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Article

The Impact of Greenhouse and Field Growth Conditions on Chenopodium quinoa Willd Accessions’ Response to Salt Stress: A Comparative Approach

by
Narmine Slimani
1,
Soumaya Arraouadi
2,3,*,
Hafedh Hajlaoui
4,5,
Mohamed Ali Borgi
1,
Nour El Houda Boughattas
6,
Vincenzo De Feo
7,* and
Mejdi Snoussi
8,9
1
Laboratory of Biotechnology and Bio-Monitoring of the Environment and Oasis Ecosystems, Department of Life Sciences, Faculty of Sciences of Gafsa, Sidi Ahmed Zarroug University Campus, Gafsa 2112, Tunisia
2
Regional Center of Agricultural Research (CRRA) Sidi Bouzid, Gafsa Road Km 5, PB 357, Sidi Bouzid 9100, Tunisia
3
Laboratory of Valorization of Unconventional Waters, INRGREF, University of Carthage, Road Hedi El Karray, El Menzah IV, PB 10, Ariana 2080, Tunisia
4
Faculty of Sciences and Technology of Sidi Bouzid, University of Kairouan, Campus University Agricultural City, Sidi Bouzid 9100, Tunisia
5
Laboratory of Plant-Soil-Environment Interactions, LR21ES01, Faculty of Sciences of Tunis, University of Tunis EL Manar, Tunis 2092, Tunisia
6
Higher Institute of Agronomy of Chott-Mariem, University of Sousse, P.B 47 Chott Mériem, Sousse 4042, Tunisia
7
Department of Pharmacy, University of Salerno, Via Giovanni Paolo II 132, 84084 Fisciano, Italy
8
Department of Biology, College of Science, Hail University, P.O. Box 2440, Ha’il 2440, Saudi Arabia
9
Laboratory of Genetics, Biodiversity and Valorization of Bio-Resources (LR11ES41), Higher Institute of Biotechnology of Monastir, University of Monastir, Avenue Tahar Haddad, BP74, Monastir 5000, Tunisia
*
Authors to whom correspondence should be addressed.
Agronomy 2023, 13(9), 2303; https://doi.org/10.3390/agronomy13092303
Submission received: 29 July 2023 / Revised: 14 August 2023 / Accepted: 28 August 2023 / Published: 31 August 2023
(This article belongs to the Special Issue Adaptation of Crops to the Environment under Climate Change: Physiological and Agronomic Strategies — Volume II)
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Abstract

:
Quinoa’s exceptional capacity to tolerate high salt levels presents a promising solution to the agricultural challenges posed by salt stress. This study aimed to explore salt stress effects on three quinoa accessions (18 GR, R-132, and DE-1) and to compare the influence of greenhouse and field growing conditions on their salinity tolerance. The plants were irrigated by 50, 100, 150, and 200 mM NaCl concentrations. The results showed that quinoa plants’ response to morphological, physiological, biochemical, and enzymatic parameters was influenced by NaCl concentration, accession, growing conditions, and their interactions. As salinity irrigation increased, aerial part length and leaf area decreased significantly (p < 0.05) for all studied accessions, correlating with plant photosynthetic parameters. Greenhouse conditions promote faster and more vigorous growth with a larger leaf area compared to field cultivation. Furthermore, at 200 mM concentration, the DE-1 accession displayed greater photosynthetic activity, recording values of 195.66 ± 3.56 and 120 ± 1.13 µmol·m−2·s−1 for greenhouse and open field conditions, respectively. NaCl stimulated MDA and H2O2 in both conditions for all accessions, and the DE-1 accession displayed the lowest levels. Proteins, sugars, proline, peroxidase, ascorbate peroxidase, and catalase were stimulated by salt stress, except in the R-132 accession. Field cultivation resulted in a more severe salinity response. Greenhouse conditions may enhance quinoa’s salt tolerance due to the less demanding growth conditions. DE-1 exhibited the highest salt tolerance, while R-132 showed the lowest. This study sets the stage for further research into the genetic basis of salt tolerance in various quinoa accessions, optimizing growth in salty regions through farming practices, and confirming the obtained results in real-world conditions for sustainable agriculture.

1. Introduction

Currently, there is growing global concern about soil salinity, as it significantly affects more than 20% of irrigated land and 6% of total land areas [1]. These percentages are continually increasing, primarily due to climate change, which is projected to exacerbate the problem further. Moreover, [2] estimated that the human population is expected to reach 9 billion by 2050. The combination of a rising global population and the issue of soil salinity poses substantial challenges to achieving achieve food security and sustainable agriculture. The increasing demand for food, driven by population growth, calls for higher agricultural production. In response to these limitations, scientists and researchers have proposed the use of resistant crops to combat abiotic stressors, especially salinity, to address these pressing concerns [3,4]. Among the examples cited, Chenopodium quinoa (family: Amaranthaceae) has shown the most promising potential.
Quinoa, a significant pseudo-cereal, is renowned for its ability to withstand environmental stress and its high nutritional content, making it a widely advocated cultivar for human consumption and nutrition [5]. Native to South America’s Andean mountains, quinoa exhibits a wide range of biological diversity, as highlighted by Abd El-Hakim et al. [6]. Notably, quinoa is considered a complete food with attractive nutritional value, boasting a high level of high-quality protein that surpasses rice and wheat [7]. Recognized by the Food and Agriculture Organization (FAO), the quinoa grain stands out as a plant-based food that provides all essential amino acids, fulfilling dietary requirements for human nutrition [8]
Soil salt is one of the primary abiotic stresses that plants encounter, especially in arid and semiarid environments. The ability to withstand high salt levels is a crucial agronomic trait, essential for sustaining and preserving food production [9]. Quinoa has been identified as a facultative halophyte crop, demonstrating higher salt tolerance than barley, wheat, and maize, with considerable variations in salt tolerance among quinoa accessions [10,11]. Generally, quinoa can tolerate moderate to high salt levels, even up to 750 mM NaCl [12]. Osmotic stress resulting from high salt concentrations triggers the production of abscisic acid (ABA) in roots, which then serves as a signal to regulate stomatal conductance. Stomatal closure reduces CO2 absorption and minimizes water loss, consequently inhibiting photosynthesis [13]. Quinoa possesses several defenses against high salt concentrations, including enhanced tolerance to reactive oxygen species (ROS), effective regulation of Na+ storage in leaf vacuoles, and efficient xylem Na+ loading [14]. The accumulation of appropriate solutes, such as proline and total phenolics, is also associated with salt tolerance in quinoa [15]. Moreover, antioxidant enzyme activities in quinoa were shown to be influenced by the extent of salinity. For instance, Panuccio et al. [16] found that the type and amount of salt affected the regulation of antioxidant enzymes in quinoa seedlings of the “Titicaca” accessions.
There have been limited studies investigating the adaptive responses of quinoa cultivated under salt stress conditions in both greenhouse and field environments. So, to gain deeper insights into how quinoa responds to salt stress at the morphological, physiological, and biochemical levels, a comparative study was conducted using three different accessions cultivated both in greenhouses and open fields. Greenhouse and field growing conditions represent two contrasting environments used for plant cultivation, each serving specific purposes. Greenhouses offer controlled and protected environments, ensuring precise conditions for optimal plant growth. On the other hand, field conditions provide a more natural setting with exposure to climate variations, which can present both challenges and opportunities for specific crop varieties and regional adaptations.

2. Materials and Methods

2.1. Materials

Experiments were conducted on three quinoa accessions, as mentioned in Table 1.

2.2. Methods

The experimental trials were conducted at two distinct sites, one situated in a plot at the CRRA (Regional Center for Agronomic Research) in Sidi Bouzid (latitude: 35.02711, longitude: 9.49184), and the other within a greenhouse, situated in the same place, with soil attributes detailed in Table 2. The plants were arranged according to the plot layout illustrated in Figure 1.
The experimental climatic conditions are presented in Table 3. We adopted a systematic method where each treatment is separate and linked to an individual reservoir, allowing a controlled supply of water and necessary additives. This approach guarantees the precise fulfillment of each treatment’s specific needs, reducing the risk of cross-contamination and maintaining the reliability of experimental outcomes (Figure 1).
In both greenhouse and open field conditions, deep plowing of the soil was undertaken to establish an optimal soil structure for the growth phases to come. Next, a meticulously designed seedbed was established to create the perfect setting for the quinoa seeds to grow. The seeds were planted in rows, with a spacing of 30 cm between seedlings within the same row and a gap of 1 m between adjacent rows. From the initial phases of seed germination to the branching stage, the quinoa seedlings were watered with borehole water containing approximately 50 mM NaCl, which was considered the control treatment. From this stage (45 days from seedling) to the flowering stage, plants were irrigated weekly, with salty solutions of 50, 100, 150, and 200 mM of NaCl.
In addition to the meticulous management of irrigation, regular hoeing activities were carried out. These actions involved the mechanical removal of unwanted weeds that could potentially compete with quinoa plants for vital nutrients, water, and sunlight. By striving to maintain a weed-free environment, the experiment cultivated an environment where quinoa plants could thrive without unnecessary competition. In both greenhouse and field conditions, various parameters (detailed in the measured parameters section) were assessed during the flowering stage to evaluate the impact of salt stress on the plants’ performances.

2.3. Measured Parameters

2.3.1. Plant Morphological Attributes

Two morphological traits were recorded, such as plant height and leaf area (cm).

2.3.2. Plant Physiological Attributes

-
Photosynthetic parameters: In clear weather between 09:00 and 11:00 local time, photosynthetic activity, stomatal conductance, and evapotranspiration of fully-grown leaves were measured by using a CI.340 photosynthesis device. Measurements were acquired from the fourth leaf starting from the top of the principal axis of the plant for all the studied accessions.
-
Dry matter and water content: At the flowering stage, plants were harvested, and the aerial part was weighed after desiccation at 75 °C for 72 h to determine the dry matter.

2.3.3. Plant Biochemical Attributes

Soluble sugar, proline, and soluble protein levels were assessed using the methods outlined in references [17,18,19], respectively. The hydrogen peroxide (H2O2) concentration was measured following the procedure detailed by [20], while lipid peroxidation was determined using the approach described by [21].

2.3.4. Plant Enzymatic Activities

A weight of 250 mg of leaves was homogenized in 0.1 M phosphate buffer (pH 7.0), and the mixture was centrifuged at 15,000× g for 30 min at 4 °C. After centrifugation, the supernatant was collected to determine antioxidant enzyme activities.
-
Catalase activity was determined as described by [22]. For this determination, 200 μL of enzyme extract was mixed with 50 mM phosphate buffer (pH 7.0) and 15 mM H2O2. Absorbance was recorded at 240 nm for 45 s.
-
Peroxidase (POD) activity was measured by the method described in [23]. An amount of 200 μL of plant extract was mixed with 50 mM phosphate buffer (pH 6), 15 mM H2O2, and 12 mM guaiacol. Absorbance was recorded at 470 nm for 90 s.
-
Ascorbate peroxidase activity was assayed according to the method described in [24]. Amounts of 50 mM potassium phosphate (pH 7.0) and hydrogen peroxide, and 0.5 mM ascorbic acid were added to 1 mL of extract. At 290 nm, absorbance was recorded for 90 s.

2.4. Statistical Analysis

All data were subjected to one-way variance analysis using SPSS 26.0 software (IBM; (Paris (GMT + 1, France)) and differences between means were compared by Duncan tests (p < 0.05). Averages followed by the same letters are not significantly different at p < 0.05.

3. Results

3.1. Plant Morphological Parameters

In general, as irrigation salinity levels increased, the areal part length and leaf area decreased significantly for all studied accessions. These findings suggest that the inhibitory effect of salt stress is evident in both growing conditions. However, the quinoa plant’s response to salt stress depends on several factors, including accessions, treatment, growing conditions, and their interaction (Table 3). Indeed, the inhibition percentages of areal part length for 18 GR, R-132, and DE-1 cultured under greenhouse conditions were −22%, −53%, and −11%, respectively, under 100 mM NaCl treatment; −42%, −59%, and −26% under 150 mM; and −54%, −63%, and −32% under 200 mM. However, when these accessions 18 GR, R-132, and DE-1 were grown in the open field, the inhibition percentages were −40%, −79%, and −31%, respectively, under 100 mM treatment; −50%, −86%, and −44% under 150 mM treatment; and −83%, −89%, and −50% under 200 mM treatment (Figure 2). In a similar manner, the leaf areas of 18 GR, R-132, and DE-1 experienced substantial reductions of −73%, −72%, and −50%, respectively, when subjected to 200 mM treatment under field conditions. Under the same treatment but in greenhouse conditions, these reductions were smaller but still noteworthy, measuring −44%, −59%, and −37% for the respective accessions. These results strongly suggested that plants cultivated in greenhouse conditions exhibited more vigorous growth, compared to their counterparts in the field. This discrepancy was also evident in the observed differences in leaf area, with greenhouse-grown plants demonstrating larger leaf areas than those grown in the field. Furthermore, in terms of accession response to salinity, DE-1 exhibited higher resistivity compared to the other two accessions (18 GR and R-132). This finding highlights the variability in salt stress tolerance among different quinoa accessions, making DE-1 more resistant to the adverse effects of salinity compared to the other tested accessions (Figure 2).

3.2. Plant Physiological Attributes

The study of salt stress effect on dry matter and water content is presented in Figure 3. It becomes evident that there is a gradual decrease in dry matter and water content with increasing treatment levels in both conditions. In greenhouse conditions and at the highest treatment level (200 mM), the R-132 accession showed a dry matter inhibition of up to 47% and water content inhibition of 32%. For the 18 GR accession, dry matter inhibition reached 40%, while water content inhibition was 23%. However, the DE-1 accession exhibited a less pronounced inhibition, with maximum reductions of 38% for dry matter and 22% for water content. Similarly, under field conditions, the DE-1 accession consistently displayed higher dry matter and water content values compared to the other accessions. These results indicate that these quinoa accessions exhibit distinct responses to the applied treatments, implying differences in their stress tolerance and adaptability to changing environmental conditions.

3.3. Photosynthetic Parameters

This study conducted an analysis of the impacts of salinity level, accession, and growing conditions on various photosynthetic parameters such as chlorophyll content, net photosynthesis rate, transpiration rate, and stomatal conductance. The results showed a significant influence of these factors and their interactions on photosynthetic attributes. Additionally, statistical analysis revealed that salt stress negatively and significantly affected all photosynthetic parameters compared to the control (50 mM). The study also found that plant sensitivity increased in field conditions, and the DE-1 accession exhibited the highest values and the lowest percentage of inhibitions in the two conditions. On the other hand, the R-132 accession showed more pronounced inhibitions (Table 4). For the DE-1 accession, chlorophyll content, net photosynthesis rate, transpiration rate, and stomatal conductance gradually decreased by approximately −17%, −6%, −22%, and −7%, respectively, under 200 mM treatment in greenhouse conditions. Under field conditions, the reductions were more substantial, reaching −29%, −21%, −34%, and −15%, respectively. These values were significantly higher for the R-132 accession, providing clear evidence for its exceedingly high sensitivity compared to the other accessions. These findings demonstrate the complex interplay between salt stress, accession, and growing conditions in the photosynthetic performance of quinoa plants.

3.4. Biochemical Study

Analysis of obtained effects showed that osmolyte contents (soluble sugar, proline, and protein) were highly influenced by salinity level, accessions, and growing conditions effect as well as their interactions (Table 3). Moreover, under greenhouse conditions, all these contents were stimulated significantly in a NaCl-concentration-dependent manner, except for the R-132 accession, which showed completely different behavior marked by a significant and progressive decrease in these osmolyte contents. For this accession, proline, sugar, and protein contents were inhibited to reach progressively −86%, −24%, and −12% under 200 mM. By contrast, the DE-1 accession accumulated the highest osmolyte concentrations (Figure 4A).
Elsewhere, the soluble sugar, proline, and protein contents of field-grown quinoa plants displayed significant fluctuations. Despite these variations, a statistical analysis suggested that the DE-1 accession had a notable capacity to accumulate higher levels of osmolytes, enabling it to better cope with salt stress. By contrast, the R-132 accession exhibited the lowest osmolyte levels and the highest percentage of inhibition, indicating its heightened susceptibility to salt stress (Figure 4B).
An assessment of oxidative stress induced by salinity was conducted by measuring malondialdehyde (MDA) and hydrogen peroxide (H2O2) levels in quinoa leaves. The results from the means comparison indicated a significant increase in MDA and H2O2 accumulation in response to higher salinity levels in water irrigation. Notably, this accumulation was more pronounced in the field-grown plants (Figure 5).
Moreover, this study identified distinct variations among the different quinoa accessions in terms of their response to salinity-induced oxidative stress. Based on statistical analysis, the accessions were classified into three distinct groups. The DE-1 accession displayed the lowest levels of MDA and H2O2, along with the lowest stimulation percentages, indicating its greater ability to mitigate the impact of salinity-induced oxidative stress. On the other hand, the R-132 accession exhibited the highest averages for MDA and H2O2 contents, resulting in the highest stimulation percentages compared to the control under both growing conditions.
Under field conditions, the stimulation percentages of MDA contents for 18 GR, R-132, and DE-1 were observed as follows: 83%, 450%, and 19% under 100 mM treatment; −29%, 261%, and 55% under 150 mM treatment; and 86%, 174%, and 250% under 200 mM treatment. However, when the same accessions were grown in a greenhouse, the stimulation percentages were as follows: 76%, 118%, and 51% under 100 mM treatment; 107%, 171%, and 0.3% under 150 mM treatment; and 130%, 210%, and 51% under 200 mM treatment for 18 GR, R-132, and DE-1, respectively.
Meanwhile, for H2O2 contents, the stimulation percentages for 18 GR, R-132, and DE-1 grown in field conditions were 154%, 45%, and 50%, respectively, under 100mM treatment; 195%, 293%, and 141% under 150 mM; and 64%, 422%, and −63% under 200 mM. However, under greenhouse conditions, the stimulation percentages were 61%, 98%, and 22% under 100 mM treatment; 212%, 16%, and 80% under 150 mM treatment; and 147%, 388%, and 125% under 200 mM treatment for the 18 GR, R-132, and DE-1 accessions, respectively.

3.5. Enzymatic Study

This study investigated the activities of antioxidant enzymes, such as peroxidase, ascorbate peroxidase, and catalase, to assess the manner by which the studied quinoa accessions coped with oxidative stress induced by salinity. Following a statistical analysis of these enzyme activities, the data revealed three distinct groups based on their levels, with the DE-1 accession exhibiting the highest activities and the R-132 accession displaying the lowest. Furthermore, the enzyme activities were significantly increased under 100, 150, and 200 mM salinity compared to the control groups, except for the R-132 accession, which exhibited significant inhibition under the aforementioned treatments (Figure 6). Interestingly, the study also concluded that the enzymatic response of the accessions to salinity was more pronounced under greenhouse conditions compared to those grown in the field. In fact, the DE-1 accession exhibited a superior potential to overcome oxidative stress caused by salinity to the R-132 accession. Moreover, the profound influence of environmental conditions on determining the enzymatic response of accessions to salinity-induced oxidative stress was observed. This acknowledgment is valuable for understanding the mechanisms behind the salinity tolerance of quinoa plants and could be used to develop strategies for enhancing their stress resistance in diverse agricultural settings.

4. Discussion

To fulfill the rising need for nourishing food caused by the expanding global human population, researchers are focusing on developing adaptive crops. Emphasis is placed on growing crops in marginal locations, where agricultural production is low due to harsh environmental factors such as high soil salinity, low fertility, and poor quality of water irrigation. Quinoa, which resists soil salinity and low water availability and provides significant nutritional value, has become a promising alternative. The purpose of this study was to compare the behavior of three quinoa accessions (18 GR, R-132, and DE-1) under various NaCl concentrations (50, 100, 150, and 200 mM) and to evaluate the effect of greenhouse and open field conditions on quinoa response.
Variance analysis revealed that the variations in responses to salt stress may be attributed to the impacts of accessions, treatments, cultural conditions, and their interactions (Table 5). The significance levels correspond to the statistical significance of these factors on the observed traits. Notably, the accession factor exerted the most substantial influence. The condition factor showed a greater impact on leaf area (56.44%). Furthermore, the growth conditions significantly influenced H2O2 content (43.67%), as well as the activities of ascorbate peroxidase (32.97%) and peroxidase (58.23%). This outcome can be rationalized by the pivotal roles of ascorbate peroxidase and peroxidase as essential components of cellular defense mechanisms against oxidative stress. These enzymes aid in preserving cellular integrity and functionality in the presence of reactive oxygen species, particularly hydrogen peroxide, which can inflict cellular damage. Interestingly, catalase, responsible for converting hydrogen peroxide into water and oxygen, exhibited greater susceptibility to the accession factor (64.22%). Conversely, photosynthetic activity seemed equally influenced by both the accession (45.40%) and condition (45.23%) factors.
Salinity stress led to a significant decline in plant dry matter production, length of plants, and leaf area in both growth conditions. This drop might be ascribed to the reduction in water absorption and metabolic activity, or to the toxicity caused by excess toxic ions which results in a nutritional deficiency [25,26]. Additionally, [27,28] attributed plant length and leaf area decreases to the reduction in cell division and expansion provoked by salinity. The observed results are comparable with findings that showed that salinity reduced the plant height, leaf number, leaf area, and dry weight of barley plants [29].
Photosynthetic parameters and statistical analysis indicated that the gradual increase in salinity levels in water irrigation progressively inhibited chlorophyll synthesis in all tested quinoa accessions under both growing conditions. A similar outcome has been documented by other research on quinoa exposed to salt stress [30,31]. According to [32], this decrease could be explained by the overproduction of reactive oxygen species in plants under high NaCl levels, which causes chlorophyll structure breakdown. This hypothesis is in line with our results where we found a negative and significant correlation between chlorophyll and MDA and H2O2 contents (r = −0.8; p < 0.01). Munns et al. [33] suggested that the reduction in chlorophyll concentration was due to metabolic limits of photosynthesis in leaves at higher salinity levels. In another study, the authors suggested that the low chlorophyll content was linked to enzymatic chlorophyll degradation caused by increased salt stress [34].
The correlation analysis revealed a significant and positive relationship between chlorophyll content and photosynthetic activity (r = 0.9; p < 0.01), stomatal conductance (r = 0.8; p < 0.01), and transpiration (r = 0.9; p < 0.01) in both conditions. As the intensity of salt stress increased, these parameters gradually decreased in all studied accessions. Similar observations were reported in previous studies on wheat subjected to salt and combined salt and drought stress by [35,36], respectively. The decline in photosynthetic activity could be the result of the degradation that occurred when plants were stressed, leading to the transfer of nutrients such as magnesium from older leaves to younger ones [36]. Additionally, the closure of stomata and the decrease in leaf conductance impede the diffusion of CO2 to the carboxylation site, resulting in a decline in photosynthetic uptake. As noted by [37], salinity induces the inhibition of CO2 diffusion, leading to reduced photosynthetic processes. Salinity stress directly interferes with stomatal opening, affecting gas exchange, and consequently influencing both photosynthesis and mesophyll metabolism [38,39]. In our ongoing study, irrespective of the growth conditions, the imposition of NaCl-induced stress caused a reduction in photosynthetic activity, stomatal conductance, and evapotranspiration. However, the salt-tolerant DE-1 accession exhibited higher levels compared to the salt-sensitive R-132. This highlights the capacity of the salt-tolerant variety (DE-1) to maintain elevated CO2 assimilation even under salt stress, thus preserving nearly normal photosynthetic rates. The decrease in CO2 assimilation during salt stress could potentially be linked to limitations in CO2 diffusion within the leaf, coupled with hindered ATP synthesis and Rubisco activity.
Under conditions of high salinity, plants produce specific organic molecules like sugars, proline, and protein compounds. These molecules are considered suitable osmolytes, which help plants adjust to osmotic stress caused by salinity [40,41]. The concentration of these osmolytes increases and accumulates in response to the severity of the stress [42]. The present study revealed that regardless of the growth conditions, the levels of proline significantly increased in the leaves of the 18 GR and DE-1 accessions when irrigated with salty water. This finding aligns with earlier research by [43,44] who also observed elevated proline levels in wheat and quinoa leaves subjected to NaCl stress, which provides further support to the importance of this compound as an osmoprotectant against salt stress.
As the concentration of NaCl in the irrigation water steadily increased, there was a notable rise in the sugar content of the 18 GR and DE-1 accessions. Our results support the findings of [45,46] who demonstrated that quinoa plants counteracted the negative effects of salt stress by accumulating osmolytes like soluble carbohydrates. Saddhe et al. [47] suggested that this overproduction of sugar serves multiple purposes, such as protecting protein structures, storing carbon, neutralizing reactive oxygen species (ROS), and adjusting the cellular osmotic balance. However, the R-132 accession exhibited a different response, with a lower level of sugar content. Similar results were reported by [48] who observed a reduced soluble sugar content in quinoa plants (Masr 1 variety) grown in salty soil. Various theories suggest that exposure to salt may force plants to expend more energy to remove excess Na+ or secrete it into vacuoles, leading to reduced carbohydrate accumulation [49]. Additionally, other studies have indicated that under salt stress, plants may store carbohydrates in organs other than their leaves; for instance, Meloni et al. [50] found that sugars were accumulated exclusively in the roots of Prosopis alba. Furthermore, when subjected to salt stress, the 18 GR and DE-1 accessions exhibited increased protein synthesis in their leaves, while the R-132 accession showed a significant reduction in protein levels. In this context, Aymen et al. [51] observed a decrease in total protein content in quinoa plants (Red Faro variety) under salt stress, where the lowest content was recorded at 300 mM NaCl.
The concentrations of these osmolytes (proline, sugars, and proteins) were found to be positively and significantly correlated with water content, both in greenhouse and field conditions (r = 0.9, p < 0.01 and r = 0.8, p < 0.01, respectively). Similar results were reported by [41,52], who proposed that these osmolytes play a crucial role in regulating water content in quinoa plants under salinity stress.
Salt stress is a complex phenomenon that leads to water scarcity due to osmotic reactions. As a result, ROS like superoxide, hydrogen peroxide, and hydroxyl radical (OH) are generated [42]. To understand the extent of damage and the oxidative state of plants, MDA and H2O2 concentrations were measured in quinoa leaves. For all three studied accessions, these contents increased significantly as the NaCl concentration in water irrigation rose. Similar research on quinoa by [53] demonstrated that salt stress causes substantial oxidative damage through MDA and H2O2 production.
To combat these ROS, plants employ their antioxidant defense systems, consisting of enzymatic and non-enzymatic molecules [54,55,56]. In this study, the enzyme activities were evaluated, showing that in the 18 GR and DE-1 accessions, the catalase, peroxidase, and ascorbate peroxidase activities increased under salt stress. These findings are supported by [57] who observed similar stimulatory effects of salt stress on antioxidant enzyme activities in sunflower cultivars.
According to [25], the increase in antioxidant enzyme activities can be interpreted as a signal of elevated ROS generation and activation of a defense mechanism to counteract oxidative damage caused by plant responses to stress. Research by [58] on tobacco plants showed that the overproduction of ascorbate peroxidase reduced the harm induced by H2O2. Similarly, an experiment carried out by [59] introduced ascorbate and peroxidase enzymes (OsAPXa and OsAPXb) into Arabidopsis plants and demonstrated that both enzymes are crucial for defending against salt stress by maintaining proper H2O2 levels. The authors of [60] studied the effects of genes associated with ascorbate peroxidase production in transgenic plum trees and found that enhanced ascorbate peroxidase activity was linked to high salt tolerance. By contrast, the R-132 accession exhibited a significant reduction in these antioxidant enzyme activities. Similar findings reported by [61] showed that salt-stressed wheat cultivars had lower ascorbate peroxidase activity. The authors of [62] also found reduced catalase activity in alfalfa plants exposed to high NaCl concentrations, likely due to extremely high ROS levels induced by stress.
This inhibition could be explained by the extremely high ROS levels found in stressed plants [63]. H2O2 and MDA overproduction under salt stress was explained by the inability of these plants to overcome the water stress caused by the osmotic stress produced by the excess of Na+ and Cl− ions [64]. So, the development of additional ROS is encouraged by this water stress. Therefore, strong dehydration of plant cells stimulates more ROS overproduction and renders them unable to synthesize certain proteins, such as enzymes like catalase and ascorbate peroxidase. This hypothesis could explain the drop in these antioxidant activities in the R-132 accession.
In brief, the response to oxidative stress is regulated by the concentration of ROS produced, which is influenced by the water status of the plants. In fact, a high dose of ROS can induce cell death in some varieties, while a low dose allows for the establishment of antioxidant enzymes necessary to neutralize free radicals.
The results suggest that quinoa may handle salt stress more effectively when grown in greenhouse conditions compared to field conditions. The increased sensitivity of quinoa to salinity in the field could be explained by the additional stressors the plant faces in this environment.
One significant factor contributing to the higher stress levels in the field is the increased competition that quinoa encounters from other plants, primarily weeds. Although efforts are made to minimize the effects of competition through manual weeding, it remains challenging to eliminate all unwanted plants. Weeds and other vegetation in the field can compete with quinoa for essential resources such as water, nutrients, and light [65]. This intensified competition can weaken the quinoa plants, making them more vulnerable to environmental stressors like salinity. Moreover, the environmental conditions in the field are generally more unpredictable and harder to control, compared to greenhouse experiments. Variations in temperature, humidity, and sunlight can significantly affect quinoa’s ability to tolerate salinity. For instance, the combination of high temperatures with high salinity can increase the plant’s susceptibility to stress [66]. Additionally, other stressors, such as diseases, pests, and aerial herbivores, present in the field can interact with salinity to exacerbate the negative effects on quinoa’s growth and yield [67].

5. Conclusions

This study highlights the importance of understanding the effects of salt stress on quinoa plants and how different growing conditions impact their tolerance to salinity. This study provides evidence that quinoa plants possess the ability to tolerate salt and can be cultivated in saline environments, which has potential implications for improving food safety. The findings from this study suggest that quinoa’s response to salt stress can differ significantly depending on the cultivation conditions. Greenhouse conditions appear to offer more controlled and less stressful environments, enabling quinoa to better cope with salinity. By contrast, the field environment, with its higher competition, variability, and potential interaction with other stressors, may render quinoa more vulnerable to the negative effects of salt stress. Furthermore, the study identified the DE-1 accession as the most tolerant to salinity, while the R-132 accession exhibited the lowest tolerance.
Overall, this study underscores the significance of comprehending the factors influencing plant responses to salt-induced stress. The findings offer valuable insights that may contribute to enhancing agricultural yield and food security in regions affected by soil salinity. The insights gained from this study provide a stepping stone for broader research initiatives aimed at addressing the complex interplay between environmental stressors and plant responses. Further investigations could delve into the molecular mechanisms underlying quinoa’s salt tolerance, unraveling the genetic pathways and key factors responsible for its resilience. Understanding these intricacies at a molecular level could pave the way for targeted breeding programs, accelerating the development of even more salt-tolerant quinoa varieties.

Author Contributions

Conceptualization, N.S., S.A., H.H., M.A.B. and M.S.; methodology, S.A., N.S. and H.H.; formal analysis, H.H., N.S. and S.A.; software, S.A. and N.S.; investigation, S.A., N.S., N.E.H.B. and H.H.; writing—original draft preparation, S.A., N.S., H.H. and M.A.B.; writing—review and editing, S.A., H.H., N.S., M.S. and M.A.B.; supervision, H.H. and S.A.; funding acquisition, V.D.F. and M.S.; project administration, S.A., H.H., M.A.B. and M.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research has been supported by the Regional Center of Agricultural Research (CRRA) Sidi Bouzid (IRESA), and Mixed Tunisian Moroccan Laboratory of Plant Physiology and Biotechnology and Climate Change (LR11ES09).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We gratefully acknowledge D. Brenner at USDA-NPGS, Iowa State University, for taxonomic suggestions and seed contribution.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 13 02303 g001
Figure 1. Tank connection system for precise NaCl treatment differentiation and controlled water in the open field and greenhouse conditions.
Figure 1. Tank connection system for precise NaCl treatment differentiation and controlled water in the open field and greenhouse conditions.
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Figure 2. NaCl effect on the areal part length and leaf area of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
Figure 2. NaCl effect on the areal part length and leaf area of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
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Figure 3. NaCl effect on dry matter and water content of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
Figure 3. NaCl effect on dry matter and water content of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
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Agronomy 13 02303 g004aAgronomy 13 02303 g004b
Figure 4. NaCl effect on the protein, proline, and sugar contents of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
Figure 4. NaCl effect on the protein, proline, and sugar contents of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
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Figure 5. NaCl effect on MDA and H2O2 contents of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
Figure 5. NaCl effect on MDA and H2O2 contents of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
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Agronomy 13 02303 g006aAgronomy 13 02303 g006b
Figure 6. NaCl effect on the catalase, ascorbate peroxidase, and peroxidase activities of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
Figure 6. NaCl effect on the catalase, ascorbate peroxidase, and peroxidase activities of quinoa accessions grown under greenhouse (A) and field conditions (B). Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test (indication is valid for all figures and tables).
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Table 1. Name, origin, and source of each of the three studied quinoa accessions.
Table 1. Name, origin, and source of each of the three studied quinoa accessions.
Name AccessionOrigin Source
18 GRAmes 13724EcuadorUSDA-NPGS
R-132PI 478418Potosi, BoliviaUSDA-NPGS
DE-1PI 674266New Mexico, USAUSDA-NPGS
USDA-NPGS, United States Department of Agriculture—North Central Regional Plant Introduction Station of the US National Plant Germplasm System.
Table 2. Pedological parameters of experimental soil.
Table 2. Pedological parameters of experimental soil.
Apparent density3.02 g/cm3
TextureSandy loam (clay = 6.66; loam = 15.66; sand = 77.68)
Electrical conductivity1.33 ms/cm
Salinity0.931 g/100 g soil
pH8.24
Total limestone (CaCO3)1.73%
Total carbon0.106%
Organic material0.18%
Potassium (K2O)280 ppm
Available phosphate (P2O5)15 ppm in the first 20 cm and 3.87 ppm in the rest.
Remark: Saturated paste is the method used to measure the conductivity of soil. The pH is measured using a pH meter with a conventional soil/solution ratio of (1/2.5) (m/v).
Table 3. Climatic data of the experimental area (Lat, long 35.02711,9.49184).
Table 3. Climatic data of the experimental area (Lat, long 35.02711,9.49184).
Year20202021
MonthSEPOCTNOVDECJANFEB
TS (°C)25.4918.7414.839.378.6311.45
RH (%)58.6259.8167.070.5664.1257.31
PREC (mm/day)2.240.960.90.890.00.0
ALLSKY_SFC_PAR (W/m2)93.6181.8754.9548.6753.769.56
TS: Earth skin temperature (°C); RH: relative humidity at 2 m (%); PREC: precipitation corrected (mm/day); ALLSKY_SFC_PAR: All Sky Surface Photosynthetically Active Radiation Total (W/m2). Data source “https://power.larc.nasa.gov/” (10 March 2021).
Table 4. NaCl effect on the photosynthetic parameters of quinoa accessions grown under greenhouse and field conditions. Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test.
Table 4. NaCl effect on the photosynthetic parameters of quinoa accessions grown under greenhouse and field conditions. Means comparison based on the Duncan test was calculated between accessions (capital letters) and between treatments (lowercase letters) (a, b, c, d; A, B, C). Averages followed by the same letters are not significantly different at p < 0.05 according to the Duncan test.
Greenhouse ConditionsField Conditions
Treatments (mM)18 GRR-132DE-118 GRR-132DE-1
Chlorophyll content (mole)5046 ± 1.95 aB37.66 ± 0.65 aC50.33 ± 1.72 aA26.6± 1.72 bB30 ± 1.13 bC43.66 ± 2.35 bA
10038.33 ± 0.65 bB34.33 ± 1.3 bC48.66 ± 0.65 bA21.33 ± 2.35 dC25.33 ± 0.65 cB45.33 ± 0.65 aA
15036.83 ± 0.86 cB29.66 ± 0.65 cC45 ± 1.13 cA31.66 ± 2.35 aC35.33 ± 2.35 aB39.66 ± cA
20035.33 ± 0.65 dB25.33 ± 0.65 dC41.33 ± 0.65 dA26.33 ± 2.35 cB20.66 ± 2.35 dC31 ± 1.13 dA
Photosynthetic activity
(μmol m −2 s−1)		50128.76 ± 3.41 aB96.2 ± 6.92 aC210.2 ± 1.71 aA101.1 ± 1.4 aB91.66 ± 0.6 aC153.66 ± 1.72 aA
100113.63 ± 12.77 bB85.93 ± 12.55 abC200.33 ± 0.34 bA82.63 ± 12.77 bB61.93 ± 12.55 bC144.66 ± 0.65 bA
150103.3 ± 7.72 cB75.9 ± 6.85 bC196.36 ± 5.82 bcA72.3 ± 7.72 cB44.9 ± 6.85 cC132.66 ± 2.34 cA
20075.83 ± 6.17 dB64.17 ± 4.19 cC195.66 ± 3.56 cA44.83 ± 6.17 dB33.17 ± 4.19 dC120 ± 1.13 dA
Evapotranspiration
(μmol m −2 s−1)		50514.46 ± 15.33 aB420.03 ± 7.93 aC699.16 ± 3.74 aA487.33 ± 9.88 aB397 ± 7.27 aC545 ± 5.65 aA
100471.7 ± 18.63 bB254.96 ± 13.75 dC688.9 ± 18.03 aA369 ± 18.63 bB152.26 ± 13.75 cC431 ± 1.13 bA
150396.56 ± 10 cB298.56 ± 9.02 cC618.43 ± 14.78 bA293.86 ± 10 cB195.86 ± 9.02 bC416 ± 4.52 cA
200375.1 ± 27.3 dB328.63 ± 29.96 bC543.96 ± 27.98 cA295 ± 2.8 cB190.3 ± 10 bC355.1 ± 36.02 dA
Stomatal conductance
(μmol m −2 s−1)		503400 ± 78.8 aB2872.1 ± 78.57 aC3547.73 ± 47.95 aA2957.9 ± 78.82 aB2639.26 ± 82.9 aC3187.5 ± 107.7 aA
1003107.26 ± 124.48 bB2247.56 ± 57.49 bC3257.83 ± 51.08 cA2507.16 ± 124.4 bB2033.86 ± 64.9 bC2954.6 ± 55.5 bA
1502608.63 ± 66.29 cB1996.4 ± 7.64 cC3310.8 ± 56.67 bA2185.5 ± 39.5 cB1895.4 ± 104.67 cC2710.7 ± 56.67 cA
2002569 ± 115.35 cB1742.8 ± 56.74 dC3294.53 ± 69.84 bcA2142.53 ± 44.53 cB1758.4 ± 37.48 dC69.8 cA
Table 5. Proportions (%) and significance levels of accessions, treatments, conditions, and their interaction effects on measured traits for the studied quinoa accessions under the salt stress effect.
Table 5. Proportions (%) and significance levels of accessions, treatments, conditions, and their interaction effects on measured traits for the studied quinoa accessions under the salt stress effect.
EffectCTAC * TC * AT * AC * T * A
Areal part lengthF1246.759 ***1639.51 ***3868.08 ***15.766 *214.539 ***26.929 *9.543 ns
%17.7623.3555.090.223.060.380.14
Leaf areaF4826.243 ***1838.827 ***1540.347 *13.823 *237.172 *58.155 *36.671 **
%56.4421.5018.010.162.770.680.43
Chlorophyll contentsF603.581 **164.333*671.62 *54.353 *69.068 *23.737 *17.86 **
%37.6210.2441.863.394.301.481.11
Dry matterF670.416 ***1715.736 ***1728.376 *58.865 **35.485 *44.746 *17.399 **
%15.7040.1740.471.380.831.050.41
Water contentsF37.308 ns151.308 ns874.654 *12.075 **93.22 *32.671 **14.987 **
%3.0712.4471.920.997.662.691.23
CatalaseF809.055 ***146.232 ns1903.884 **8.135 ***82.469 *11.23 *3.562 **
%27.294.9364.220.272.780.380.12
Photosynthetic activityF1911.94 ***205.594 *1919.447 *5.373 **131.01 *49.732 *4.296 ns
%45.234.8645.400.133.101.180.10
EvapotranspirationF563.143 ***470.699 *1286.899 *0.55256.526 *33.725 **7.389 *
%23.2819.4653.200.022.341.390.31
Stomatal conductanceF93.582 *710.4 **2175.235 **221.028 ***261.757 ***355.488 ***152.36 ***
%2.3617.8954.795.576.598.953.84
Protein contentsF64.288 ns156.513 ns688.666 *71.269 *42.903 **109.006 ***96.258 **
%5.2312.7456.045.803.498.877.83
Proline contentsF20.93 ns349.178 **2494.116 **199.597 **49.465 **398.643 ***244.597 **
%0.569.3066.395.311.3210.616.51
Sugar contentsF359.277 ***128.201 ns385.539 *43.166 ns71.007 *59.44 ns51.036 **
%32.7311.6835.123.936.475.424.65
MDA contentsF11.747 ns481.275 **1092.21 **59.805 *21.609 ns260.008 ***22.452 **
%0.6024.6956.043.071.1113.341.15
H2O2 contentsF1140.573 ***130.6261079.051 **21.319 *136.308 *72.504 *31.125 **
%43.675.0041.320.825.222.781.19
Ascorbate peroxidase activityF2083.98 ***663.297 **1865.142 **396.204 ***679.014 ***449.802 ***182.961 **
%32.9710.4929.516.2710.747.122.89
Peroxidase activityF3946.343 ***86.811800.212 **77.186 **588.078 ***166.547 **111.747 *
%58.231.2826.561.148.682.461.65
Significance levels: * p ≤ 0.05; ** p ≤ 0.01; *** p ≤ 0.001; ns: not significant; F: Snedecor–Fisher coefficient. A: accession; T: treatment; C: condition; C * T: condition–treatment interaction; C * A: condition–accession interaction; T * A: treatment–accession interaction; C * T * A: condition–treatment–accession interaction.
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MDPI and ACS Style

Slimani, N.; Arraouadi, S.; Hajlaoui, H.; Borgi, M.A.; Boughattas, N.E.H.; De Feo, V.; Snoussi, M. The Impact of Greenhouse and Field Growth Conditions on Chenopodium quinoa Willd Accessions’ Response to Salt Stress: A Comparative Approach. Agronomy 2023, 13, 2303. https://doi.org/10.3390/agronomy13092303

AMA Style

Slimani N, Arraouadi S, Hajlaoui H, Borgi MA, Boughattas NEH, De Feo V, Snoussi M. The Impact of Greenhouse and Field Growth Conditions on Chenopodium quinoa Willd Accessions’ Response to Salt Stress: A Comparative Approach. Agronomy. 2023; 13(9):2303. https://doi.org/10.3390/agronomy13092303

Chicago/Turabian Style

Slimani, Narmine, Soumaya Arraouadi, Hafedh Hajlaoui, Mohamed Ali Borgi, Nour El Houda Boughattas, Vincenzo De Feo, and Mejdi Snoussi. 2023. "The Impact of Greenhouse and Field Growth Conditions on Chenopodium quinoa Willd Accessions’ Response to Salt Stress: A Comparative Approach" Agronomy 13, no. 9: 2303. https://doi.org/10.3390/agronomy13092303

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