Simulated Analysis of Influence of Changes in H+-ATPase Activity and Membrane CO2 Conductance on Parameters of Photosynthetic Assimilation in Leaves

Abstract

Photosynthesis is an important process in plants which influences their development and productivity. Many factors can control the efficiency of photosynthesis, including CO₂ conductance of leaf mesophyll, which affects the CO₂ availability for Rubisco. It is known that electrical stress signals can decrease this conductance, and the response is probably caused by inactivation of H⁺-ATPase in the plasma membrane. In the current work, we analyzed the influence of both CO₂ conductance in the plasma membrane, and chloroplast envelopes and H⁺-ATPase activity on photosynthetic CO₂ assimilation, using a two-dimensional mathematical model of photosynthesis in leaves. The model included a description of assimilation on the basis of the Farquhar-von Caemmerer-Berry model, ion transport through the plasma membrane, diffusion of CO₂ in the apoplast, and transport of CO₂ through the plasma membrane and chloroplast envelope. The model showed that the photosynthetic CO₂ assimilation rate was mainly dependent on the plasma membrane and chloroplast envelope conductance; direct influence of the H⁺-ATPase activity (through changes in pH and CO₂/HCO₃^- concentration ratio) on this rate was weak. In contrast, both changes in CO₂ conductance of the plasma membrane and chloroplast envelopes and changes in the H⁺-ATPase activity influenced spatial heterogeneity of the CO₂ assimilation on the leaf surface in the simulated two-dimensional system. These effects were also observed under simultaneous changes in the CO₂ conductance of the plasma membrane and H⁺-ATPase activity. Qualitatively similar influence of changes in the CO₂ conductance of the plasma membrane and chloroplast envelopes, and changes in the H⁺-ATPase activity on photosynthesis were shown for two different densities of stomata in the simulated leaf; however, lowering the density of stomata decreased the assimilation rate and increased the heterogeneity of assimilation. The results of the model analysis clarify the potential influence of H⁺-ATPase inactivation on photosynthesis, and can be the basis for development of new methods for remote sensing of the influence of electrical signals.

Keywords: H+-ATPase; chloroplast envelope CO2 conductance; electrical signals; photosynthetic CO2 assimilation; plasma membrane CO2 conductance; spatial heterogeneity; two-dimensional photosynthetic model.

Figure 1

(a) A general scheme of the two-dimensional model of photosynthesis in a leaf. The simulated leaf is round and is composed of cells which are connected through the apoplast. Small arrows show transport of carbon dioxide, H⁺, and K⁺ between apoplastic volumes of neighboring cells and across the plasma membrane. PAR is the photosynthetically active radiation. (b) A description of ion and CO₂ fluxes, the activities of ion transporters, buffer capacities, and photosynthetic and respiratory processes simulated by the model. pH_ap, pH_cyt, and pH_str are the pH in the apoplast, cytoplasm, and stroma of chloroplasts, respectively. B_cyt⁻ and B_cytH are the free and proton-bound cytoplasmic buffers. B_ap⁻, B_apH, and B_apK are the free, proton-bound, and potassium-bound apoplastic buffers. E_m is the gradient of electrical potential across the plasma membrane. FvCB-model is the Farquhar–von Caemmerer–Berry model. The main systems of ion transport at rest, including H⁺-ATP-ases, H⁺/K⁺-antiporters, inwardly rectifying K⁺ channels, and outwardly rectifying K⁺ channels are described in the two-dimensional photosynthetic model. The schemes from [42], with modifications, are used.

Figure 2

Light dependence of the photosynthetic CO₂ assimilation rate A_hv (a) and the coefficient of variation of assimilation CV(A_hv) (b). PAR is photosynthetically active radiation. Each stomata in the simulated leaf was located in center of a 3 × 3 cell square or a 5 × 5 cell square. The basic values of the model parameters were used.

Figure 3

Simulated dependence of the photosynthetic CO₂ assimilation rate (A_hv) on the H⁺-ATPase activity in variants with stomata located in center of the 3 × 3 cell square (a) or in center of the 5 × 5 cell square (b) under various intensities of PAR. The value of the H⁺-ATPase activity from our previous work [42] was used as 100%.

Figure 4

Simulated dependence of variation coefficient of spatial distribution of the photosynthetic CO₂ assimilation rate (CV(Ahv)) on the H⁺-ATPase activity in variants with stomata located in center of 3 × 3 cells square (a) or in center of 5 × 5 cells square (b) under various intensities of PAR. Value of the H⁺-ATPase activity from our previous work [42] was used as 100%.

Figure 5

Dependence of the photosynthetic CO₂ assimilation rate (A_hv) (a) and the coefficient of variation of the spatial distribution of this rate (CV(A_hv)) (b) on the plasma membrane CO₂ conductance under PAR intensity equaling to 221 μmol m⁻² s⁻¹. Each stomata in the simulated leaf was located in center of a 3 × 3 cell square or in center of a 5 × 5 cell square. The value of the plasma membrane CO₂ conductance from our previous work [42] was used as 100%.

Figure 6

Dependence of the photosynthetic CO₂ assimilation rate (A_hv) (a) and the coefficient of variation of the spatial distribution of this rate (CV(A_hv)) (b) on the CO₂ conductance of chloroplast envelopes under PAR intensity equaling to 221 μmol m⁻² s⁻¹. Each stomata in the simulated leaf was located in center of a 3 × 3 cell square or in center of a 5 × 5 cell square. The value of the CO₂ conductance of chloroplast envelopes from our previous work [42] was used as 100%.