; Lebkuecher and Eickmeier, 1992 ). For example, gymnosperms, mosses, ferns, and most algae produce chl in the dark (Burgess, 1989 ). Several species of algae, i.e., Chlamydomonas reinhardtii, synthesize some proteins associated with primary photochemistry in the dark that are light-regulated in angiosperms (Hoober, Siekevitz, and Palade, 1969 ; Guenther, Nemson, and Melis, 1990 ). Changes during the photomorphic conversion of angiosperm etioplasts to chloroplasts have been examined relative to the formation of thylakoid ultrastructure (Baker, Hardwick, and Jones, 1975 ; Baker and Leech, 1977 ; Boardman, 1977 ; Krol and Huner, 1989 ), protochlorophyllide conversion to chl (Castelfranco, Rich, and Beale, 1974 ; Lew and Tsuji, 1982 ), expression of nuclear and chloroplast genes associated with primary photochemistry (Mullet, 1988 ; Hashimoto, Akasaka, and Yamamoto, 1993 ), assembly of LHC II (Dreyfuss and Thornber, 1994 ), and appearance of electron transport activity (Baker and Leech, 1977 ; Krol and Huner, 1989 ; Ohashi, Tanaka, and Tsuji, 1989 ). Several researchers have used chl a fluorescence to examine PS-II photochemistry during the development of angiosperm chloroplasts (Baker and Butler, 1976 ; Akoyunoglou, 1977 ; Webber et al., 1984 , 1986 ; Percival et al., 1986 ). The present study extends these previous studies and examines changes in PS-II heterogeneity during the conversion of Helianthus annuus L. etioplasts to chloroplasts by measuring the chl a fluorescence characteristics of etiolated cotyledons exposed to light for various time periods.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant growth and treatments
Helianthus annuus L. achenes (Carolina Biological Supply Company, Burlington, North Carolina, USA) were potted in water-saturated potting soil. The pots were placed in continuous darkness for 6 d at 25°C and 50–65% relative humidity (RH) or placed under continuous irradiance for 6 d (100 µmol photons·m-2·s-1 white light, 24-h photoperiod, 25°C, and 50–65% RH). Excised cotyledons from dark-grown plants were placed adaxial side up on water-saturated Whatman number 1 filter-paper circles in petri dishes (100 x 15 mm) and exposed to 100 µmol photons·m-2·s-1 white light, 25°C, and 50–65% RH for time periods of 1, 3, 6, and 12 h.

Chlorophyll a fluorescence
Chl a fluorescence transients were measured at 25°C with a Plant Efficiency Analyzer (PEA; Hansatech Limited, Kings Lynn, Norfolk PE304NE, UK). Cotyledons were placed adaxial side up inside leafclips and allowed to dark adapt for 5 min to oxidize primary electron acceptors prior to fluorescence induction. All fluorescence transients were recorded during a 2-s pulse of red light (2000 µmol photons·m-2·s-1) provided by an array of six light-emitting diodes (peak at 650 nm) focused onto a 4-mm diameter area of the cotyledon. The fluorescence signals were detected using a PIN-photodiode after passing through a long pass filter (50% transmission at 720 nm). Nomenclature of fluorescence cardinal points (Fig. 1) is as described by Schreiber and Neubauer (1987) .



View larger version (13K):
[in this window]
[in a new window]
  		Fig. 1. Example chlorophyll a fluorescence curve (solid line) showing cardinal points. Figure Abbreviations: FO = origin fluorescence yield, FM = maximum fluorescence yield, FV(M) = maximum variable fluorescence yield, FI1 = first inflection of the variable fluorescence rise, FI2 = second inflection of the variable fluorescence rise.

 
Origin fluorescence yield (FO) was calculated automatically by the instrument by determining the line of best fit through the data points from the first 4–12 µs of fluorescence induction. Maximum fluorescence yield (FM) was determined as the maximum fluorescence level. Relative quantification of PS II was determined as the maximum variable fluorescence yield [FV(M)] and calculated as FV(M) = FM - FO (Guenther, Nemson, and Melis, 1990 ; Strasser, Srivastava, and Govindjee, 1995 ). Quantum efficiency of PS II was determined as FV(M)/FM (Kitajima and Butler, 1975 ; Krause and Weis, 1991 ). Relative quantification of quinoneB (QB)-nonreducing centers was estimated as the amplitude of variable fluorescence rise to the first inflection (FI1; Guenther, Nemson, and Melis, 1988 , 1990 ; Cao and Govindjee, 1990 ). Relative quantification of QB-reducing centers was estimated as the amplitude of the FI1 to FV(M) rise and calculated as FV(M) - FI1 (Schwab, Schreiber, and Heber, 1989 ). The fraction of QB-nonreducing centers to total PS II was estimated as FI1/FV(M) (Guenther, Nemson, and Melis, 1988 , 1990 ; Cao and Govindjee, 1990 ; Srivastava, Strasser, and Govindjee, 1995 ). Relative quantification of fast QB-reducing centers was estimated as the amplitude of variable fluorescence rise from the first inflection (FI1) to the second inflection (FI2) and calculated as FI2 - FI1 (Schreiber and Neubauer, 1987 ; Strasser, Srivastava, and Govindjee, 1995b ). The relative concentration of slow QB-reducing centers and the ratio of slow QB-reducing centers to total QB-reducing centers were calculated as FV(M) - FI2 and [(FV(M) - FI2]/[FV(M) - FI1], respectively (Strasser, Srivastava, and Govindjee, 1995 ).

Chlorophyll concentration
Chlorophyll was extracted by grinding excised leaf discs (7 mm2) with a mortar and pestle for 2 min in 80% acetone buffered with 2.5 mmol/L NaPhosphate buffer, pH 7.8 at 25°C. The homogenate was filtered through Whatman number 1 filter-paper circles, and the chl a + chl b content determined spectrophotometrically. Chl concentrations were calculated following the equations of Porra, Thomson, and Kriedemann (1989) .

Statistical analyses
Statistical procedures followed Sokal and Rohlf (1995) and Day and Quinn (1989) . The experimental design employed a fixed-model, one-way ANOVA with the factor being irradiance time (Zar, 1984 ). A logarithmic transformation was applied to the data prior to ANOVA to equalize variances among cells. All treatment means were based on four replicates. Data from cotyledons exposed to irradiance for 1, 3, 6, and 12 h were compared using nonorthoganal, T-method tests (Sokal and Rohlf, 1995 ). Means were determined as significantly different if they were dissimilar at or below the experimentwise error rate of {alpha} = 0.05 probability level. Assay means from cotyledons exposed to 12 h of irradiance and 6 d of irradiance were compared with each other using T-method tests. Means were determined as significantly different if they were dissimilar at or below the {alpha} = 0.05 probability level.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Chlorophyll concentration of cotyledons increased significantly with increased time of irradiance exposure up to 12 h (Table 1). The mean chl concentration of cotyledons from dark-grown seedlings followed by exposure to 12 h of 100 µmol photons·m-2·s-1 did not differ significantly from cotyledons of seedlings grown for 6 d at 100 µmol photons·m-2·s-1, 24-h photoperiod (Table 1).


View this table:
[in this window]
[in a new window]
  		Table 1. Chlorophyll concentration and chlorophyll a fluorescence characteristics of cotyledons from Helianthus annuus seedlings germinated in continuous darkness for 6 d followed by 1, 3, 6, and 12 h of irradiance exposure (100 {µ}mol photons · m-2·s-1) and from seedlings germinated at continuous irradiance (100 {µ}mol photons ·m-2·s-1) for 6 d. Means ± 1 SE represent four replicates. Assay means from 1, 3, 6, and 12 h irradiance-exposed cotyledons are significantly different if followed by a different letter at the experimentwise error rate of {{alpha}} = 0.05. Assay means from cotyledons exposed to 12 h and 6 d of irradiance are not significantly different from each other at {{alpha}} = 0.05

 
Chl a fluorescence characteristics were affected significantly by irradiance exposure time (Table 1). The mean chl a fluorescence characteristics of cotyledons from dark-grown seedlings followed by exposure to 12 h of 100 µmol photons·m-2·s-1 did not differ significantly from cotyledons of seedlings grown for 6 d at 100 µmol photons·m-2·s-1, 24-h photoperiod (Table 1). Chl a fluorescence characteristics prior to QA reduction were significantly affected by irradiance exposure time as indicated by significantly decreased origin fluorescence yields (FO) and FO to chl ratios with increased irradiance-exposure time (Table 1; Srivastava, Strasser, and Govindjee, 1985; Krause and Weis, 1991 ).

The quantum efficiency of PS II increased dramatically from 1 h to 3 h of irradiance exposure times and gradually increased to typical values (~0.83; Björkman and Demmig, 1987 ; Lebkuecher and Eickmeier, 1991 ) by 12 h of irradiance exposure (Table 1). Light-induced synthesis of PS II is evident by the significantly increased concentrations of PS II with increased irradiance exposure time. Slower rates of PS-II center synthesis relative to chl synthesis following 3 h of irradiance are indicated by the significantly decreased PS II/chl values.

Even among the background of continuing PS-II synthesis, there is a reduction in the concentration of QB-nonreducing centers following 6 h of irradiance (Table 2). Increased QB-reduction capacity with increased irradiance time is also evident from the significantly increased concentrations of QB-reducing centers and decreased ratios of QB-nonreducing center to total PS II. The highest ratio of slow QB-reducing centers to total QB-reducing centers occurred following the largest increase in the rate of PS-II synthesis, from the 1-h to 3-h irradiance period, and then decreased significantly during the 3-h to 12-h irradiance period (Table 2).


View this table:
[in this window]
[in a new window]
  		Table 2. Heterogeneous aspects of PS II determined by chlorophyll a fluorescence characteristics of cotyledons from Helianthus annuus seedlings germinated in continuous darkness for 6 d followed by 1, 3, 6, and 12 h of irradiance exposure (100 {µ}mol photons·m-2·s-1) and from seedlings germinated at continuous irradiance (100 {µ}mol photons·m-2·s-1) for 6 d. Means ± 1 SE represent four replicates. Assay means from 1, 3, 6, and 12 h irradiance-exposed cotyledons are significantly different if followed by a different letter at the experimentwise error rate of {{alpha}} = 0.05. Assay means from cotyledons exposed to 12 h and 6 d of irradiance are not significantly different from each other at {{alpha}} = 0.05

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The time course of light-induced development of chloroplast components is dependent on irradiance conditions and is highly variable among species, requiring minutes to days (Boardman, 1977 ; Possingham, 1980 ). Conversion of Helianthus annuus etioplasts to chloroplasts was complete by 12 h as indicated by the lack of significant differences in chl concentration and chl a fluorescence characteristics of 12-h irradiated cotyledons relative to those grown under continuous irradiance for 6 d. That conversion is complete by 12 h of irradiance exposure is also supported by the facts that following 12 h of irradiance, quantum efficiency of PS II is 0.85 and the QB-nonreducing center to PS II ratio is 0.30, values that are typical of mature plants (Eickmeier, Lebkuecher, and Osmond, 1992 ; Lebkuecher and Eickmeier, 1993 ; Strasser, Srivastava, and Govindjee, 1995 ). Somewhat similar time courses to maximum quantum efficiencies of PS II occur during irradiance of etiolated bean (Phaseolus vulgaris variety red kidney) leaves (Baker and Butler, 1976 ; Akoyunoglou, 1977 ). Akoyunoglou (1977) found that during continuous irradiance at ~180 µmol photons·m-2·s-1, the quantum efficiency of PS II increased from 0.30 following 1 h of irradiance to 0.67 following 12 h to a steady state of 0.72 following 24 h.

Light-induced conversion of Helianthus annuus etioplasts to chloroplasts includes the synthesis of PS-II complexes that cannot initially reduce QB. This conclusion is based on the high QB-nonreducing center to PS II ratio following 1 h of irradiance exposure of etiolated cotyledons (Table 2). During irradiance exposure up to 12 h, PS-II complexes are synthesized and then converted from QB-nonreducing centers to QB-reducing centers as indicated by significantly increased concentrations of PS II and significantly decreased ratios of QB-nonreducing center to PS II with increased times of irradiance. These results are consistent with the findings of Guenther, Nemson, and Melis (1990) , who provided evidence that QB-nonreducing centers are synthesized and then converted to QB-reducing centers during the construction of PS II in Chlamydomonas reinhardtii.

Photoactivation of the oxygen-evolving complex (OEC) requires the incorporation of Mn and binding to the PS-II core (Eickmeier, Lebkuecher, and Osmond, 1992 ; Hashimoto, Akasaka, and Yamamoto, 1993 ). Decreased rates of water oxidation by OEC inhibitors or by Mn depletion significantly reduce the concentration of fast QB-reducing centers, yet have no or minor effects on the concentration of slow QB-reducing centers (Schreiber and Neubauer, 1987 ). This suggests that fast QB-reducing center, slow QB-reducing center heterogeneity may reflect differences in OEC efficiency. The decreased ratio of slow to total QB-reducing centers during the 3-h to 12-h irradiance period (Table 2) suggests possible increased OEC efficiency. During the 1-h to 3-h irradiance period, the significant increase in the ratio of slow QB-reducing centers to total QB-reducing centers together with the significant decrease in the ratio of QB-nonreducing centers to total QB-reducing centers suggests that the development of water-oxidation activity may lag behind the development of QA to QB electron-transport capacity. This possibility is consistent with analysis of PS-II proteins during irradiance-induced greening of Hordeurn vulgure L. (barley) etioplasts, which indicates that the rate-limiting step during PS-II construction is the attachment of OEC components to the PS-II core (Hashimoto, Akasaka, and Yamamoto, 1993 ).

Changes in FO may represent alterations in energy transformations prior to QA reduction (Krause and Weis, 1991 ). Such alterations may include changes in: (1) integration of free chl into LHC II (Cahen et al., 1976 ; Cahen, Malkin, and Ohad, 1977 ; Ohashi, Tanaka, and Tsuji, 1989 ; Franck et al., 1995 ), (2) efficiency of resonance-energy transfer within LHC II (Mathis and Paillotin, 1981 ; Joshi and Mohanty, 1995 ), (3) distribution of excitation energy between PS II and PS I (Krause and Weis, 1991 ), (4) functional attachment of LHC II to the PS-II core (Schreiber and Armond, 1978 ), and (5) efficiency of excitation-energy trapping by PS II (Russell et al., 1995 ). In the present study, the significantly decreased FO and FO/chl values with increased irradiance exposure most likely reflect increased development of PS-II function as suggested by increased concentrations of PS II with increased irradiance exposure. Similar magnitudes of decreased FO values have been observed along the length of young wheat (Triticum species) leaves from the basal meristem to the tip (Baker and Butler, 1976 ; Percival et al., 1986 ).

In mature vascular plants, PS II{alpha} typically accounts for ~75% and PS IIß for ~25% of total PS II (Melis, 1985 ; Ghirardi and Melis, 1988 ; Greene, Staehelin, and Melis, 1988 ). Changes in the ratio of PS II{alpha} to PS IIß occur during development of PS II and during acclimation to different irradiance conditions (Guenther, Nemson, and Melis, 1988 , 1990 ; Harrison, Melis, and Allen, 1992 ; Falk, Bruce, and Huner, 1994 ). A change from small to large LHC II during the conversion of sunflower etioplasts to chloroplasts during the 3-h to 12-h irradiance period is indicated by decreased values for PS II/chl (Table 1; Cahen and Malkin, 1976 ; Humbek and Bishop, 1986 ; Franck et al., 1995 ) and support conclusions that PS IIß is a precursor to PS II{alpha} (Larsson, Anderson, and Anderson, 1987 ; Ghirardi and Melis, 1988 ; Guenther, Nemson, and Melis, 1990 ).

Our paper provides information on the development of primary photochemistry during the light-induced conversion of Helianthus annuus etioplasts to chloroplasts. The results support the hypothesis that synthesis of PS II involves assembly of complexes that initially have small LHC II and are deficient in electron-transfer capacity between QA and QB (Cahen and Malkin, 1976 ). The results also suggest that during chloroplast maturation heterogeneous aspects of PS-II pools may represent different developmental states (Guenther, Nemson, and Melis, 1990 ).


   FOOTNOTES
 
1 The authors thank Dr. David M. O'Drobinak and Steven M. Lebkuecher for technical assistance, and Drs. William G. Eickmeier, Govindjee, Thomas G. Owens, and Thomas G. Sharkey for reviewing the manuscript and offering suggestions for improvement. The research was funded by the Department of Biology and The Center for Field Biology, both of Austin Peay State University. Back

2 Author for correspondence. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Akoyunoglou, G. 1977 Development of the photosystem II unit in plastids of bean leaves greened in periodic light. Archives of Biochemistry and Biophysics 183: 571–580.[CrossRef][ISI][Medline]

Baker, N. L., and W. L. Butler. 1976 Development of the primary photochemical apparatus of photosynthesis during greening of etiolated bean leaves. Plant Physiology 58: 526-529.[Abstract/Free Full Text]

———, K. Hardwick, and P. Jones. 1975 Biochemical and physiological aspects of leaf development in cocoa (Threobroma cacao). New Phytologist 75: 513–518.[CrossRef][ISI]

———, and R. M. Leech. 1977 Development of photosystem I and photosystem II activities in leaves of light-grown maize (Zea mays). Plant Physiology 60: 640–644.[Abstract/Free Full Text]

Björkman, O., and B. Demmig. 1987 Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origin. Planta 170: 489–504.[CrossRef][ISI]

Black, M. T., T. H. Brearley, and P. Horton. 1986 Heterogeneity in chloroplast photosystem II. Photosynthesis Research 89: 193–207.

Boardman, N. K. 1977 Development of Chloroplast Structure and Function. In V. A. Trebst and M. Avron [eds.], Encyclopedia of plant physiology, vol. 5, 149–167, Springer-Verlag, Berlin.

Burgess, J. 1989 An introduction to plant cell development. Cambridge University Press, Cambridge.

Butler, W. L. 1977 Chlorophyll fluorescence: a probe for electron transfer and energy transfer. In V. A. Trebst and M. Avron [eds.], Encyclopedia of plant physiology, vol. 5, 149–167, Springer-Verlag, Berlin.

Cahen, D., S. Malkin, and I. Ohad. 1977 Development of photosystem II in Chlamydomonas reinhardi mutants. Plant Physiology 60: 845–849.[Abstract/Free Full Text]

———, ———, S. Shochat, and I. Ohad. 1976 Development of photosystem II complex during greening of Chlamydomonas reinhardi y-1. Plant Physiology 58: 257–267.[Abstract/Free Full Text]

Cao, J., and Govindjee. 1990 Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes. Biochimica et Biophysica Acta 1015: 180–188.[Medline]

Castelfranco, P. A., and S. I. Beale. 1983 Chlorophyll biosynthesis: recent advances and areas of current interest. Annual Review of Plant Physiology 34: 241–78.[ISI]

———, P. M. Rich, and S. I. Beale. 1974 The abolition of the lag phase in greening cucumber cotyledons by exogenous {delta}-aminolevulinie acid. Plant Physiology 53: 615–618.[Abstract/Free Full Text]

Cleland, R. E., and A. Melis. 1987 Probing the events of photoinhibition by altering electron transport activity and light-harvesting capacity in chloroplast thylakoids. Plant, Cell and Environment 10: 747–752.

Day, R. H., and G. P. Quinn. 1989 Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59: 433–463.[CrossRef][ISI]

Demmig, B., K. Winter, A. Krüger, and F.-C. Czygan. 1987 Photoinhibition and zeaxanthin formation in leaves. Plant Physiology 84: 218–224.[Abstract/Free Full Text]

Demmig-Adams, B. 1990 Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta 1020: 1–24.[CrossRef]

Dreyfuss, B. W., and J. P. Thornber. 1994 Assembly of the Light-Harvesting Complexes (LHCs) of Photosystem II. Plant Physiology 106: 829–839.[Abstract]

Eickmeier, W. G. 1979 Photosynthetic recovery in the resurrection plant Selaginella lepidophylla after wetting. Oecologia 39: 93–106.[CrossRef][ISI]

———, J. G. Lebkuecher, and C. B. Osmond. 1992 Photosynthetic water oxidation and water stress in plants. In G. N. Somero, C. B. Osmond, and C. L. Bolis [eds.], Water and life: comparative water relationships at the organismic, cellular, and molecular levels, 223–239. Springer-Verlag, Berlin.

Falk, S., D. Bruce, and N. P. A. Huner. 1994 Photosynthetic performance and fluorescence in relation to antenna size and absorption cross-sections in rye and barley grown under normal and intermittent light conditions. Photosynthesis Research 42: 145–155.[CrossRef]

Ford, M. J., and H. Kasemir. 1980 Correlation between 5-aminolaevulinate accumulation and protochlorophyll photoconversion. Planta 150: 206–210.[CrossRef][ISI]

Franck F., B. Schoefs, X. Barthelemy, B. Mysliwa-Kurdziel, K. Strzalka, and R. Popovic. 1995 Protection of native chlorophyll(ide) forms and of photosystem II against photodamage during early stages of chloroplast differentiation. Acta Physiologiae Plantarum 17: 123–132.

Ghirardi, M. L., and A. Melis. 1988 Chlorophyll b-deficiency in soybean mutants. I. Effects on photosystem stoichiometry and chlorophyll antenna size. Biochimica et Biophysica Acta 932: 130–137.[CrossRef]

Gilmore, A. M., T. L. Hazlett, and Govindjee. 1995 Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: formation of a quenching complex with a short fluorescence lifetime. Proceedings of the National Academy of Sciences, USA 92: 2273–2277.[Abstract/Free Full Text]

Godde, D., and M. Hefer. 1994 Photoinhibition and light-dependent turnover of the D1 reaction-centre polypeptide of photosystem II are enhanced by mineral-stress conditions. Planta 193: 290–299.[ISI]

Govindjee. 1995 Sixty-three Years Since Kautsky: chlorophyll a fluorescence. Australian Journal of Plant Physiology 22: 131–60.[ISI]

Graan, T., and D. R. Ort. 1986 Detection of oxygen-evolving Photosystem II centers inactive in plastoquinone reduction. Biochimica et Biophysica 852: 320–330.[CrossRef]

Greene, B. A., L. A. Staehelin, and A. Melis. 1988 Compensatory alterations in the photochemical apparatus of a photoregulatory, chlorophyll b-deficient mutant of maize. Plant Physiology 87: 365–370.[Abstract/Free Full Text]

Grumbach, K. H. 1981 Formation of photosynthetic pigments and quinones and development of photosynthetic activity in barley etioplasts during greening in intermittent and continuous white light. Physiologia Plantarum 51: 53–62.

Guenther, J. E., and A. Melis. 1990 The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynthesis Research 23: 105–109.

———, J. A. Nemson, and A. Melis. 1988 Photosystem stoichiometry and chlorophyll antenna size in Dunaliella salina (green alga). Biochimica et Biohysica Acta 934: 108–117.

———, ———, and ———. 1990 Development of photosystem II in dark grown Chlamydomonas reinhardtii. A light dependent conversion of PS IIß, QB-nonreducing centers to the PS II{alpha}, QB-reducing form. Photosynthesis Research 24: 35–46.[CrossRef]

Gunning, B. E. S., and M. W. Steer. 1975 Ultrastructure and biology of plant cells. E. Arnold, London.

Hansson, Ö., and T. Wydrzynski. 1990 Current perceptions of Photosystem II. Photosynthesis Research 23: 131–162.

Harrison, M. A., A. Melis, and J. F. Allen. 1992 Restoration of irradiance-stressed Dunaliella salina (green alga) to physiological growth conditions: changes in antenna size and composition of Photosystem II. Biochimica et Biophysica Acta 1100: 83–91.[CrossRef]

Hashimoto, A., T. Akasaka, and Y. Yamamoto. 1993 Characteristics of the assembly of the 33 kDa oxygen-evolving complex protein in the etioplasts and the developing chloroplasts of barley seedlings. Biochimica et Biophysica Acta 1183: 397–407.[CrossRef]

Hendricks, S. B., and W. J. Van Der Woude. 1993 How phytochrome acts—perspectives on the continuing quest. Encyclopedia of Plant Physiology, New Series 16A: 3–23.

Hoober, J. K., P. Siekevitz, and G. E. Palade. 1969 Formation of Chloroplast Membranes in Chlamydomonas reinhardi y-1. The Journal of Biological Chemistry 244(10): 2621–2631.

Humbeck, K., and N. I. Bishop. 1986 Components and development of function in chloroplasts of a greening mutant of Scenedesmus-Obliquus. Plant Cell Physiology 27: 1407–1418.

Joshi, M. K., and P. Mohanty. 1995 Probing photosynthetic performance by chlorophyll a fluorescence: analysis and interpretation of fluorescence parameters. Journal of Scientific and Industrial Research 54: 155–174.

———, ———, J. S. Van Rensen, and S. Bose. 1994 Alterations in the chlorophyll fluorescence and thermoluninescence characteristics of photosynthetic apparatus by SAN 9785 treatment. Journal of Photochemistry and Photobiology 23: 63–68.

Kawaguchi, H., I. Fukuda, T. Shiina, and Y. Toyoshima. 1992 Dynamical behavior of psb gene transcripts in greening wheat seedlings. I. Time course of accumulation of the psbA through psbN gene transcripts during light-induced greening. Plant Molecular Biology 20: 695–704.[CrossRef][ISI][Medline]

Kitajima, M., and W. L. Butler. 1975 Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta 376: 105–115.[Medline]

Klein, S., E. Katz, and E. Neeman. 1977 Induction of {delta}-aminolevulinic acid formation in etiolated maize leaves controlled by two light systems. Plant Physiology 60: 335–338.[Abstract/Free Full Text]

Klinkovsky, T., and J. Naus. 1994 Sensitivity of the relative FpI level of chlorophyll fluorescence induction in leaves to the heat stress. Photosynthesis Research 39: 201–204.[CrossRef]

Klosson, J. R., and G. H. Krause. 1981 Freezing injury in cold-acclimated and unhardened spinach leaves. II. Effects of freezing on chlorophyll fluorescence and light scattering reactions. Planta 151: 347–352.[CrossRef][ISI]

Krause, G. H. 1988 Photoinhibition of photosynthesis: an evaluation of damaging and protective mechanisms. Physiologia Plantarum 74: 313–349.

———, and E. Weis. 1984 Chlorophyll fluorescence as a tool in plant physiology. II. Interpretation of fluorescence signals. Photosynthesis Research 5: 139–157.

———, and ———. 1991 Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42: 313–349.[CrossRef][ISI]

Krol, M., and N. P. A. Huner. 1989 Low temperature development under intermittent light conditions results in the formation of etiochloroplasts. Journal of Plant Physiology 134: 623–628.[ISI]

Larsson, U. K., J. M. Anderson, and B. Andersson. 1987 Variations in the relative content of the peripheral and inner light-harvesting chlorophyll a/b-protein complex (LHC II) subpopulations during thylakoid light adaptation and development. Biochimica et Biophysica Acta 894: 69–75.[CrossRef]

Lavergne, J. 1982 Two types of primary acceptors in chloroplasts photosystem II. Photobiochemistry and Photobiophysiology 3: 257–285.

Lebkuecher, J. G. 1997 Desiccation-time limits of photosynthetic recovery in Equisetum hyemale (Equisetaceae) spores. American Journal of Botany 84: 792–797.[Abstract]

———, and W. G. Eickmeier. 1991 Reduced photoinhibition with stem curling in the resurrection plant Selaginella lepidophylla. Oecologia 88: 597–604.

———, and ———. 1992 Photoinhibition of photophosphorylation, adenosine triphosphate content, and the light-activated enzyme glyceraldehyde-3-phosphate dehydrogenase (NADP+) following high-irradiance desiccation of Selaginella lepidophylla. Canadian Journal of Botany 70: 205–211.

———, and ———. 1993 Physiological benefits of stem curling in the resurrection plant Selaginella lepidophylla. Ecology 44: 1073–1080.

Leech, R. M. 1984 Chloroplast development in angiosperms: current knowledge and future prospects. In N. R. Baker, and J. Barber [eds.], Topics in photosynthesis, chloroplast biogenesis, vol. 5, 1–21. Elsevier Science, Amsterdam.

Lew, R., and H. Tsuji. 1982 Effect of benzyladenine treatment duration on {delta}-aminoevulinic acid accumulation in the dark, chlorophyll lag phase abolition, and long-term chlorophyll production in excised cotyledons of dark-grown cucumber seedlings. Plant Physiology 69: 663–667.[Abstract/Free Full Text]

Mathis, P., and G. Paillotin. 1981 Primary processes in photosynthesis. In M. D. Hatch and N. K. Boardman [eds.], The biochemistry of plants, vol. 8, 129–137. Academic Press, New York, NY.

Maxwell, D. P., S. Falk, and N. P. A. Huner. 1995 Photosystem II excitation pressure and development of resistance to photoinhibition. Plant Physiology 107: 687–694.[Abstract]

Melis, A. 1985 Functional properties of photosystem IIß in spinach chloroplasts. Biochimica et Biophysica Acta 808: 334–342.[CrossRef]

———. 1991 Dynamics of photosynthetic membrane composition and function. Biochemica et Biophysica 1058: 87–106.

———, and P. H. Homann. 1975 Kinetic analysis of the fluorescence induction in 3-(3,4-Dichlorophenyl)-1,1-dimethylurea poisoned chloroplasts. Photochemistry and Photobiology 21: 431–437.[CrossRef]

Mullet, J. E. 1988 Chloroplast development and gene expression. Annual Review of Plant Physiology and Plant Molecular Biology 39: 475–502.[CrossRef][ISI]

Ohashi, K., A. Tanaka, and H. Tsuji. 1989 Formation of the Photosynthetic electron transport system during the early phase of greening in barley leaves. Plant Physiology 91: 409–414.[Abstract/Free Full Text]

Ono, T.-A., H. Kajikawa, and Y. Inoue. 1986 Changes in protein composition and Mn abundance in photosystem II particles on photoactivation of the latent O2-evolving system in flash-grown wheat leaves. Plant Physiology 80: 85–90.[Abstract/Free Full Text]

———. 1991 Dynamics of photosynthetic membrane composition and function. Biochimica et Biophysica Acta 1058: 87–106.[CrossRef]

Pakrasi, H., and W. F. J. Vermaas. 1992 Protein engineering of photosystem II. In J. Barber [ed.], The photosystems: structure, function and molecular biology, 231–257. Elsevier Science Publishers, New York, NY.

Park, Y. II, M. C. Park, and Y. N. Hong. 1994 Correlative changes between photosynthetic activities and chlorophyll fluorescence in wheat chloroplasts exposed to high temperature. Plant Biology 37: 37–42.

Percival, M. P., A. N. Webber, J. P. Markwell, and N. R. Baker. 1986 Modification of the interaction between photosystem II and the light-harvesting chlorophyll a/b-protein complex by protein phosphorylation in developing wheat thylakoids exhibiting different degrees of lateral heterogeneity. Biochimica et Biophysica Acta 848: 317–323.[CrossRef]

Porra, R. J., W. A. Thompson, and P. E. Kriedemann. 1989 Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975: 384–394.[CrossRef]

Possingham, J. V. 1980 Plastid replication and development in the life cycle of higher plants. Annual Review of Plant Physiology 31: 113–29.[ISI]

Russell, W., A. C. Critchley, S. A. Robinson, L. A. Franklin, G. R. Seaton, W. C. Chow, J. M. Anderson, and C. B. Osmond. 1995 Photosystem II regulation and dynamics of the chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition. Plant Physiology 107: 943-952.[Abstract]

Schreiber, U., and P. A. Armond. 1978 Heat-induced changes of chlorophyll fluorescence in isolated chloroplasts and related heat damage at the pigment level. Biochimica et Biophysica Acta 502: 138–151.[Medline]

———, and C. Neubauer. 1987 The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the photosystem II donor side and possible ways of interpretation. Zeitschrift fur Naturforschung 42c: 1255–1264.

Schwab, K. B., U. Schreiber, and U. Heber. 1989 Response of photosynthesis and respiration of resurrection plants to desiccation and rehydration. Planta 177: 217–227.[CrossRef][ISI]

Sokal, R. R., and F. J. Rohlf. 1995 Biometry. W. H. Freeman, New York, NY.

Srivastava, A., R. J. Strasser, and Govindjee. 1995a Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutants of Chlamydomonas reinardtii. Photosynthesis Research 43: 131–141.

———, ———, and ———. 1995b Differential effects of dimethylbenzoquinone and dichlorobenzoquinone on chlorophyll fluorescence transient in spinach thylakoids. Journal of Photochemistry and Photobiology 31: 163–169.

Strasser, R. J., A. Srivastava, and Govindjee. 1995 Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology 61: 32–42.[CrossRef]

Thielen, A. P. G. M., and H. J. Van Gorkom. 1981 Electron transport properties of photosystem II{chi} and IIß. In G. Akoyunoglou [ed.], Photosynthesis, Proceedings of the fifth International Congress. vol. 2, 57–64. Balaban International Science Services, Philadelphia, PA.

Webber, A. N., N. R. Baker, K. Platt-Aloia, and W. W. Thomson. 1984 Appearance of state 1–state 2 transition during chloroplast development in the wheat leaf: energetic and structural considerations. Physiolgia Plantarum 60: 171–179.[CrossRef]

———, ———, C. D. Paige, and M. F. Hipkins. 1986 Photosynthetic electron transport and establishment of an associated trans-thylakoid proton electrochemical gradient during development of the wheat leaf. Plant, Cell and Environment 9: 203–208.

Williams, W. P., and J. F. Allen. 1987 State 1/State 2 changes in higher plants and algae. Photosynthesis Research 13: 19–45.

Zar, J. E. 1984 Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ.




This article has been cited by other articles:


Home page
 ANN BOT (LOND)Home page
K. Solymosi, B. Vitanyi, E. Hideg, and B. Boddi
Etiolation Symptoms in Sunflower (Helianthus annuus) Cotyledons Partially Covered by the Pericarp of the Achene
Ann. Bot., May 1, 2007; 99(5): 857 - 867.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (7)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lebkuecher, J. G
Right arrow Articles by Minton, D. A
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lebkuecher, J. G
Right arrow Articles by Minton, D. A
Agricola
Right arrow Articles by Lebkuecher, J. G
Right arrow Articles by Minton, D. A

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS