1. Introduction
Soil degradation due to salinity is a big issue in agriculture and forestry, especially in marginal environments. Several factors, such as scarce water resources, loss of topsoil due to wind erosion, sandy soils and high temperature in desert ecosystems are major constraints for crop production [
1,
2,
3] affecting 250 million people [
4]. Many arid and semi-arid regions of the world exhibit a significant portion of salt and degraded marginal lands. According to Wang et al. [
4], approximately 20% of the land area is degraded. Global Assessment of Soil degradation (GLASOD) reported that 12 million heactares of land are degraded each year in arid ecosystems, at a cost to the global economy of up to US
$42 billion per annum [
5]. Furthermore, the continuous increase in global demand for food, fuel and feed has shifted the focus towards degraded lands, because land suitable for food production is shrinking worldwide [
6]. This situation is further aggreviated by strong winds in arid and semi arid areas that cause erosion and land degradation, removing the top productive soil layers that can support plant growth [
7].
Salinity is a complex phenomenon that critically impacts the morphological and physiological traits of crops through modifications in the osmotic balance, ion homeostasis, and reactive oxygen species regulation, each having a complex and less understandable genetic basis. High accumulation of salts in saline soils results into reduced water potential of soil solutions which causes difficulty for plants to extract water from soil experiencing “osmotic stress” [
8]. Specific ion toxicity, the result of excessive uptake of certain ions (Na
+ and Cl
−) is the primary cause of growth reduction [
2,
9,
10,
11]. Toxic ions in salt-affected soils are usually sodium, chloride and sulphate [
2,
12]. The excessive Na
+ accumulation causes ion toxicity and interferes with plant metabolism, while accumulation of K
+ can alleviate Na
+ toxicity by adjusting osmotic potential and through ion balance. Crop performance may also be adversely affected by salinity-induced nutritional imbalances [
13,
14]. These imbalances may result from the effect of salinity on nutrient availability, competitive uptake, transport and/or partitioning within the plant caused by physiological inactivation of a given nutrient resulting in increased plant’s internal requirement for that essential element [
2,
15,
16]. One or more of these processes may occur at the same time, but whether they ultimately affect crop yield or quality depends on the level of salt stress, composition of salts, crop species, the nutrient in question and a number of environmental factors [
15,
16]. Therefore, it is imperative to advance our knowledge regarding the identification and evaluation of genotypes and landraces that can be cultivated in nutrient poor and sandy marginal soils. Moreover, these germplasms might have the potential for the restoration of these regions. Several studies concerning salinity tolerance in cultivated crops have been reported, while considerable advances have been made in the development of crop genotypes resistant to drought or salinity [
17,
18]. Therefore, salt-affected soils can be utilized by growing salt tolerant plants, whether halophytes or non-halophyte crops. The use of halophytic crop species can be considered as a valuable option to sustain agricultural production under saline and dry conditions and potentially under irrigation with saline waters [
19,
20]. However, it is imperative to explore intra-specific (inter-cultivar) variation for salt tolerance of a crop by screening its available germplasm.
Halophytes have shown potential to be useful resources for global food production, and contribute to the rehabilitation of salt-degraded lands. Quinoa (
Chenopodium quinoa Willd.) is an important facultative halophyte, and its demand has increased recently in all continents [
21]. Quinoa is a highly nutritious pseudo-cereal and has a wide potential to enhance food security through tolerating saline and marginal lands and to alleviate pressure on fertile agricultural soils [
22]. Quinoa seeds are enriched in proteins, amino acids (lysine, methionine, threonine) [
23]. Different fatty acids (linoleic and linole) and oleic acids have been reported in the seed oil [
23]. From a human health perspective these fatty acids are of high quality as compared to those reported from other cereals [
24]. Moreover, quinoa seeds are free from any allergic effects that may be caused by harmful chemicals or gluten, which is present in other cereals [
25]. Quinoa exhibit various minerals like calcium, phosphorus, potassium, magnesium, phosphorus and zinc in sufficient quantity and protein contents (12–17%) [
26]. The quinoa crop has been internationally recognized as a contributor to global food security because it is tolerant to many environmental constraints, such as frost [
27,
28], drought [
29], and salinity [
30]. In many developing African countries, quinoa has been significantly introduced in agro-ecosystem and has contributed to the regional food security [
31,
32]. However, evaluation of salinity tolerance potential of different quinoa genotypes and the possible evaluation of their growth, development and yield behaviour in salt-degraded marginal Arabian Peninsula Sandy desert soils are rarely studied.
The phenotypic plasticity, genotype variability and agronomic adaptation of quinoa are extremely wide and varied significantly from hot arid to subtropical humid climates [
33]. Under these circumstances, it is viable to select, introduce, adapt and breed different quinoa genotypes in a wide range of environments. However, to increase food security and agriculture productivity in resource poor and degraded marginal lands like those of United Arab Emirates, it is imperative to study the salt tolerance potential of different quinoa genotypes and assess their yield stability without losing the grain quality. Jacobsen et al. [
33], the quinoa plant photoperiod is a critical functional trait and should be evaluated before introducing it in a particular environment. Most of the previously referred studies have been carried out in quinoa germination and seedling growth responses under the control growth chambers. It is important to understand that germination and early seedling establishment stage is critical in the life cycle of plants, and many colleagues have documented these phenomena [
34,
35]. However, yield response factors of different quinoa genotypes to saline and marginal soil environment and their salinity tolerance mechanisms that may regulate seedling growth, yield and grain quality attributes need to be evaluated under marginal and nutrient poor sandy soils.
Studying the salinity tolerance potential of different quinoa genotypes and the elucidation of seed yield and yield stability is of paramount importance. Therefore, the evaluation of salinity tolerance potential of different quinoa genotypes was conducted under the hyper arid climate of Dubai, UAE with the following main objectives: (i) evaluation of the adaptation of accessions of different origins to the UAE sandy desert marginal environment with spring sowing, (ii) assessment of the salinity tolerance potential of six quinoa genotypes, (iii) determination of the variation and heritability of quinoa morphological and quality traits and their interrelationship with yield attributes and (iv) identification of the impact of saline water in growth, yield stability and grain protein content. The study will help to discriminate between resistant and sensitive quinoa genotypes and to understand the mechanisms of adaptation, for selecting genotypes tolerant to saline water irrigation in order to adapt to salt-degraded marginal sandy desert in the hyper arid UAE environment.
4. Discussion
The rising global demand for nutritious and healthy food has challenged scientists to look for alternate crops, especially for the marginal areas where agricultural production is inefficient due to unfavorable climatic conditions, low soil fertility and lack of good quality irrigation water. In the Arabian Peninsula, scientists are experimenting with quinoa production because it is rich in nutrients, tolerant to salinity and uses much less water than other crops. Against this backdrop, this study identified the agro-morphological traits (PDM, BN, PN) that showed a decreasing trend with increasing salinity. Gómez-Pando et al. [
13] showed that germination and plant height were highly decreased in quinoa plants that were subject to different salinity levels. Additionally, some genotypes (total 15 genotypes) were tolerant and less affected while others were susceptible and their agro-physiological attributes were decreased significantly following salinity treatment.
Under the saline and marginal UAE environment, some agro-physiological traits (PH, NBP, and NPP) were decreased after salt stress while PL was unaffected at various salinity levels. A decrease in dry matter yield with increasing soil salinity levels might be due to the inhibition of water availability and hydrolysis of reserved foods and their translocation to the growing shoots [
43,
44]. Other factors responsible for lower dry biomass yield may include panicle length, chlorophyll concentrations, number of productive tillers, number of primary branches per panicle, and fertility percentage [
45]. The reduction in number and size of the panicles per plant is directly related to lower seed yield [
46]. Plant biomass, height and seed yield, number of branches, number of panicles, panicle weight and harvest index were reduced in response to saline water irrigation and were subject to genotypic variation [
8]. Genotypic variability in seed yield and biomass has been reported before for quinoa plants growing under comparable agroecological conditions [
8,
43,
46]. Moreover, the significant interaction between genotype and irrigation conditions for seed yield, biomass and different agronomical traits highlights not only the genotypic plasticity available in the species but also the need to assess genotypic performance within each growing condition [
47]. In the present study, PH was decreased after salinity treatment and AMES 13,761 was the tallest variety while Q22 was dwarf genotype. This was due to the stunted growth of plants caused by the high salt concentration in the nutrient medium. Adolf et al. [
48] evaluated 14 quinoa genotypes at different salinity levels and recorded growth and biomass attributes. Pandela rosada and Utusaya were least affected and had capacity to be adapted to the harsh climate of southern altiplano of Bolivia (3600 m above sea level). Another quinoa variety, Amarilla de Maranganí was more tolerant and was not affected with respect to height and biomass production. The results of this study also suggest that plant morphological and agro-physiological characteristics are interrelated factors that highly impact the plant establishment, seedling growth, and yield. Meanwhile, the responses of different quinoa genotypes against salinity were different indicating their genetic diversity. According to different researchers, several mechanisms might contribute towards genotypic differences in salinity tolerance in quinoa. These mechanisms may include Na
+ exclusion from leaf mesophyll cells, better H
+ pumping to restore membrane potential, and Na
+ exclusion from leaf cells demonstrating salinity tolerance of quinoa [
32,
33,
49]. The information about these functional attributes might facilitate the restoration programs of degraded marginal salt affected soils and will help to convert waste to wealth assets.
The evaluation and selection of salt tolerant quinoa genotypes is an important step to pursue their adaptation uder marginal and sandy soils and to check the effect of salinity on grain yield and grain protein contents. The present results demonstrated that significant genetic diversity exists between different quinoa genotypes. Yield components like NPP and PL were different among genotypes. Salinity significantly affected the number of panicles per plant and average panicle length also varies from one to other genotype. According to the report of Long Nguyen [
50]; panicle length in quinoa is interconnected with grain yield and variation in this trait lead to significant variation in the final yield. Several researchers have noticed that long panicle bearing genotypes demonstrated higher yield than genotypes with shorter panicles [
45,
46]. From the results of present study, it was concluded that differences in panicle length were connected with genotypic difference rather than salinity impact.
The seed yield was significantly decreased (60%) at high salinity. It is a typical phenomenon of plants affected by environmental stresses that showed a restricted supply of CO
2 as well as reduced activity of RuBisCO. These processes leads to reduced photosynthesis, carbon assimilation, growth and yield of the plants [
16,
51,
52,
53,
54]. Previously published data showed that the small panicle length, chlorophyll concentrations, number of productive tillers, and lower number of primary branches per panicle were responsible factors in the low yield of quinoa [
45].
The salinity treatment did not affect very much the leaf C and N. However, the allocation of N and C was different among the different genotypes and changed in respect to the genetic variability. Grain protein contents (GP) differed significantly after salinity treatment that was stimulated to a cetain extent. Genotype, NSL106398 showed higher grain protein contents while the lowest was observed in Q29. The reduction in quinoa plant dry biomass was 23.7% and 36% after treatment at 10 and 20 dS m
−1 respectively. The growth of quinoa (cv. Hualhuas) was slightly increased following salinity treatment [
55]. The present results demonstrated the competitive advantage of salinity tolerant quinoa genotypes in terms of morphological and ecophysiological attributes [
6,
13,
18,
21,
43,
45,
56].
Our results indicate a difference in grain and biological yield (harvest index) among quinoa genotypes, showing that Q21 had a higher seed yield, followed by AMES13761, and both genotypes showed a typical genetic variation. Adolf et al. [
48] reported similar results. They found that quinoa genotype, Utusaya (Bolivian origin) had high stomatal conductance compared to control plants and showed a reduction (25%) in CO
2 while “Titicaca” (from Denmark) demonstrated higher reduction (67%) in CO
2 assimilation. To counteract the salinity, Utusaya variety possessed some genetically improved salt tolerance mechanism (osmoprotectants) and water loss through transpiration was much less than other genotypes. Recent studies highlighted that some adaptation mechanisms exist in certain quinoa genotypes that control transpiration and thus, WUE, under saline conditions. Lately, it was correlated with morphological features (stomatal size reduction, density or both) [
22,
23,
47,
48,
49]. A significant variation was also oberved in HI among genotypes while AMES13761 showed higher HI, followed by NSL106398 and it was lowest in Q22. Morover, salinity also reduced HI after treatment at 10 dS m
−1 and 20 dS m
−1. These results demonstrated a greater adaptability of quinoa genotypes to the agro-climatic conditions of UAE. Other researchers also documented that Chilean varieties were less sensitive to photoperiod and hence more adaptable to saline and marginal environments [
27,
28,
29].
The correlation between diggerent physiological, yield and quality characteristics of quinoa are presented in
Table 6. Several parameters were positively correlated with other contributing attributes while some also have negative correlation. More prominent +ve correlation was found betweeen NOB, NOI and AIL, TB, C:N ratio). The correlation among grain yield, biological yield and protein contents of grains is often misleading. This can lead to wrong conclusions and policy guidlines for future breeding strategies for marginal environments [
57]. Confusion was largely provoked by the fact that the relations between biomass, number of panicle and yield were positive or negative, and sometimes there was no correlation depending on the crop and growing conditions.
Lessons from Different Stress Levels: Trade-off between Survival and Growth
In the present study, the Chilean-based quinoa genotypes displayed remarkable variation in plant establishment, seedling growth, biomass yield, and panicle attributes and salinity responses yield potential. Different salinity treatments (10, 20 dSm
−1) caused a significant reduction in biological and grain yield. Even though seed yield was reduced, quinoa was still able to perform relatively well under these sandy, nutrient poor and marginal soil conditions as compared to other high productive soil environments. Under low salt stress (10 dSm
−1), average panicle length of quinoa varieties did not differ in their responses to salinity. However, at high salinity (20 dSm
−1), seed yield was not highly reduced in all the tested varieties. In this regard, Q21 was highest yielder while Q18 was the most affected with lowest seed yield. We speculate that Q18 employed a “survival” strategy with a more reduced growth rate, biological yield (HI) but higher number of branches and number of panicles and medium level of leaf C% and N%. The grain protein contents were comparative to AMES13761 and Q21 but its seed yield was highly reduced at overall salinity, compared to other varieties. These adaptations allowed Q18 to survive longer, but at the trade-off of the very high reduction in growth rate and seed production. Several authors documented that there is great variation in salinity tolerance among quinoa genotypes [
22,
23,
43,
47,
48,
49,
58,
59,
60]. Previously, it was assumed that only Bolivian Salares originated genotypes are high salt tolerance while, now, it is well known that salinity tolerance does not related with geographic distribution and genotypes from Chile coastal areas and highlands are even more salt tolerant [
58,
59,
60]. Furthermore, it was recently reported that a wild relative of quinoa (
Chenopodium hircinum) was found to have a much higher salinity tolerance level than quinoa cultivars [
59]. Photoperiod and temperature attributes also played a significant role in the growth, development and final grain yield of quinoa. Some researchers demonstrated that quinoa genotypes originated from dry and cold environments were sensitive to the temperature as compared to varieties originated from hot and humid climates [
38]. It was evidenced previously that solar rays affects phyllochron in the quinoa varieties. Thus varieties from these regions (Peru, Southern Chile and Bolivia) were more sensitive to solar radiation than Ecudorian varieties. While, it was demonstrated that Ecuadorian quinoas were more sensitives to photoperiod becuase they posess longest phyllochron. However, in the present studies, we did not observe any growth and yield loss due to photoperiod and most of the yield reduction was due to nutrient poor sandy soils and salt stress.
Salinity tolerance evaluation of quinoa indicated a significant diversity in growth strategies, agro-physiological attributes, yield stability and salinity coping phenomena’s that will assist in the restoration of sat-degraded marginal sandy soils. Quinoa as a highly nutritious crop and can be a potential candidate in nutrient poor sandy and salt-degraded marginal soils in arid and semi arid regions and will help to adapt the harsh environment, as well as also offer food security. The present studies also suggest the supply of essential plant nutrients through chemical fertilizers and organic manures as soil amendments may be a possible strategy to increase nutrient availability and soil water holding capacity in salt-degraded marginal sandy soils. Other management strategies could include strong seeding establishment at the start of the sowing using fresh water encouraging seedling survival for later irrigation with saline water under nutrient poor, sandy and vulnerable environment.