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. 2021 Feb 19;27(2):313–325. doi: 10.1007/s12298-021-00956-w

ABA and BAP improve the accumulation of carbohydrates and alter carbon allocation in potato plants at elevated CO2

Mohammad Javad Ahmadi-Lahijani 1,✉, Mohammad Kafi 1, Ahmad Nezami 1, Jafar Nabati 2, John E Erwin 3
PMCID: PMC7907407  PMID: 33707871

Abstract

Elevated CO2 interactions with other factors affects the plant performance. Regarding the differences between cultivars in response to CO2 concentrations, identifying the cultivars that better respond to such conditions would maximize their potential benefits. Increasing the ability of plants to benefit more from elevated CO2 levels alleviates the adverse effects of photoassimilate accumulation on photosynthesis and increases the productivity of plants. Despite its agronomic importance, there is no information about the interactive effects of elevated CO2 concentration and plant growth regulators (PGRs) on potato (Solanum tuberosum L.) plants. Hence, the physiological response and source-sink relationship of potato plants (cvs. Agria and Fontane) to combined application of CO2 levels (400 vs. 800 µmol mol−1) and plant growth regulators (PGR) [6-benzylaminopurine (BAP) + Abscisic acid (ABA)] were evaluated under a controlled environment. The results revealed a variation between the potato cultivars in response to a combination of PGRs and CO2 levels. Cultivars were different in leaf chlorophyll content; Agria had higher chlorophyll a, b, and total chlorophyll content by 23, 43, and 23%, respectively, compared with Fontane. The net photosynthetic rate was doubled at the elevated compared with the ambient CO2. In Agria, the ratio of leaf intercellular to ambient air CO2 concentrations [Ci:Ca] was declined in elevated-CO2-grown plants, which indicated the stomata would become more conservative at higher CO2 levels. On the other hand, the increased Ci:Ca in Fontane showed a stomatal acclimation to higher CO2 concentration. The higher leaf dark respiration of the elevated CO2-grown and BAP + ABA-treated plants was associated with a higher leaf soluble carbohydrates and starch content. Elevated CO2 and BAP + ABA shifted the dry matter partitioning to the belowground more than the above-media organs. The lower leaf soluble carbohydrate content and greater tuber yield in Fontane might indicate a more efficient photoassimilate translocation than Agria. The results highlighted positive synergic effects of the combined BAP + ABA and elevated CO2 on tuber yield and productivity of the potato plants.

Keywords: Dark respiration, Hydroponics, Photosynthetic rate, Photosynthetic pigments, Soluble carbohydrates, Starch

Introduction

Elevated CO2 concentration increases the photosynthetic efficiency of C3 plants through the inhibition of photorespiration (Drake et al. 1997). The growth and productivity of C3 plants are stimulated through a higher photosynthetic rate and water use efficiency at elevated CO2 concentrations (Reddy et al. 2010). The photosynthetic rate of potato plants have grown at an enriched CO2 open-top chamber increased by 40% compared with the control (Katny et al. 2005). Besides, higher sucrose and starch synthesis were observed in the plants grown at elevated CO2. The study of the source-sink relationship is important to evaluate the effect of elevated CO2 on plants. Physiological sinks are considered as a place to store photoassimilates. At elevated CO2, sink limitation suppresses photosynthesis due to negative feedback of starch accumulation, which can be improved through a balanced source-sink relationship (Long et al. 2004; Reddy et al. 2010).

Leaf dark respiration is widely considered as a determining factor in plant growth (Li et al. 2013). Studies revealed the important role of mitochondrial respiration in maintaining an optimal photosynthetic rate (Fuentes et al. 2011). Therefore, higher photosynthesis at elevated CO2 can be associated with higher dark respiration. The leaf dark respiration was differently affected by the elevated CO2 (Davey et al. 2004; Gifford 2004; Gomez-Casanovas et al. 2007). Due to the determining role of the respiratory pathway in the global carbon cycle in the cell, whole plant, and ecosystem levels (Wang et al. 2004), and its capability to return 40–50 percent of the fixed carbon into the atmosphere, a better understanding of dark respiration response to elevated CO2 might be of great importance.

Phytohormones regulate a wide range of processes in plants. Plant growth and metabolism regulation are intricate processes and controlled by the interactions of phytohormones (LeNoble et al. 2004). Depending on their content or the ratio, phytohormones regulate the photoassimilate distribution and productivity in plants (Aksenova et al. 2012). Remarkable effects of phytohormones on potato tuberization (the process of tuber formation) have previously been reported (Ewing 1995; Rodríguez-Falcón et al. 2006; Aksenova et al. 2012). Cytokinin (CK) and abscisic acid (ABA) are phytohormones that regulate the source-sink relationships and the senescence process in plants (Pospisilova et al. 2005). Cytokinins play essential roles in regulating plant growth and the demand for carbohydrates (Ramawat and Merillon 2013). Cytokinins affect potato tuberization (Palmer and Smith 1970; Aksenova et al. 2012). Tuberization is related to cell division; CK provokes cell division in plants, which is a vital component of the tuberization process (Romanov 2009). Starch biosynthesis is also enhanced by CK, which increases the sink capacity of developing tubers (Ramawat and Merillon 2013). The application of BAP in vitro increased plant dry matter and tuber yield of potato (Solanum tuberosum L.) plants (Roosta et al. 2015). The tuber number was also increased by the exogenous application of CK in potato (Solanum tuberosum L.) plants (Ewing and Struik 2010; Ramawat and Merillon 2013). Ewing and Struik (2010) observed that the plant ABA content was increased under short days; as an essential condition for the tuber initiation. Abscisic acid has an opposite effect to gibberellic acid (GA) activity (Wang et al. 2015). Ramawat and Merillon (2013) showed that ABA inhibited GA activity in the tuberization process.

Viral diseases are known as the main limiting factor of the productivity of potato plants. Producing virus-free tubers from micro-propagated plantlets helps reduce the risk of crop yield loss. Minitubers are virus-free tubers producing on micro-propagated potato plantlets in vitro (Struik and Wiersema 2012). Potato minitubers have the least pathogens with a faster proliferation rate for a greater yield (Sharma and Pandey 2013). An increase in the tuber number and mean tuber weight is of great desire in the minituber production industry. An increase in potato tuber yield was related to either the greater tuber number or mean tuber weight at elevated CO2 levels (Finnan et al. 2002, 2005; Sharma and Pandey 2013; Aien et al. 2014). Any possible strategy is required to enhance the quantity and quality of plant products to meet food security in the future. One of those strategies is the study of higher CO2 levels interaction with environmental factors, resulting in various responses in different plant species in the future climate change. Although various studies have evaluated the interactive effects of enriched CO2 and some environmental factors on plants, e.g., temperature (Thinh et al. 2017), drought (Yuhui et al. 2017), nitrogen (Yong et al. 2000), and salinity (Piñero et al. 2014), to our knowledge, no studies evaluated the interactive effects of simultaneous application of BAP and ABA, and elevated CO2 on potato plants. Hence, we hypothesized that the combined application of BAP and ABA under the elevated CO2 conditions improve the physiological and biochemical traits, minituber production, and the source-sink relationship in potato plants.

Materials and methods

Plant growth conditions

Micro-propagated potato plantlets (cvs. Agria and Fontane) were obtained from shoot cuttings grown in agar culture plates containing the Murashige and Skoog medium and supplemented with 3% sucrose, provided by the Yekta Seed Technology Company, Mashhad, Iran, in 2018. The uniform plantlets (5 cm length) were grown in plastic pots (15 and 30 cm, diameter and depth, respectively, one per pot) containing a sterile medium (perlite: coco peat, 1:1, v:v) in the controlled chambers (Conviron, Winnipeg, Canada). The environmental conditions inside the chambers were as follows: 400 µmol photons m−2 s−1 PPFD on the leaf surface supplied by fluorescent/incandescent lamps, 24/16 °C day/night air temperature, photoperiod 12/12 h (day/night), and 50/60 ± 5% (day/night) relative humidity. The plantlets were watered daily and fertilized by the standard Hoagland solution every 5 days (Hoagland and Arnon 1950).

CO2 treatments

Plantlets were divided into two groups of nine, and each group was subjected to 800 ± 10 µmol mol−1 (elevated) or 400 ± 10 µmol mol−1 (ambient) CO2 concentrations from the first day of the experiment. The enriched CO2 air was injected into the chambers at a flow rate of 1 l min−1, from a compressed gas cylinder (a mixture of ambient air with commercial CO2). The CO2 concentrations were continuously monitored using a calibrated infrared gas analyzer (High-performance CO2 meter, 77,535, China).

Plant growth regulator treatments (PGR)

At the time of tuber initiation (55 days after transplant; DAT), the plantlets were foliar sprayed by 50 µM BAP + ABA (6-Benzylaminopurine and ± -Abscisic Acid, Sigma Aldrich®) (Ahmadi-Lahijani et al. 2018). The control plants were sprayed with distilled water. 10 mL of solution was applied to each plant using a handheld sprinkler. PGRs were applied at the end of the daytime, avoiding photo-degradation or -oxidation.

Collection of experimental samples

Gas exchange variables were recorded on the youngest fully expanded leaves one week after PGR treatment (62 DAT). Then, the same leaves were collected, frozen immediately in liquid nitrogen, and stored at − 80 °C for biochemical analysis (Cao et al. 1994).

Gas exchange measurements

Net photosynthetic (Np) and dark respiration (Rd) rates, stomatal conductance (gs), transpiration rate (Tr), and intercellular CO2 concentration (Ci) of leaves were measured using a photosynthesis system (HCM-1000, Waltz, Germany) at the respective CO2 level at which the plants were grown. Ci:Ca ratio was calculated by dividing the intercellular to ambient CO2 concentration. Nine leaflets per cultivar were analyzed (three per replication; n = 9). Leaves photosynthetic parameters were allowed to stabilize for five min to a constant rate before each measurement. The leaf temperature, relative humidity, and air-to-leaf vapor pressure deficit (ALVPD) inside the cuvette were set to 25 °C, 50%, and 50 Pa/kPa, respectively. The leaf Rd was obtained by averaging three CO2 efflux rates at zero PPFD for each plant at the end of the daily dark period from 05:00 to 07:00 h (Li et al. 2013). The adaxial attached leaf surface was used to measure the chlorophyll fluorescence. Measurements were taken after a 15 min dark period using a handheld PEA Chlorophyll Fluorimeter (Hansatech, UK) from the same leaves. The actual quantum yield of photosystem II (Φ) was calculated according to Genty et al. (1989).

Leaf pigments and biochemical analysis

The method of Knudson et al. (1977) was used to assay the leaf pigments. 100 mg leaf fresh weight was homogenized in 98% ethanol using a mortar and pestle. The data were recorded at 665 and 649 nm using a spectrophotometer (Unico 2100, USA). The leaf soluble carbohydrate content (SC) was measured by the method of Dubois et al. (1956). Leaf fresh weight (100 mg) was homogenized in 70% ethanol using a mortar and pestle. A glucose standard curve was plotted to quantify the SC content. The residuals that remained from the SC measurement were used to assay the leaf starch content (ST); the residuals were rinsed three times by perchloric acid (Schlegel 1956). Absorbance was recorded at 485 nm spectrophotometrically. A glucose standard curve was plotted to determine the starch content of the leaves.

Plant harvest, dry matter, and tuber yield

The plants were harvested 90 DAT at the physiological maturity and then, divided into above-media (leaf and stem) and belowground parts (root and tuber). Tuber number (TN), mean tuber weight (MTW), and tuber yield per plant were determined. The tubers were categorized based on their diameters into small (< 15 mm), medium (15–25 mm), and large (> 25 mm). Tubers and roots were rinsed, and all tissues were oven-dried at 75 °C until constant weight. Dry matter (DM) allocation to different parts of the plants was calculated as a percentage of DM dedicated to the leaves, stems, roots, and tubers concerning the whole plant DM.

Statistical analysis

The experiment was carried out as a factorial arrangement (two CO2 concentrations, two hormonal treatments, and two cultivars) based on the completely randomized design with three replications. A two-way analysis of variance was used to specify the effects of the CO2 levels, PGRs, cultivars, and their interactions. Tukey's Studentized Range (HSD) test was performed to determine the mean difference at p ≤ 0.05. Data were presented as the mean ± SE. Statistical analysis was performed with SAS (v. 9.4) and MINITAB (v. 17) statistical software.

Results

Gas exchange variables

CO2 levels and cultivar interacted to affect Np (Table 1). The highest Np was recorded in BAP + ABA-treated Agria plants at elevated CO2 (Fig. 1). Leaf dark respiration (Rd) was significantly affected by foliar application of BAP + ABA and CO2 levels (Table 1). Elevated CO2 increased leaf Rd by 22 and 40% in Agria and Fontane, respectively, compared with the ambient. The highest leaf Rd was observed when BAP + ABA was applied at the elevated CO2. In Agria, application of BAP + ABA at elevated CO2 increased leaf Rd 46% compared with the untreated plants (Figs. 1 and 2). Leaf transpiration rate was significantly influenced by the interaction of CO2 levels and PGR (Table 1). Elevated CO2 significantly decreased Tr compared with the ambient CO2. BAP + ABA application decreased Tr at the ambient CO2; however, leaf Tr increased when BAP + ABA applied at the elevated CO2 (Fig. 1). CO2 levels and the interaction of CO2 × BAP + ABA affected gs (Table 1). The highest gs was recorded in untreated-Agria plants at the ambient CO2. Foliar application BAP + ABA diminished gs by 28 and 22% at the ambient and elevated CO2-grown Agria, respectively. While in Fontane, BAP + ABA increased gs by 48% at elevated CO2 compared with the untreated plants.

Table 1.

ANOVA results of growth regulators (PGR) and CO2 levels on leaf gas exchange variables of potato cultivars

Variables S.O.V‡ C.V.§
PGR (H)† Cultivar (C) CO2 concentration (G) H × C H × G G × C H × G × C
Np NS ** ** NS NS ** NS 19.9
Rd * NS ** NS NS NS NS 17.9
Tr ** NS ** NS ** NS NS 24.5
gs NS NS * * NS NS NS 25.1
Ci NS NS ** NS * ** NS 11.7
Ci:Ca * NS NS NS NS ** NS 13.8
Φ NS NS NS NS NS NS NS 0.43
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*Significant at P < 0.05; **Significant at P < 0.01, ns Not significant at P > 0.05. ‡S.O.V source of variation, §CV coefficient of variation, †H PGR, C Cultivar, G CO2 concentration, Np net photosynthetic rate, Rd dark respiration, gs stomatal conductance, Tr transpiration rate, Ci intercellular CO2, Ci:Ca intercellular to ambient partial pressure of CO2, Φ quantum yield of photosystem II

Fig. 1.

Fig. 1

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Effects of growth regulators (PGR) and CO2 levels on gas exchange variables of potato cultivars. A: net photosynthetic rate, B: dark respiration, C: stomatal conductance, D: intercellular CO2, E: Ci:Ca; intercellular to the ambient partial pressure of CO2, F: transpiration rate, G: quantum yield of photosystem II. AC; ambient CO2-no PGR, AH; ambient CO2-BAP + ABA (50 µM, tuberization), EC; elevated CO2-no PGR, EH; elevated CO2- BAP + ABA (50 µM, tuberization). PGR; plant growth regulator (55 days after transplant). Columns are means of three replicates (n = 9). Vertical bars are ± SE

Fig. 2.

Fig. 2

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Percent changes of gas exchange variables (a), biochemical traits (b), and growth and tuber yield parameters (c) of potato cultivars affected by a combination of elevated CO2 and BAP + ABA application compared with the control

Leaf intercellular CO2 concentration was affected by the interaction of CO2 levels with cultivar and BAP + ABA (Table 1). Hormonal treatment increased Ci by 46% at the ambient CO2 in Fontane. Elevated CO2 increased Ci by 10 and 28% in BAP + ABA-treated and untreated Agria plants, respectively, compared with the ambient CO2 (Fig. 1). At the ambient CO2, Ci was 28% higher in Agria than Fontane, while Fontane Ci was 34% higher compared with Agria at the elevated CO2. BAP + ABA and CO2 × cultivar interacted to affect Ci:Ca. Elevated CO2 decreased Ci:Ca in BAP + ABA-treated and untreated plants by 40 and 24%, respectively, compared with the ambient (Fig. 2). In Fontane, Ci:Ca increased by 31% when BAP + ABA applied at the ambient CO2, while Ci:Ca decreased by 32% in BAP + ABA-treated plants at the elevated CO2. Quantum yield was not affected by any of the treatments. However, BAP + ABA-treated and elevated CO2-grown plants slightly stimulated Φ compared with the untreated and ambient-grown plants, respectively (Figs. 1 and 2).

Biochemical analysis

Cultivars were different in leaf chlorophyll a (Chla), b (Chlb), and a + b (Chla + b) (Table 2). Generally, Agria had higher Chla, Chlb, and Chla + b by 23, 43, and 23%, respectively, compared with Fontane (Fig. 3). On the other hand, leaf carotenoid content was affected by the CO2 levels, cultivars, and BAP + ABA. In Agria, leaf carotenoid content decreased in BAP + ABA-treated plants by 21 and 18%, respectively, at the ambient and elevated CO2 compared with the untreated plants. Generally, Agria leaf carotenoid content was 20% greater than Fontane; however, in Fontane, elevated CO2 increased leaf carotenoid content by 30% compared with the ambient.

Table 2.

ANOVA results of growth regulators (PGR) and CO2 levels on leaf pigments and biochemical parameters of potato cultivars

Variables S.O.V‡ C.V.§
PGR (H)† Cultivar (C) CO2 concentration (G) H × C H × G G × C H × G × C
Chla NS ** NS NS NS NS NS 7.8
Chlb NS * NS NS NS NS NS 18.8
Chla + b NS ** NS NS NS NS NS 10.8
Chla:b NS NS NS NS NS NS NS 25.3
Car * ** ** NS NS NS NS 10.9
SC * ** NS NS NS * NS 10.9
ST ** NS NS NS NS NS NS 19.2
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*Significant at P < 0.05; **Significant at P < 0.01, ns Not significant at P > 0.05. ‡S.O.V source of variation, §CV coefficient of variation, †H PGR, C Cultivar, G CO2 concentration, Chla chlorophyll a, Chlb chlorophyll b, Chla + b total chlorophyll, Chla:b chlorophyll a/b ratio, Car carotenoids, SC soluble carbohydrates, ST starch

Fig. 3.

Fig. 3

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Effects of growth regulators (PGR) and CO2 levels on the leaf biochemistry of potato cultivars. A: chlorophyll a, B: chlorophyll b, C: total chlorophyll, D, carotenoids, E: soluble carbohydrates, F: starch G: chlorophyll a:b ratio. AC; ambient CO2-no PGR, AH; ambient CO2-BAP + ABA (50 µM, tuberization), EC; elevated CO2-no PGR, EH; elevated CO2- BAP + ABA (50 µM, tuberization). PGR; plant growth regulator (55 days after transplant). Columns are means of three replicates (n = 9). Vertical bars are ± SE

BAP + ABA, cultivar, and CO2 × cultivar affected the leaf soluble carbohydrate content (SC) (Table 2). Agria leaf SC was 17% greater than Fontane. In Agria, foliar application of BAP + ABA increased leaf SC by 20% compared with the untreated plants (Fig. 3). Elevated CO2 increased Agria leaf SC by 20% compared with the ambient; however, in Fontane, leaf SC remained unchanged at the elevated CO2. Leaf Starch content (ST) was only affected by BAP + ABA (Table 2). Foliar application of BAP + ABA increased leaf ST by 26 and 36% in Agria and by 15 and 10% in Fontane, respectively, at the ambient and elevated CO2 compared with the untreated plants (Fig. 3).

Plant DM and DM partitioning

Leaf dry matter (LDM) was affected by the CO2 levels and cultivar (Table 3). Generally, Fontane LDM was 53% greater compared with Agria (Fig. 4). At the elevated CO2, Agria and Fontane LDM were 32 and 21% greater, respectively, compared to those at the ambient CO2. Cultivar × BAP + ABA and cultivar × CO2 interacted to affect stem dry matter (SDW). In Agria, foliar application of BAP + ABA increased SDW by 32% at both CO2 levels compared with the untreated plants. Under the ambient CO2, Agria had a greater SDW than Fontane by 12%; however, elevated CO2 increased Fontane SDW by 20% higher compared to Agria (Fig. 4). Root dry matter (RDM) was affected by the interactions of elevated CO2 and cultivar (Table 3). Fontane RDM was higher at both CO2 levels compared with Agria. Elevated CO2 increased RDM by 52 and 67% in Agria and Fontane, respectively, compared with the ambient CO2 (Fig. 4). CO2 levels and cultivar interacted to affect the tuber dry matter (TDM). Fontane TDM was greater by 64% compared to Agria; however, elevated CO2 increased Agria TDM by 90% compared with the ambient CO2 (Fig. 4).

Table 3.

ANOVA results of growth regulators (PGR) and CO2 levels on plant dry matter, tuber yield, and yield component of potato cultivars

Variables S.O.V‡ C.V.§
PGR (H)† Cultivar (C) CO2 concentration (G) H × C H × G G × C H × G × C
LDM NS ** ** NS NS NS NS 15.3
SDM ** NS ** * NS * NS 11.3
RDM NS ** ** NS NS * NS 18.6
TDM NS ** ** NS NS ** NS 18.3
TY * ** ** NS NS NS NS 16.9
TN NS NS NS NS NS NS NS 20.6
MTW NS ** ** NS NS NS NS 17.3
ST (< 15 mm) NS * * NS NS NS NS 23
MT (15-25 mm) * * NS NS NS NS NS 19.9
LT (> 25 mm) NS NS ** NS NS NS NS 20.6
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*Significant at P < 0.05; ** Significant at P < 0.01, ns Not significant at P > 0.05. ‡S.O.V source of variation, §CV coefficient of variation, †H PGR, C Cultivar, G CO2 concentration, LDM leaf dry matter, SDM stem dry matter, RDM root dry matter, TDM tuber dry matter, TY tuber yield, MTW mean tuber weight, TN tuber number, ST small-size tuber, MT medium-size tuber, LT large-size tubers

Fig. 4.

Fig. 4

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Effects of growth regulators (PGR) and CO2 levels on dry matter, tuber yield, yield components of potato cultivars. A: leaf dry matter, B: stem dry matter, C: root dry matter, D, tuber dry matter, E: tuber yield, F: mean tuber weight G: tuber number. AC; ambient CO2-no PGR, AH; ambient CO2-BAP + ABA (50 µM, tuberization), EC; elevated CO2-no PGR, EH; elevated CO2- BAP + ABA (50 µM, tuberization). PGR; plant growth regulator (55 days after transplant). Columns are means of three replicates (n = 9). Vertical bars are ± SE

Elevated CO2 affected the DM partitioning pattern of the potato plants (Fig. 5). Elevated CO2 increased the above-media and belowground DM of the plants; generally, the roots and tubers gained more DM compared with the above-media parts of the plants. While above-media DM increased by 32 and 38%, belowground DM increased by 71 and 40% in Agria and Fontane, respectively, at the elevated CO2. Foliar application of BAP + ABA also increased DM partitioning toward stems, roots, and tubers. For instance, BAP + ABA significantly decreased DM accumulation in Agria leaves compared with the untreated plants at the ambient CO2. The greatest tuber and root DM were observed in BAP + ABA-treated and untreated Fontane plants, respectively, at the elevated CO2, while the lowest TDM was observed in untreated Agria plants at the ambient CO2.

Fig. 5.

Fig. 5

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Effect of elevated CO2 and BAP + ABA on dry matter partitioning of potato cultivars. Ambient CO2; 400 µmol mol−1, Elevated CO2; 800 µmol mol−1, Control; untreated plants, PGR; BAP + ABA-treated plants (50 µM, tuberization, 55 days after transplant). Columns with the same letters are not significantly different at P < 0.05, according to the Tukey test

The tuber yield per plant (TY) was affected by the CO2 levels, cultivar, and BAP + ABA (Table 3). Fontane TY was 22% greater than Agria. Foliar application of BAP + ABA increased Agria and Fontane TY by 48 and 14%, respectively, compared with the untreated plants (Fig. 4). Tuber yield was also increased by 70 and 61%, respectively, in Agria and Fontane at the elevated compared with the ambient CO2. Tuber yield per plant was more affected by the foliar application of BAP + ABA at the ambient compared with the elevated CO2. Mean tuber weight (MTW) was affected by CO2 levels and cultivar. Fontane MTW was greater by 40% compared with that of Agria. Mean tuber weight enhanced by 48 and 36% in Agria and Fontane, respectively, at elevated compared with the ambient CO2. Percent distribution of tubers was also affected by experimental factors (Table 3). Generally, hormonal treatment and elevated CO2 increased the medium- and large-size tubers. Elevated CO2 increased the percent distribution of large-size tubers by 54 and 59% in Agria and Fontane, respectively, compared with the ambient CO2. BAP + ABA also enhanced the medium-size tubers by 32 and 18% in Agria and Fontane, respectively, compared with the untreated plants (Fig. 6).

Fig. 6.

Fig. 6

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Effect of elevated CO2 and BAP + ABA on the percentage distribution of tubers produced per size category in potato cultivars. Ambient CO2; 400 µmol mol−1, Elevated CO2; 800 µmol mol−1, Control; untreated plants, PGR; BAP + ABA-treated plants (50 µM, tuberization, 55 days after transplant). Size category (mm). The vertical bar shows the parameter's mean ± SE. n = 9

Discussion

The photosynthesis of C3 plants is limited under the present atmospheric CO2 concentration. Carbon dioxide enrichment enhances the photosynthetic rate and stimulates crop growth and productivity (Reddy et al. 2010; Fleisher et al. 2014). Plant growth regulators are widely used to improve the physiological processes in plants (Aksenova et al. 2012). It has been reported that the application of BAP and ABA improved photosynthesis and increased leaf chlorophyll content of potato (Solanum tuberosum L.) and soybean (Glycine max) plants (Caldiz et al. 1998; Reinoso et al. 2011). While BAP + ABA-treated plants showed a lower Tr at the ambient CO2, the foliar application of BAP + ABA stimulated Tr at the elevated CO2. A similar behavior was also observed in the leaf gs. It seems Tr was not decreased by the hormonal treatment under elevated CO2; however, BAP + ABA tended to diminish the subtractive effects of the higher CO2 concentration on gs and Tr. Pospíšilová (2003) observed that stomatal conductance could be inhibited by higher concentrations of BAP, although the effects depend on the CK type, concentration, and method of application. Furthermore, the inhibitory effect of ABA on stomatal aperture has already been reported (Davies et al. 2005). Reinoso et al. (2011) observed that ABA application decreased gs in soybean (Glycine max) plants.

Stomatal conductance has been reported to be suppressed at higher CO2 concentrations (Ainsworth and Rogers 2007). According to the results of Vandermeiren et al. (2002), we also found that potato (Solanum tuberosum L.) plants grown at elevated CO2 had lower gs and higher Ci. Generally, the photosynthetic rate is regulated by both stomatal and non-stomatal factors. In this experiment, the higher Np was accompanied by a higher Ci, which indicates that the photosynthesis was mainly controlled by the stomatal factors. At the elevated CO2, while Ci:Ca tended to decrease in Agria, it was increased in Fontane. The decreased Ci:Ca in Agria indicated the role of the stomatal factor in photosynthetic regulation. It has already been reported that elevated CO2 decreased Ci:Ca (Long et al. 2004). However, no changes (Bunce 2001) and an increase (Kaminski et al. 2014) in Ci:Ca have also been reported in potato (Solanum tuberosum L.) plants at elevated CO2. Bunce (2001) believed that a higher Ci:Ca at prolonged elevated CO2 probably indicates the photosynthetic acclimation to such conditions.

Agria Rd was increased by the foliar application of BAP + ABA at the elevated CO2. It has been observed that leaf Rd was stimulated at elevated CO2, indicating a higher demand for maintenance due to the accelerated senescence (Donnelly et al. 2001; Vandermeiren et al. 2002). A simultaneous increase in the leaf Rd and SC and ST content was observed in our experiment. An increase in the leaf SC content and Rd was also reported in tomato (Solanum lycopersicum), and potato (Solanum tuberosum L.) plants grown under elevated CO2 (Li et al. 2013). They concluded that greater availability of carbohydrates and energy demand resulted in a higher leaf dark respiration rate at elevated CO2. The higher accumulation of carbohydrates due to higher photosynthesis might be due to the greater availability of substrate for stimulating the respiratory pathway (Aranjuelo et al. 2011).

Elevated CO2 accelerates the senescence process in plants, mainly due to the accumulation of starch granules in chloroplasts and lower stomatal conductance that increase the leaf temperature. The trend of leaf Chl content changes of the cultivars was different. Agria senescence started sooner than Fontane at the elevated CO2, which could be observed through a slight decrease in the leaf Chl content of Agria exposed to the elevated CO2. It might be due to the greater accumulation of SC and ST content in Agria leaves. Furthermore, Fontane TY was greater than Agria regardless of lower Np, which might indicate that Fontane translocated the photoassimilates more efficiently than Agria from the leaves to the tubers, which has been proved by a lower leaf SC content of Fontane. Therefore, the higher accumulated carbohydrates in Agria leaves tended to more rapid senescence onset compared with Fontane. On the other hand, it might also indicate that Fontane was more affected by ABA, as a stimulator of dry matter remobilization, compared with Agria.

Leaf carotenoid content decreased when BAP + ABA was applied, or CO2 was enriched. Carotenoids, as the auxiliary pigments, protect the photosynthetic apparatus from the extra sunlight energy through the nonphotochemical quenching (NPQ) process (Taiz and Zeiger 2006). Foyer and Shigeoka (2011) found that a lower CO2 concentration led to an increase in the reactive oxygen species (ROS), under which the carotenoids may protect the photosynthetic apparatus against the ROS damages. In the present study, the lower carotenoid content of leaves might probably be due to the role of elevated CO2 in decreasing ROS production. The slightly higher leaf Chl content due to the BAP + ABA application might also decrease the demand for a greater carotenoid content.

The availability of physiological sinks is a critical factor in enhancing the photosynthesis of C3 plants (Chen and Setter 2012). The elevated CO2 enhanced MTW of the plants. Finnan et al. (2005) observed that the higher levels of CO2 stimulate the tuberization of potato plants and increase the physiological sink strength to store higher photoassimilates, leading to reduce inhibition feedback of starch accumulation on photosynthesis. Aranjuelo et al. (2011) believed that an increase in soluble sugar accumulation indicates an impairment in the sink strength. It has been reported that the allocation of photoassimilates is regulated by the plant hormones, environmental conditions, and developmental stage (Geiger and Servaites 1991). BAP and ABA, by stimulating the photosynthesis and mobilization of photoassimilates to economic organs, provoke the tuberization process (Ewing and Struik 2010; Aksenova et al. 2012). Sansberro et al. (2004) observed that the DM accumulation enhanced when ABA was foliar sprayed on Ilex paraguariensis. Fischer et al. (2008) believed that a higher accumulation of carbohydrates could be due to a higher photosynthetic rate of PGR-treated potato (Solanum tuberosum L.) plants. The enhancement of the TY in our experiment might be due to the positive effects of the elevated CO2 and BAP + ABA on leaf Np and Rd, leading to higher carbohydrate production. Carbohydrates play vital roles in tuber growth and starch biosynthesis and are known as the tuber initiation stimulator (Ramawat and Merillon 2013). Kloosterman et al. (2005) stated that higher soluble carbohydrate activate many genes involved in starch biosynthesis, leading to an increase in the tuber DM accumulation capacity.

Various studies have shown that DM allocation was increased more to belowground organs than to shoots at elevated CO2 levels (Fleisher et al. 2008; Högy and Fangmeier 2009). Agria LDM and TDM comprised 33 and 18%, respectively, of the total biomass of untreated plants at the ambient CO2, while it altered to 23 and 26%, respectively, when BAP + ABA and elevated CO2 were applied. It indicated that the elevated CO2 and hormonal treatment altered DM allocation toward the plant's belowground organs. The tuber classification results also showed that the proportion of large- and medium-size tubers increased at elevated compared with the ambient CO2. Högy and Fangmeier (2009) also reported that the size of tubers increased at elevated CO2. They concluded that the stimulation of potato tuber yield was mainly due to an increase in the tuber weight compared to the tuber number.

Conclusion

Our results showed that the elevated CO2 and BAP + ABA foliar application at the tuberization stage affected physiobiochemical traits, tuber yield, and source-sink relationship in two potato cultivars. The lower Tr and higher Ci were coupled with a moderate decrease in gs at the elevated CO2. Agria Ci:Ca was declined at the elevated CO2, indicating that the stomata may become more conservative under the higher CO2 concentrations. On the other hand, the increase in Fontane Ci:Ca showed a stomatal acclimation to the elevated CO2. Elevated CO2 and BAP + ABA shifted DM partitioning to belowground organs; lower DM was allocated to the leaves compared with the roots and tubers. Manipulating the plant's ability to benefit from the higher photoassimilates, alleviates the negative effects of photosynthetic acclimation and increases the productivity of plants at elevated CO2. Our results showed that the application of BAP + ABA with doubling the CO2 level could positively increase MTW and TY in potato minituber production. The greater tuber yield of Fontane might indicate the role of a greater leaf number (data not shown), as the photosynthetic area, than photosynthesis per leaf area unit, and a more efficient photoassimilates translocation. The variations between the cultivars might help to identify those cultivars which are better adapted to elevated CO2 and to improve the productivity of plants to meet the food demand and security in the future climate change.

Abbreviations

CO2

Carbon dioxide

PGR

Plant growth regulator

BAP

6-Benzylaminopurine

ABA

Abscisic acid

Ci/Ca

The ratio of leaf intercellular to ambient air CO2 concentrations

SC

Soluble carbohydrate content

ST

Starch content

CK

Cytokinins

GA

Gibberellic acid

Chla

Chlorophyll a

Chlb

Chlorophyll b

Chl a + b

Total chlorophyll

Chl a:B

Chlorophyll a/b ratio

Car

Carotenoids

Np

Net photosynthetic rate

Rd

Dark respiration

gs

Stomatal conductance

Tr

Transpiration rate

Ci

Intercellular CO2

Φ

Quantum yield of photosystem II

LDM

Leaf dry matter

SDW

Stem dry matter

RDM

Root dry matter

TDM

Tuber dry matter

Y

Tuber yield

MTW

Mean tuber weight

TN

Tuber number

Footnotes

Publisher's Note

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