Development of Modified Farquhar-von Caemmerer-Berry Model Describing Photodamage of Photosynthetic Electron Transport in C3 Plants under Different Temperatures

Abstract

Photodamage of photosynthetic electron transport is a key mechanism of disruption of photosynthesis in plants under action of stressors. This means that investigation of photodamage is an important task for basic and applied investigations. However, its complex mechanisms restrict using experimental methods of investigation for this process; the development of mathematical models of photodamage and model-based analysis can be used for overcoming these restrictions. In the current work, we developed the modified Farquhar-von Caemmerer-Berry model which describes photodamage of photosynthetic electron transport in C₃ plants. This model was parameterized on the basis of experimental results (using an example of pea plants). Analysis of the model showed that combined inactivation of linear electron flow and Rubisco could induce both increasing and decreasing photodamage at different magnitudes of inactivation of these processes. Simulation of photodamage under different temperatures and light intensities showed that simulated temperature dependences could be multi-phase; particularly, paradoxical increases in the thermal tolerance of photosynthetic electron transport could be observed under high temperatures (37-42 °C). Finally, it was shown that changes in temperature optimums of linear electron flow and Rubisco could modify temperature dependences of the final activity of photosynthetic electron transport under photodamage induction; however, these changes mainly stimulated its photodamage. Thus, our work provides a new theoretical tool for investigation of photodamage of photosynthetic processes in C₃ plants and shows that this photodamage can be intricately dependent on parameters of changes in activities of linear electron flow and Rubisco including changes induced by temperature.

Keywords: Farquhar–von Caemmerer–Berry model; photodamage; photosynthesis; temperature dependences; thermal tolerance.

Figure 1

The general scheme of the modified FvCB model describing photodamage of photosynthetic electron transport (see text for details).

Figure 2

Experimental (blue markers) and model (black line) dependences of the linear electron flow (J) through the ETC on the intensity of the blue actinic light. Experimental J values were calculated on basis of Equation (17) (n = 7). The model dependence was approximated by Equation (4) at J_max = 55 µmol∙m⁻²∙s⁻¹ and θ = 0.25. The determination coefficient between these dependences (R²) was 0.9862.

Figure 3

Experimental (blue markers) and model (black line) dependences of the mesophyll conductance to CO₂ (g_m) on the intensity of the blue actinic light. The model dependence was approximated by Equation (10) at g_d = 0.018 mol∙m⁻²∙s⁻¹, Δg_max = 0.25 mol∙m⁻²∙s⁻¹, n = 2 and K = 1000 µmol∙m⁻²∙s⁻¹. The determination coefficient between these dependences (R²) was 0.992.

Figure 4

Experimental (blue markers) and model (black line) dependences of the damage rate constant (k_d) on the intensity of the blue actinic light (n = 6–7). The model dependence was calculated on basis of Equation (11) at ${\mathrm{k}}_{\mathrm{d}}^0$ = 0.00008 s⁻¹ and α = 0.09; W_j and W were calculated using Equations (1) and (3)–(6), standard parameters of the FvCB model [35] and results from Table 1. The determination coefficient between these dependences (R²) was 0.856.

Figure 5

Experimental (blue markers) and model (black line) dependences of activity of the CO₂ carboxylation by RuBP (Act(RuBP) (a) and linear electron flow (Act(J)) (b) on temperature. Experimental parameters (A_hv and J) were normalized on maximal values. Equation (12) was used for approximation of experimental dependences. Act(RuBP) was approximated at t_o = 25 °C and σ₁ = σ₂ = 22 °C; R² = 0.942. Act(J) was approximated at t^o = 31 °C and σ₁ = 36 and σ₂ = 15.5 °C; R² = 0.988.

Figure 6

Heatmaps of the final damage of photosynthetic electron transport (the final A_j) induced by decreasing activity of J (Act(J)) and RuBP (Act(RuBP)) under the actinic light with low (108 µmol∙m⁻²∙s⁻¹) (a) and high (758 µmol∙m⁻²∙s⁻¹) (b) intensities. Act(J) and Act(RuBP) in heatmaps show their values under imitation of stressful conditions. The final A_j, which is calculated on basis of Equation (11) and can range from 0 to 1, are shown by pseudo-colors. This A_j shows photodamage of the electron transport because its increase corresponded to decreasing photodamage.

Figure 7

Simulated temperature dependences of the final rate of photosynthetic electron transport (A_j) under different intensities of light for the basic model parameters. The final A_j, which can range from 0 to 1, shows photodamage of the electron transport because its increase corresponded to decreasing photodamage.

Figure 8

Simulated temperature dependences of the final rate of photosynthetic electron transport (A_j) under different intensities of light at the decreased g_s (10% from the basic value). The final A_j, which can range from 0 to 1, shows photodamage of the electron transport because its increase corresponded to decreasing photodamage.

Figure 9

Simulated temperature dependences of the final rate of photosynthetic electron transport (A_j) under modifications of temperature optimums of RuBP or J under the 425 µmol∙m⁻²∙s⁻¹ light. (a) ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{J}}=31 °\mathrm{C}$ and ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{C}}=20 °\mathrm{C}$. (b) ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{J}}=31 °\mathrm{C}$ and ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{C}}=30 °\mathrm{C}$. (c) ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{J}}=26 °\mathrm{C}$ and ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{C}}=25 °\mathrm{C}$. (d) ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{J}}=36 °\mathrm{C}$ and ${\mathrm{t}}_{\mathrm{o}}^{\mathrm{C}}=25 °\mathrm{C}$. The final A_j, which can range from 0 to 1, shows photodamage of the electron transport because its increase corresponded to decreasing photodamage.