Next Article in Journal
Physiological, Productive, and Nutritional Performance of Tomato Plants Treated with Iron and Zinc Nanoparticles via Foliar Application Under Deficit Irrigation
Previous Article in Journal
MSHLB-DETR: Transformer-Based Multi-Scale Citrus Huanglongbing Detection in Orchards with Aggregation Enhancement
Previous Article in Special Issue
Exogenous Spermidine Enhances Drought Resistance of Mango Seedlings by Regulating Physiological and Biochemical Metabolism
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 11
Issue 10
10.3390/horticulturae11101226
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Drought Tolerance Mechanisms in Grain and Vegetable Amaranthus Species: Physiological, Biochemical and Molecular Insights

by
Mulisa Nkuna
1,
Pfunzo Gavhi
1,
Alice Mwanjiwa Kanyerere
1,
Vivian Chigozie Ikebudu
1,
Nzumbululo Ndou
1,
Andrew Faro
1,
Ibrahima Zan Doumbia
1,
Rachel Fanelwa Ajayi
2,
Azwimbavhi Reckson Mulidzi
3,
Nike Lewu
3 and
Takalani Mulaudzi
1,*
1
Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
2
SensorLab, Department of Chemical Sciences, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
3
Department of Soil Science, Agricultural Research Council, Infruitec-Nietvoorbji, Private Bag X5026, Stellenbosch 7599, South Africa
*
Author to whom correspondence should be addressed.
Horticulturae 2025, 11(10), 1226; https://doi.org/10.3390/horticulturae11101226
Submission received: 3 September 2025 / Revised: 2 October 2025 / Accepted: 7 October 2025 / Published: 11 October 2025
(This article belongs to the Special Issue Responses to Abiotic Stresses in Horticultural Crops—2nd Edition)
Browse Figures
Review Reports Versions Notes

Abstract

Drought limits plant growth, development and productivity, leading to more than 50% crop loss globally. Drought-induced oxidative stress disturbs the plant’s metabolism; however, plants activate signaling pathways to respond and adapt to drought stress. Although drought response mechanisms are well reported in several crops, these mechanisms are poorly understood in Amaranthus. As a highly nutritious crop, rich in antioxidants with the ability to survive in extreme agro-climatic environments, Amaranthus has the potential to serve as a climate-smart future crop. This review provides evidence of some drought response traits in grain and vegetable Amaranthus species. Grain amaranths are the most tolerant species, mainly through improved osmoregulation, antioxidant capacity, and gene expression. While biomass partitioning, efficient water use, and membrane stability have been reported in both grain and vegetable amaranth, the molecular response of vegetable amaranth remains limited. Thus, future research must focus on integrated biochemical, molecular, and multi-omics applications to screen and identify resilient Amaranthus genotypes under drought for sustainable agriculture.

1. Introduction

Food insecurity continues to be a major livelihood threat at a global level. With the human population expected to increase to 10 billion by the year 2050, many countries remain food insecure [1]. As a result, there is great pressure weighing on the agricultural sector to increase food production by over 70%, sufficient to cater for an additional 2.3 billion people. Globally, it has been estimated that between 5 and 170 million people are at risk of being food-insecure due to the impacts of climate change [2,3]. Thus, food security is highly dependent on the development of crops with inherent adaptations to environmental stresses. Although certain crops are relatively stress-tolerant, their growth, development, and yield are negatively impacted by prolonged droughts [4,5]. The occurrence and severity of drought-induced injuries depend on plant species, cultivar type, plant growth stage, duration of exposure, and intensity of the stress [6].
Drought triggers water loss and reduction in water potential, which lead to a reduction in cell turgor [7]. Extended droughts induce osmotic imbalance and ion-mediated oxidative stress, which negatively affect plant physio-chemical responses [8]. However, plants activate different morphological, physiological, biochemical, and molecular drought response mechanisms, as shown in Figure 1. These mechanisms are broadly divided into the following categories: drought avoidance, escape, and tolerance. Drought avoidance is coordinated through morphological adaptations such as leaf curling, wax deposition on the leaf surface, and a decrease in the shoot-root ratio [9]. Drought avoidance also includes physiological responses such as a reduction in relative water content (RWC), a vital indicator of the plant’s water status, which triggers stomatal closure to prevent extensive water loss due to transpiration [6]. Drought escape is an adaptive mechanism whereby plants complete their life cycle before the start of a severe drought [10]. Lastly, plants induce drought tolerance through osmotic adjustment, antioxidant metabolism activation, and drought-responsive gene expression [11].
Drought-induced alterations disrupt the photosystems I and II (PSI and PSII) in the chloroplasts and activate the generation of reactive oxygen species (ROS), mainly superoxide anion (O2•−), hydrogen peroxide (H2O2), and hydroxyl radicals (OH•). Overproduction of ROS causes oxidative damage to membranes, lipids, proteins, and nucleic acids, which then induces cell death [12]. Plants synthesize proteins and amino acids, together with the accumulation of minerals, to survive stress. Plants alter water relations by inducing osmotic adjustment (OA), which is mediated through the accumulation of low molecular weight solutes such as proline, glycine betaine, sugars, and free amino acids. OA assists with turgor pressure, water content maintenance [13,14] and the recovery of metabolic activities in plants [15,16]. Increased activity of enzymes such as the late embryogenesis abundant (LEA) and ROS detoxifying enzymes, namely, superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), glutathione reductase (GR), and enzymes of the ascorbate-glutathione cycle, are among the most reported biochemical means utilized by plants to prevent oxidative stress and induce tolerance [13,14]. Stress-tolerant plants produce more osmolytes and non-enzymatic antioxidants and express stress-responsive genes to enhance their antioxidant capacity. Although sensitive crops utilize the same mechanisms of stress response, they are unable to grow and produce high yields under intense stress [8]. Thus, the introduction and cultivation of indigenous traditional crops with the potential to grow under a wide range of agro-climatic environments can serve as a solution to overcome food insecurity [17].
Amaranth is an underutilized ancient crop that is diversely distributed in different regions of the world. This crop has gained much attention regarding its potential to combat food and nutrition insecurity. This is due to: (i) its C4 photosynthetic pathway that mediates efficient CO2 fixation, prevents photorespiration, and increases water use efficiency (WUE) under hot and dry conditions, thereby allowing its growth under diverse climatic environments [18,19,20,21], and (ii) a high nutrient content, which is superior to that of most crops [22,23,24,25]. The genus Amaranthus consists of more than 70 species, ranging from pseudo-grain, leafy vegetables, to ornamental and weedy amaranth [26]. Currently, only 17 species are considered vegetable amaranths since their leaves are edible, and only three are categorized as grain amaranths [27]. However, according to Assad et al. [26], the total number of Amaranthus species is still debatable owing to some contradictory findings on genus systematics [26]. A clear understanding of the mechanisms of drought tolerance in Amaranthus species may assist in the classification and identification of drought-tolerant genotypes, and this is crucial for plant breeding programs. Thus, the current review provides a brief description of Amaranthus’s nutritional content and comprehensive insights into the data encompassing the morpho-physiological, biochemical, and molecular drought response traits of grain and vegetable Amaranthus species.

2. Amaranth’s Nutritional Value

Amaranthus is a multipurpose crop supplying high-nutritive-quality grains and leafy vegetables for human consumption and animal feed. Amaranthus seeds have a high protein content of about 17.5–38.3%, with lysine and sulphur-containing amino acids being the most abundant. Lysine is the principal amino acid component, constituting about 5% of the total amino acid content. Such a high lysine content is lacking in other cereal and tuberous crops [28]. The essential amino acid index of 90.4% in amaranth makes it comparable with egg protein and can be used as a meal substitute [28,29]. Furthermore, the amaranth protein is highly digestible since it is gluten-free, making amaranth very suitable for patients with celiac disease. Fresh young amaranth leaves and stems are good sources of iron (66.09 mg/100 g), calcium (336.67 mg/100 g), manganese (26.23 mg/100 g), vitamin A, and vitamin C [30,31]. When dried, the leaves also contain high potassium (54.20 mg/100 g), sodium (7.43 mg/100 g), calcium (44.15 mg/100 g), iron (13.58 mg/100 g), magnesium (231.22 mg/100 g), zinc (3.8 mg/100 g) and phosphorus (34.91 mg/100 g) [31,32]. In comparison to other cereals, the nutrient content of grain amaranth (especially iron and zinc) surpasses that of maize, rice, and wheat [33], further highlighting amaranth as a significant source of these essential minerals to comply with the daily nutritional recommendation. Furthermore, de la Rosa [34] found that leafy amaranth contains an average oil content of 11 to 14%, with high saponification and iodine values. In addition, grain amaranth is a highly nutritious pseudocereal rich in phytochemicals, promoting numerous health benefits, including protection against chronic conditions such as hypertension, diabetes, cancer, and cardiovascular disorders. Amaranth flour contains polyphenols such as flavonoids and phenolic acids with high antioxidant activity [34,35,36,37], making Amaranthus a potential remedy for the treatment of different human disorders [38,39,40]. Despite these attractive traits, grain amaranth remains significantly underutilized as a food and medicinal source worldwide.

3. The Response of Amaranthus Species to Drought Stress

Amaranthus is a special type of crop that can be cultivated on any soil type, including marginal areas in arid and semi-arid regions with poor soil conditions with low moisture. This is possible because Amaranthus requires no special agricultural practice and can tolerate abiotic stresses [19,41,42]. Among the different Amaranthus groups, grain amaranth is more tolerant to drought than leafy vegetable amaranth, which requires day-to-day irrigation to sustain soil moisture. Vegetable amaranth can be harvested at different growth stages, from young seedlings to the late juvenile stage [43]. The first harvest is possible from 25–35 days after sowing and can be achieved by uprooting a whole plant or by repeatedly clipping the growing shoot at 7- to 10-day intervals [19]. For example, A. tricolor is preferably harvested a month after sowing, followed by a second harvest three weeks later from the re-growth of the smallest plants [26]. In Africa, only a few Amaranthus species are cultivated primarily for their young, fresh green leaves. These species are mainly regarded as leafy vegetable amaranth [22]. Grain amaranth is not commonly cultivated in the African region, although it was reported that some farmers from a few African countries, including Zimbabwe, Kenya, Uganda, and Ethiopia, have started its cultivation and distribution [26]. However, the economic value of amaranth is not yet clear as it is not traded formally and is rarely cultivated [42,44].
Understanding the agronomic traits and cultivation practices of Amaranthus is an important step in unveiling the fundamental importance of this crop in developing countries and influencing its global cultivation. The following sections will briefly review studies done on the cultivation of different Amaranthus species in response to water stress, focusing specifically on the morpho-physiological (growth, biomass, relative water content, photosynthetic parameters, and electrolyte leakage (EL)), biochemical (osmolytes, non-enzymatic and enzymatic antioxidants), and molecular traits. Although Amaranthus species are considered drought-tolerant [45], limited water supply may affect their performance [46], either positively (by increasing mineral, nutrient, and antioxidant accumulation in both leaves and seeds) [7] or negatively (by reducing growth and yield). This review will specifically focus on grain Amaranthus species, including Amaranthus hypochondriacus, A. cruentus, and A. caudatus [35] (Figure 2A–C), and leafy vegetable species, including A. tricolor, A. hybridus, and A. dubius, in response to water scarcity.

3.1. Grain Amaranthus Species and Their Response to Drought Stress

Grain amaranths are considered the most important species, as both the leaves and grains are edible and rich in nutrients [47]. They are characterized by fast growth, with an average height of 2 m, a sturdy stem, and an inflorescence that may appear greenish or reddish depending on the presence of betalain [44]. The most cultivated grain species include Amaranthus hypochondriacus (Figure 2A), A. cruentus (Figure 2B), and A. caudatus (Figure 2C). Their fresh leaves can be added to green salad dishes or prepared as a vegetable, whereas the grains, which are rich in bioactive compounds, can be milled into flour for baking bread, cakes, and biscuits [35,36,37,48].

3.1.1. Physiological Traits

While grain Amaranthus species are considered drought-tolerant, several studies reported significant decreases in some physiological traits, such as total performance index (~50%), RWC (~50%), and EL (13.52%) in A. hypochondriacus [12,49,50]. Similarly, in A. cruentus, drought stress negatively affects RWC, gas exchange, WUE, and leaf nitrate levels [5]. Interestingly, A. caudatus maintains an increased WUE, stomatal conductance, carotenoid content, and biomass accumulation under drought stress. These traits might be linked to A. caudatus’s C4 photosynthetic efficiency [51,52,53]. Other interesting traits of A. caudatus under drought are the superior grain yield, diameter, and thickness, which are not affected by low water availability, unlike other grain species [54]. This suggests that A. caudatus shifts its energy towards growth through biomass accumulation and grain maintenance under stress instead of inducing stress tolerance. Stress-induced growth reduction can also be measured by the photosynthesis rate [5]; however, Huerta-Ocampo et al. [50] and Motyleva et al. [55] reported contrary results, shown by high chlorophyll and carotenoid content in A. cruentus under drought stress. This could suggest a possible drought stress response mechanism employed by A. cruentus.

3.1.2. Biochemical Traits

Osmotic adjustment (OA), an important drought tolerance trait, that is influenced by the accumulation of osmolytes in plants under stress conditions, is necessary to maintain leaf turgor [56,57,58]. In grain Amaranthus species, OA was recorded based on average water potential, recovery rates, and osmolyte content. Grain Amaranthus species were reported to exhibit high water potential (−0.23 and −2.80 MPa) and recovery rates (over 90%) for A. hypochondriacus, followed by A. cruentus’s leaf water potential of −0.27 and −4.05 MPa and recovery rates of 60 and 30%. During the same experiment, A. caudatus exhibited the lowest water potential (−0.41 and −8.25 MPa) and recovery rates (0–70%) compared to the other two grain species [12]. Although A. caudatus can be considered the least drought-tolerant grain species based on its low OA, it exhibits better drought tolerance traits when compared with A. hybridus, a leafy vegetable [12]. High OA as a drought tolerance trait in grain Amaranthus species could be linked to high soluble carbohydrate content, including fructose, glucose, and sucrose, soluble non-structural carbohydrates (NSCs), raffinose-family oligosaccharides (RFOs), and proline [5,12,59,60]. Furthermore, inducing the activities of several enzymes such as α-amylase, sucrose synthase and raffinose biosynthesis enzymes in grain Amaranthus spp. under drought can serve as a major driver of OA-mediated drought tolerance [12,56,57,60].
Accumulation of antioxidants is one of the important pathways in stress response and adaptation through ROS scavenging [61], and evidence shows that this pathway is also induced in Amaranthus spp., especially under harsh environmental conditions [62,63,64]. Similar findings were observed in A. hypochondriacus under a 10% Field Capacity (FC) [65]. Drought and heat stress induced the accumulation of total antioxidant capacity (TAC), total flavonoids (TFC), and total phenolic (TPC) compounds in A. caudatus and A. hypochondriacus, and 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging capacity and polyphenols in A. cruentus, representing a high degree of ROS detoxification in Amaranthus species [66]. Several studies reported on high levels of antioxidant compounds in the leaves, stems, flowers, and seeds of A. caudatus, suggesting that it could be a key source of antioxidants among the Amaranthus spp. [38,67,68]. However, a comparative study on the antioxidant content of grain Amaranthus spp. is necessary to confirm these observations.

3.1.3. Molecular Traits

For any species, the availability of the sequenced genome is key to understanding metabolic processes that are based on molecular and genetic responses [69]. Genome sequencing revealed a genome size of 466 Mb, with a diploid chromosome number of 32, coding for at least 24,829 proteins for A. hypochondriacus [70], whereas A. cruentus and A. caudatus share similar genome characteristics, such as a genome of 370.9 Mb (for A. cruentus) and 398 Mb (for A. caudatus) with a haploid chromosome number of 17, coding for 25,477 proteins [71].
The availability of these genomes led to an advancement in understanding stress tolerance mechanisms in Amaranthus. Few studies [50,60] reported on the differential protein expression in the roots of A. hypochondricus, which revealed the upregulation of stress-responsive proteins such as the chloroplast α and β subunits of the chaperonin 60 kDa (Cpn 60α and Cpn 60β), and heat shock protein 70 (HSP70) under drought stress. These studies led to the conclusion that chloroplasts and mitochondria are the main role players in A. hypochondriacus’s adaptation to drought stress [48]. Upregulation of these proteins is relevant to drought stress tolerance, as they play important roles in protecting other proteins from degradation and aid in refolding denatured proteins under normal and stress conditions [72]. Amaranthus hypochondriacus seems to employ coordinated signaling pathways that control growth signals, such as the upregulation of cell growth proteins (tyrosine phosphatases), ROS-scavenging proteins, glutathione S-transferase, HSPs, and RNA-binding proteins (RBPs) [60].
González-Rodríguez, Cisneros-Hernández [12], reported on the differential expression of genes coding for RFO biosynthesis synthases [Amaranthus hypochondicaus Gol synthase 1 and 2 (AhGolS1 and AhGolS2)], raffinose synthase (AhRafS), and Staquiose (Sta) synthase (AhStaS) in grain Amaranthus spp. in both leaves and the roots under moderate (MDS) and severe drought stress (SDS) [12]. RFOs are known for protecting embryos from desiccation and also acting as signaling molecules in response to wounding or pathogen attack [73]. The AhGolS1 and AhRafS transcripts were highly induced in the leaves of all grain spp. under SDS, and this further correlated with the increased accumulation of raffinose. The study further reported a strong expression of AhGolS and AhStaS transcripts in the roots but not in the leaves of both A. hypochondriacus and A. cruentus. This might be due to the tissue-specific roles played by each gene. By contrast, the genes coding proteins involved in trehalose biosynthesis and degradation, including class I and II trehalose phosphate synthase, were downregulated under drought stress in A. hypochondriacus and A. caudatus [12]. Due to the critical role of abscisic acid (ABA) in regulating plant water status, mediated via the guard cells, it is important to also determine the expression profiles of genes involved in ABA-signaling [5]. Huerta-Ocampo et al. reported higher transcript levels of the ABA signaling-related genes, AhDREB2A (transcription factor-encoding gene), AhABI5 (bZIP transcription factor), AhRAB18 (ABA-responsive gene), and AhLEA14 (stress adaptation gene) in the roots of A. hypochondriacus and A. cruentus under drought stress [12]. However, AhDREB2A was strongly expressed in the leaves under MDS [12]. Casique-Arroyo et al. [74] investigated three A. hypochondriacus genotypes, namely Nutrisol (AhNut), India Red (AhIR), and India Green (AhIG), to understand the induction of betacyanin biosynthetic genes under drought stress. The study recorded downregulation of 4,5 DOPA-extradiol-dioxygenase isoforms (AhDODA-2) and cytochrome P-450 R gene (AhCYP76) in the AhNut leaves. However, analysis of the stem showed the induction of AhDODA-1, betanidin 5-O-glucosyltransferase (AhB5-GT), cyclo-DOPA 5-O glucosyltransferase (AhcDOPA5-GT), and AhB5-GI in the drought-stressed genotypes AhNut and AhIG [74]. Furthermore, Palmeros-Suarez et al. showed that the overexpression of A. hypochondriacus Nuclear-factor-Y (NF-Y), a transcription factor, conferred drought stress tolerance in Arabidopsis thaliana, a drought-sensitive model plant [75]. It can be concluded that improved osmotic adjustment and stronger expression of ABA marker genes represent the biochemical and molecular drought response traits in grain Amaranthus spp., particularly A. hypochondriacus (Figure 3).

3.2. Leafy Vegetable Amaranth Species and Their Responses to Drought Stress

Leafy vegetable Amaranthus spp. are among the most important crops, as they remain available during the summer months when other foliage crops may not be readily available [76]. These species are characterized by short plants of approximately 1.5 m in height, large smooth leaves, small auxiliary inflorescences, and succulent stems. Leafy vegetable amaranths are better sources of nutrients, including vitamins, carotenoids, minerals, proteins, and antioxidants, compared to commercially cultivated leafy vegetables such as lettuce and spinach [48,77]. There are several Amaranthus species categorized as leafy vegetables; however, this review will only focus on three main types, namely, A. tricolor (Figure 4A), A. hybridus “smooth pigweed or slim amaranth” (Figure 4B), and A. dubius (Figure 4C), based on the availability of the drought stress data (Figure 4).

3.2.1. Morphological Traits

Moyo et al. [78] studied the impacts of drought stress in A. dubius induced by high-molecular-weight polyethylene glycol (PEG 6000), and revealed a reduction in final germination percentage, mean germination time, germination index, and germination rate index. Ribeiro et al. [79] conducted a comparative study to analyze the response of A. tricolor and A. hybridus to different water levels, including 20% (SDS), 50% (MDS), 80% (low drought stress; LDS), and 100% (control) total available water, at the vegetative growth stage. The study showed that LDS resulted in shorter internodes, more side shoots, and smaller leaves compared to A. hybridus, while no changes were observed in the leaf area of both species. A study by Amma and Rajakshmi [80] also reported that A. tricolor was shorter than A. dubius under progressive drought stress. Similarly, a study by Sarker and Oba [81] proved that A. tricolor biomass can be severely affected under MDS (50% FC) and SDS (25% FC). Jamalluddin et al. [43] screened 44 A. tricolor accessions under drought stress and observed significant decreases in yield and biomass. Similar findings were observed in A. hybridus under greenhouse conditions, wherein drought reduced plant height by 43.18% [82]. Furthermore, Liu and Stützel [83] suggested that the A. tricolor cultivar “Hin Choi” showed better recovery from water stress since the leaf area developed faster and exceeded the height of A. blitum and A. cruentus [84]. Changes in biomass, especially growth reduction, are considered a morphological drought response trait used by vegetable Amaranthus spp. [43] to minimize water loss under drought stress [79].

3.2.2. Physiological Traits

Plant physiological traits are characterized by water relations and photosynthetic parameters. Among the vegetable Amaranthus spp., A. dubius maintained a higher RWC (85.66% under drought vs. 45.41% for control) than A. tricolor (RWC of 72.29% for drought vs. 50.94% for control), whereas in A. hybridus, RWC was reduced by 30% after 10 days of water deprivation [85]. Interestingly, when comparing A. dubius to a grain amaranth (A. cruentus), Ferrarotto [86] reported a 43% decrease in RWC for A. dubius, representing higher water loss compared to grain amaranth. Chlorophyll fluorescence and leaf gas exchange are some of the parameters that are not affected under LDS (80% FC) in A. tricolor, but show significant changes under MDS (50% FC) and SDS (25% FC) [44,81]. Similarly, a 50% reduction in chlorophyll a and chlorophyll b has been recorded under SDS (12.5% WHC) in A. hybridus [87]. By contrast, Matyleva et al. [55] recorded a two-fold increase in chlorophyll and carotenoid content in A. tricolor cv. “Valentina” genotype under moderate/severe drought (30–40% soil moisture content) conditions. Additionally, in A. hybridus, chlorophyll fluorescence parameters, including quantum efficiency, photochemical quenching, and electron transport rate, were significantly reduced under drought stress [79]. Maintaining membrane integrity and stability under drought stress is an important factor for plant stress tolerance. However, the chlorophyll stability index decreased by 70–75% in A. dubius and 50% in A. tricolor, while cell membrane stability decreased by 55–60% in A. dubius and 65–70% in A. tricolor during a 4- to 5-day water stress treatment [80]. Although A. hybridus shows potential to be drought-tolerant [83], its tolerance is lower compared to grain Amaranthus spp. [12] under SDS. Based on the above studies, leaf-to-stem biomass partitioning and low water use are the main mechanisms of drought stress tolerance used by vegetable Amaranthus spp. and could be considered cultivar/genotype-specific. These contrasting results highlight the need to further screen several genotypes under drought stress to fully unveil the physiological mechanisms of drought tolerance in Amaranthus spp. Further research will assist with the identification of genotypes that combine high yield and drought tolerance.

3.2.3. Biochemical Traits

Several studies have been conducted on the biochemical responses of A. tricolor under drought stress, including a study by Sarker and Oba [81], that revealed non-significant accumulation of oxidative stress markers malondialdehyde (MDA) and H2O2, EL, proline and non-enzymatic antioxidants such as carotenoids, ascorbic acid, polyphenols, flavonoids and total antioxidant capacity under LDS (80% FC). The content of these parameters increased gradually under MDS (50% FC) and SDS (25% FC) in A. tricolor cultivars. Leafy vegetable Amaranthus spp. seem to exhibit OA as a mechanism of stress tolerance. This is based on the increased content of osmolytes as recorded in A. hybridus and A. dubius under drought stress, mainly proline in both spp. [82,85,87] and total soluble sugar content in A. hybridus under SDS conditions [85]. There is also evidence of antioxidant signaling in leafy vegetable Amaranthus spp., as reported by Motyleva et al. [55], based on high DPPH radical scavenging capacity and TPC [55] and increased amino acids, reducing sugars and ascorbic acid [88] in A. tricolor under drought stress, whereas in A. dubius, high antioxidant scavenging activities, such as DPPH and 2,2′-azino-bis 3-ethylbenzthiazoline-6-sulfonic acid (ABTS), were recorded under non-stress conditions [39]. Antioxidant enzyme activities of SOD, CAT, and enzymes of the ascorbate-glutathione cycle [GR, monodehydroascorbate reductase (MDHAR), APX and DHAR] were induced in drought-tolerant (VA13) and drought-sensitive (VA15) A. tricolor genotypes. A higher degree of activation was observed in the VA13 genotype [64], except for GPOX activity, which significantly increased in the sensitive VA15 genotype. Enhanced antioxidant enzyme (SOD, CAT and glutathione peroxidase (GPOX)) activities were also recorded in A. hybridus under extreme drought conditions of 12.5% water capacity [39]. Based on these observations, it could be suggested that the antioxidant pathway is one of the main biochemical drought tolerance mechanisms in vegetable amaranth, and this correlates with the low levels of H2O2, MDA and EL as observed in the drought-tolerant A. tricolor genotype (VA13), displaying effective ROS detoxification [64]. Similar observations that show correlations between low ROS and high antioxidants suggest better drought tolerance mechanisms [89,90] and suggest that A. tricolor might represent a higher degree of genetic diversity underlying mechanisms of drought tolerance than other vegetable Amaranthus spp.

3.2.4. Molecular Traits

An advantage to researchers is the complete chloroplast genome sequencing of some vegetable amaranth [91]. The complete chloroplast genome of A. tricolor is 150,027 bp, characterized by 36.6% GC content, and coding for 140 proteins [92]. The complete chloroplast genome of A. hybridus [84], and A. dubius share a similar chloroplast genome of ~150,520–150,709 bp, ~36.56% GC, 130 identified genes, ~86 total protein-coding genes, eight rRNA genes, and 37 tRNA genes [91]. Currently, reports on the molecular response of vegetable amaranth to drought stress remain limited. However, the molecular response of A. hybridus under drought stress has been discussed in a comparative study with grain Amaranthus species, where most studied traits indicated A. hybridus as the most sensitive Amaranthus species (see Section 3.1) [12].
To date, only a few genetic markers, including the maturase K (matk) gene (~1.570 kb chloroplast maturase coding gene, also suggested as the plant barcode), simple-sequence repeats (SSRs), and single-nucleotide polymorphisms (SNP), have been employed in the identification and classification of Amaranthus species [93,94]. A variety of accessions collected from different gene banks, including Vietnam (272), the World Vegetable Center (27), and GRIN (45), were analyzed based on the matk and SSRs markers, which revealed 96.8% constant sites, while 120 accessions were assigned to A. tricolor based on the phylogenetic analysis [93]. Hoshikwa et al. [95] analyzed the genetic diversity among 440 A. tricolor accessions conserved at the World Vegetable Center, USDA, and private gene banks, representing 24 countries, based on genome-wide SNPs developed by the double-digest restriction-site-associated DNA (ddRAD) sequencing method. Briefly, among the 440 A. tricolor accessions, the ddRAD approach detected 5638 high-quality SNPs, using the A. hypochondriacus genome sequence [55]. The results confirmed the genetic diversity among the different A. tricolor accessions collected from different countries, and suggest that some of the accessions might have been incorrectly assigned. The results of this study also pointed to the possibility that China and India might be the hotspots for the ancestral cultivation of A. tricolor cultivars [95]. Great work has been conducted on the diversification of A. tricolor accessions; however, with the current climatic changes and instabilities, to date, a full comprehensive genetic and molecular analysis under drought stress has not been conducted. This gap in the genetic and molecular studies of the vegetable Amaranthus spp. presents an important opportunity for future research in the sustainable cultivation of vegetable amaranths.

4. Conclusions

The main objective of this review was to provide comprehensive insights into the drought response mechanisms of grain and vegetable Amaranthus spp. Generally, plants adapt to stress by adjusting their growth and response traits, which involves integration by various signaling pathways and differs among plant species and genotypes. Grain Amaranthus spp. represents the most studied and highly tolerant Amaranthus spp. to date, as extensively discussed in this review; however, there is still a need to screen different genotypes under drought stress. The proposed mechanism of drought tolerance (Table 1; Figure 3) in grain amaranth is mediated via the ABA signaling pathway, which further signals the expression of stress-responsive genes, such as chaperonin and heat shock proteins, as well as other genes that code for osmolyte and ROS-scavenging enzymes and carbohydrate biosynthesis enzymes, for effective ROS detoxification and osmotic adjustment, thereby inducing tolerance (Figure 3). The proposed mechanism of drought tolerance in vegetable Amaranthus spp., using A. tricolor as an example, is based on biomass partitioning and antioxidant signaling. A. tricolor is the most cultivated and studied vegetable amaranth spp. and, hence, considered the most drought-tolerant among the vegetable Amaranthus spp. that are described in this review. This could mainly be due to the limited research evidence on other vegetable Amaranthus spp. under drought, highlighting the need for extensive biochemical and molecular analysis of A. tricolor and other leafy/vegetable Amaranthus spp. to fill the gaps regarding the agronomic traits of leafy Amaranthus spp. under drought. Previous drought-related studies on these species are largely limited to morphological and physiological assessments such as height, water relations, and biochemical responses based on antioxidant activity; however, molecular analysis, which provides more robust information, has not been fully explored. Thus, bridging the molecular knowledge gap for vegetable amaranth, by taking advantage of the advanced genomics resources available for grain spp., should be a top priority. Furthermore, comprehensive proteomics, transcriptomics, and metabolomics studies on both grain and vegetable amaranths are necessary to uncover drought-responsive traits in these crops, offering promising avenues for plant breeding to enhance drought tolerance in other crops.

Author Contributions

Conceptualization, T.M.; supervision, T.M., I.Z.D., A.R.M., R.F.A. and N.L.; formal analysis, T.M., M.N., A.F. and A.R.M.; resources, T.M.; writing—original draft preparation, T.M., M.N., P.G., A.M.K., V.C.I., N.N. and A.R.M.; writing—review and editing, T.M., A.R.M., A.F., R.F.A., N.L., M.N., V.C.I., N.N. and I.Z.D.; project administration, T.M. and A.R.M.; funding acquisition, T.M. and A.R.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Water Research Commission (WRC; grant No: C2023/2024-01359) and the National Research Foundation of South Africa (NRF; grant No: MND210520602807).

Data Availability Statement

Not applicable.

Acknowledgments

We would like to acknowledge the colleagues at the Department of Biotechnology, UWC, and the Agricultural Research Council, Nietvoorbji, Soil Science Department, for providing the infrastructure for field and greenhouse research.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Aryal, J.P.; Manchanda, N.; Sonobe, T. Expectations for household food security in the coming decades: A global scenario. In Future Foods; Elsevier: Amsterdam, The Netherlands, 2022; pp. 107–131. [Google Scholar]
  2. Grote, U. Can we improve global food security? A socio-economic and political perspective. Food Secur. 2014, 6, 187–200. [Google Scholar] [CrossRef]
  3. Masipa, T. The impact of climate change on food security in South Africa: Current realities and challenges ahead. Jàmbá J. Disaster Risk Stud. 2017, 9, 411. [Google Scholar] [CrossRef]
  4. Van der Merwe, J.D.; Cloete, P.C.; Van der Hoeven, M. Promoting food security through indigenous and traditional food crops. Agroecol. Sustain. Food Syst. 2016, 40, 830–847. [Google Scholar] [CrossRef]
  5. Cechin, I.; da Silva, L.P.; Ferreira, E.T.; Barrochelo, S.C.; de Melo, F.P.d.S.R.; Dokkedal, A.L.; Saldanha, L.L. Physiological responses of Amaranthus cruentus L. to drought stress under sufficient-and deficient-nitrogen conditions. PLoS ONE 2022, 17, e0270849. [Google Scholar] [CrossRef]
  6. Pirasteh-Anosheh, H.; Saed-Moucheshi, A.; Pakniyat, H.; Pessarakli, M. Stomatal responses to drought stress. Water Stress Crop Plants Sustain. Approach 2016, 1, 24–40. [Google Scholar]
  7. Hura, T.; Grzesiak, S.; Hura, K.; Thiemt, E.; Tokarz, K.; Wędzony, M. Physiological and biochemical tools useful in drought-tolerance detection in genotypes of winter triticale: Accumulation of ferulic acid correlates with drought tolerance. Ann. Bot. 2007, 100, 767–775. [Google Scholar] [CrossRef]
  8. Laxa, M.; Liebthal, M.; Telman, W.; Chibani, K.; Dietz, K.-J. The role of the plant antioxidant system in drought tolerance. Antioxidants 2019, 8, 94. [Google Scholar] [CrossRef]
  9. Ahmad, M.; Waraich, E.A.; Shahid, H.; Ahmad, Z.; Zulfiqar, U.; Mahmood, N.; Al-Ashkar, I.; Ditta, A.; El Sabagh, A. Exogenously Applied Potassium Enhanced Morpho-Physiological Growth and Drought Tolerance of Wheat by Alleviating Osmotic Imbalance and Oxidative Damage. Pol. J. Environ. Stud. 2023, 32, 4447–4459. [Google Scholar] [CrossRef]
  10. Kim, K.S.; Park, S.H.; Jenks, M.A. Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. J. Plant Physiol. 2007, 164, 1134–1143. [Google Scholar] [CrossRef] [PubMed]
  11. Shavrukov, Y.; Kurishbayev, A.; Jatayev, S.; Shvidchenko, V.; Zotova, L.; Koekemoer, F.; De Groot, S.; Soole, K.; Langridge, P. Early flowering as a drought escape mechanism in plants: How can it aid wheat production? Front. Plant Sci. 2017, 8, 1950. [Google Scholar] [CrossRef] [PubMed]
  12. González-Rodríguez, T.; Cisneros-Hernández, I.; Acosta Bayona, J.; Ramírez-Chavez, E.; Martínez-Gallardo, N.; Mellado-Mojica, E.; López-Pérez, M.G.; Molina-Torres, J.; Délano-Frier, J. Identification of factors linked to higher water-deficit stress tolerance in Amaranthus hypochondriacus compared to other grain amaranths and A. hybridus, their shared ancestor. Plants 2019, 8, 239. [Google Scholar] [CrossRef]
  13. Aranda-Rivera, A.K.; Cruz-Gregorio, A.; Arancibia-Hernández, Y.L.; Hernández-Cruz, E.Y.; Pedraza-Chaverri, J. RONS and oxidative stress: An overview of basic concepts. Oxygen 2022, 2, 437–478. [Google Scholar] [CrossRef]
  14. Ashraf, M. Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol. Adv. 2009, 27, 84–93. [Google Scholar] [CrossRef]
  15. Lisar, S.; Motafakkerazad, R.; Hossain, M.M.; Rahman, I. Causes, effects and responses. Water Stress 2012, 25, 33. [Google Scholar]
  16. Zivcak, M.; Brestic, M.; Sytar, O. Osmotic adjustment and plant adaptation to drought stress. In Drought Stress Tolerance in Plants, Vol 1: Physiology and Biochemistry; Springer: Cham, Switezerland, 2016; pp. 105–143. [Google Scholar]
  17. Pawlak, K.; Kołodziejczak, M. The role of agriculture in ensuring food security in developing countries: Considerations in the context of the problem of sustainable food production. Sustainability 2020, 12, 5488. [Google Scholar] [CrossRef]
  18. Ebert, A.W. Potential of underutilized traditional vegetables and legume crops to contribute to food and nutritional security, income and more sustainable production systems. Sustainability 2014, 6, 319–335. [Google Scholar] [CrossRef]
  19. Ozeki, K.; Miyazawa, Y.; Sugiura, D. Rapid stomatal closure contributes to higher water use efficiency in major C4 compared to C3 Poaceae crops. Plant Physiol. 2022, 189, 188–203. [Google Scholar] [CrossRef]
  20. Sage, R. C3 versus C4 photosynthesis in rice: Ecophysiological perspectives. In Studies in Plant Science; Elsevier: Amsterdam, The Netherlands, 2000; pp. 13–35. [Google Scholar]
  21. Achigan-Dako, E.G.; Sogbohossou, O.E.; Maundu, P. Current knowledge on Amaranthus spp.: Research avenues for improved nutritional value and yield in leafy amaranths in sub-Saharan Africa. Euphytica 2014, 197, 303–317. [Google Scholar] [CrossRef]
  22. Kunyanga, C.N. Development of a Supplementary Food from Selected Local Food Ingredients to Optimize Nutritional and Sensory Qualities. Ph.D. Thesis, University of Nairobi, Nairobi, Kenya, 2011. [Google Scholar]
  23. Phiarais, B.P.N.; Arendt, E.K. Malting and brewing with gluten-free cereals. In Gluten-Free Cereal Products and Beverages; Elsevier: Amsterdam, The Netherlands, 2008; pp. 347–372. [Google Scholar]
  24. Ruth, O.N.; Unathi, K.; Nomali, N.; Chinsamy, M. Underutilization versus nutritional-nutraceutical potential of the Amaranthus food plant: A mini-review. Appl. Sci. 2021, 11, 6879. [Google Scholar] [CrossRef]
  25. Grubben, G.; Denton, O.A. Plant Resources of Tropical Africa 2. Vegetables. 2004. Available online: https://portals.iucn.org/library/node/28236 (accessed on 30 May 2024).
  26. Assad, R.; Reshi, Z.A.; Jan, S.; Rashid, I. Biology of amaranths. Bot. Rev. 2017, 83, 382–436. [Google Scholar] [CrossRef]
  27. Netshimbupfe, M.H.; Berner, J.; Van Der Kooy, F.; Oladimeji, O.; Gouws, C. The importance and use of Amaranthus for crop diversification in the SADC region. S. Afr. J. Bot. 2023, 152, 192–202. [Google Scholar] [CrossRef]
  28. Poutanen, K.S.; Kårlund, A.O.; Gómez-Gallego, C.; Johansson, D.P.; Scheers, N.M.; Marklinder, I.M.; Eriksen, A.K.; Silventoinen, P.C.; Nordlund, E.; Sozer, N. Grains–a major source of sustainable protein for health. Nutr. Rev. 2022, 80, 1648–1663. [Google Scholar] [CrossRef] [PubMed]
  29. Písaříková, B.; Kráčmar, S.; Herzig, I. Amino acid contents and biological value of protein in various amaranth species. Czech J. Anim. Sci. 2005, 50, 169–174. [Google Scholar] [CrossRef]
  30. Nyonje, W.A. Nutrients, Anti-Nutrients and Phytochemical Evaluation of Ten Vegetable Amaranth (Amaranthus spp.) Varieties at Two Stages of Growth. 2015. Available online: http://ir.jkuat.ac.ke/handle/123456789/1591 (accessed on 15 March 2025).
  31. Muriuki, E.N. Nutritional Diversity of Leafy Amaranth (Amaranthus) Species Grown in Kenya. 2015. Available online: http://ir.jkuat.ac.ke/handle/123456789/1592 (accessed on 15 March 2025).
  32. Rangarajan, A.; Kelly, J.F. 218A further studies exploring iron nutritional quality from amaranthus species. HortScience 1994, 29, 459–467. [Google Scholar] [CrossRef]
  33. Vidal Torres, E.; Valencia, E.; Simsek, S.; Ramírez, A.M.L. Amaranth: Multipurpose agroindustrial crop. Agronomy 2024, 14, 2323. [Google Scholar] [CrossRef]
  34. de la Rosa, A.B.; Fomsgaard, I.S.; Laursen, B.; Mortensen, A.G.; Olvera-Martínez, L.; Silva-Sánchez, C.; Mendoza-Herrera, A.; González-Castañeda, J.; De León-Rodríguez, A. Amaranth (Amaranthus hypochondriacus) as an alternative crop for sustainable food production: Phenolic acids and flavonoids with potential impact on its nutraceutical quality. J. Cereal Sci. 2009, 49, 117–121. [Google Scholar] [CrossRef]
  35. Tetyannikov, N.V.; Motyleva, S.M.; Gins, M.S.; Kozak, N.V.; Panischeva, D.V.; Mertvischeva, M.E.; Kabashnikova, L.F.; Domanskaya, I.N.; Pilipovich, T.S. Drought Effects on Mineral Composition of the Leaves and Seeds of Amaranthus tricolor and Amaranthus cruentus. SABRAO J. Breed. Genet. 2022, 54, 426–436. [Google Scholar] [CrossRef]
  36. Repo-Carrasco-Valencia, R.; Hellström, J.K.; Pihlava, J.-M.; Mattila, P.H. Flavonoids and other phenolic compounds in Andean indigenous grains: Quinoa (Chenopodium quinoa), kañiwa (Chenopodium pallidicaule) and kiwicha (Amaranthus caudatus). Food Chem. 2010, 120, 128–133. [Google Scholar] [CrossRef]
  37. Jimoh, M.; Afolayan, A.; Lewu, F. Therapeutic Uses of Amaranthus caudatus L. Trop. Biomed. 2019, 36, 1038–1053. [Google Scholar]
  38. Li, H.; Deng, Z.; Liu, R.; Zhu, H.; Draves, J.; Marcone, M.; Sun, Y.; Tsao, R. Characterization of phenolics, betacyanins and antioxidant activities of the seed, leaf, sprout, flower and stalk extracts of three Amaranthus species. J. Food Compos. Anal. 2015, 37, 75–81. [Google Scholar] [CrossRef]
  39. Aderibigbe, O.; Ezekiel, O.; Owolade, S.; Korese, J.; Sturm, B.; Hensel, O. Exploring the potentials of underutilized grain amaranth (Amaranthus spp.) along the value chain for food and nutrition security: A review. Crit. Rev. Food Sci. Nutr. 2022, 62, 656–669. [Google Scholar] [CrossRef]
  40. Mekonnen, G.; Woldesenbet, M.; Teshale, T.; Biru, T. Amaranthus caudatus production and nutrition contents for food security and healthy living in Menit Shasha, Menit Goldya and Maji Districts of Bench Maji Zone, South Western Ethiopia. Nutr. Food Sci. Int. J. 2018, 7, 23–30. [Google Scholar]
  41. Shukla, S.; Bhargava, A.; Chatterjee, A.; Pandey, A.C.; Mishra, B.K. Diversity in phenotypic and nutritional traits in vegetable amaranth (Amaranthus tricolor), a nutritionally underutilised crop. J. Sci. Food Agric. 2010, 90, 139–144. [Google Scholar] [CrossRef]
  42. Das, S.; Das, S. Amaranths: The crop of great prospect. In Amaranthus: A Promising Crop of Future; Springer: Dordrecht, The Netherlands, 2016; pp. 13–48. [Google Scholar]
  43. Jamalluddin, N.; Massawe, F.J.; Mayes, S.; Ho, W.K.; Singh, A.; Symonds, R.C. Physiological Screening for Drought Tolerance Traits in Vegetable Amaranth (Amaranthus tricolor) Germplasm. Agriculture 2021, 11, 994. [Google Scholar] [CrossRef]
  44. Emmanuel, O.C.; Babalola, O.O. Amaranth production and consumption in South Africa: The challenges of sustainability for food and nutrition security. Int. J. Agric. Sustain. 2022, 20, 449–460. [Google Scholar] [CrossRef]
  45. Van Rensburg, W.J.; Van Averbeke, W.; Slabbert, R.; Faber, M.; Van Jaarsveld, P.; Van Heerden, I.; Wenhold, F.; Oelofse, A. African leafy vegetables in South Africa. Water SA 2007, 33, 317–326. [Google Scholar] [CrossRef]
  46. Liu, F.; Stützel, H. Leaf water relations of vegetable amaranth (Amaranthus spp.) in response to soil drying. Eur. J. Agron. 2002, 16, 137–150. [Google Scholar] [CrossRef]
  47. Bang, J.-H.; Lee, K.J.; Jeong, W.T.; Han, S.; Jo, I.-H.; Choi, S.H.; Cho, H.; Hyun, T.K.; Sung, J.; Lee, J. Antioxidant activity and phytochemical content of nine Amaranthus species. Agronomy 2021, 11, 1032. [Google Scholar] [CrossRef]
  48. Rastogi, A.; Shukla, S. Amaranth: A new millennium crop of nutraceutical values. Crit. Rev. Food Sci. Nutr. 2013, 53, 109–125. [Google Scholar] [CrossRef]
  49. Gamboa, A.; Valenzuela, E.; Murillo, E. Biochemical changes due to water loss in leaves of Amaranthus hypochondriacus L. J. Plant Physiol. 1991, 137, 586–590. [Google Scholar] [CrossRef]
  50. Huerta-Ocampo, J.A.; Briones-Cerecero, E.P.; Mendoza-Hernandez, G.; De Leon-Rodriguez, A.; Barba de la Rosa, A.P. Proteomic analysis of amaranth (Amaranthus hypochondriacus L.) leaves under drought stress. Int. J. Plant Sci. 2009, 170, 990–998. [Google Scholar] [CrossRef]
  51. Gimplinger, D.; Dobos, G.; Kaul, H.-P. Optimum crop densities for potential yield and harvestable yield of grain amaranth are conflicting. Eur. J. Agron. 2008, 28, 119–125. [Google Scholar] [CrossRef]
  52. Pulvento, C.; Sellami, M.H.; Lavini, A. Yield and quality of Amaranthus hypochondriacus grain amaranth under drought and salinity at various phenological stages in southern Italy. J. Sci. Food Agric. 2022, 102, 5022–5033. [Google Scholar] [CrossRef]
  53. Pulvento, C.; Riccardi, M.; Lavini, A.; d’Andria, R.; Ragab, R. Parameterization and field validation of SALTMED Model for grain amaranth tested in South Italy. Irrig. Drain. 2015, 64, 59–68. [Google Scholar] [CrossRef]
  54. Valdayskikh, V.; Voronin, P.Y.; Artemyeva, E.; Rymar, V. Amaranth responses to experimental soil drought. AIP Conf. Proc. 2019, 2063, 030023. [Google Scholar] [CrossRef]
  55. Motyleva, S.; Gins, M.; Kabashnikova, L.; Kozak, N.; Tetyannikov, N.; Panischeva, D.; Mertvischeva, M.; Domanskaya, I.; Pilipovich, T. Drought effects on the physiological and biochemical parameters of amaranth (C-3) and actinidia (C-4) plants. SABRAO J. Breed. Genet. 2021, 53, 248–262. [Google Scholar]
  56. Ozturk, M.; Turkyilmaz Unal, B.; García-Caparrós, P.; Khursheed, A.; Gul, A.; Hasanuzzaman, M. Osmoregulation and its actions during the drought stress in plants. Physiol. Plant. 2021, 172, 1321–1335. [Google Scholar] [CrossRef] [PubMed]
  57. Sánchez, F.J.; Manzanares, M.a.; de Andres, E.F.; Tenorio, J.L.; Ayerbe, L. Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crops Res. 1998, 59, 225–235. [Google Scholar]
  58. Zahoor, R.; Zhao, W.; Abid, M.; Dong, H.; Zhou, Z. Potassium application regulates nitrogen metabolism and osmotic adjustment in cotton (Gossypium hirsutum L.) functional leaf under drought stress. J. Plant Physiol. 2017, 215, 30–38. [Google Scholar] [CrossRef]
  59. Farshbaf-Jafari, S.; Pirzad, A.; Tajbakhsh, M.; Ghassemi-Golezani, K. Effects of water supply and plant density on leaf characteristics of Amaranth (Amaranthus caudatus L.). In Proceedings of the 2nd International Conference on Sustainable Environment and Agriculture IPCBEE, San Diego, CA, USA, 29–30 October 2014. [Google Scholar]
  60. Huerta-Ocampo, J.; León-Galván, M.; Ortega-Cruz, L.; Barrera-Pacheco, A.; De León-Rodríguez, A.; Mendoza-Hernández, G.; Barba De La Rosa, A. Water stress induces up-regulation of DOF1 and MIF1 transcription factors and down-regulation of proteins involved in secondary metabolism in amaranth roots (Amaranthus hypochondriacus L.). Plant Biol. 2011, 13, 472–482. [Google Scholar] [CrossRef] [PubMed]
  61. Wang, J.; Yuan, X.; Jin, Z.; Tian, Y.; Song, H. Free radical and reactive oxygen species scavenging activities of peanut skins extract. Food Chem. 2007, 104, 242–250. [Google Scholar] [CrossRef]
  62. Khanam, U.K.S.; Oba, S. Bioactive substances in leaves of two amaranth species, Amaranthus tricolor and A. hypochondriacus. Can. J. Plant Sci. 2013, 93, 47–58. [Google Scholar] [CrossRef]
  63. Sarker, U.; Islam, M.T.; Rabbani, M.G.; Oba, S. Genotypic diversity in vegetable amaranth for antioxidant, nutrient and agronomic traits. Indian J. Genet. Plant Breed. 2017, 77, 173–176. [Google Scholar] [CrossRef]
  64. Sarker, U.; Oba, S. Drought stress effects on growth, ROS markers, compatible solutes, phenolics, flavonoids, and antioxidant activity in Amaranthus tricolor. Appl. Biochem. Biotechnol. 2018, 186, 999–1016. [Google Scholar] [CrossRef] [PubMed]
  65. Kumar, S.; Jena, P.K.; Tripathy, P.K. Study of wild edible plants among tribal groups of Simlipal Biosphere Reserve Forest, Odisha, India; with special reference to Dioscorea species. Int. J. Biol. Technol. 2012, 3, 11–19. [Google Scholar]
  66. Netshimbupfe, M.H.; Berner, J.; Gouws, C. The interactive effects of drought and heat stress on photosynthetic efficiency and biochemical defense mechanisms of Amaranthus species. Plant Environ. Interact. 2022, 3, 212–225. [Google Scholar] [CrossRef]
  67. Karamać, M.; Gai, F.; Longato, E.; Meineri, G.; Janiak, M.A.; Amarowicz, R.; Peiretti, P.G. Antioxidant activity and phenolic composition of amaranth (Amaranthus caudatus) during plant growth. Antioxidants 2019, 8, 173. [Google Scholar] [CrossRef]
  68. López-Mejía, O.A.; López-Malo, A.; Palou, E. Antioxidant capacity of extracts from amaranth (Amaranthus hypochondriacus L.) seeds or leaves. Ind. Crops Prod. 2014, 53, 55–59. [Google Scholar] [CrossRef]
  69. Kersey, P.J.; Collemare, J.; Cockel, C.; Das, D.; Dulloo, E.M.; Kelly, L.J.; Lettice, E.; Malécot, V.; Maxted, N.; Metheringham, C. Selecting for useful properties of plants and fungi–Novel approaches, opportunities, and challenges. Plants People Planet. 2020, 2, 409–420. [Google Scholar] [CrossRef]
  70. Sunil, M.; Hariharan, A.K.; Nayak, S.; Gupta, S.; Nambisan, S.R.; Gupta, R.P.; Panda, B.; Choudhary, B.; Srinivasan, S. The draft genome and transcriptome of Amaranthus hypochondriacus: A C4 dicot producing high-lysine edible pseudo-cereal. DNA Res. 2014, 21, 585–602. [Google Scholar] [CrossRef]
  71. Ma, X.; Vaistij, F.E.; Li, Y.; Jansen van Rensburg, W.S.; Harvey, S.; Bairu, M.W.; Venter, S.L.; Mavengahama, S.; Ning, Z.; Graham, I.A. A chromosome-level Amaranthus cruentus genome assembly highlights gene family evolution and biosynthetic gene clusters that may underpin the nutritional value of this traditional crop. Plant J. 2021, 107, 613–628. [Google Scholar] [CrossRef]
  72. Clerico, E.M.; Meng, W.; Pozhidaeva, A.; Bhasne, K.; Petridis, C.; Gierasch, L.M. Hsp70 molecular chaperones: Multifunctional allosteric holding and unfolding machines. Biochem. J. 2019, 476, 1653–1677. [Google Scholar] [CrossRef] [PubMed]
  73. Sengupta, S.; Mukherjee, S.; Basak, P.; Majumder, A.L. Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front. Plant Sci. 2015, 6, 656. [Google Scholar] [CrossRef] [PubMed]
  74. Casique-Arroyo, G.; Martinez-Gallardo, N.; Gonzalez de la Vara, L.; Delano-Frier, J.P. Betacyanin biosynthetic genes and enzymes are differentially induced by (a) biotic stress in Amaranthus hypochondriacus. PLoS ONE 2014, 9, e99012. [Google Scholar] [CrossRef]
  75. Palmeros-Suarez, P.A.; Massange-Sanchez, J.A.; Martinez-Gallardo, N.A.; Montero-Vargas, J.M.; Gomez-Leyva, J.F.; Delano-Frier, J.P. The overexpression of an Amaranthus hypochondriacus NF-YC gene modifies growth and confers water deficit stress resistance in Arabidopsis. Plant Sci. 2015, 240, 25–40. [Google Scholar] [CrossRef]
  76. Shukla, S.; Bhargava, A.; Chatterjee, A.; Srivastava, A.; Singh, S. Genotypic variability in vegetable amaranth (Amaranthus tricolor L for foliage yield and its contributing traits over successive cuttings and years. Euphytica 2006, 151, 103–110. [Google Scholar] [CrossRef]
  77. Jiménez-Aguilar, D.M.; Grusak, M.A. Minerals, vitamin C, phenolics, flavonoids and antioxidant activity of Amaranthus leafy vegetables. J. Food Compos. Anal. 2017, 58, 33–39. [Google Scholar] [CrossRef]
  78. Moyo, M.; Amoo, S.O.; Van Staden, J. Aqueous smoke and karrikin influence seed germination of Amaranthus dubius in varying light, temperature and osmotic stress conditions. S. Afr. J. Bot. 2022, 148, 704–709. [Google Scholar] [CrossRef]
  79. Ribeiro, J.E.M.M.; Pieterse, P.J.; Famba, S.I. Vegetative growth of Amaranthus hybridus and Amaranthus tricolor under different watering regimes in different seasons in southern Mozambique. S. Afr. J. Plant Soil. 2017, 34, 201–210. [Google Scholar] [CrossRef]
  80. Amma, C.S.; Rajalakshmi, R. Morphological and Physiological Responses in Red Amaranthus (Amaranthus tricolor L.) and Green Amaranthus (Amaranthus dubius Mart. ex Thell.) Under Progressive Water Stress. Asian J. Biol. Life Sci. 2023, 12, 61. [Google Scholar] [CrossRef]
  81. Sarker, U.; Oba, S. Catalase, superoxide dismutase and ascorbate-glutathione cycle enzymes confer drought tolerance of Amaranthus tricolor. Sci. Rep. 2018, 8, 16496. [Google Scholar] [CrossRef]
  82. Manyatsi, A.M.; Masarirambi, M.T.; Hachigonta, S. Southern African Agriculture and Climate Change: A Comprehensive Analysis-Swaziland. 2012. Available online: https://cgspace.cgiar.org/server/api/core/bitstreams/93f8681a-a04b-4387-a2fe-2b1b39c45355/content (accessed on 8 June 2024).
  83. Liu, F.; Stützel, H. Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to drought stress. Sci. Hortic. 2004, 102, 15–27. [Google Scholar] [CrossRef]
  84. Bai, X.; Ye, X.; Luo, Y.; Liu, C.; Wu, Q. Characterization of the first complete chloroplast genome of Amaranthus hybridus (Caryophyllales: Amaranthaceae) with phylogenetic implications. Mitochondrial DNA B Resour. 2021, 6, 3306–3308. [Google Scholar] [CrossRef] [PubMed]
  85. Vargas-Ortiz, E.; Ramírez-Tobias, H.M.; González-Escobar, J.L.; Gutierrez-Garcia, A.K.; Bojorquez-Velazquez, E.; Espitia-Rangel, E.; de la Rosa, A.P.B. Biomass, chlorophyll fluorescence, and osmoregulation traits let differentiation of wild and cultivated Amaranthus under water stress. J. Photochem. Photobiol. B Biol. 2021, 220, 112210. [Google Scholar] [CrossRef]
  86. Ferrarotto, S. Proline accumulation in pigweed plants (Amaranthus dubius Mart, and Amaranthus cruentus L.) growing under water stress conditions. Rev. Fac. Agron. 2003, 20, 453–460. [Google Scholar]
  87. Asadollahzadeh, M.; Rezvani, M.; Zaefarian, F.; Mobasser, H. Physiological Modifications and Enzymatic Defense System of Amaranthus blitoides S. Watson and Amaranthus hybridus L. in Response to Water Deficit Stress. Russ. J. Plant Physiol. 2023, 70, 106. [Google Scholar] [CrossRef]
  88. Chatti, D. Physiological and Molecular Analyses of Drought Tolerance Responses in Amaranthus (Amaranthus tricolor L.) under Elevated Carbon Dioxide Environments. Chem. Sci. Rev. Lett. 2017, 6, 2025–2031. [Google Scholar]
  89. Gill, S.S.; Tuteja, N. Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 2010, 5, 26–33. [Google Scholar] [CrossRef] [PubMed]
  90. Zhou, R.; Kong, L.; Yu, X.; Ottosen, C.-O.; Zhao, T.; Jiang, F.; Wu, Z. Oxidative damage and antioxidant mechanism in tomatoes responding to drought and heat stress. Acta Physiol. Plant. 2019, 41, 20. [Google Scholar] [CrossRef]
  91. Xu, X.Y.; Yan, J.; Li, H.R.; Feng, Y.Q.; Qi, Z.C.; Yan, X.L. The complete chloroplast genome sequence of spleen amaranth (Amaranthus dubius Mart. ex Thell., Amaranthaceae). Mitochondrial DNA B Resour. 2021, 6, 3267–3268. [Google Scholar] [CrossRef] [PubMed]
  92. Viljoen, E.; Odeny, D.A.; Coetzee, M.P.; Berger, D.K.; Rees, D.J. Application of chloroplast phylogenomics to resolve species relationships within the plant genus Amaranthus. J. Mol. Evol. 2018, 86, 216–239. [Google Scholar] [CrossRef] [PubMed]
  93. Nguyen, D.C.; Tran, D.S.; Tran, T.T.H.; Ohsawa, R.; Yoshioka, Y. Genetic diversity of leafy amaranth (Amaranthus tricolor L.) resources in Vietnam. Breed. Sci. 2019, 69, 640–650. [Google Scholar] [CrossRef] [PubMed]
  94. Lee, J.-R.; Hong, G.-Y.; Dixit, A.; Chung, J.-W.; Ma, K.-H.; Lee, J.-H.; Kang, H.-K.; Cho, Y.-H.; Gwag, J.-G.; Park, Y.-J. Characterization of microsatellite loci developed for Amaranthus hypochondriacus and their cross-amplifications in wild species. Conserv. Genet. 2008, 9, 243–246. [Google Scholar] [CrossRef]
  95. Hoshikawa, K.; Lin, Y.-P.; Schafleitner, R.; Shirasawa, K.; Isobe, S.; Nguyen, D.C.; Ohsawa, R.; Yoshioka, Y. Genetic diversity analysis and core collection construction for Amaranthus tricolor germplasm based on genome-wide single-nucleotide polymorphisms. Sci. Hortic. 2023, 307, 111428. [Google Scholar] [CrossRef]
Horticulturae 11 01226 g001
Figure 1. Plant response to drought stress changes at the morphological, physiological, biochemical, and molecular levels. ABA = abscisic acid, ABTS = 2,2′-azino-bis 3-ethylbenzthiazoline-6-sulfonic acid; APX = ascorbate peroxidase; CAT = catalase; CO2 = carbon dioxide; DPPH = 2,2-diphenyl-1-picrylhydrazyl; GPX = glutathione peroxidase; GR = glutathione reductase; LEA = late embryogenesis abundant protein; ROS = reactive oxygen species; RWC = relative water content; SOD = superoxide dismutase; WUE = water use efficiency.
Figure 1. Plant response to drought stress changes at the morphological, physiological, biochemical, and molecular levels. ABA = abscisic acid, ABTS = 2,2′-azino-bis 3-ethylbenzthiazoline-6-sulfonic acid; APX = ascorbate peroxidase; CAT = catalase; CO2 = carbon dioxide; DPPH = 2,2-diphenyl-1-picrylhydrazyl; GPX = glutathione peroxidase; GR = glutathione reductase; LEA = late embryogenesis abundant protein; ROS = reactive oxygen species; RWC = relative water content; SOD = superoxide dismutase; WUE = water use efficiency.
Horticulturae 11 01226 g001
Horticulturae 11 01226 g002
Figure 2. Grain Amaranthus species. Amaranthus hypochondriacus (A), Amaranthus cruentus (B), Amaranthus caudatus (C). [Pictures were taken by Mulisa Nkuna at the Agricultural Research Council, Infruitec-Nietvoorbji, South Africa, using a Canon camera (Canon Inc., Japan, EOS 2000D-EF–S 18–55 IS II Kit), purchased from Game store, South Africa].
Figure 2. Grain Amaranthus species. Amaranthus hypochondriacus (A), Amaranthus cruentus (B), Amaranthus caudatus (C). [Pictures were taken by Mulisa Nkuna at the Agricultural Research Council, Infruitec-Nietvoorbji, South Africa, using a Canon camera (Canon Inc., Japan, EOS 2000D-EF–S 18–55 IS II Kit), purchased from Game store, South Africa].
Horticulturae 11 01226 g002
Horticulturae 11 01226 g003
Figure 3. A proposed mechanism of Amaranthus drought stress tolerance. Drought stress ROS = induce osmotic stress and reduce osmolytes such as amino acids (proline) and soluble carbohydrates (structural and non-structural), both contributing to osmotic adjustment. In parallel, under ROS-induced oxidative stress, antioxidant signaling is activated, including both non-enzymatic antioxidants—such as total antioxidant capacity (TAC), total flavonoid content (TFC), and total phenolic content (TPC)—and enzymatic antioxidants, such as ascorbate peroxidase (APX), catalase (CAT), monodehydroascorbate reductase (MDHAR), and superoxide dismutase (SOD), thereby enhancing antioxidant capacity and ROS scavenging. As the molecular drought stress response activates transcription factors such as abscisic acid (ABA)-responsive, basic leucine zipper (bZIP), DNA-binding one finger (DOF), dehydration-responsive element binding (DREB), and mini zinc finger 1 (MF1) regulate downstream gene expression. The encoded genes include ABA and drought-responsive genes, raffinose family oligosaccharides, chaperones, RNA-binding proteins, and ROS-scavenging genes. Solid and dotted blue arrow indicate direct and indirect regulation, respectively, while solid red arrow indicates induced expression. [Amaranthus picture was taken by Mulisa Nkuna at the Agricultural Research Council, Infruitec-Nietvoorbji, South Africa, using a Canon EOS 2000D].
Figure 3. A proposed mechanism of Amaranthus drought stress tolerance. Drought stress ROS = induce osmotic stress and reduce osmolytes such as amino acids (proline) and soluble carbohydrates (structural and non-structural), both contributing to osmotic adjustment. In parallel, under ROS-induced oxidative stress, antioxidant signaling is activated, including both non-enzymatic antioxidants—such as total antioxidant capacity (TAC), total flavonoid content (TFC), and total phenolic content (TPC)—and enzymatic antioxidants, such as ascorbate peroxidase (APX), catalase (CAT), monodehydroascorbate reductase (MDHAR), and superoxide dismutase (SOD), thereby enhancing antioxidant capacity and ROS scavenging. As the molecular drought stress response activates transcription factors such as abscisic acid (ABA)-responsive, basic leucine zipper (bZIP), DNA-binding one finger (DOF), dehydration-responsive element binding (DREB), and mini zinc finger 1 (MF1) regulate downstream gene expression. The encoded genes include ABA and drought-responsive genes, raffinose family oligosaccharides, chaperones, RNA-binding proteins, and ROS-scavenging genes. Solid and dotted blue arrow indicate direct and indirect regulation, respectively, while solid red arrow indicates induced expression. [Amaranthus picture was taken by Mulisa Nkuna at the Agricultural Research Council, Infruitec-Nietvoorbji, South Africa, using a Canon EOS 2000D].
Horticulturae 11 01226 g003
Horticulturae 11 01226 g004
Figure 4. Leafy vegetable Amaranthus species. Amaranthus tricolor (A), Amaranthus hybridus (B), Amaranthus dubius (C). [Pictures were taken by Mulisa Nkuna at the Agricultural Research Council, Infruitec-Nietvoorbji, South Africa, using a Canon camera (Canon Inc., Japan, EOS 2000D-EF–S 18–55 IS II Kit), purchased from Game store, South Africa].
Figure 4. Leafy vegetable Amaranthus species. Amaranthus tricolor (A), Amaranthus hybridus (B), Amaranthus dubius (C). [Pictures were taken by Mulisa Nkuna at the Agricultural Research Council, Infruitec-Nietvoorbji, South Africa, using a Canon camera (Canon Inc., Japan, EOS 2000D-EF–S 18–55 IS II Kit), purchased from Game store, South Africa].
Horticulturae 11 01226 g004
Table 1. A summary of drought response traits in Amaranthus species.
Table 1. A summary of drought response traits in Amaranthus species.
SpeciesMorphological and PhysiologicalBiochemicalMolecular
Grain amaranth
A.
hypochondriacus		Decrease in total performance index, RWC and EL [49,50,66]Accumulation of osmolytes:
1. Proline.
2. Total soluble sugars, soluble non-structural carbohydrates and raffinose-family oligosaccharides [12,66,69].
3. Increase in non-enzymatic antioxidants content (i.e., TAC, TPC and TFC) [69].		Upregulation of stress-responsive genes:
1. Chaperonin 60 kDa (Cpn 60α and Cpn 60β) and heat shock protein 70 (Hsp70) [66].
2. Cell growth genes.
3. ROS-scavenging proteins.
4. RNA-binding proteins [12]
DODA-1, B5-GT, cDOPA5-GT and B5-GI [75].
5. ABA signalling genes (DREB2A (transcription factor-encoding gene), ABI5 (bZIP transcription factor) and AhRAB18 (ABA-responsive gene) and stress adaptation genes [60].
6. Upregulation of RFO biosynthesis genes; Gol Synthase 1 (GolS1), genes involved in trehalose synthesis and degradation (TPS11), drought-responsive genes; LEA14 [12].
A. cruentusImproved leaf water potential, RWC, gas exchange, WUE, and leaf nitrate levels [49].
Increase in photosynthetic pigments such as chlorophyll and carotenoid content.		Increase in proline, soluble carbohydrates, starch, and sucrose synthase activity.
Induction of non-enzymatic antioxidants, DPPH scavenging capacity, and polyphenols.
Expression of RFO biosynthesis genes, Rafs synthase and Staquiose synthase genes in the leaves and in the roots. Upregulation of drought-responsive genes (GolS1, LEA14) [49].
A. caudatusIncrease in stomatal conductance and carotenoids.Increase in soluble carbohydrates and proline content. Increase in alpha-amylase activities, verbascose and starch content [49].
Induction of non-enzymatic antioxidants and total antioxidant capacity (DPPH).		Expression of RFO biosynthesis genes in both leaves and roots; upregulation of drought-responsive genes (GolS1, LEA14) and genes involved in trehalose synthesis and degradation (TPS11) [49].
Vegetable amaranth
A. tricolorReduced internodes, leaf size, leaf area, total plant biomass, chlorophyll fluorescence and leaf gas exchange.Increased accumulation of oxidative stress markers (MDA and H2O2), EL, proline, non-enzymatic antioxidants such as polyphenols, carotenoids, ascorbic acid, flavonoids and DPPH scavenging capacity [65,69,88].N/A
A. hybridusReduced plant height, leaf number, leaf area [79], RWC [64], chlorophyll fluorescence and electron transport [42,64].Increased accumulation of osmolytes (proline and non-structural carbohydrates (glucose, fructose and sucrose).
Improved enzymatic activity, antioxidants, and amylase [81].		Upregulation of drought-responsive genes (GolS1, LEA14) and genes involved in trehalose synthesis and degradation (TPS11)
A. dubiusReduced germination, growth rate, and chlorophyll stability index.
High RWC and cell membrane stability.		Increased proline content [80].N/A
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Nkuna, M.; Gavhi, P.; Kanyerere, A.M.; Ikebudu, V.C.; Ndou, N.; Faro, A.; Doumbia, I.Z.; Ajayi, R.F.; Mulidzi, A.R.; Lewu, N.; et al. Drought Tolerance Mechanisms in Grain and Vegetable Amaranthus Species: Physiological, Biochemical and Molecular Insights. Horticulturae 2025, 11, 1226. https://doi.org/10.3390/horticulturae11101226

AMA Style

Nkuna M, Gavhi P, Kanyerere AM, Ikebudu VC, Ndou N, Faro A, Doumbia IZ, Ajayi RF, Mulidzi AR, Lewu N, et al. Drought Tolerance Mechanisms in Grain and Vegetable Amaranthus Species: Physiological, Biochemical and Molecular Insights. Horticulturae. 2025; 11(10):1226. https://doi.org/10.3390/horticulturae11101226

Chicago/Turabian Style

Nkuna, Mulisa, Pfunzo Gavhi, Alice Mwanjiwa Kanyerere, Vivian Chigozie Ikebudu, Nzumbululo Ndou, Andrew Faro, Ibrahima Zan Doumbia, Rachel Fanelwa Ajayi, Azwimbavhi Reckson Mulidzi, Nike Lewu, and et al. 2025. "Drought Tolerance Mechanisms in Grain and Vegetable Amaranthus Species: Physiological, Biochemical and Molecular Insights" Horticulturae 11, no. 10: 1226. https://doi.org/10.3390/horticulturae11101226

APA Style

Nkuna, M., Gavhi, P., Kanyerere, A. M., Ikebudu, V. C., Ndou, N., Faro, A., Doumbia, I. Z., Ajayi, R. F., Mulidzi, A. R., Lewu, N., & Mulaudzi, T. (2025). Drought Tolerance Mechanisms in Grain and Vegetable Amaranthus Species: Physiological, Biochemical and Molecular Insights. Horticulturae, 11(10), 1226. https://doi.org/10.3390/horticulturae11101226

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop