Exploring the Potential of Selenium-Containing Amine (Se-AMA) to Enhance Photosynthesis and Leaf Water Content: New Avenues for Carbonic Anhydrase Modulation in Arabidopsis thaliana

Abstract

Global changes and growing demands have led to the development of new molecular approaches to improve crop physiological performances. Carbonic anhydrase (CA) enzymes, ubiquitous across various life kingdoms, stand out for their critical roles in plant photosynthesis and water relations. We hypothesize that the modulators of human CAs could affect plant physiology. Our research demonstrated that foliar treatments with a synthetic selenium-containing CA activator (Se-AMA) influenced the physiological performances of Arabidopsis thaliana. Se-AMA increased net photosynthesis (A + 31.7%) and stomatal conductance (g_s + 48.2%) at 100 µM, with the most notable effects after 10 days of treatment. Se-AMA at 300 µM proved to be even more effective, boosting A and g_s by 19.9% and 55.3%, respectively, already after 3 days of application. Morning treatment with Se-AMA at 300 µM enhanced photosynthetic performances throughout the day, suggesting that the positive effect of Se-AMA lasted for several hours. Additionally, Se-AMA increased water content in plants by 17.1%, suggesting that Se-AMA treatment may have improved plant water absorption and resource management. This effect might be linked to Se-AMA's role in modulating specific CA isoforms working with aquaporins. Although preliminary, these findings suggest that Se-AMA could enhance plant physiological performances under the conditions of non-limiting water availability.

Keywords: apparent carboxylation efficiency; leaf gas exchange; net photosynthesis; stomatal conductance; synthetic activators.

Figure 1

Impact of different doses of Se-AMA on the physiological performances of Arabidopsis thaliana (experiment 1). Three separate groups of plants were treated with foliar sprays containing varying concentrations of the tested molecule (25, 50, or 100 µM of Se-AMA dissolved in an aqueous solution). An additional group of plants was sprayed with a mock solution (without Se-AMA) to serve as controls (0 µM of Se-AMA). During the experiment, the plants were monitored for phytotoxic symptoms (a) and subjected to a gas exchange analysis, which included the measurements of net photosynthesis (A) (b), stomatal conductance (g_s) (c), apparent carboxylation efficiency (A/C_i) (d), and transpiration rate (E) (e). Three time points were assessed: 8 h after treatment (AT), 10 days-AT, and 12 days-AT. Data are presented as means ± SD from four biological replicates, with different letters indicating significant differences between the Se-AMA treatments at each time point (two-way ANOVA with repeated measurements, followed by a post hoc Tukey test, p < 0.05, n = 4). A comprehensive summary of the statistical analysis is provided in Table S1, including details on the effect of time on the photosynthetic performances for each treatment.

Figure 2

Effect of different doses of Se-AMA application on Arabidopsis thaliana water content and dry matter (Experiment 1). After 10 days of treatments, parameters relative to plant fresh weight (FW) and plant dry weight (DW) on the plants treated either with a control solution (0 µM Se-AMA) or with different concentrations of Se-AMA (25, 50, or 100 µM) were assessed: FW (a) and DW (b). Data are presented as means ± SD from four biological replicates, with different letters indicating significant differences between the Se-AMA treatments (one-way ANOVA, followed by a post hoc Tukey test, p < 0.05, n = 4).

Figure 3

Impact of high doses of Se-AMA on the physiological performances of Arabidopsis thaliana (experiment 2). Treatment was performed by spraying the plants with an aqueous solution containing 300 µM Se-AMA for three consecutive days. A mock solution (without Se-AMA) was applied to an additional group of plants serving as controls (0 µM of Se-AMA). At three days after treatment (AT), the plants were monitored for phytotoxic symptoms (a) and subjected to a gas exchange analysis: net photosynthesis (A) (b), stomatal conductance (g_s) (c), apparent carboxylation efficiency (A/C_i) (d), and transpiration rate (E) (e). Data are presented as means ± SD, with stars indicating significant differences between the control and Se-AMA treatments (unpaired t-test, ** p < 0.01, *** p < 0.001, n = 5).

Figure 4

Impact of high doses of Se-AMA on Arabidopsis thaliana growth. At 3 days after treatment (AT), growth-related parameters of both controls (0 µM Se-AMA) and plants supplied with 300 µM Se-AMA were assessed: plant fresh weight (FW) (a) and plant dry weight (DW) (b). Data are presented as means ± SD, with stars indicating significant differences between control and Se-AMA treatments (unpaired t-test, * p < 0.05, n = 5).

Figure 5

Daily effect of Se-AMA on the physiological performances of Arabidopsis thaliana (experiment 3). The impact of a single treatment with 300 µM Se-AMA on daily photosynthetic performances was assessed by performing a gas exchange analysis at 14:00 h (h) and 18:00 h: net photosynthesis (A) (a), stomatal conductance (g_s) (b), apparent carboxylation efficiency (A/C_i) (c), and transpiration rate (E) (d) of the plants either mock-treated (0 µM Se-AMA) or supplied with Se-AMA (300 µM Se-AMA). Data are presented as means ± SD, with different letters indicating significant differences between the Se-AMA treatments at each time point (two-way ANOVA with repeated measurements, followed by a post hoc Tukey test, p < 0.05, n = 5). A comprehensive summary of the statistical analysis is provided in Table S2, including details on the effect of time on photosynthetic performances for each treatment.

Scheme 1

Synthesis of Se-AMA.