Physiological and Biochemical Responses of Pseudocereals with C3 and C4 Photosynthetic Metabolism in an Environment with Elevated CO2

Abstract

The present work aimed to investigate the effect of increasing CO₂ concentration on the growth, productivity, grain quality, and biochemical changes in quinoa and amaranth plants. An experiment was conducted in open chambers (OTCs) to evaluate the responses of these species to different levels of CO₂ {a[CO₂] = 400 ± 50 μmol mol^-1 CO₂ for ambient CO₂ concentration, e[CO₂] = 700 ± 50 μmol mol^-1 CO₂ for the elevated CO₂ concentration}. Growth parameters and photosynthetic pigments reflected changes in gas exchange, saccharolytic enzymes, and carbohydrate metabolism when plants were grown under e[CO₂]. Furthermore, both species maintained most of the parameters related to gas exchange, demonstrating that the antioxidant system was efficient in supporting the primary metabolism of plants under e[CO₂] conditions. Both species were taller and had longer roots and a greater dry weight of roots and shoots when under e[CO₂]. On the other hand, the panicle was shorter under the same situation, indicating that the plants invested energy, nutrients, and all mechanisms in their growth to mitigate stress in expense of yield. This led to a reduction on panicle size and, ultimately, reducing quinoa grain yield. Although e[CO₂] altered the plant's metabolic parameters for amaranth, the plants managed to maintain their development without affecting grain yield. Protein levels in grains were reduced in both species under e[CO₂] in the average of two harvests. Therefore, for amaranth, the increase in CO₂ mainly contributes to lowering the protein content of the grains. As for quinoa, its yield performance is also affected, in addition to its protein content. These findings provide new insights into how plants C3 (amaranth) and C4 (quinoa) respond to e[CO₂], significantly increasing photosynthesis and its growth but ultimately reducing yield for quinoa and protein content in both species. This result ultimately underscore the critical need to breed plants that can adapt to e[CO₂] as means to mitigate its negative effects and to ensure sustainable and nutritious crop production in future environmental conditions.

Keywords: Amaranthus spp.; Chenopodium quinoa (Willd); carbohydrate metabolism; climate change; photosynthetic parameters.

Figure 1

Effect of CO₂ on plant growth parameters. Shoot length (A); shoot dry matter (B); root length (C); root system dry matter (D) of amaranth and quinoa plants. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval of the mean. * Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 10).

Figure 2

Effect of CO₂ on growth parameters. Panicle length (A); number of branches per panicle (B); stem diameter (C); leaf area (D) of amaranth and quinoa plants. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval. * Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 10).

Figure 3

Effect of CO₂ concentration on photosynthetic pigments. Chlorophyll-a (CHLa) (A); chlorophyll-b (CHLb) (B); carotenoids (C) of amaranth and quinoa plants in transition stadium between vegetative and flowering. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval. * Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 10). ns indicates non-significant differences (t test p ≤ 0.05, n = 10).

Figure 4

Effect of CO₂ on leaf gas exchange. Net CO₂ assimilation (A); stomatal conductance (B); internal concentration of CO₂ (C); transpiration rate (D); water use efficiency (WUE) (E) of amaranth and quinoa plants in transition stadium between vegetative and flowering. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval. * Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 10).

Figure 5

Effect of CO₂ on sucrose metabolism-related enzyme activity in leaves: soluble neutral invertases of cytosol (CINV) (A); soluble acid invertases of the vacuole (VINV) (B); cell wall acid invertase (CWINV) (C); and sucrose synthase (SuSy) (D) activity. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval. *Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 4). ns indicates non-significant.

Figure 6

Effect of CO₂ on carbohydrate metabolism: total content of soluble sugars (A), sucrose-SUC (B), starch (C), and total soluble amino acids (D) on amaranth and quinoa leaves in transition stadium between vegetative and flowering. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval. * Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 4). ns indicates non-significant.

Figure 7

Antioxidant capacity evaluated by DPPH from amaranth and quinoa in transition stadium between vegetative and flowering, grown in the presence of different CO₂ concentrations (400 and 700 μmol mol⁻¹ CO₂). The extracts evaluated were obtained using the growing season 19/20 and 2020/2021. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂. The experiment was conducted during the 2019/2020 and 2020/2021 growing seasons. Error bars correspond to the 95% confidence interval. * Indicates significant difference between CO₂ concentration (t test p ≤ 0.05, n = 10).

Figure 8

Effects of CO₂ concentration on roots of amaranth (A) and quinoa (B) collected after grain maturation. a[CO₂] = plants grown in OTC with 400 ± 50 μmol mol⁻¹ CO₂; e[CO₂] = plants grown in OTC with 700 ± 50 μmol mol⁻¹ CO₂.