Incomplete membrane-bound photosynthetic electron transfer pathway in agranal chloroplasts

Bishop, David G.; Andersen, Kirsten S.; Smillie, Robert M.

doi:10.1016/0006-291x(71)90364-0

Cited by 27 publications

(9 citation statements)

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“…In leaf sections of plants containing the C4-dicarboxylic acid pathway of photosynthesis, in which both granal and agranal chloroplasts are present, photoreduction of the Hill oxidant, tetranitro blue tetrazolium chloride, was observed only in grana-containing chloroplasts (6, 7). Agranal chloroplasts isolated from the bundle sheath cells of the C4 plants, maize and Sorghum, contain photosystem I activity, but do not photoreduce NADP from water, whereas the granal mesophyll chloroplasts carry out this reaction (2,3,19).Similar correlations between photosystem II activity and the presence of grana have been made in algae. The chloroplasts of the green alga Chlamydobotrys stellata contain appressed lamellae and carry out normal photosynthesis when grown photoautotrophically.…”

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confidence: 58%

Photosystem II Activity in Agranal Bundle Sheath Chloroplasts from Zea mays

et al. 1972

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The photochemical activities of chloroplasts isolated from bundle sheath and mesophyll cells of maize (Zea mays var. DS606A) have been measured. Bundle sheath chloroplasts are almost devoid of grana, except in very young leaves, while mesophyli chloroplasts contain grana at all stages of leaf development.Chloroplast fragments isolated from bundle sheath cells showed a light-dependent reduction of potassium ferricyanide, 2,6-dichlorophenolindophenol, mammalian cytochrome c, plastocyanin, and Euglena cytochrome cm. These activities were inhibited by 3-(3,4-dichlorophenyl)-1 , l-dimethylurea at 1.25 micromolar. However, the photoreduction of NADP from water was extremely low or absent, except in chloroplasts from very young leaves, and the capacity for NADP reduction appeared to be related to the degree of grana formation.Photosystem I activity was present in bundle sheath chloroplast preparations at all stages of leaf growth and senescence examined. However, the activity was lower than in isolated mesophyll ehloroplasts. NADPH diaphorase activity was comparable in both types of chloroplast.Chloroplasts appearance of photosystem II activity in developing pea chloroplasts appears to be correlated with the formation of grana, rather than with the production of chlorophyll (5). In leaf sections of plants containing the C4-dicarboxylic acid pathway of photosynthesis, in which both granal and agranal chloroplasts are present, photoreduction of the Hill oxidant, tetranitro blue tetrazolium chloride, was observed only in grana-containing chloroplasts (6, 7). Agranal chloroplasts isolated from the bundle sheath cells of the C4 plants, maize and Sorghum, contain photosystem I activity, but do not photoreduce NADP from water, whereas the granal mesophyll chloroplasts carry out this reaction (2,3,19).Similar correlations between photosystem II activity and the presence of grana have been made in algae. The chloroplasts of the green alga Chlamydobotrys stellata contain appressed lamellae and carry out normal photosynthesis when grown photoautotrophically. However, when the alga was grown photoheterotrophically on acetate, nearly all the chloroplast lamellae were separated from each other and the chloroplasts lacked photosystem II activity (16,17). Both photosystem II activity and appression of lamellae were regained when photoautotrophic growth was resumed, again indicating that appressed lamellae are necessary for photosystem II activity (16)(17)(18).In contrast, photosystem II activity is present in a mutant of C. reinhardi (ac-31) which has chloroplasts that contain only unappressed lamellae (8). Algae belonging to the Rhodophyta and Cyanophyta do not contain appressed lamellae yet evolve oxygen in the light. The disruption of grana by suspension of higher plant chloroplasts in a low salt medium does not result in a loss of photosystem II activity (10). Studies on a mutant of Chlamydomonas reinhardi revealed no correlation with Hill activity and grana formation (13).The occurrence of two morphologically distinct chl...

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Photosystem II Activity in Agranal Bundle Sheath Chloroplasts from Zea mays

et al. 1972

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“…The PSII activity of isolated maize BS' chloroplasts was reported in early papers to be unmeasurably low (5,29). In subsequent papers, substantial rates of PSII-mediated electron flow to a variety of acceptors such as MV (50 lieq/hr.mg Chl; ref.…”

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“…Ten to 12 g (fresh weight) of leaves were cut transversely into Ito 2-cm segments. Two to 3 g of these segments were combined with 5 ml of the isolation medium that contained 0.5 M sucrose, 80 mM Tricine-NaOH buffer (pH 7.8), 5 Figure 3. MV acted as a very efficient electron acceptor in BS fragments (rate-saturation at 20 PM; Fig.…”

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Photosynthetic Electron Transport in Isolated Maize Bundle Sheath Cells

Walker¹,

Izawa²

1979

Plant Physiol.

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Fragments of bundle sheath strands, free of mesophyll cells and showing a chlorophyll a/b ratio of 6.0 to 6.6 were prepared from Zea mays by a mechanical method. They were unable to photoreduce ferricyanide but were able to photoreduce the membrane-permeant 2,5-dimethylquinone at a rate of 250 to 420 microequivalents per hour per mg chlorophyll (ueq/hr.mg Chi) at 21 C. In the presence of the catalase inhibitor KCN We have attempted to reevaluate the in situ photochemical activities of chloroplasts in isolated maize BS fragments by carefully optimizing the reaction conditions. We used 2,5-dimethylquinone (DMQ) as the PSII electron acceptor, which is a membranepermeant oxidant and is by far the more stable and therefore more reliable as a PSII acceptor than is unsubstituted p-benzoquinone (24). MV, a standard PSI electron acceptor for chloroplast studies, tumed out to be useful also for isolated BS cells. This was not surprising, since MV is a widely used contact herbicide ("paraquat") and is known to penetrate the leaf tissue readily (see, e.g. 3).The in situ photochemical activities of maize BS chloroplasts are quite comparable to the highest activities reported for isolated BS chloroplasts (9). Perhaps more importantly, this paper also describes experiments in which we have successfully detected an electron transport-dependent H+ uptake by isolated BS fragments. Preparation of BS Fragments. BS fragments were isolated from secondary leaves taken from 2-to 4-week-old plants. All isolation procedures were performed at 0 to 4 C using ice-chilled media. Ten to 12 g (fresh weight) of leaves were cut transversely into Ito 2-cm segments. Two to 3 g of these segments were combined with 5 ml of the isolation medium that contained 0.5 M sucrose, 80 mM Tricine-NaOH buffer (pH 7.8), 5 mM MgCl2, 10 mm KCI, 0.2% BSA, and 0.1% PVP (PVP-40, Sigma). The leaf segments were then thoroughly macerated (4-5 min) using a pair of razor blades attached to an electric kitchen knife. This step removed most of the mesophyll cells and the epidermis from the tissue. The fragments were transferred to a beaker together with the medium and kept in suspension using a magnetic stirrer. The procedure was repeated until the entire 10 to 12 g of the original material was processed. The suspension was then filtered though two layers of Miracloth, and the tissue remaining on the cloth was briefly rinsed with distilled H20. The washed fragments were resuspended in 150 ml of the isolation medium and sheared in a Waring Blendor for 9 to 15 sec in 3-sec bursts at low speed. MATERIALS

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“…Several of the C4 plants, including maize, Sorghum, and sugar cane, are characterized by chloroplasts which show little evidence of grana development in the cells surrounding the vascular bundle. Chloroplasts isolated from these cells do not photoreduce NADP (1)(2)(3)12), even though they contain demonstrable photosystem I and photosystem II activities (1-3). These and related observations (5) have raised the question of whether in the intact cell the bundle sheath chloroplasts are capable of photosynthetically reducing NADP, as is thought to occur in the grana-containing chloroplasts found in C3 plants and in the mesophyll cells of C4 plants.…”

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confidence: 99%

“…Several of the C4 plants, including maize, Sorghum, and sugar cane, are characterized by chloroplasts which show little evidence of grana development in the cells surrounding the vascular bundle. Chloroplasts isolated from these cells do not photoreduce NADP (1)(2)(3)12), even though they contain demonstrable photosystem I and photosystem II activities (1)(2)(3) important implications to the elucidation of the pathway of carbon in C4 plants and has been the subject of much recent debate (7).…”

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Photoreduction and Oxidation of Cytochrome f in Bundle Sheath Cells of Maize

1972

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The photo-oxidation of cytochrome f (cytochrome c,54) in bundle sheath cells isolated from leaves of maize (Zea mays var. DS 606A) has been compared with that in intact maize leaf and in isolated pea leaf cells (Pisum sativum L.). In all cases, illumination with red light caused a negative absorbance change at 554 nm which was attributed to the oxidation of cytochrome /. The extent of this change was greater using monochromatic red light at wavelengths above 700 nm compared with wavelengths below 700 nm. 3-(3,4-Dichlorophenyl)-1 , l-dimethylurea abolished this difference in bundle sheath cells. After illumination for 1 minute or longer in bundle sheath cells, reduction of cytochrome f in the dark was rapid only if the wavelength of the illuminating light was below 700 nm. In the presence of 3-(3,4-dichlorophenyl)-1,1-dimethlyurea, reduction was slow after illumination at all wavelengths.Cytochrome f photo-oxidation was also followed in cells of a mutant of Chlamydomonas reinhardi, ac-21, which has isolated chloroplasts that exhibit photochemical reactions similar to those shown by isolated bundle sheath chloroplasts. No evidence was obtained for photoreduction of cytochrome f in the mutant.It was concluded that in the chloroplast of the intact bundle sheath cell of maize there is electron flow between photosystem II and cytochrome f resulting in photoreduction of the cytochrome.The chloroplasts of plants possessing the Hatch-Slack or C4 pathway of photosynthesis (C4 plants) often show distinct differences in structure, composition, and photosynthetic activities compared to chloroplasts from plants containing the Calvin cycle (C3 plants) (7). Several of the C4 plants, including maize, Sorghum, and sugar cane, are characterized by chloroplasts which show little evidence of grana development in the cells surrounding the vascular bundle. Chloroplasts isolated from these cells do not photoreduce NADP (1)(2)(3)12), even though they contain demonstrable photosystem I and photosystem II activities (1-3). These and related observations (5) have raised the question of whether in the intact cell the bundle sheath chloroplasts are capable of photosynthetically reducing NADP, as is thought to occur in the grana-containing chloroplasts found in C3 plants and in the mesophyll cells of C4 plants. The answer to this question has 'Visiting scientist from Institute of Genetics, Copenhagen University, 0ster Farimagsgade 2A, DK1353, Denmark.

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Incomplete membrane-bound photosynthetic electron transfer pathway in agranal chloroplasts

Cited by 27 publications

References 7 publications

Photosystem II Activity in Agranal Bundle Sheath Chloroplasts from Zea mays

Photosystem II Activity in Agranal Bundle Sheath Chloroplasts from Zea mays

Photosynthetic Electron Transport in Isolated Maize Bundle Sheath Cells

Photoreduction and Oxidation of Cytochrome f in Bundle Sheath Cells of Maize

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