O2 Inhibition Of Photosynthesis Research Articles

Interactions between carbon dioxide and oxygen in the photosynthesis of three species of marine red macroalgae

Summary Red algae have the highest known selectivity factor (Srel) for CO2 over O2 of ribulose bisphosphate carboxylase-oxygenase (RUBISCO). This allows the prediction that a red alga relying on diffusive supply of CO2 to RUBISCO from air-equilibrated solution should have less O2 inhibition of photosynthesis than would an otherwise similar non-red alga with a lower Srel of RUBISCO. Furthermore, RUBISCO shows an increased Srel values at low temperatures. The prediction that O 2inhibition of photosynthesis should be small for marine red algae relying on diffusive CO2 entry growing in the North Sea with an annual temperature range of 4–16°C was tested in O2 electrode experiments at 12°C. Phycodrys rubens and Plocamium cartilagineum, which rely on diffusive CO2 entry showed, as predicted, only a small inhibition at lower inorganic C concentrations. Palmaria palmata, which has a CO2 concentrating mechanism, had the expected negligible O 2 inhibition of photosynthesis at any inorganic C concentration except (no...

Evidence that inducible C4‐type photosynthesis is a chloroplastic CO2‐concentrating mechanism in Hydrilla, a submersed monocot

ABSTRACT Hydrilla verticillata (L.f.) Royle exhibits an inducible C4‐type photosynthetic cycle, but lacks Kranz anatomy. Leaves in the C4‐type state (but not C3‐type) contained up to 5‐fold higher internal dissolved inorganic carbon (DIC) concentrations than the medium, indicating that they possessed a CO2‐concentrating mechanism (CCM). Several lines of evidence indicated that the chloroplast was the likely site of CO2 generation. From C4‐type leaf [DIC] measurements, the estimated chloroplastic free [CO2] was 400 mmol m−3. This gave a calculated 2% O2 inhibition of photosynthesis, which was identical to the measured value, and provided independent evidence that the estimated [CO2] was close to the true value. A homogeneous distribution of DIC in the C4‐type leaf could not account for such a high [CO2], or the resultant low O2 inhibition. For C3‐type leaves the estimated chloroplastic [CO2] was only 7 mmol m−3, which gave high, and similar, calculated and measured O2 inhibition values of 22 and 26%, respectively. The CCM did not appear to be located at the plasma membrane, as it operated at low and high pH, indicating that it was independent of use of HCO3− from the medium. Also, both C3− and C4‐type Hydrilla leaves showed pH polarity in the light, with abaxial and adaxial boundary layer values of about pH 4·0 and 10·5, respectively. Thus, pH polarity was not a direct component of the CCM, though it probably improved access to HCO3. Additionally, iodoacetamide and methyl viologen greatly reduced abaxial acidification, but not the steady‐state CCM. Inhibitor studies suggested that the CCM required photosynthetically generated ATP, but Calvin cycle activity was not essential. Both leaf types accumulated DIC in the dark by an ATP‐requiring process, possibly respiration, and C4‐type leaves fixed CO2 at 11·8% of the light rate. The operation of a CCM to minimize photorespiration, and the ability to recapture respiratory CO2 at night, would conserve DIC in a densely vegetated lake environment where daytime [CO2] is severely limiting, while [O2] and temperatures are high.

Estimation of diffusive resistance of bundle sheath cells to CO2 from modeling of C4 photosynthesis

Bundle sheath resistance to diffusion of CO2 (rc) is a critical component of C4 photosynthesis which allows accumulation of inorganic carbon in bundle sheath cells of C4 plants. Several analyses were made to evaluate the magnitude of rc in C4 plants. Experimental data on the O2 inhibition of photosynthesis (Dai et al. (1993) Plant Physiol 103: 83-90; (1995) Plant Physiol 107: 815-825) and rates of photorespiration (de Veau and Burris (1989) Plant Physiol 90: 500-511) in Z. mays at different stages of development were analyzed using mathematical models of C4 photosynthesis. In young and senescing leaves modeled values of rc and the CO2 partial pressure in bundle sheath cells (Cbs) were lower and fractional leakage of CO2 from bundle sheath cells (fL) was higher than in mature leaves. Diffusive resistance of bundle sheath cells of C4 plants was also evaluated by analyzing the response of photosynthetic rates to varying CO2 in Amaranthus edulis in which the C4 cycle was dysfunctional by chemical mutagenesis (Dever et al. (1995) J Exp Bot 46: 1363-1376) and in Sorghum bicolor, Panicum maximum and Panicum miliaceum in which the C4 cycle was chemically inhibited (Brown and Byrd (1993) Plant Physiol 103: 1183-1188). These analyses indicate that in mature leaves of C4 plants the values of rc are substantially lower (ca. 50-200 m(2) s mol(-1)) than previous suggested (ca. 500-1500 m(2) s mol(-1)) for C4 photosynthesis and that there is considerable leakage of CO2 from bundle sheath cells. Nevertheless, rc and Cbs values are sufficiently high in mature leaves to minimize photorespiration in C4 plants under normal levels of CO2.

Degree of C4 Photosynthesis in C4 and C3-C4Flaveria Species and Their Hybrids

Hybrids have been made between species of Flaveria exhibiting varying levels of C(4) photosynthesis. The degree of C(4) photosynthesis expressed in four interspecific hybrids (Flaveria trinervia [C(4)] x F. linearis [C(3)-C(4)], F. brownii [C(4)-like] x F. linearis, and two three-species hybrids from F. trinervia x [F. brownii x F. linearis]) was estimated by inhibiting phosphoenolpyruvate carboxylase in vivo with 3,3-dichloro-2-dihydroxyphosphinoylmethyl-2-propenoate (DCDP). The inhibitor was fed to detached leaves at a concentration of 4 mm, and apparent photosynthesis was measured at atmospheric levels of CO(2) and at 20 and 210 mL L(-1) of O(2). Photosynthesis at 210 mL L(-1) of O(2) was inhibited 32% by DCDP in F. linearis, by 60% in F. brownii, and by 87% in F. trinervia. Inhibition in the hybrids ranged from 38 to 52%. The inhibition of photosynthesis by 210 mL L(-1) of O(2) was increased when DCDP was used, except in the C(4) species, F. trinervia, in which photosynthesis was insensitive to O(2). Except for F. trinervia, control plants with less O(2) sensitivity (more C(4)-like) exhibited a progressively greater change in O(2) inhibition of photosynthesis when treated with DCDP. This increased O(2) inhibition probably resulted from decreased CO(2) concentrations in bundle sheath cells due to inhibition of phosphoenolpyruvate carboxylase. The inhibition of photosynthesis by DCDP is concluded to underestimate the degree of C(4) photosynthesis in the interspecific hybrids because increased direct assimilation of atmospheric CO(2) by ribulose bisphosphate carboxylase may compensate for inhibition of phosphoenolpyruvate carboxylase.

Effects of O2, pH and DIC on photosynthetic net-O2 evolution by marine macroalgae

Net photosynthetic O2 evolution by five marine macroalgae:Ulva lactuca L.,Enteromorpha sp.,Ceramium strictum Harvey,Fucus serratus L., andF. vesiculosus L., collected from Danish waters in the summer of 1983 was followed at increasing O2 and with pH either fixed close to pH 7, 8 or 9, or drifting upwards during photosynthesis in a closed chamber to determine the effects of changing O2, pH and DIC (dissolved inorganic carbon) on photosynthesis. Increasing O2, increasing pH and decreasing DIC together limited O2 evolution. Raising the O2 concentration with pH and DIC held constant resulted in less inhibition of net-O2 evolution than when all three factors acted together. The O2 inhibition of photosynthesis was similar to the reported O2 inhibition of ribulose 1,5-bisphosphate carboxylase isolated from lower and higher plants. Net-O2 evolution as a function of the molar ratio of O2 to HCO−3 + CO2 in solution provided a general, linear relationship (r2 = 0.72 to 0.84), predicting inhibition of photosynthesis based on O2 pH and DIC changing together. Slopes of this relationship, representing competition between O2 and carbon based on external concentrations, were similar for the five taxonomically different algae, suggesting that similar processes act to reduce net-O2 evolution.

A model of carbon dioxide assimilation in Chlamydomonas reinhardii

A simple model of photosynthetic CO2 assimilation in Chlamydomonas has been developed in order to evaluate whether a CO2-concentrating system could explain the photosynthetic characteristics of this alga (high apparent affinity for CO2, low photorespiration, little O2 inhibition of photosynthesis, and low CO2 compensation concentration). Similarly, the model was developed to evaluate whether the proposed defects in the CO2-concentrating system of two Chlamydomonas mutants were consistent with their observed photosynthetic characteristics. The model treats a Chlamydomonas cell as a single compartment with two carbon inputs: passive diffusion of CO2, and active transport of HCO 3 (-) . Internal inorganic carbon was considered to have two potential fates: assimilation to fixed carbon via ribulose 1,5-bisphosphate carboxylase-oxygenase or exiting the cell by either passive CO2 diffusion or reversal of HCO 3 (-) transport. Published values for kinetic parameters were used where possible. The model accurately reproduced the CO2-response curves of photosynthesis for wild-type Chlamydomonas, the two mutants defective in the CO2-concentrating system, and a double mutant constructed by crossing these two mutants. The model also predicts steady-state internal inorganic-carbon concentrations in reasonable agreement with measured values in all four cases. Carbon dioxide compensation concentrations for wild-type Chlamydomonas were accurately predicted by the model and those predicted for the mutants were in qualitative agreement with measured values. The model also allowed calculation of approximate energy costs of the CO2-concentrating system. These calculations indicate that the system may be no more energy-costly than C4 photosynthesis.

The effect of triacontanol on growth, photosynthesis and photorespiration in Chlamydomonas reinhardtii and Anacystis nidulans

Chlamydomonas reinhardtii Dangerad 11–32(90) (−), which exhibits C3 properties, and Anacystis nidulans (Strain no. UTEX 625), which exhibits C4 properties, were used to study the effects of triacontanol on growth, photosynthesis and photorespiration. Photosynthetic rate was measured as CO2 uptake and the O2 inhibition of photosynthesis was used as a measure of photorespiration. Triacontanol dissolved in chloroform and dispersed in Tween‐20 and triacontanol colloidally dispersed in an aqueous solution of sodium tallow alkyl sulfate were tested. Chlamydomonas cultures increased significantly in cell number after 4 days, and in chlorophyll content after 3 days of treatment with 2.3 × 10−8 M TRIA in chloroform/Tween‐20. In cultures of Anacystis the chlorophyll content became significantly higher 3 days after treatment with 2.3 × 10−9 M TRIA and the cell number was noticeably higher than the controls.CO2 uptake by triacontanol‐treated Chlamydomonas cultures was about the same in both 2 and 21% O2, and the O2 inhibition was significantly reduced as compared with the controls. Photosynthesis in Anacystis was O2‐insensitive under the experimental condition used. When Anacystis was treated with triacontanol there was no change in the rate of CO2 uptake and no change in the O2 sensitivity of its CO2 uptake. It appears that triacontanol affects some process which regulated the balance between photosynthesis and photorespiration, but other processes which result in increased growth are probably also affected.

Photosynthetic adaptation to temperature in four species from the Colorado shortgrass steppe: a physiological model for coexistence.

Several aspects of photosynthetic adaptation to temperature were examined in four graminoid species from the Colorado shortgrass steppe. The experimental species were chosen to provide examples of a variety of in situ seasonal phenology patterns. The cool season grass, Agropyron smithii (C3), exhibited higher photosynthesis rates when grown in a cool temperature regime (20/15°C), and compared to warm grown plants (35/15°C). The warm season species, Bouteloua gracilis (C4) and Buchloe dactyloides (C4), exhibited higher photosynthetic capacities when grown in the warmer temperature regime. The sedge, Carex eleocharis (C3), which exhibits seasonal growth potential during the cool and warm portions of the growing season, exhibited a marked capacity for photosynthetic temperature acclimation. Differential effects of growth temperature on the intracellular conductance to CO2 appeared to have a greater regulatory role in these responses for the two C3 species, relative to stomatal conductance or photorespiration (O2 inhibition of photosynthesis). In the two C4 species decreases in the intracellular conductance in cool grown plants were correlated with the decreased photosynthetic capacity in normal air for B. gracilis, but not for B. dactyloides. Analysis of the Arrhenius relationship for CO2 saturated net photosynthesis at low leaf temperatures (4.5-17°C) indicated sharp breaks in the apparent energy of activation at 5.8-9.0°C in the warm season species B. gracilis and B. dactyloides. Leaves of A. smithii and C. eleocharis exhibited no significant low temperature limitations according to this analysis. The low temperature limitations in the warm season species were partially reflected in an inhibition of the quantum yield for CO2 uptake after 2 h at 5-6°C in the presence of high photon flux densities. Temperature dependent increases in the chlorophyll fluorescence yield at high temperatures revealed the lowest breakpoint values for A. smithii, and the highest values for B. gracilis. The differential patterns of temperature adaptation among the species further extend the proposal of Kemp and Williams (1980; Ecology 61:846-858) that seasonal temperature gradients in the shortgrass steppe have a regulatory role in maintaining offset patterns of resource utilization and decreasing interspecific competition.

Oxygen inhibition of photosynthesis in the C4 species Amaranthus graecizans L.

In the C4 plant, Amaranthus graecizans, increasing [O2] from 2% up to 100% inhibited photosynthesis, quantum yield, and the carboxylation efficiency, and increased the CO2 compensation point (Γ) from 2 to about 12 μl/l. The O2 inhibition of photosynthesis was fully reversible. When changing from 2.5 to 40% O2 and vice versa, about 1 h was required for full equilibration with an O2 inhibition of 18%; whereas in wheat, a C3 species, inhibition of photosynthesis and its reversal occurs within minutes after changing [O2], resulting in 63% inhibition of photosynthesis by 45% O2. These differences in O2 inhibition between a C4 and C3 species can be explained by high diffusive resistance across bundle-sheath cells of C4 plants and the increased CO2/O2 ratio in bundle-sheath cells which is the consequence of the C4 cycle. In A. graecizans, Γ increased with increasing [O2] but tended to reach a maximum at relatively high O2 levels. The lack of a linear increase in Γ as previously observed for C3 species indicates that a considerable amount of photorespired CO2 may be re-fixed with increasing levels of O2. In comparison to previous reports with other C4 species, photosynthesis of A. graecizans shows greater sensitivity to O2, with a noticeable inhibition occurring with shifts from 2 to 21% O2. A. graecizans has characteristics of other C4 species with respect to Kranz anatomy, localization of PEP carboxylase in mesophyll cells and RuBP carboxylase in bundle-sheath cells, and little fractionation among carbon isotopes during CO2 fixation. The basis for the higher sensitivity of photosynthesis of A. graecizans to O2 may be based upon a lower diffusive resistance of gases across bundle-sheath cells than in some other C4 species.