Oxygen Inhibition of Photosynthesis

Abstract

The magnitude of the percentage inhibition of photosynthesis by atmospheric levels of 02 in the C3 species Solanum tuberosum L., Medicago sativa L., Phaseolus vulgaris L., Glycine max L., and Triti-cum aestivum L. increases in a similar manner with an increase in the apparent solubility ratio of 02/CO2 in the leaf over a range of solubility ratios from 25 to 45. The solubility ratio is based on calculated levels of 02 and CO2 in the intercellular spaces of leaves as derived from whole leaf measurements of photosynthesis and transpiration. The solubility ratio of 02/C02 can be increased by increased leaf temperature under constant atmospheric levels of 02 and CO2 (since 02 is relatively more soluble than CO2 with increasing temperature); by increasing the relative levels of 02/CO2 in the atmosphere at a given leaf temperature, or by increased stomatal resistance. If the solubility ratio of 02/CO2 is kept constant, as leaf temperature is increased, by varying the levels of 02 or CO2 in the atmosphere, then the percentage inhibition of photosynthesis by 02 iS similar. The decreased solubility of CO2 relative to 02 (de-creased C02/02 ratio) may be partly responsible for the increased percentage inhibition of photosynthesis by 02 under atmospheric conditions with increasing temperature. 02 inhibition of apparent photosynthesis occurs in higher plants which fix CO2 directly via the Calvin-Benson pathway (C3 plants). Gas exchange studies with leaves of C: plants showed that the percentage inhibition of apparent photosynthesis by O., is reduced by increasing the CO2, concentration, by decreasing the 02 levels, or by decreasing the temperature (1, 5, 11, 12, 14, 15, 18, 22). One suggestion is that O., inhibition of photosyn-thesis is related to the kinetic properties of RuDP2 carboxylase-oxygenase. Bowes et al. (6) showed that RuDP carboxylase, the enzyme for CO., fixation, also catalyzes the oxidation of RuDP by 02 to form phosphoglycolate, a suggested substrate for pho-torespiration, and that CO2 and 02 show competitive interactions for the substrate RuDP. Thus, 02 competitively inhibits carboxylase activity with respect to CO2, and CO2 competitively inhibits oxygenase activity with respect to 02 The effect of temperature on O., inhibition of photosynthesis recently has been attributed to the differential alteration of the kinetic properties of RuDP carboxylase-oxygenase such that the ratio of RuDP oxygenase activity to carboxylase activity increased with increased temperature (4, 20). Over a temperature range of 5 to 40 C, the percentage inhibition of photosynthesis by 02 (rate of photosynthesis at 1.5 % 0,-rate of photosynthesis at 21 % 02/ rate of photosynthesis at 1.5% O,)x 100 in various C3 species This research was supported by the College of Agricultural and Life Sciences. University of Wisconsin, Madison. 2 Abbreviation: RuDP: ribulose 1,5-diphosphate. (1, 11, 12, 14, 15, 18, 22) increased with increasing temperature although the absolute rate of 02 inhibition of photosynthesis (rate of photosynthesis at 1.5% 02-rate of photosynthesis at 21 % 02) shows an optimum temperature. Generally only atmospheric levels of CO.2 and 02 have been considered in comparative studies on 02 inhibition of photosynthesis in various species and on 02 inhibition of photosynthesis as affected by temper.a-ture. In the present study the percentage inhibition of photosyn-thesis by O., was analyzed with several C3 species in relation to calculated intercellular levels of CO., and O., and solubility ratios of 02/CO2 in the leaf. MATERIALS AND METHODS Growth Condition. Plants of potatoes (Solanum tuberosun L.) were grown in greenhouse at a day/night temperature range of 20 to 25/15 to 20 C with a light/dark period of 16/8 hr. Plants of wheat (Triticum aestivum L.), alfalfa (Medicago sativa L.), bean (Phaseolus vulgaris L.), and soybean (Glycine max L.) were grown in controlled environments at a day/night temperature regime of 20/15 C with a light/dark period of 16/8 hr and 50 to 60% relative humidity. Light was provided by a combination of fluorescent and incandescent lamps giving an irradiance of 40 neinsteins/cm2 sec between 400 and 700 nm. Plants were watered alternate days with a nutrient solution and water. The nutrient solution contained Rapid Grow (Ra-pid-Gro Corp., Dansville, N.Y.), 2 g/l; and micronutrients according to Johnson et al. (13) except iron chelate as Sequestrene 138 Fe (Geigy Agric. Chem., Ardsley, N.Y.), 0.8 g/l. Newly expanded leaves of 2-week-old plants were used for the various experiments. Gas Exchange Measurements. Rates of photosynthesis and transpiration were measured simultaneously and continuously with a Barnes multispec IR CO., and water vapor analyzer in an open circuit system as described previously (18). The attached leaves were enclosed in a 180 cm:' Plexiglas chamber similar to that designed by Ku and Hunt (19). Eight ports in the sidewalls of the leaf chamber were connected to a closed and independent airconditioning system which established the leaf temperature. The air recirculates in this system at 13 1/min which minimizes the boundary layer resistance of the leaves to water vapor and CO2 transfer. Using wet filter paper of similar size and orientation as the leaves, the boundary layer resistance to water vapor transfer was determined for each species under such conditions. Leaf temperature was measured with a 75-,ukm diameter chro-mel-constantan thermocouple held against the adaxial surface of the leaf, and was maintained within ±0.3 C of the desired leaf temperature without detectable fluctuation. Using an air conditioner , the temperature around the plant was also kept within +3 C of the leaf temperature. Irradiance was provided by a 400 w Lucolux lamp (General Electric) in the horizontal position, and was filtered through a 5-cm water tank. Light was measured using a quantum flux sensor (Lambda Instruments, Lincoln. Neb.). Various gas mixtures were provided by mixing gases from 986