Commercial Cultivation of Edible Halophytes: The Issue of Oxalates and Potential Mitigation Options

Abstract

Saline agriculture, including the commercial cultivation of edible halophytes, is expanding rapidly to address the increase in salinised soil due to natural and man-made causes, the decline in availability of fresh water, the increased use of poor-quality water, and increasing food insecurity. Halophytes, as food crops, offer an innovative new opportunity in agriculture, many being highly nutritious and containing bioactive compounds. However, the commercial production of edible halophytes to meet emerging consumer demands faces several challenges. This review examines the market potential for the expansion of edible halophyte crops and the challenges of consumer acceptance and production capacity beyond wild harvest. In addition to beneficial compounds, halophytes are known to contain several anti-nutrient compounds, which can have negative health consequences. In edible halophytes, oxalates are of particular concern. However, research has shown that there are ways to mitigate the accumulation of oxalate through processing, agronomic practice, and genetic engineering. These approaches are presented as potential strategies that can be used in commercial farming systems to reduce the levels of this compound.

1. Introduction

As our world population continues to grow, with projections it will reach 9.7 billion by 2050 [1], there will be an increased demand for the calories, proteins, fats, and nutrients people need from a plant-based diet that will not be met through the cultivation of traditional agricultural crops. Conservative estimates forecast only an increase of up to 1.5% in annual crop yield; this amount is not sufficient to meet the requirements of a growing population [2]. It is estimated that about 30% of the world population already experience moderate or severe food insecurity [1], and this number will continue to increase with the threat of climate-change-driven land degradation, which will have negative consequences for agricultural productivity.

Land degradation can result from either environmental or human-induced processes, and it includes soil salinisation, which occurs through the use of poor-quality irrigation water, coastal seawater inundation, and rising water tables [3,4]. The loss of agricultural productivity globally due to salinisation is a significant environmental and economic problem, with conservative estimates suggesting that up to 1.5 million ha of farmland is taken out of production each year, while another 50 million ha shows decreased productivity [5]. This represents a projected annual income loss in the order of USD 27.3 billion based solely on lost crop yields, not considering either environmental or social costs [6]. While there has been some progress made towards processes that would remediate salinised soils, including chemical remediation, physical remediation, and remediation using microbes [7,8], these are all extremely costly processes and unlikely to succeed considering the magnitude of the scale needed.

The exploitation of highly salt-tolerant plants, those classified as halophytes, is a focus for use in saline agriculture. Much of the focus has been on testing salt-tolerant varieties, or wild relatives of traditional crop species [9]. However, in most cases, these do not have the level of salt tolerance needed to grow successfully in the degraded environment or withstand the use of saline irrigation water. Progress in engineering more salt-tolerant varieties of conventional crops has also had limited success due to the complex nature of tolerance with multiple genes involved [10].

Because of this, the focus has moved towards exploiting highly salt-tolerant plants, those classified as halophytes—“salt loving”—for use in saline agriculture. According to Flowers and Colmer [11], halophytes are plants that can complete their lifecycle at a salt concentration of 200 mM NaCl or higher. This represents approximately 350 species across multiple orders, accounting for approximately 0.25% of all angiosperms. A more conservative definition, based on less severe salt levels, can be found in the eHALOPH database (https://www.sussex.ac.uk/affiliates/halophytes/index.php, accessed on 7 November 2023), where 80 mM NaCl, equivalent to a conductivity of 7.8 dS m⁻¹, was used as the defining tolerance level [12]. This results in a list of approximately 1560 plant species being classified as halophytes, including both monocots and dicots [3]. While halophytes have promising uses as oils, biofuels, and animal fodder [13], there is also a growing industry using halophytes as food, primarily for the high-end gourmet market for wild collected plants. However, there is considerable opportunity to develop these crops for a wider consumption using degraded agricultural land [14]. The exploitation of endemic edible halophytes for saline agriculture allows for developing local or regional food crops to feed people most at risk for food insecurity in regions where land degradation is severe. Halophytes have been consumed by humans for centuries [13] and have long had a place in the traditional diets of indigenous peoples around the world [14]. A range of halophytes from the families Amarathaceae, Apiaceae, Asteraceae, Brassicaceae, Capparaceae, Chenopodiaceae, Plantaginaceae, Portulacaceae, and Zygophyllaceae have traditionally been consumed [15].

The demand for edible halophytes in specialty markets is partially owing to the natural salty flavour of halophytes due to their salt (NaCl) accumulation in the aerial parts of the plant, and as many have succulent leaves, this gives them a pleasant light and crispy texture [16]. However, the increasing interest in edible halophytes as high-value food crops is also due to the modern awareness of a healthier diet and their nutritional value, with many showing a high content of bioactive compounds [13,14,17].

While edible halophytes remain a key part of traditional diets in some regions [18], commercial production of edible halophytes to meet emerging consumer demands faces several challenges. This review examines the market potential for the expansion of edible halophyte crops and the challenges of consumer acceptance and production capacity beyond wild harvest, with a focus on oxalate levels and potential mitigation options in commercial farming systems.

2. Edible Halophytes: Costs and Emerging Market Demand

Halophytes offer an innovative new market opportunity in agriculture; however, analysis of the economic potential of saline-degraded lands for food production is complex and needs to balance both the cost of saline land degradation and the added value of saline agriculture [19]. The global loss of income due to salinity, based on crop yield losses, have been estimated at about USD 12.6 billion, considering both irrigated and non-irrigated land, with the former accounting for approximately 90% of those costs [20]; in another study, losses for irrigated areas alone were calculated as USD 27.3 billion [6]. These large differences in the estimated costs are not surprising given the different methodologies used, but also the type of land degradation considered and the criteria used to assess the degree of degradation [6]. There is a lack of a comprehensive overview of the economic potential of saline agriculture, and very few studies have addressed the added value for growing crops for human consumption, rather than for biofuels or as forage crops. An average value of between USD 200 and 600 per hectare was estimated by Negacz and Vellinga [19], although this comes from a limited number of studies used in their meta-analysis.

There is growing demand from consumers for healthy, nutrient-rich foods that are sustainably produced. Most halophytes meet these criteria, as they are rich in bioactive secondary metabolites such as antioxidants, including polyphenols, b-carotene, and ascorbic acid [14]. Like other fresh vegetables, halophytes can be sold in packages as fresh-cut and minimally processed products, but the majority have a limited shelf life [21,22]. However, sensory evaluation by panellists on product freshness for the halophytes Sarcocornia perennis and Salicornia ramosissima showed that the flavour and texture of the product were maintained after 14 days at 4 °C [23]. In Europe, where the cultivation of halophytes has been carried out for several decades, and the market is quite advanced [24], several halophyte products from species including Salicornia spp. and Aster tripoliumare are already being sold as vegetables and salad in markets at comparatively high prices to traditional leafy green vegetables. This highlights the current status of the halophyte edible market as being a niche market, with a strong focus of use in high-end gourmet restaurants, etc. [14]. Due to high costs of cultivation, lack of year-round supply, and limited information on efficient cultivation systems, production costs are high [22], and these will naturally be passed on to the consumer. For markets to grow, there also needs to be a focus on building public awareness around the uses of halophytes in the diet, and increasing knowledge on their nutritional benefits, so that the consumer demand increases.

3. Anti-Nutrients and Consumer Acceptance

In addition to the accumulation of beneficial nutrients and bioactive compounds in halophytes (including amino acids, polyols, and antioxidants), these plants can also accumulate undesirable, anti-nutritional factors which can have negative effects on human health. Anti-nutritional factors are compounds present in the edible portion of the plant that can interfere with the absorption of nutrients and/or reduce their bioavailability, or can be toxic when consumed [25]. In halophytes, the major anti-nutrients that have been reported include oxalates [13,14,26,27,28], nitrates [29,30], phenolics, saponins [29,30], and tannins [31].

Plants synthesise oxalates via three metabolic pathways using glycolate, isocitrate, and ascorbic acid as precursors [32]. In the plant, oxalates are present as a free salt; as a soluble salt of potassium, magnesium, and sodium; or an insoluble crystal with calcium [32]. The concentration of oxalates varies greatly between plant species, accounting for 3 to 80% of the plant dry weight, with the highest concentrations found in leaf tissue [33]. Many halophytes accumulate oxalates to levels similar to or higher than those found in spinach (

Table 1. Levels of oxalates measured in different halophyte species.

Halophyte Species		Oxalate (mg/100 gFW or mg/100 gDW *) Range or Mean	Reference
Common Name	Scientific Name
Pig Spinach	Chenopodium spp.	1100 †	[35]
Purslane	Portulaca oleracea	910–1679 †	[35]
Warragal Greens	Tetragonia expansa	890 †	[35]
Seapurslane	Sesuvium portulacastrum	385 * ± 35	[36]
Seablite	Suaeda arbusculoides	280 * ± 20	[36]
Saltbush	Atriplex nummularia	215 * ± 49	[36]
Saltbush	Atripex nummularia	120 ± 4–5014 ± 42 *a	[37]
Ice plant	Mesembryanthemum crystallinum L.	288 ± 27.5–8141 ± 86 *a	[37]
Quinoa	Chenopodium quinoa	184 †	[38]
Spinach	Spinacia oleracea	404 ± 75 *	[36]
Spinach	Spinacia oleracea	320–1260 †	[35]

^a Values were taken from greenhouse-grown plants treated with differing NaCl concentrations (0, 200, 400 NaCl) and differing ratios of NO₃ to NH₄ (details can be found in [37]). * values reported in mg/100 gDW ^† Standard deviation not reported.

). Oxalates in these plants have been suggested to play roles in charge or osmotic balance for sodium accumulation [34] but also may act as an internal CO₂ source [33].

High levels of oxalates in the diet are particularly undesirable due to the increasing risk of kidney stones and low plasma levels of iron and calcium, which can lead to hy-posideraemia and hypocalcaemia [39,40].

Nitrates are taken up by plants and are an essential nutrient for nucleic acids, proteins, and chlorophyll synthesis [41]. Because nitrate has a positive effect on plant growth, it is usually supplied to plants at relatively high concentrations and can accumulate in the aerial portion of the plant. In the case of halophytes, salinity has been shown to increase the amount of nitrates accumulated [14]. While nitrate itself is non-toxic to humans, accumulation of its byproducts and metabolites, such as nitrite and other N-nitrous compounds, can have negative effects on health. Nitrate is converted into nitrite by bacterial enzymes found in saliva and the gut [41]. This process of conversion is usually very slow, and in healthy adults, nitrite accumulation should not present a health risk, but in patients with gastroenteritis, particularly infants, the conversion and subsequent accumulation of nitrite can be much higher. This can result in a condition called methaemoglobinaemia, which results in low oxygen in the blood and can be fatal [42]. High levels of nitrates can also result in gastric cancer [42].

Saponins are a class of plant secondary metabolites known for their ability to cause foaming and historically were used to produce soap. In halophytes, the acid saponins are most common, consisting of a polycyclic aglycone triterpenoid [43]. There is a large body of evidence that these compounds have beneficial properties, showing anti-asthmatic, anti-tumour, anti-hypertensive, and antimicrobial activity [44]. However, at high concentrations, saponins can cause adverse toxic effects in humans, reducing the absorption of essential minerals and causing diarrhoea and weight loss [Sharma]. In the halophyte quinoa (Chenopodium quinoa Willd.), which accumulates relatively high amounts of saponins in the seeds (2 to 5%) and lesser amounts in the leaves, the levels of saponins were shown to decrease when plants were grown in the presence of salt [43].

Halophytes also produce a range of secondary metabolites collectively known as phenolics. These compounds help them survive the harsh conditions of their native environment, and while many are used as a defence against free radicals and show antioxidant properties, they also play roles in protection from UV radiation and defence against insects and herbivores [45]. Despite a range of health benefits, including, as mentioned above, their antioxidant properties and demonstrated anti-inflammatory and anti-carcinogenic properties [46], phenolics are considered an anti-nutrient because they can reduce the availability of zinc and other essential minerals. Additionally, oxidised phenolics can combine with amino acids, reducing their uptake [45]. Many halophyte species have been shown to have more than 20 mg/g dry weight of total phenolic content [45], and much of this is attributed to the accumulation of flavonoids. Salinity treatment has been shown to increase the amount of phenolics, with both the developmental state and time of treatment influencing the levels [47].

Phytate or phytic acid is the main storage form of phosphorus in the plant. In the human diet, it has been shown to have a number of health benefits, with roles as an antioxidant, anti-tumour, and anti-diabetic agent, as well as preventing osteoporosis [48]. As an anti-nutrient, phytate forms insoluble salts with cations, including magnesium, zinc, iron, and thus negatively impacts their bioavailability. It has also been shown to reduce the digestibility of proteins [22]. With the exception of quinoa, where the seeds are consumed, and seed phytate levels are high, reports in other halophytes show that generally, where it has been measured, the phytate level is relatively low and does not change with salinity treatment [43].

Oxalates are one of the most abundant anti-nutrients in halophytes, so they have been targeted by several approaches to reduce the levels in the edible portion of the plant (Figure 1). In the remaining sections, we focus on the recent strategies for reducing the level of this anti-nutrient in edible halophytes.

4. Processing as a Means to Reduce Oxalates

Concentrations of specific anti-nutrients in foods can be reduced by processing, including fermenting, soaking, and heating [22]. However, these treatments can reduce the nutritional value of the plant material. While fermenting and soaking treatments work well for grains and seeds, they are not options that can be used when the edible material is leaves.

Blanching has been shown to be effective in removing oxalates from vegetables [49]. In a study of the edible halophyte Portulaca oleracea, boiling the leaves, stems, or flower buds for five minutes reduced the total oxalate in the tissues by, on average, 27% [50]. In a similar study on P. oleracea, Badawy et al. [51] showed that as the heating time and temperature were increased, soluble oxalate levels in the tissue decreased concomitantly. Blanching the leaves of the halophyte Tetragonia expansia reduced the total oxalate by 25% when they were placed into boiling water for two minutes [52]. Pickling leaves in vinegar has also been successfully used to reduce the oxalate content, although to a lesser extent than blanching [50,51]. While blanching is an option for the removal of oxalates from leaves, it causes wilting due to breakdown of the tissue, and it is therefore not recommended when crisp salad leaves are the desired product. None of the above studies monitored how boiling/blanching affected the nutrient content of the halophyte leaves. Evidence from studies on vegetables, including those where leaves are usually eaten raw, such as chard and spinach, showed that boiling for five minutes resulted in a complete loss of vitamin C from chard but only a 35% reduction in this vitamin in spinach [53]. Blanching for one minute reduced vitamin C to a lesser extent: 17% and 24% for spinach and chard, respectively [53]. Interestingly in the same study, vitamin K and vitamin E increased with both blanching and boiling [53], most likely due to the heat treatment making these fat-soluble vitamins easier to extract and measure. This balance between removing anti-nutrients, preserving nutritional content, and achieving a desirable texture or appearance complicates the choice of processing methods for specific halophyte foods.

Agronomic approaches tailored to the specific characteristics of halophytes could present more desirable and innovative solutions to manage anti-nutrient contents effectively, offering a more sustainable and nutritionally rich outcome. Research in this direction is critical for the development of practical strategies that can be implemented at the agricultural level to enhance the overall nutritional quality of halophyte-based foods.

5. Agronomic Options for Minimising Anti-Nutrients in Commercial Productions Systems

Many edible halophytes are already cultivated in greenhouse production systems or in the field to meet market demands [54], and numerous studies have investigated nutrition and harvest regimes for optimised yields across a range of edible halophytes (see [14] for a review). However, as premium markets emerge, a reduction in anti-nutritional compounds will be essential for consumer acceptance, in addition to the optimisation of yields to ensure profitable production. The concentrations of both nutritional and anti-nutritional compounds vary between plant species and genotypes. They are also influenced by agronomic practices, including fertilisation and harvesting regimes, salinity levels in irrigation water, plant age, and the plant tissue harvested [13,14,37]. Halophytes grow naturally across a wide range of habitats [55] and, thus, soil types, which may impact on the anti-nutrient levels in plant tissues. However, information regarding the effects of specific soil conditions on the levels of anti-nutrients in halophytes is scarce. The following section therefore focuses on specific agronomic and genetic aspects of halophyte cultivation that can be manipulated to lower the concentrations of key anti-nutrients in shoot tissues.

A key strategy for lowering oxalate concentrations is an increase in NH₄⁺ nutrition over NO₃⁻ nutrition (

Table 2. Effect of the NH₄⁺:NO₃⁻ ratio on the yield and oxalate concentration in various edible halophytes. Data represent the mean ± SEM.

Species	NH4+:NO3−	Salinity Level	Dry Matter Yield	% Reduction in Yield (Compared to 100% NO3−)	Oxalate	% Reduction in Oxalate (Compared to 100% NO3−)	Reference
Tetragonia tetragonoides			g/plant		%		[26]
	100:0	180 mS	8.15 ± 1.1		7.8 ± 0.7
	97:3	180 mS	9.38 ± 1.0	no reduction	7.1 ± 0.7	9.0
	80:20	180 mS	8.01 ± 0.8	1.7	6.7 ± 0.9	14.1
	50:50	180 mS	8.09 ± 0.8	0.7	4.9 ± 0.9	37.2
	0:100	180 mS	7.09 ± 9	13.3	0.5 ± 0.1	93.6
Atriplex nummularia			g/plant		%		[27]
	100:0	50 mM	5.6 ± 0.8		7.8 ± 0.5
	0:100	50 mM	2.5 ± 0.5	55.4	1.9 ± 0.2	75.6
	100:0	200 mM	5.9 ± 0.3		10 ± 0.5
	0:100	200 mM	1.8 ± 0.1	69.5	2.9 ± 0.05	71.3
	100:0	500 mM	3.1 ± 0.5		10 ± 0.4
	0:100	500 mM	1.8 ± 0.1	41.9	2.3 ± 0.2	77.9
Portulaca oleracea			g/pot		mmol/g leaf DW		[28]
	100:0		1.1		1.0
	75:25		1.2	no reduction	0.9	10
	50:50		1.1	no reduction	0.7	30
	25:75		0.9	18.2	0.6	40
Portulaca oleracea			g/plant		mmol/g DW		[40]
	60:40		72		0.77
	40:60		80	no reduction	0.67	13
	0:100		48	33	0.61	21
Portulaca oleracea			g/plant		mg/100 g FW		[28]
	100:0		2.2		397
	75:25		2.2	no reduction	297	25
	50:50		2.1	5	248	38
	25:75		1.9	14	239	40
Portulaca oleracea			mg/plant		mg/g DW		[60]
Ecotype ET	100:0	0 mM	95 ± 3		109 ± 22
	66:33	0 mM	76 ± 3	20	55 ± 8	49.5
	25:75	0 mM	62 ± 5	34.7	18 ± 3	83.5
	100:0	50 mM	100 ± 2		170 ± 25
	66:33	50 mM	81 ± 3	19.0	106 ± 11	37.6
	25:75	50 mM	63 ± 3	37.0	23 ± 3	86.5
Ecotype RN	100:0	0 mM	79 ± 6		82 ± 7
	66:33	0 mM	84 ± 4	no reduction	25 ± 4	69.5
	25:75	0 mM	60 ± 3	24.1	17 ± 1	79.3
	100:0	50 mM	73 ± 2		82 ± 7
	66:33	50 mM	77 ± 3	no reduction	35 ± 4	57.3
	25:75	50 mM	63 ± 3	13.7	19 ± 1	76.8
Portulaca sp.			mg/plant		mg/g DW		[61]
P. sativa	100:0		140 ± 5		2.62 ± 0.2
	75:25		105 ± 10	25	2.46 ± 0.3	6
	50:50		101 ± 5	28	1.52 ± 0.3	42
	25:75		112 ± 15	20	1.05 ± 0.1	60
P. nitida	100:0		215 ± 18		3.15 ± 0.3
	75:25		155 ± 18	28	2.41 ± 0.2	23
	50:50		131 ± 15	39	1.85 ± 0.2	41
	25:75		128 ± 17	40	0.42 ± 0.1	87
P. papillato-stellulata	100:0		195 ± 21		2.48 ± 0.2
	75:25		166 ± 21	15	1.83 ± 0.2	20
	50:50		129 ± 8	34	2.77 ± 0.3	no reduction
	25:75		133 ± 19	32	1.45 ± 0.1	41
Enchylaena tomentosa			mg/pot		mg/g DW		[51]
	100:0	0 mM	8.0 ± 0.4		33 ± 6.5
	75:25	0 mM	7.4 ± 0.4	7.5	22 ± 3.9	33
	50:50	0 mM	6.8 ± 0.7	15	11 ± 3.2	67
	25:75	0 mM	6.4 ± 0.7	20	5.7 ± 1.0	83
	0:100	0 mM	3.8 ± 0.4	53	2.9 ± 0.2	91
	100:0	200 mM	8.4 ± 0.5		32 ± 5.3
	75:25	200 mM	8.6 ± 0.4	no reduction	27 ± 5.8	16
	50:50	200 mM	7.6 ± 0.9	10	20 ± 4.3	38
	25:75	200 mM	6.4 ± 0.3	24	9.6 ± 1.6	70
	0:100	200 mM	3.6 ± 0.2	57	2.6 ± 0.2	92
	100:0	400 mM	6.1 ± 0.3		50 ± 4.2
	75:25	400 mM	5.7 ± 0.2	7	38 ± 4.1	24
	50:50	400 mM	5.9 ± 0.9	3	20 ± 3.2	60
	25:75	400 mM	5.5 ± 0.8	10	7.2 ± 1.9	86
	0:100	400 mM	3.0 ± 0.3	51	1.2 ± 0.0	98
Mesembryanthemum crystallinum			mg/pot		mg/g DW		[51]
	100:0	0 mM	1.9 ± 0.4		80 ± 7.9
	75:25	0 mM	1.6 ± 0.3	16	62 ± 8.5	23
	50:50	0 mM	1.3 ± 0.2	32	55 ± 9.9	31
	25:75	0 mM	1.4 ± 0.3	26	50 ± 5.6	38
	0:100	0 mM	0.8 ± 0.2	58	29 ± 2.8	64
	100:0	200 mM	2.3 ± 0.2		81 ± 8.6
	75:25	200 mM	2.3 ± 0.3	no reduction	70 ± 12	14
	50:50	200 mM	2.0 ± 0.3	13	63 ± 8.7	22
	25:75	200 mM	1.8 ± 0.2	22	56 ± 4.8	31
	0:100	200 mM	1.3 ± 0.2	43	40 ± 7.4	51
	100:0	400 mM	1.3 ± 0.2		64 ± 6.2
	75:25	400 mM	1.5 ± 0.2	no reduction	51 ± 3.3	20
	50:50	400 mM	1.2 ± 0.2	8	48 ± 0.8	25
	25:75	400 mM	1.1 ± 0.3	15	45 ± 3.1	30
	0:100	400 mM	0.7 ± 0.1	46	41 ± 8.6	36

). The degree to which oxalate concentrations are decreased by increasing NH₄⁺ nutrition varies with the plant species, genotype, and other growing conditions, including the level of salinity in the growing medium (Table 2). Reductions in the oxalate concentration of 70–98% occur in the halophytes Portulaca and Ruby saltbush when 75–100% of N is supplied as NH₄⁺ (Table 2), indicating the effectiveness of this strategy for some edible halophytes. Increasing NH₄⁺ nutrition over NO₃⁻ nutrition has the additional advantage of decreasing shoot nitrate concentrations [37]. However, while NH₄⁺:NO₃⁻ ratios can be readily manipulated in greenhouse production systems, increasing the NH₄⁺ nutrition of field-grown plants can be challenging owing to the conversion of NH₄⁺ to NO₃⁻ by nitrifying microbes in soils [56]. Under warmer temperatures and in soils high in microbial activity, the conversion of NH₄⁺ to NO₃⁻ can be particularly rapid [57], limiting the exposure of plant roots to high concentrations of NH₄⁺. One potential management option for field-grown halophytes may be the use of N fertilisers containing nitrification inhibitors. Commercially-available nitrification inhibitors such as 3,4-dimethylpyrazole phosphate (DMPP), can limit nitrification for up to a month in the field [58], which may be sufficient time to influence shoot oxalate concentrations in short-term halophyte crops. Further, highly acidic soils can naturally suppress nitrification (e.g., [59]), and it is possible that acid-soil-tolerant halophytes could be cultivated on such soils to minimise shoot oxalate concentrations. The use of N fertiliser with nitrification inhibitors, or other management strategies that minimise the build-up of NO₃⁻ pools in soils, warrants further investigation as a tool to reduce the concentrations of oxalates and nitrates in field-grown edible halophytes.

One key issue with increasing the proportion of NH₄⁺-N nutrition for oxalate minimisation is the typical trade-off incurred with biomass yields (Table 2). The degree to which biomass yields decline with increasing NH₄⁺-N nutrition varies with the plant species, genotype, and growing conditions (Table 2), which suggests that yield losses may be minimised through optimised management or genotype selection/breeding. For example, Szalai et al. [61] reported yield losses of up to 40% in one Portulaca ecotype with increasing NH₄⁺-N nutrition, but only 20–28% in another. Only three Portulaca ecotypes were investigated in the study, but greater variation in yield response to NH₄⁺-N nutrition may exist in a wider germplasm set. Breeding specifically for low shoot oxalate concentrations, regardless of N nutrition, may also be a feasible option given that variation in the shoot oxalate concentration has been reported for a number of edible halophyte species, including Portulaca sp. [62,63] and Silene vulgaris [64].

6. Genetic Engineering to Reduce Oxalates

Advanced genomic techniques, such as RNAi, gene editing, gene over-expression, and genomics-assisted breeding, allow for the manipulation of biochemical pathways in the plant, which can help to lower the amounts of anti-nutrients. This can be accomplished by either down-regulating genes that are involved in the synthesis of the compound or, conversely, up-regulating genes that are involved in the degradation of the compound. This approach opens the opportunity to produce crops in which negative anti-nutritional traits are reduced or even eliminated, allowing for crop-specific strategies and the production of “smart foods” [65]. While no evidence was found for specific cases where this approach has been carried out with edible halophytes, several studies have looked into reducing oxalate levels in vegetables through metabolic engineering. In the oxalic-acid-accumulating tomato fruit, over-expression of a fungal oxalate decarboxylase, an enzyme which breaks down oxalate into formic acid and carbon dioxide, significantly reduced oxalate levels in the fruit [66]. Lower oxalate levels resulted in increases in micronutrients, including manganese, magnesium, and zinc, with no obvious morphological effects [66]. A similar approach was taken to lower oxalate levels in soybean and grass pea to improve the nutritional quality of these legumes [67].

It is likely that the lack of evidence for undertaking this approach in edible halophytes is due to the limited information on biochemical pathways for oxalate synthesis and degradation in these plants. Additionally, the lack of genomic resources and ability to transform these plants restricts any research that can be done in this area. As these tools are developed and the use of gene editing becomes more commonplace, we should see more rapid advancement in this area.

7. Conclusions

While the breeding of new cultivars of halophytes for increased salt tolerance has been undertaken (e.g., [68]), we are unaware of any breeding attempts to minimise halophyte anti-nutrient levels. Identifying genetic variation with regard to anti-nutrient concentrations in emerging edible halophyte crops should be a priority for future research. While increasing the NH₄⁺ to NO₃⁻ ratio generally reduces the levels of two key anti-nutrients, oxalate and nitrate, in shoots, manipulating these ratios in field conditions can be challenging, and trade-offs with plant biomass production are species-specific or even genotype-specific. Optimisation of agronomic factors for the production of nutritious halophytes will therefore need to be undertaken under local production settings and for the specific species/genotypes being cultivated.