Adaptive mechanisms in quinoa for coping in stressful environments: an update

Introduction

It is expected that the human population will increase from six billion to nine billion in 2050 with an increase in food demand between 70 and 100% that strongly impacts reliable food production (Godfray et al., 2010). It is estimated that about one in every eight individuals is suffering from undernourishment with the mounting prevalence of obesity, diabetes, osteoporosis, fragility, and other metabolic disorders (Nguyen & Lau, 2012; Zimmet et al., 2014). Food can play a significant role in disease prevention and treatment and serve as a strong integrative strategy to combat age-related disorders and metabolic diseases. Food that gives beneficial effects on humans is termed functional food and its effects range from reduction of disease risk to its specific treatment strategy (Bigliardi & Galati, 2013). It is estimated that about 30 to 70% of the human daily energy requirement depends upon cereal-based foods (Poutanen, Sozer & Valle, 2014).

Quinoa (Chenopodium quinoa) is a food crop that is increasingly used as a food source worldwide but has been used in Andean Indigenous cultures for thousands of years (Alandia et al., 2020). Quinoa is also known as a superfood because of its super nutritious quality and stress-tolerant properties. Quinoa is mistakenly considered pseudocereal because of its property similar to that of cereal grains like corn, wheat, and rice, however, quinoa is classified as a dicot (Kadereit et al., 2003). Quinoa is morphologically and systemically different from cereal grains because it belongs to the family Amaranthaceae with unique seed and fruit anatomy. Quinoa fruits are achenes with a single seed enclosed by the outer pericarp. A quinoa seed consists of central periplasm with localized carbohydrate reserves surrounded by circular protein-rich and oil-rich embryos with endosperm and enclosed by a seed coat (Ruiz et al., 2014). Quinoa seeds undergo de-saponification/de-husking via washing and mechanical abrasion to remove bitter saponins and leave the nutrient-rich embryo and endosperm intact. The leaves of quinoa have been consumed similarly to spinach and are also used in salads (McKeown et al., 2013). The quinoa seed has been consumed in many different ways such as an important component of soup, as breakfast cereals, or used as flour in baked and toasted goods (bread, noodles, biscuits, cookies, flakes, pancakes, and tortillas). The whole quinoa plant also has been used as a rich source of food for livestock such as pigs, poultry, and cattle (Bhargava, Shukla & Ohri, 2006).

Quinoa is a unique and culturally important stress-tolerant crop with different phytochemical compositions and high nutritional value. Quinoa has a unique micro- and macronutrient profile such as lipids, amino acids, and carbohydrates and its secondary metabolites may also contribute to health benefits (Angeli et al., 2020). The most important group of secondary metabolites reported in quinoa are phenolics, glycine betaine, betalains, triterpenoids (phytosterols, saponins, phytoecdysteroids), etc. The quality and quantity of protein in quinoa are better than those of other cereal grains with high digestibility and gluten-free property. Quinoa has higher total protein content as compared to other cereal grains such as barley, rice, maize, oats, etc. the storage proteins mostly consist of albumin and globulin and a minor amount of prolamins (Sindhu & Khatkar, 2019). An in vitro study on the presence of gluten in quinoa plants revealed that only two out of 15 cultivars showed celiac toxic prolamin epitopes and these results show that quinoa is gluten-free and safe for consumption. Chenopodin is a protein that constitutes about 37% of the total protein content in quinoa which is a rich source of isoleucine, leucine, tyrosine, and phenylalanine recommended by Food and agriculture organization (FAO) (Suárez-Estrella et al., 2018).

Quinoa comprises 58.1 to 64.2% of starch and has a low glycemic index (Sharma & Lakhawat, 2017). The starch mainly consists of glucose with small amounts of maltose,D-xylose and fructose. The starch consists of small granules and is highly branched and smaller than the particle size of common cereal grains (Vega-Gálvez et al., 2010). Dietary fibers in quinoa plants are resistant to digestion by enzymes in the small intestine and even absorption and undergo partial fermentation in the large intestine. Dietary fiber can reduce the risk of infection and inflammation by reducing lipid and cholesterol absorption, improving microbiota in the intestine, and modulating postprandial insulin response (Brownawell et al., 2012; De Carvalho et al., 2014). Insoluble quinoa fiber is mainly composed of arabinose, xylose, galacturonic acid, and glucose that constitute about 78% of total fiber content while soluble fiber content such as arabinose, galacturonic acid, and glucose constitute about 22% of total fibers which is higher than that of maize and wheat (Lamothe et al., 2015).

Lipid content in quinoa is higher than that of maize and ranges from 2 to 10%. The composition of seed oil in the quinoa plant includes 54.2 to 58.3% polyunsaturated fatty acids and 89.4% unsaturated fatty acids. The ratio of polyunsaturated fatty acids is mostly 18:2n-6 and 18:3n-3 with a 6:1 ratio of omega-6 and omega-3 which is more favorable as compared to other plant oils (Tang et al., 2015a). The main essential fatty acids in quinoa include linolenic acid and linoleic acid which are metabolized to decosahexaenoic acid and arachidonic acid respectively and are well protected from oxidation by vitamin E and other antioxidants (McCusker & Grant-Kels, 2010; Vega-Gálvez et al., 2010; Sharma & Lakhawat, 2017).

Quinoa contains a rich source of vitamins including vitamin A, vitamin B1/thiamin, vitamin B2/riboflavin, vitamin B3/niacin, vitamin B5/pantothenic acid, vitamin B6/pyridoxine, vitamin B9/folic acid, vitamin C/ascorbic acid and tocopherols/vitamin E and carotenoids (Bhargava, Shukla & Ohri, 2006; Tang et al., 2015a). The mineral contents of quinoa include copper, calcium, iron, phosphorus, potassium, magnesium, and zinc (Bhargava, Shukla & Ohri, 2006; Vega-Gálvez et al., 2010). The bioavailability of iron in quinoa is higher because it contains less amount of phytic acid as it has a strong binding affinity with iron. However, the germination of quinoa seeds activates phytase, which hydrolyzes the complex between phytic acid and minerals. Moreover, the processing of quinoa seeds by soaking, cooking, and fermentation further reduced the phytic acid contents (Caballero, Trugo & Finglas, 2003).

The outer seed coat of quinoa consists of saponin, steroidal, and triterpenoids aglycone, with one or more sugar moieties. The sugar moiety includes galactose, glucose, xylose, glucuronic acid, and arabinose (Yendo et al., 2010). Common properties possessed by saponin include hemolytic activity in contact with blood cells, foaming capacity in aqueous solution, and complex formation with steroidal and cholesterol components of the plasma membrane. Saponin, therefore, protects plants from insects attack and microbial infection. The formation of saponin is an adaptive strategy in response to abiotic stress and other environmental factors (Ramakrishna & Ravishankar, 2011). Synthesis of triterpenoids takes place via an isoprenoid pathway leading to the formation of the triterpenoid backbone such as ursane, dammarane, lupeol or oleanane, and various other enzymes cause several structural modifications such as oxidation, glycosylation, and substitution (Cammareri et al., 2008).

Phytosterols present in quinoa seeds are stigmasterols, campesterol, sitosterols, and β sitosterols (Poveda et al., 2013). β sitosterol is present in much higher quantities than those of rye, barley, maize, and millet (Ryan et al., 2007). Phytosterols show hypocholesterolemic effects in humans and this property demonstrates the similarity between cholesterol and phytosterols. Phytosterols compete with cholesterol for the absorption of cholesterol in the intestine and decrease the production of atherogenic lipoprotein in the intestine and liver (Marangoni & Poli, 2010). Quinoa seeds contain the highest amount of phytoecdysteroids in the range of 138 to 570 µg/g in comparison with other edible crops. 20-hydroxyecdysteroids are the most abundant of 13 different phytoecdysteroids isolated from quinoa seeds. Extracts of plants containing phytoecdysteroids have been used as stress reducers, muscle builders, and adaptogens (Dinan, 2009).

Phenolics are a diverse class of compounds with a hydroxyl group attached to one aromatic hydrocarbon ring. Because of the presence of the hydroxyl group, phenolic compounds possess antioxidant, anti-inflammatory, antidiabetic, antiobesity, cardioprotective, and anticancer activity (Harborne & Williams, 2000; Da-Silva et al., 2007; Kelly, 2011; Jeong et al., 2012). Phenolic acids are associated with pectins of the quinoa cell wall (Gómez-Caravaca et al., 2011). The most widely investigated subgroup of polyphenols is flavonoids (Tsao, 2010). The presence of daidzein (0.70 to 2.05 mg/100 g) and genistein (0.05 to 0.41 mg/100 g) in quinoa was identified by Lutz, Martínez & Martínez (2013). Isobetanin and betanin are rich in quinoa, also have anti-inflammatory and antioxidant properties. Also, their presence in quinoa gives them their black, yellow, and red color (Tang et al., 2015b).

In today’s fast-paced community, different technological revolutions generate packaged ready-to-eat products with fast cooking time to deliver health-beneficial phytochemicals. Quinoa is processed with specific technologies to develop targets in specific areas of human health such as weight loss, fitness enhancement, celiac diseases, and other metabolic complications such as hyperlipidemia, obesity, hypertension, and diabetes (Adetunji et al., 2021). Quinoa should be formulated and processed. Quinoa undergoes superheated oil treatment to remove saponin and also expending the seed to reduce cooking time for consumers (Bendevis et al., 2014). Rhizopus oligosporus Saito is used in solid-state fermentation for tempeh productions in quinoa seeds. Tempeh produced in this way contains all essential amino acids with lower isoflavone compounds. Various methods have been developed to concentrate quinoa oils, saponins, phytoecdysteroids, and proteins. Quinoa protein concentrate has been produced via hydrolysis and precipitation via enzyme or alkali.

Geographical distribution

Quinoa was first described as a native species of South America by Wildenow in 1778. According to Buskasov, Peru and Bolivia are the main centers of origin of quinoa (Cárdenas, 1944). Gandarillas corroborated its wide range of geographical distribution with a great variety of ecotypes and its economic and social importance both in wild and technically cultivated varieties. The Andean region is considered one of the most important centers of origin of cultivated species (Arriz et al., 2016). Quinoa is divided into five categories depending upon agricultural conditions such as Yungas, valleys, salt flats, altiplano, and sea levels with different agronomic, adaptive, and botanical characteristics.

From 7,000 years ago until the beginning of the 1980s, the cultivation of quinoa was only relative for the civilizations within the Andes (Jacobsen, 2003). Growing experimentations on the quinoa plant lead researchers in other countries to recognize the benefits and potential of quinoa. Quinoa growth in several countries has increased rapidly. In 1980, the total number of countries growing quinoa species was eight increased to 75 by 2014 with a further increase in countries in 2015 (Bazile, Jacobsen & Verniau, 2016). The first experiments were conducted in Kenya in 1935 outside the Andes, with varieties obtained from the Royal Botanical Gardens, UK (Bazile, Jacobsen & Verniau, 2016). Different trials were conducted on quinoa resistance to varied environments such as the response in nutrient deficiency conducted in 1948, tolerance in varied temperatures conducted in 1968, and growth response in salinity conducted in 1950. Chilean germplasm was then used by researchers at Colorado State University, USA in 1980. Quinoa was also cultivated commercially in Canada in the same period. After that, quinoa cultivation was introduced in the UK, Tibet, Denmark, India, China, Netherlands, Cuba, and Brazil (Bazile & Baudron, 2015; Quae & Bazile, 2015).

Food production and distribution to varied environments depend upon the different pillars of food security, such as access to available food and its consumption and utilization. Quinoa due to its genetic variability, nutritional quality, low production costs, and adaptability to varied soil and climate condition is considered a strategic crop that contributes to food sovereignty and security. The main producer of quinoa in the world is Peru and Bolivia (Quae & Bazile, 2015). In 2013, the total area under the cultivation for quinoa was 45,000 ha in Peru and 75,000 ha in Bolivia. It is estimated that more than 20% of quinoa was produced by these two countries followed by the USA, Chile, China, Ecuador, France, Argentina, Canada, and Ecuador, which together represent about 15–20% of the total world production. The area under cultivation for quinoa plants in Europe was 5,000 ha in 2015 mainly in the UK, Spain, and France. FAO has tested different varieties of quinoa cultivated in different regions outside the Andean region. FAO testing aims to promote resistance to stress, nutritional quality, and food security. Quinoa is cultivated in almost 95 countries of the world now a day (Quae & Bazile, 2015).

Quinoa as an ideal plant for cultivation in multiple environmental conditions

Quinoa is considered an ideal crop for cultivation in terms of abiotic stress tolerance and is also recognized as the model crop for agricultural production worldwide. Quinoa is used an ideal food crop as a means to fight malnutrition globally because of its outstanding nutritional property (Fig. 1). Screening of various quinoa cultivars revealed their efficiency to use water, tolerance to salinity, and various other attributes leading to growing interest in quinoa cultivation (Hasegawa, 2013). Quinoa has been considered a climate-resistant crop with multiple positive attributes, including drought, frost, and salinity resistance and has created a global interest in its cultivation (Zeglin et al., 2013). Seeds of quinoa are highly nutritious with high protein contents (methionine, lysine, and threonine), minerals contents (Fe, Ca, and Mg) and vitamins and lack gluten that are limited in legumes and cereals. The United Nations designated 2013 as the year of quinoa because of its exceptional nutritional quality and ability to grow in varied environments (Bazile et al., 2012). Knowledge about the effect of extreme conditions on the nutritional and anti-nutritional properties of quinoa will provide information about the introduction of quinoa in different environmental conditions (Pulvento et al., 2012). Quinoa is thought to be an ideal crop for NASA’s Controlled Ecological Life support System (CELSS). Criteria on which quinoa is considered a potential crop according to CELSS include its canopy stature, desired nutritional composition, duration of life cycle and harvest index, and high productivity rate (Schlick & Bubenheim, 1996). The amino acid profile in quinoa seeds is generally well-balanced. Saponins are present in the pericarp of quinoa seeds which is considered useful for long-term travel. In the international market, the prices of quinoa in the US and European markets per matric tone are five times higher as compared to soya thus providing a promising economic advantage in comparison with other crops thus opening a substantial opportunity for an efficient and viable chain production (Hossam & Helmy, 2014).

The main task of research on food production is the safety and efficacy of food production for the growing population under low input management. Today, the scarcity of several resources important for irrigation such as salinity in soils and water resources is the primary cause of loss in crop production worldwide (Jacobsen et al., 2013). The remarkable tolerance of quinoa to the hostile environment makes it a suitable candidate crop for facing these challenges to food security. Quinoa may also allow farmers in water shortages and quinoa also grows in salt-affected environments for remediation and revegetation (Adolf et al., 2012). Different varieties of quinoa cultivated in environmental conditions outside their traditional growing areas are exposed to different climate conditions and this expansion of cultivation brings about a broad spectrum of diseases and pests.

The use of quality food for the aging and growing population has focused attention on nutraceutical and functional foods. Quinoa accomplishes all the nutritional requirements with properties that promote human health. Quinoa seeds also have antioxidant properties (Repo-Carrasco-Valencia et al., 2010; Vega-Gálvez et al., 2010). Flavonoids found in quinoa such as quercetin and kaempferol show antioxidant and anticancer properties. Quinoa also contains ecdysteroids that protect plants against nematodes and insects (Kumpun et al., 2011). These compounds show strong antioxidant activity and also prevent aging by inhibiting collagenase. The presence of phytoecdysteroids is limited to a few cultivated plants, so quinoa is an important source of such metabolites. Saponins present in quinoa have antibiotic, insecticide, pharmacological, and fungicidal properties (Ramakrishna & Ravishankar, 2011).

Drought

Quinoa is a model crop with the capacity to grow and produce seeds in Chile with semi-desert conditions, arid mountain regions present in northwest Argentina, and the Altiplano region in Bolivia and Peru (Fathi & Kardoni, 2020). These areas have less than 200 mm of rainfall and are considered extremely arid (Hinojosa et al., 2018; Fathi & Kardoni, 2020).

Different drought mechanisms are involved in plants to cope with water shortages. Three different approaches involved are molecular, morphological, and physiological strategies. The presence of aquaporins and activating stress proteins are included in the molecular strategy. The morphological strategy includes the presence of deep roots and scape that are involved in phenotypic flexibility while the physiological strategy involves cell membrane stabilization, osmotic adjustment, stomatal conductance, and antioxidant defense mechanisms (Hinojosa et al., 2018).

Physiological adaptation and antioxidant response of quinoa under drought condition

Quinoa’s response to low water availability is categorized into stress tolerance and stress avoidance. Mechanisms involved in stress avoidance are the maintenance of water loss and water uptake (Bandurska, 2022). Water uptake is enhanced by the accumulation of solutes which decrease the potential of tissues by increasing the growth of roots. Loss of water through evaporation is inhibited by closing the stomata resulting in the restricted growth of the shoot and increased leaf senescence (Shakeel et al., 2011). The stress tolerance mechanism is involved in protecting cells from damage when stress becomes more severe. Stress tolerance mechanisms involved the detoxification by solutes, such as proline and late embryogenesis abundant proteins or by using antioxidants (Ali, Bano & Fazal, 2017). The involvement of abscisic acid- in both tolerance and avoidance response and abscisic acid- independent mechanism including dehydration response element-binding proteins have also been also extensively elucidated (Roychoudhury, Paul & Basu, 2013). Quinoa has a unique ability to cope with drought by resuming former photosynthetic levels in low water levels (Jacobsen, Liu & Jensen, 2009; Silva et al., 2015). Because of the ability to respond to water shortage, quinoa plant is suitable for growing in semi-arid and arid regions (Bhargava, Shukla & Ohri, 2006). Quinoa has a deep root and branch system that penetrates up to 1.5 m in the soil (Flores, 2012) and transpiration could be reduced by the presence of calcium oxalate (Siener et al., 2006). The plant can also avoid drought by shedding its leaves that reduce surface area, by stomatal regulation, and by the formation of thick-walled cells that preserve turgor (Jensen et al., 2000; Silva et al., 2015). Precocity, also known as early genotype, is a crucial defense mechanism in regions that might face a water scarcity towards the end of the growth season. It also works through low osmotic potential and the capacity to keep leaves turgor even at extremely low water potential (Bhargava, Shukla & Ohri, 2006). Mechanism of modifications of quinoa in drought such as increased level of abscisic acid, rapid closing of stomata, increased osmoprotectants such as proline and betaine, etc. are common. However, other mechanisms such as calcium oxalate accumulation, increased thermostability of chlorophyll, and protein stability are not indicated as shown in Fig. 2.

Recent reports suggest that quinoa displays a different mechanism to respond to water shortage as compared to other plants such as maize (Jacobsen, Liu & Jensen, 2009). Osmotic adjustment may play a major role in quinoa to maintain turgor under drought conditions (Jensen et al., 2000). The specific surface area of leaf and photosynthetic rate during early vegetative growth may cause early vigor that increases tolerance to drought. Stomatal exposure induced by drought may be explained by mechanisms involving the role of cytokinins which are classical antagonists of abscisic acid (Jacobsen, Liu & Jensen, 2009). The limited supply of N reduces the cytokinin transport in the xylem, and stomatal sensitivity to abscisic acid may be elevated. So it is concluded that the quinoa plant closes its stomata during soil drying, maintaining leaf potential and rate of photosynthesis that results in the increased efficiency of water usage (Jacobsen, Liu & Jensen, 2009). Increased levels of sugars proline, glycine, and betaine were reported in the quinoa plant during conditions of salt stress (Ruffino et al., 2010). These sugars have been recognized as the major osmolyte in different quinoa species. Proline scavenges free radicals, thus preventing membrane protein denaturation during the condition of severe osmotic stress (Shabala et al., 2012). Accumulation of proline and other sugar contents maintain the turgor inside the cell that is necessary for the expansion of cells during stress condition Fig. 3 (Ruiz-Carrasco et al., 2011).

Biochemical stress induced by a change in water availability may be associated with enhanced production of reactive oxygen species (ROS) in plants which is responsible for oxidative damage. Increased activity of antioxidant enzymes, such as superoxide dismutase (SOD), peroxidase, catalase (CAT), and polyphenol oxidase, was observed in drought conditions with a significant increase by 39% to 90% (Iqbal et al., 2018).

Quinoa response under salinity conditions

Halophytes are plants that are adapted to survive under a high concentration of salts and thus represent an ideal crop to understand different genetic and physiological adaptations in salinity stress tolerance. Thus halophyte farming is a potential source of global food production in a progressively salinized world (Bromham, 2015; Flowers & Colmer, 2015). Quinoa is considered a crop that has the potential to survive in varied salt conditions as shown in Fig. 4.

Genetic diversity

Quinoa is divided into five ecotypes with broad genetic variability that is adapted to the altiplano, valley, sea level, tropics, and salt desert (Murphy et al., 2016). The genetic variability of quinoa and its biodiversity is confirmed by using different molecular methods. Comparison of quinoa genotypes under different growth, germination, and yield under varied saline conditions is important to understand the salinity stress tolerance in quinoa (Hussain, Al-Dakheel & Reigosa, 2018). Almost 3,000 quinoa accessions are available that show different responses in saline conditions during germination and growth. An observation of Jacobsen, Mujica & Jensen (2003) reveals that quinoa can germinate under saline conditions of up to 57 dS m21. The previous study reported that 15 out of 182 Peruvian accessions were shown to be the most tolerant crop with a germination rate of 60% at a salinity level of 25 dS m21 (Gómez-Pando, Álvarez-Castro & Eguiluz-De La Barra, 2010). Another study reported the effect of salinity in four Chilean coastal accessions and observed its effect on in vitro germination, growth, and other short-term physiological responses (Ruiz-Carrasco et al., 2011). The expression level of two Na transporter genes CqNHX salty over sensitive 1 CqSOS1 and their association with these parameters were observed. A significant reduction in the length of roots and germination rate of seeds was observed in genotype BO78 from southern Chile at the highest NaCl level (300 mM). The lowest level of root/shoot fresh weight ratio was also observed in BO78. The following observations suggested the least salinity-tolerant property of BO78 (Ruiz-Carrasco et al., 2011; Bueno & Cordovilla, 2020). Moreover, another observation on four Chilean genotypic varieties showed that with a NaCl concentration of 200 mM, Hueque was shown to be the most affected genotype with a 50% decrease in germinability and the lowest decrease in germination rate was observed in Amarilla (Delatorre-Herrera & Pinto, 2009). Several mechanisms may contribute towards different genotypic differences in salinity tolerance includes the high exclusion of Na and retention of K ion from leaf mesophyll, increased rate of H pumping, and reduction of vacuolar channels activity under salinity condition. The development of these mechanisms in quinoa causes an increase in the salinity tolerance of quinoa (Bonales-Alatorre et al., 2013).

Morphological adaptations

Several findings have indicated that halophytes can be sensitive to salinity during seed emergence and germination (Debez et al., 2004). Understanding the mechanisms involved in the sensitivity and tolerance of seed in the accumulated Na concentration is, therefore, an important concern (Hasegawa et al., 2000). It is indicated that the preservation of ion homeostasis is the main mechanism involved. The distribution and maintenance of other ions in tissues and seeds are also important features. A study by Koyro & Eisa (2008) studied the mineral distribution of seeds that were taken from plants grown under high salt concentrations. They noticed the altered concentration of salt but highly regulated and did not cause any harm to seeds and also affect the viability of seeds. Although the weight of the seed is decreased at high concentration of salts, reduction in dry matter including carbon-containing compounds that were mainly compensated by increasing ash content (Koyro & Eisa, 2008). An increase in ash content induced by high salt concentration was due to high concentrations of Na, K, Mg, and Ca. Therefore, there was a stable buildup of K ions and other essential nutrients including P and S, even under high salinity. Thus seed coat restricted the passage of possibly toxic Na ions and Cl ions to the interior of seeds, as 0.90% Na ion and Cl ions were present inside the seed coat (Koyro & Eisa, 2008). The study revealed that the seeds of quinoa plants that were grown under high salt concentration exhibit a tolerance mechanism that was based on the presence of periplasm that serves as a protective barrier and integrity of coat that ensures the exclusion of Na and Cl ions and the maintenance of balanced Na and Cl ion ratios in the interior of seed. Similarly, the viability of the seed depends on its ability to avoid toxicity by excluding Na ions from the developing embryo (Hariadi et al., 2011).

A most distinctive characteristic of quinoa is the presence of bladders or salt glands also known as trichomes. Accumulation of the absorbed salts into these bladders may provide an efficient strategy contributing to salinity resistance in quinoa and other salt-tolerant species (Agarie et al., 2007; Ben Hassine et al., 2009). They are involved in the compartmentalization of accumulated salts and then exclusion from mesophylls. They act as the secondary epidermis and reduce the loss of water and UV-induced damage. In chenopods, these types of structures are present on lower and upper leaf surfaces, panicles, inflorescences, and stems, and, are also termed as epidermal bladder cells (EBCs). The presence of EBC in rich density in young leaves of quinoa protects Photosystem II (PSII) from UV damage (Shabala et al., 2012). Thus, EBCs may accumulate organic compounds with chaperone ability and scavenging of reactive oxygen species (ROS). Quinoa leaves possess calcium oxalate crystals that are related to the accumulation of excessive Ca under salt stress and drought (Riccardi et al., 2014). Further studies are required to study the genetic variability of EBC and their specific importance and composition in quinoa.

Saline conditions generally decrease the transpiration rate. The observed reduction in stomatal conductance in halophyte leaves is assumed to be important for better water use efficiency. This may originate from both physiological, e.g., control over stomatal aperture, and morphological, e.g., stomatal density and size, adaptive responses to salinity. A reduction of up to 50% in stomatal density under strongly saline conditions (600,750 mM NaCl) accompanied by reduced stomatal size was reported in the relatively salt-sensitive Chilean cultivar BO78 (Orsini et al., 2011). In a comparative study between 14 varieties of quinoa differing in salinity tolerance, Shabala et al. (2012) demonstrated that, while all had reduced stomatal density under saline conditions, this morphological parameter was differentially affected in different genotypes.

Increase in antioxidant metabolism in quinoa under salt stress

Water absorption reduced as a result of high salt concentration directly affects CO₂ absorption and stomatal closure that leads to restricted CO₂ fixation (Munns, James & Läuchli, 2006). Limited CO₂fixation causes a decrease in NADPH oxidation by the Calvin cycle. As a result of that, the electron of NADPH that causes the reduction of NADP+ goes to O₂ resulting in the production of excessive ROS. ROS reacts with different macromolecules causing protein denaturation, DNA mutations, and lipid peroxidation (Gill & Tuteja, 2010). Plants show different antioxidant responses to minimize ROS-induced tissue damage. Quinoa plants increase the activity of different antioxidant enzymes such as superoxide dismutase (SOD) and catalase (CAT) (Khalofah, Migdadi & El-Harty, 2021). SOD catalyzes the conversion of O₂.- into H₂O₂ and O₂ and CAT cause the conversion of H₂O₂ into H₂O and O₂ (Gill & Tuteja, 2010). Moreover, betalains secondary metabolites in the leaves and stems of quinoa also shows antioxidant properties (de Oliveira Junkes et al., 2019). Betalains as osmolytes cause the protection of different physiological processes against abiotic stresses (Wang et al., 2021). Generally, high salinity causes the accumulation of amino acids such as phenylalanine that act as a precursors for the biosynthesis of betalains (Tanaka, Sasaki & Ohmiya, 2008).

A study by Shabala et al. (2012) indicated that under different sodium concentrations, the dry weight of roots and shoots of seedlings of quinoa were unaffected. A high level of betacyanin content was reported after treating with 0 to 150 mM of sodium chloride. Moreover, higher activities of antioxidants such as CAT and SOD, were also reported in roots and shoots of early seedlings in 150–200 mM of sodium chloride concentrations. Levels of ascorbate were also higher in shoots under 100–200 mM of sodium chloride concentration. However, in roots higher ascorbate concentration was reported at 50 mM of sodium chloride. On the other hand, increased lipid peroxidation was observed in shoots under 200 mM of sodium chloride. Nevertheless, no differences were reported in roots between treatments. As far as the levels of H₂O₂ are concerned increased levels were observed in shoots under 150–200 mM of sodium chloride. However, in roots, no differences were observed between treatments. Superoxide dismutase is considered as the first line of defense under stress conditions (Gill & Tuteja, 2010). Increased SOD activity in high sodium chloride concentration causes the overproduction of H₂O₂ that causes toxicity which results in increased catalase (CAT) and ascorbate peroxidase (APX) activity for the detoxification of ROS (Tang et al., 2015b). These enzymes work with different affinities for H₂O₂. CAT shows a low affinity to H₂O₂ and needs a high concentration of its substrate whereas APX exhibits a high affinity to H₂O₂ and is capable of detoxifying H₂O₂ even at a low concentration of substrate (Munjal et al., 2019). Under low concentrations of sodium chloride low levels of H₂O₂ were produced but higher APX activity was observed confirming the active role of APX even under lower H₂O₂ concentrations (Sharma et al., 2012). Under 150–200 mM of sodium chloride concentration, an early seedling of quinoa required the higher activity of CAT to detoxify the H₂O₂ produced due to the higher activity of SOD. These findings support the role of CAT in the antioxidant system which mainly shows activity under higher H₂O₂ concentrations. This coordinated activity of antioxidant metabolism was able to keep lower lipid peroxidation as control plants until the concentration of sodium chloride increases up to 150 mM (Sharma et al., 2012).

Adaptation of quinoa in heat stress

The markedly elevated temperature during the early growth phase of plants is described as one of the most important abiotic stresses due to abrupt climatic change (Awasthi, Bhandari & Nayyar, 2015). Worldwide, a broad range of agricultural losses has been accredited to heat alone or most often in combination with drought (Suzuki et al., 2014; Sehgal et al., 2017). Heat stress can be defined as an elevated level of air temperature that is above the optimum temperature for plant growth and remains elevated for a while adequate to cause damage and hence decrease plant growth and development (Wahid et al., 2007). Plants show different responses to heat stress depending on the duration of temperature and developmental stages of plants (Driedonks, Rieu & Vriezen, 2016; Prasad, Bheemanahalli & Jagadish, 2017).

Heat causes different morphological, anatomical, phenological, and physiological changes. Morphological changes include the inhibition of root and shoot growth and increased branching of stems. Anatomical changes, such as the reduced size of cells and increased trichome and stomatal densities. In addition to these changes, heat stress also causes certain physiological effects including increased fluidity of the membrane, protein denaturation; instability of cytoskeleton, changes in the rate of photosynthesis and respiration and carbon metabolism enzymes; osmolyte accumulation; mitochondrial and chloroplast enzyme inactivation; changes in salicylic acid, ABA, and ethylene; and increased production of secondary metabolites (Wahid et al., 2007; Bita & Gerats, 2013). Heat stress prompts the production of oxidative stress by generating ROS, in the same way as in salinity and drought stress which results in serious toxicity in plants; however, ROS in low concentration also acts as a signaling molecule that activates other plants’ cellular processes, such as apoptosis (Hasanuzzaman et al., 2013).

Heat-shock proteins (HSPs) play a crucial role during gradual or abrupt changes in temperature to cope with the heat stress response (HSR) (Kotak et al., 2007; Wahid et al., 2007). Several findings have reported that HSPs play an important role in thermo-tolerance in different species of plants. The study indicated that the indispensable role of HSP70 and HSP90 induced tolerance to heat stress response. Heat stress factors (HSFs) are mainly involved in the induction of signaling pathways in HSP expression (Ohama et al., 2017). Different genes belonging to heat shock transcription factors were identified. A total of 23 different heat shock transcription factor genes were identified and their expression profiles were identified by RNA seq data. Results indicated that CqHsfs9 and CqHsfs3 showed higher expression levels after 6 h of heat treatment, while CqHsfs10 and CqHsfs4 exhibited a higher expression level after 12 h (Tashi et al., 2018). Quinoa plants have an excellent heat shock protein network that intervenes caspase cascade at multiple levels Fig. 5.

Several studies have been carried out to indicate the effect of temperature fluctuations on the germination of quinoa (Mamedi, Afshari & Oveisi, 2017; Strenske et al., 2017). Studies have indicated a positive correlation between temperature and the germination rate of quinoa (Bois et al., 2006; González et al., 2017). Results suggested that the maximal temperature at which Quinoa germinate is 50 °C, and the minimum germination temperature is 3 °C (Jacobsen & Bach, 1998; González et al., 2017). In contrast, Bois et al. (2006) reported germination temperature fluctuations in 10 different varieties that vary between −1.9 °C and 0.2 °C. Another study reported that the optimum temperature range in three different varieties of quinoa was 18–36 °C however; the maximum and base temperature range was 54.0 °C and 1.0 °C respectively. Seeds of the quinoa plant can be stored at 25 °C for up to 430 days under controlled environmental conditions, before germination fully declines (Strenske et al., 2017).

Quinoa response to heavy metals

Lead is considered as a persistent toxic pollutant because of rapidly increasing anthropogenic stress on the environment (Pourrut et al., 2011). Excessive accumulation of lead may cause various physiological, morphological, and biochemical changes in plants (Shahid et al., 2013). A study by Haseeb et al. (2022) reported a reduction in dry and fresh weight of roots and shoots and root length of four different quinoa varieties in the lead concentration of 100 mg/kg as compared to 50 mg/kg lead concentration. The results revealed that a 100 mg/kg concentration of lead did not stop the growth of all quinoa lines, however; the dry biomass of the plant was affected. When the plant was exposed to 100 mg/kg of lead concentration at the panicle emergence stage significantly less plant height was observed in all quinoa lines.

Lead accumulation inhibits the development and growth of plants due to poor uptake of essential minerals (Gopal & Rizvi, 2008). Accumulation of heavy metals in plants is of great concern due to the risk of food contamination through the interface between soil and root (Mukhtar et al., 2010). Absorption of lead from soil solution in plants usually takes place through roots via the apoplast pathway or through Ca²⁺ permeable channels (Sharma & Dubey, 2005). Bioconcentration factor (BCF) is defined as the ratio between the accumulated metal ion in plant roots to the concentration of metals in soil (Zhuang et al., 2007). Less than 1 BCF value was detected in all quinoa varieties. On the other hand, the translocation factor is the ratio between accumulated metal concentrations in shoots of plants to the metal concentration in plant roots. It is estimated that during the reproductive stage, lead taken up by quinoa varieties was not translocated to other parts of plants. This is a unique property present in quinoa however, other plants require external adjustments to reduce the sequestration of metals at the seedling stage and stop its transfer to the flowering stage by immobilizing lead through biochar and decreasing its bioavailability as in rice plants (Li et al., 2016). Lead accumulated in high concentrations in plants may block the translocation of other essential nutrients such as Ca, Mg, P, Cu, K, and Zn resulting in the deficiency of these ions. Biochar from animal and plant origin as well as compost influence positively on chemical and biological properties of Ni-contaminated and salt-affected soils. Biochar increases the bioavailability of essential nutrients by decreasing metal toxicity and improving water retention (Fig. 6). Lead toxicity may lead to the reduction in the contents of carotenoids and chlorophylls a and b in mung beans (Deshna & Bafna, 2013) and wheat (Lamhamdi et al., 2013). The results of this study were similar to the study of Akinci, Akinci & Yilmaz, 2010 who indicated the destruction of the thylakoid membrane and grana in lead toxicity. In quinoa plants, lead at high concentrations may destroy chlorophyll A and b. Overproduction of reactive oxygen species may lead to the disruption of the chloroplast which is the main cause of reduction in photosynthetic pigments (Pourrut et al., 2011). Increased oxidative stress due to lead toxicity may lead to the destruction of chlorophyll in rice plants (Zeng et al., 2007). Under abiotic stress conditions, carotenoids work as antioxidants in addition to photosynthesis (Kasote et al., 2015). Under high lead concentration in quinoa lines, increase carotenoid concentration was reported as compared to chlorophyll. High carotenoid concentration may play an important role in quenching free radicals produced during stress conditions under lead toxicity (Kong et al., 2015). Different defense strategies are used to cope with lead toxicity. Such strategies include reduced lead uptake into the cell; sequestration of lead into vacuoles by the formation of complexes; binding of lead by phytochelatins, glutathione, and synthesis of osmolytes (Pourrut et al., 2011). Phenolic compounds synthesized in the plants prevents the diffusion of free radicals and stabilize the membrane. Phenolic compounds make hydrogen bonds with polar heads of phospholipids of present in membranes (Michalak, 2006). Quinoa plants exhibited a high concentration of phenolic compounds in lead toxicity. Zeng et al. (2007) described that the accumulation of lead negatively affected the sugar beet (Beta vulgaris) yield.

Conclusion and future perspectives

The main challenge of today’s world is to meet fiber needs and future food requirements which was more discouraging than experienced under the green revolution. The primary growth-stimulating factors are chemical fertilizers and irrigation water which cannot be expected to increase yield at the required rate. About one-third of the world’s land surface is facing drought, salinity, extreme variation in temperature, and many other abiotic problems due to an increase in global warming. Quinoa is the only crop that has resistance to adverse environmental factors. The improved knowledge of mechanisms involved in the resistance of quinoa to adverse abiotic and biotic stress environments will help to overcome the limitations imposed by these stresses all over the world. There are expectations of increased commercial production of quinoa so there is a need for time to regulate the international framework on different genetic resources that are needed to facilitate the breeding of quinoa plants in varied environmental conditions.