The regulation of Rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato

Abstract

The temperature response of net CO(2) assimilation rate (A), the rate of whole-chain electron transport, the activity and activation state of Rubisco, and the pool sizes of ribulose-1,5-bisphosphate (RuBP) and 3-phosphoglyceric acid (PGA) were assessed in sweet potato (Ipomoea batatas) grown under greenhouse conditions. Above the thermal optimum of photosynthesis, the activation state of Rubisco declined with increasing temperature. Doubling CO(2) above 370 mubar further reduced the activation state, while reducing CO(2) by one-half increased it. At cool temperature (<16 degrees C), the activation state of Rubisco declined at CO(2) levels where photosynthesis was unaffected by a 90% reduction in O(2) content. Reduction of the partial pressure of CO(2) at cool temperature also enhanced the activation state of Rubisco. The rate of electron transport showed a pronounced temperature response with the same temperature optimum as A at elevated CO(2). RuBP pool size and the RuBP-to-PGA ratio declined with increasing temperature. Increasing CO(2) also reduced the RuBP pool size. These results are consistent with the hypothesis that the reduction in the activation state of Rubisco at high and low temperature is a regulated response to a limitation in one of the processes contributing to the rate of RuBP regeneration. To further evaluate this possibility, we used measured estimates of Rubisco capacity, electron transport capacity, and the inorganic phosphate regeneration capacity to model the response of A to temperature. At elevated CO(2), the activation state of Rubisco declined at high temperatures where electron transport capacity was predicted to be limiting, and at cooler temperatures where the inorganic phosphate regeneration capacity was limiting. At low CO(2), where Rubisco capacity was predicted to limit photosynthesis, full activation of Rubisco was observed at all measurement temperatures.

Figure 1.

The light responses of A of sweet potato at leaf temperature of 25°C (solid lines) with C_i of 140 (white triangle), 250 (white square), and 500 (white circle) μbar; or at leaf temperature of 35°C (dashed lines) with C_i of 140 (black triangle), 250 (black square), and 500 (black circle) μbar.

Figure 2.

The temperature responses of fully activated Rubisco activity (white circles) and electron transport rate (black circles) in sweet potato leaves. Mean ± se, n = 4 per point.

Figure 3.

A, The temperature response of the Rubisco activation state in sweet potato leaves measured at the indicated C_i of 140 (black circle), 250 (white square), and 500 (black triangle) μbar. Mean ± se, n = 4. In B, the modeled temperature response of the capacity for RuBP regeneration to the capacity of RuBP consumption by Rubisco is shown for the three CO₂ levels at which the activation state measurements were conducted. The ratio of the RuBP regeneration capacity to the RuBP consumption capacity was modeled according to Sage (1990) with input parameters as described in the Supplemental Appendix. In determining the RuBP consumption capacity, the maximum capacity of Rubisco was multiplied by 0.9 to account for the observation that the maximum activation state of Rubisco in sweet potato is 90%.

Figure 4.

The temperature response of the pool sizes of RuBP (A) and PGA (B), and the RuBP to PGA ratio (C) in sweet potato leaves measured at C_i of 140 (black circle), 250 (white circle) and 500 (black triangle) μbar. Mean ± se, n = 4. The mean Rubisco content in sweet potato was determined to be 22.6 μmol catalytic sites m⁻², which is equivalent to 1.6 g Rubisco m⁻².

Figure 5.

The rate of net CO₂ assimilation in sweet potato leaves as a function of C_i. Data in A were obtained in O₂ partial pressure of 200 mbar and at the indicated leaf temperatures. The data in B were obtained in O₂ partial pressures of 200 mbar (solid lines) at the indicated leaf temperatures, or in an O₂ partial pressure of 30 mbar (dashed lines) at the indicated leaf temperatures. A and B are derived from independent measurements of different sweet potato leaves.

Figure 6.

The temperature response of the IS in sweet potato. Black circles are measured data from A versus CO₂ responses. Each point represents the IS of a single A versus C_i response, calculated by fitting a least-squares linear regression through at least two (and usually three to five) gas exchange data points. The open circles are estimated IS calculated according to the equation IS = V_cmax/(Γ_* + K_c(1 + O/K_o) from Farquhar and von Caemmerer (1982), using mean Rubisco activities in Figure 2, the kinetic equations in the Supplemental Appendix, and the measured activation state at 140 μbar C_i in Figure 3A. The solid line is the modeled response for the IS using the regression of measured Rubisco V_cmax versus temperature (Eq. A2 in Supplemental Appendix) and the kinetic responses given in the Supplemental Appendix.

Figure 7.

The temperature response of day respiration rate in sweet potato leaves. Data were calculated using the IS and the CO₂ compensation point in the absence of nonphotorespiratory CO₂ evolution (Brooks and Farquhar, 1985). The solid line is the modeled response of R_d according to Harley et al. (1985; see the Supplemental Appendix for equation).

Figure 8.

The temperature response of A in sweet potato leaves measured at the C_i of 140 (black circle), 250 (white circle), and 500 (black triangle) μbar; or modeled from fully activated Rubisco activities from Figure 2 modified to account for the Rubisco activation state from Figure 3A at C_i of 140, 250, and 500 μbar (diamonds). In A, the solid lines are theoretical temperature responses of A modeled for conditions assuming the Rubisco capacity is limiting. In B, the dashed lines are modeled temperature responses of A under conditions of an electron transport limitation; the dotted line is the modeled temperature response of A assuming the capacity for Pi regeneration is limiting A. Modeled data were calculated as described in the Supplemental Appendix.