Development of Two-Dimensional Model of Photosynthesis in Plant Leaves and Analysis of Induction of Spatial Heterogeneity of CO2 Assimilation Rate under Action of Excess Light and Drought

Abstract

Photosynthesis is a key process in plants that can be strongly affected by the actions of environmental stressors. The stressor-induced photosynthetic responses are based on numerous and interacted processes that can restrict their experimental investigation. The development of mathematical models of photosynthetic processes is an important way of investigating these responses. Our work was devoted to the development of a two-dimensional model of photosynthesis in plant leaves that was based on the Farquhar–von Caemmerer–Berry model of CO2 assimilation and descriptions of other processes including the stomatal and transmembrane CO2 fluxes, lateral CO2 and HCO3− fluxes, transmembrane and lateral transport of H+ and K+, interaction of these ions with buffers in the apoplast and cytoplasm, light-dependent regulation of H+-ATPase in the plasma membrane, etc. Verification of the model showed that the simulated light dependences of the CO2 assimilation rate were similar to the experimental ones and dependences of the CO2 assimilation rate of an average leaf CO2 conductance were also similar to the experimental dependences. An analysis of the model showed that a spatial heterogeneity of the CO2 assimilation rate on a leaf surface should be stimulated under an increase in light intensity and a decrease in the stomatal CO2 conductance or quantity of the open stomata; this prediction was supported by the experimental verification. Results of the work can be the basis of the development of new methods of the remote sensing of the influence of abiotic stressors (at least, excess light and drought) on plants.

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

“…It was shown that the CO 2 assimilation rate and its coefficient of variation (CV(A hv )) were increased with increasing photosynthetically active radiation (PAR). The light saturation of these parameters was observed under illumination intensities equal to 500 µmol m −2 s −1 and more; this value was similar to the light saturation of A hv in pea leaves [42]. It should be noted that the CO 2 assimilation rate was more in the variant with stomata localized in center of a 3 × 3 cell square than in the variant with stomata localized in center of a 5 × 5 cell square (Figure 2a).…”

“…In accordance with our previous work [42], influence of light intensity on the photosynthetic CO 2 assimilation rate and on its spatial heterogeneity on the leaf surface was investigated at the first stage of the current analysis. Light dependence of the CO 2 assimilation rate and the variation coefficient of this assimilation are shown in Figure 2.…”

“…The two-dimensional model of photosynthesis in leaves, which was earlier developed and verified [42], was used in the current investigation. A detailed description of the equations and parameters of this model is shown in File S1 (Supplementary Materials).…”

“…These models show the role of different leaf structures in mesophyll conductance, and simulate the dependence of CO 2 assimilation on its distance from the illuminated leaf surface [4,41]. However, analysis of the influence of surface distribution of the photosynthetic processes can also be important for understanding the role of H + -ATPase in photosynthetic regulation [42], because lateral propagation of carbon dioxide and its influx into cells can be dependent upon the ratio of CO 2 to HCO 3 − , and on the CO 2 conductance of the plasma membrane and chloroplast envelopes. Additionally, it is notable that analysis of spatial distribution of the photosynthetic CO 2 assimilation rate on the leaf surface can show changes in this distribution, which can be markers of electrical signal-induced photosynthetic response [43,44].…”

“…Earlier, we developed the two-dimensional model of photosynthetic processes in leaves [42], which can be used for investigation of the influence of membrane conductance and H + -ATPase activity on the photosynthetic CO 2 assimilation rate and the spatial heterogeneity of this rate on the leaf surface. The current work has the following specific aims: (i) Analysis of the influence of changes in H + -ATPase activity on the photosynthetic CO 2 assimilation rate.…”