Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought

Abstract

Stomatal closure can explain the inhibition of net CO2 uptake by a leaf subjected to a mild drought: the photosynthetic apparatus appears resistant to lack of water. Changes in both the water content of leaves maintained in a constant environment and the ambient CO2 molar fraction during measurements on well-hydrated leaves lead to similar effects on net CO2 uptake and whole chain electron transport as estimated by leaf chlorophyll fluorescence measurements. In particular, it is shown that photosystem II (PSII) functioning and its regulation are not qualitatively changed during desiccation and that the variations in PSII photochemistry can simply be understood by changes in substrate availability in this condition. Moreover, an analysis of the literature shows that when inhibition of net CO2 uptake by C3 leaves under drought (Phaseolus vulgaris L., Helianthus annus L. and Solanum tuberosum L.) was lower than 80 %, elevated CO2 completely restored the photosynthetic capacity. The CO2 molar fraction in the chloroplasts declines as stomata close in drying leaves. As a consequence, in C3 plants, ribulose-1,5-bisphosphate oxygenation increases and becomes the main sink for photosynthetic electrons. Depending on the prevailing photon flux density, the O2 uptake through photorespiratory activity can entirely replace carbon dioxide as an electron acceptor, or not. The rate of the Mehler reaction remains low and unchanged during desiccation. However, drought could also involve CO2-sensitive modification of the photosynthetic metabolism depending on plant growth conditions and possibly also on plant species.

Fig. 1. Φ_PSII (A), q_p (B) and F_v′/F_m′ (C) as a function of Φ_CO2. Measurements were made on Zea mays L. plants either at different ambient CO₂ molar ratios (C_a) on well‐hydrated leaves (closed circles) or after water was withheld, on dehydrating leaves (open circles) at normal C_a (about 360 ppm). Gas exchange chlorophyll fluorescence emission measurements were coupled as described in Cornic and Briantais (1991). Conditions during measurements were as follows: leaf temperature, 23·5 ± 0·6 °C; O₂ molar ratio, 21 % in nitrogen; vapour pressure deficit (VPD), 0·7 ± 0·1 kPa; photon flux density (PFD), 450 µmol m^–2 s^–1 (K. Saccardy and G. Cornic, unpubl. res.).

Fig. 2. Relationship between A_max, the net photosynthesis (net CO₂ or net O₂ evolution) measured at elevated C_a (up to 10 %) and A, the net CO₂ uptake by leaves maintained at normal C_a. Both A_max and A were measured during a drought. A is taken as an indicator of the water status in the leaf: it decreases as desiccation increases. Data are taken from Cornic et al. (1989, Figs 1 and 2A), Graan and Boyer (1990, Fig. 5A) and Tourneux and Peltier (1995, Figs 4C and 5).

Fig. 3. Relationships between relative value of Φ_PSII and A during desiccation of detached leaves from P. vulgaris. The O₂ molar fraction during measurements was either 21 % (closed circles) or 1 % (open circles) in nitrogen. Other conditions were as follows: leaf temperature, 23·5 °C initially, increasing to 24·9 °C at the end of the measurements; PFD, 450 µmol m^–2 s^–1; and C_a, about 360 ppm. Relative water content of the leaves at the end of the experiments was 76·2 and 72·8 % in 21 and 1 % O₂, respectively (G. Cornic, unpubl. res.).

Fig. 4. Relationship between A and the leaf internal CO₂ molar ratio (C_i) measured on detached Lavatera trimestris L. leaves either before (well‐hydrated, closed circles) or after (open circles) a rapid desiccation. Plants were grown in winter, in a peat soil, in a temperature‐controlled glasshouse in the University of Illinois at Urbana‐Champaign, USA (temperature from about 20 °C during the day to 17 °C during the night). Measurements were made with a LICOR 6400 under either a PFD of 450 (A) or 990 (B) µmol m^–2 s^–1. Other conditions were as follows: leaf temperature 25 ± 0·3 °C; C_a, 350 ppm; and VPD, 1·5 ± 0·5 kPa. Relative water content of the leaves at the end of the experiments was 70·4 and 67·7 % for A and B, respectively (G. Cornic and S. Long, unpubl. res.).

Fig. 5. Relation between A_G (estimation of gross photosynthesis = A + dark respiration) and J_c/J_o where J_c is the rate of RuBP carboxylation and J_o the rate of RuBP oxygenation calculated as in Epron and Cornic (1993) by measuring chlorophyll fluorescence emission (with an FMS2, Hansatech fluorometer) in parallel with net CO₂ uptake during the experiments presented in Fig. 4. As explained in the text, the ratio J_c/J_o is proportional to C_c, the carbon dioxide molar fraction in the chloroplasts. Measurements were performed at a PFD of 450 µmol m^–2 s^–1 (LL, circles) or under a PFD of 990 µmol m^–2 s^–1 (HL, triangles and squares), on well‐hydrated leaves (closed symbols) at different C_a, or during dehydration of the cut leaves at constant C_a (open symbols). Data were taken from Fig. 4A and B (circles and triangles). Other data from measurements taken under a PFD of 990 µmol m^–2 s^–1 were added (squares). Experimental conditions as in Fig. 4. The correlation line was calculated for all data corresponding to J_c/J_o < 1·4 (G. Cornic and S. Long, unpubl. res.).

Fig. 6. Variation in relative values of Φ_PSII and A during desiccation of cut leaves of L. trimestris. Chlorophyll fluorescence emission was done in parallel with net CO₂ uptake during the experiments (see Figs 4 and 5). Closed symbols, Φ_PSII measurements; open symbols, A measurements. Light conditions 450 (circles) or 990 (squares) µmol m^–2 s^–1. These measurements were performed simultaneously with the measurements presented in Fig. 4A and B.

Fig. 7. Variation in Φ_PSII and q_p as a function of A during dehydration of Pisum sativum L. plants obtained by withholding water. Plants were grown on a peat soil in a growth cabinet and watered every 2 d. A, Plants grown at 25/20 °C (day/night), 16 h light period (normal temperature); relative water content of the leaves was about 62 % at the end of the experiment. B, Plants grown at 8–9/6 °C (day/night), 16 h light period (low temperature); relative water content of the leaves was about 69 % at the end of the experiment. In both conditions, PFD at the top of the plants during growth was 350 µmol m^–2 s^–1. Measurements were made as explained in Fig. 1. Conditions during measurements were: leaf temperature, 23·5 ± 0·5 °C; C_a, 360 ± 5 ppm; VPD, 0·6 ± 0.2 kPa; and PFD, 450 µmol m^–2 s^–1. The standard deviation of the mean is shown when it was possible to calculate the mean of three to five close measurements (N. Manuel and G. Cornic, unpubl. res.).

Fig. 8. Typical variation over time of Φ_PSII when C_a was changed abruptly from 350 to 4000 ppm around dehydrated leaves of P. sativum plants grown at normal temperature (relative water content of the leaf = 68·2 %). Other experimental conditions were as in Fig. 7. The line parallel to the x‐axis is the mean Φ_PSII value measured on well‐hydrated leaves ± s.e. (dotted lines, n = 4).

Fig. 9. Typical variation over time of Φ_PSII when C_a was changed abruptly from 350 to 4000 ppm around dehydrated leaves of P. sativum plants grown at low temperature (relative water content of the leaf = 74·5 %). For details see Fig. 8 legend.