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31 May 2023

Ascophyllum nodosum (L.) Le Jolis, a Pivotal Biostimulant toward Sustainable Agriculture: A Comprehensive Review

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1
Department of Botany, Maharshi Dayanand University, Rohtak 124001, Haryana, India
2
Department of Genetics & Plant Breeding, CCS Haryana Agricultural University, Hisar 125004, Haryana, India
3
Sarvodya College of Pharmacy, Imlota 127306, Haryana, India
4
Division of Seed Science and Technology, Indian Agricultural Research Institute, New Delhi 110012, Delhi, India
Agriculture2023, 13(6), 1179;https://doi.org/10.3390/agriculture13061179
This article belongs to the Special Issue Remediation of Contaminated Soil for Sustainable Agriculture
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Abstract

Algae are existing macroscopic materials with substantial benefits, including as important growth regulators and macronutrients and micronutrients for the growth of healthy crop plants. Biofertilizers obtained from algae are identified as novel production fertilizers or innovative biofertilizers without the detrimental impacts of chemicals. Seaweeds contain many water-soluble minerals and nutrients that plants can easily absorb and that are valuable for crop plants’ growth. At present, Ascophyllum nodosum (L.) Le Jolis extract outperforms chemical fertilizers in terms of increasing seed germination, plant development, and yield, as well as protecting plants from severe biotic and abiotic stresses. A. nodosum contains bioactive compounds that exhibit an array of biological activities such as antibiotic, anti-microbial, antioxidant, anti-cancer, anti-obesity, and anti-diabetic activities. A. nodosum extract (AnE) contains alginic acid and poly-uronides that improve soil’s water-carrying ability, morsel structure, aeration, and capillary action, stimulating root systems in plants, increasing microbial activity in soil, and improving mineral absorption and availability. The scientific literature has comprehensively reviewed these factors, providing information about the different functions of A. nodosum in plant growth, yield, and quality, the alleviation of biotic and abiotic stresses in plants, and their effects on the interactions of plant root systems and microbes. The application of AnE significantly improved the germination rate, increased the growth of lateral roots, enhanced water and nutrient use efficiencies, increased antioxidant activity, increased phenolic and flavonoid contents, increased chlorophyll and nutrient contents, alleviated the effects of abiotic and biotic stresses in different crop plants, and even improved the postharvest quality of different fruits.

1. Introduction

The existing global scenario decisively highlights the need to accept eco-friendly agricultural tools for sustainable development. Chemicals have adverse impacts on the soil and the valuable soil microbes and microbial communities and the plants cultivated on these soils. Organic farming is a therapy for the evils of modern chemical agriculture. Many viable alternatives must be explored to meet the increasing demand for organic inputs. One such alternative is the application of seaweed extracts as plant stimulants, sources of nutrients, and biofertilizers [1]. According to the European Union (EU) Regulation 2019/1009, a plant biostimulant is “a product stimulating plant nutrition processes independently of the product’s nutrient content with the sole aim of improving one or more of the following plant or plant rhizosphere characteristics: (a) nutrient use efficiency; (b) tolerance to abiotic stress; (c) quality traits; or (d) availability of confined nutrients in the soil or rhizosphere” [2]. Biostimulants may be any substance or microorganism. The immediate use of seaweed is in the production of hydrocolloids such as alginates, carrageenan, and agar [3]. Various structures of natural products or bioactive components have been established in seaweed, such as carotenoids, terpenoids, polyphenols, peptides, sulfated polysaccharides, and fibers. These bioactive products demonstrate an array of biological properties, for instance, antibiotic, antioxidant, cytotoxic, anti-inflammatory, anti-diabetic, and anti-cancer activities [3,4]. Unlike synthetic chemicals, biofertilizers composed of algae are eco-friendly, non-toxic, pollution-free, and harmless to plants [5].
In various parts of the globe, a continuous reduction in rainfall is generating a high frequency of drought stress, which is negatively manipulating crop productivity and food security. In addition to water stress, salinity, heat, nutrient, and oxidative stresses limit agricultural productivity [6]. Leaf area and photosynthetic activity are reduced by drought stress due to partial stomatal closure, resulting in reduced growth, development, and productivity of crop plants [7]. Salt stress has a negative impact on approximately 6% of the world’s arable land area, including 30% of irrigated land [8]. Alleviating these abiotic stresses is a major challenge in various parts of the globe, mainly in arid and semi-arid regions [6].
Seaweed extracts are used as plant biostimulants and are considered the most economic and effective way to improve the growth, development, quality, and quantity of plants by increasing water and mineral use efficiencies under various environmental stresses [9]. The application of AnE significantly improved the germination rate, increased the growth of lateral roots, enhanced water and nutrient use efficiencies, increased antioxidant activity, increased phenolic and flavonoid contents, increased chlorophyll and nutrient contents, alleviated the effects of abiotic and biotic stresses in different crop plants, and even improved the postharvest quality of fruits [10].
Brassica napus, Solanum lycopersicum, Daucus carota, Cucumis sativus, Glycine max, Spinacia oleracea, and Hordeum vulgare were all stimulated by agricultural biostimulants (AnE) [10]. Seaweed extracts have the capacity to sustainably increase the quality and yield of crops with different soil types and farming systems; for example, foliar and soil applications of seaweed extract enhanced the yield and post-harvest qualities of strawberries, tomatoes, vegetables, and sugarcane [11,12]. Many other studies on the interactions of soil microbes showed that the application of seaweed extracts altered the microbial activity in the rhizosphere located in the soil, and these modifications coincided with improved plant development and yield [12,13]. According to the study by Renaut et al. [13], the effect of AnE on the soil and root microbiota diversity of pepper plants altered the bacterial diversity in the soil. AnE applied to tomato and sweet pepper crops significantly enhanced the upregulation of the gene transcripts Ga2Ox, IAA, and IPT, which are involved in the biosynthesis of gibberellin, auxin, and cytokinin, respectively [14]. The foliar spray of AnE on Paspalum vaginatum during protracted irrigation intervals and under conditions of salinity improved lipid peroxidation by means of linoleic acid and DPPH assays and increased the activities of antioxidant enzymes such as SOD, CAT, and APX, leading to the depletion of reactive oxygen species in the AnE-treated plants [15].
Seaweed extracts are used in plants to protect them from pathogenic infections, either directly or indirectly. A. nodosum has the potential to act as a protectant to control plant diseases. Both foliar (spray) and soil applications of seaweed extract were found to be effective in reducing foliar and soil-borne pathogens against a variety of crops [16,17]. Bioactive compounds present in A. nodosum are also considered potent elicitors of plant defense responses against various pathogens. The AnE improved plant disease resistance against Phytopthora melonis in cucumber [18] and against Phytophthora capsica in tomato [19].
This review represents the current state of biostimulants and their effects on plant growth and development. Biostimulants could be a long-term and cost-effective tool for improving plant development and resistance to various stresses. Recent research has shown that biostimulants defend plants and crops from different biotic and abiotic stresses, suggesting their potential for field application and measurement as organic inputs as they are safe for human health and are cost-effective and environmentally friendly alternatives.

2. Seaweeds

There are about 9000 species of marine algae integrated into different algal groups, such as Phaeophyta (brown), Chlorophyta (green), and Rhodophyta (red), depending upon their pigments, such as chlorophylls, carotenoids, and phycobilins [5]. For a long time, industries have used seaweeds as edible sources, fodder, green compost, and unprocessed materials [20]. Seaweeds, as important oceanic assets, are used in soil reformation to improve the plant growth of crops. In horticulture, using seaweed products is becoming a time-honored practice [21]. Seaweed extract can improve plant growth, yield, and quality by containing different plant growth hormones and hormones such as growth regulators, auxins, abscisic acid, gibberellins, cytokinins, betaines, brassinosteroids, jasmonates, polyamines, salicylates, and signal peptides. In addition to this, trace elements such as iron (Fe), copper (Cu), zinc (Zn), cobalt (Co), molybdenum (Mo), manganese (Mn), and nickel (Ni), as well as vitamins, and amino acids [5,22], are also found in seaweeds. Seaweed extract highly influences the cellular metabolism of plants, and its application has been used to raise the uptake of essential macro- and micronutrients from the soil and to improve plant resistance to pests, diseases, and stresses [23]. Many algal products are significant sources of plant biostimulants and are extensively used to increase agricultural productivity [24]. The most studied seaweed is the brown intertidal alga Ascophyllum nodosum (L.) Le Jolis. It is used as a source of many industrial and commercial plant growth stimulators to improve the regulation of physiological, biochemical, and molecular processes to enhance plant defenses against biotic and abiotic stresses [25]. The significance of Ascophyllum nodosum Extract (AnE) in the improvement of plant growth via different modes of action is shown in Figure 1.
Figure 1. Significance of Ascophyllum nodosum extract (AnE) in improving plant growth via different modes of action.
In the subsequent sections, we provide a detailed and plant-centered review of the composition, commercial products, and effects of AnE on different plants under various environmental biotic and abiotic stresses. We also show tables that provide an overview of the morphological, physiological, and biochemical changes in plants in response to AnE treatment.

3. Ascophyllum nodosum (L.) Le Jolis and Its Composition

Ascophyllum nodosum (L.) Le Jolis belongs to the group Phaeophyta (brown algae), and it is the most studied seaweed among other groups of seaweeds [26]. It is primarily found in the cold water of the North Atlantic Ocean, which stretches from eastern Canada to parts of northern Europe [27]. A. nodosum is a brown alga that is edible and is also known as rockweed, knotted kelp, Norwegian kelp, and knotted wrack (egg wrack). A. nodosum seaweed extract has the potential to improve plant growth, yield, and quality as it contains plant growth regulators such as auxins, cytokinins, gibberellins, betaines, mannitol, organic acids, polysaccharides, amino acids, and proteins [28]. Phlorotannins are unique polyphenolic compounds found only in some brown algae and not in terrestrial plants. A. nodosum is one of the most significant sources of phlorotannins [29].
A. nodosum has bioactive biopolymers, including alginates, fucoidan, and laminarin, as well as non-polysaccharide bioactive components such as polyphenols [30]. A. nodosum contains sulfated polysaccharide chains known as fucoidans, which have alternate (1–3) and (1–4) linkages [31,32] with both disulfate and trisulfate sugars. Most of them have disulfated sugars [33]. Ascophyllan [34] is the common name for a fucoidan with a high amount of sulfur residue that is found in Ascophyllum. It has a molecular size of 390 kDa [35]. Brown algae, i.e., the Phaeophyceae family, reveal high levels of phlorotannins. Phlorotannins are a type of polyphenol that is unique to aquatic organisms. These are oligomers and polymers of phloroglucinol (1,3,5-trihydroxy benzene) [36] that are linked by the acetate malonate pathway and have molecular sizes ranging from 126 to 650 kDa [37,38,39].
Components of A. nodosum contain the following sulfated polysaccharides (fucoidans):
  • Foley et al. [40] found a fucoidan with a dry weight of 1.75%, carbohydrates at 65.4%, polyphenols at 13.5%, and proteins at 18.5%. The carbohydrates comprise L-fucose (52.1%), glucose (21.3%), galactose (6.1%), and xylose (16.5%) at a molecular size of 420 kDa.
  • Kloareg et al. [41] discovered sulfated polysaccharide, a fucoidan with 38.7% L-fucose and 33.7% sulfate by weight.
  • Fucoidan sulfate at 26.1%, uronic acid at 5.7%, and L-fucose at 31.3% at 556 kDa [42].
  • A fucoidan of 47% L-fucose, 30% sulfate, and 6% uronic acid at 25 kDa [43].
  • A fucoidan of L-fucose (39.7%), sulfate (27%), and uronic acid (4.1%) with a molecular weight of 18.6 kDa [44].
  • The fucoidan of L-fucose is 45.4%, sulfate is 22.1%, and uronic acid is 9.9% at 417 kDa [45].
  • At 1323 kDa, the fucoidan of sulfate contains 19.4% sulfate, 28.4% L-fucose, and 5.8% uronic acid [45].
Other different, useful components are also found in A. nodosum (Table 1).
Table 1. Other components of A. nodosum.

4. Ascophyllum nodosum Extract (AnE) Enhances Plant Morphological and Physiological Characteristics

Ascophyllum nodosum extract (AnE) commercial products have been confirmed to regulate growth-stimulating behaviors. When low concentrations of AnE are applied to plants, they are commonly referred to as “biostimulants”, “biostimulators”, “biofertilizers”, and “plant growth stimulators” [59] (Table 2). A. nodosum seaweed extract is a well-known growth promoter for vascular family plants due to its ability to improve nutrient absorption via root tissues, thereby increasing yield while reducing the damaging effects of biotic and abiotic stresses [5,22,60]. The development and efficiency of crops are improved by applying AnE, which increases nutrient uptake and availability at the plant roots [24].
Table 2. Commercial A. nodosum seaweed products utilized in farming and horticulture as biofertilizers and biostimulators for plant growth [59,60].
Commercial seaweed products significantly enhanced the yield and quality of citrus fruit [21] and grapes [61]. For example, a representative AnE-based biostimulant produced by PI Industries Ltd., India, BIOVITA, an agriculture product, is shown in Figure 2. Using seaweed extracts in Petunia and Ageratum improved vegetative plant growth, stomatal conductance, photosynthesis, transpiration rate, the water potential of leaves, and the relative water content (RWC) under prolonged irrigation conditions [62]. AnE transforms the concentration and localization of auxins, and it serves as a plant hormone that enhances plant growth [63]. AnE treatments extensively improve the number of leaves and their area, the height and dry weight of plants, antioxidant activity, and the phenolic, flavonoids, and tannin contents of Calibrachoa × hybrida (an ornamental plant) [64]. Crops treated with Bio-Algeen® have been accounted for in the yield, as in clover [65], sugar beet [66], tomatoes [67,68], and carrot [69]. Macro- and micronutrients in tomato fruit were increased using two commercial products derived from AnE, Rygex®, and Super Fifty® [70].
Figure 2. Example of biostimulant (AnE) produced by PI Industries Ltd., Sagar, Madhya Pradesh, India.
In another study, Danesh et al. [71] observed that Ascophyllum seaweed extract affected the growth parameters of tropical crops. When treated with AnE, tomato plants (Lycopersicum esculentum Mill.) showed an increase in plant height and root and shoot biomass, with a significant enhancement in numerous minerals and nutrients in the shoots and fruits of tomato plants at a concentration of 0.5%. The mineral nutrients of the fruits were significantly increased: nitrogen by 81%, phosphorus by 8%, potassium by 50%, calcium by 57%, iron by 25%, and zinc by 33%, and the intensity of sodium was reduced by 2% [71]. The AnE enhanced the yield and quality of the tomato fruit, as betaines in the extract enhanced the chlorophyll pigment in the tomato leaves and decreased its deterioration rate [72,73]. The seaweed-treated tomato plants exhibited improved concentrations of minerals in their shoots and a significant increase in fruit quality and other attributes, including size, color, total soluble solids, ascorbic acid, and minerals under tropical growing conditions [73]. Mohamed et al. [74] observed that the foliar application of AnE in the chickpea cultivar Giza 195 improved the seed quality and amino acid and mineral contents in the seeds and induced favorable changes in the protein profile.
Similarly, the foliar application of AnE influenced the growth, yield, and quality attributes in four onion cultivars; a 0.5% concentration of AnE caused a significant increase in total soluble sugar, mineral-like N, P, and K, bulb weight, and yield (Table 3). In contrast, at a concentration of 3%, AnE enhanced ascorbic acid content compared to the respective controls [75]. Likewise, an A. nodosum-based biostimulant enhanced the protein content and nutrition value of green beans [76].
Table 3. Physiological, morphological, and biochemical effects of A. nodosum extract (AnE) and commercial products of AnE on different plants.

5. Ascophyllum nodosum Extract (AnE) Promote Abiotic Stress Tolerance in Plants

A wide range of organic molecules such as alginates, fucoidan, laminarin, mannitol, polyphenols, and polysaccharides are present in AnE. These compounds could potentially promote stress tolerance and improve plant growth (Table 4) [60].
Table 4. Effects of commercial products and ANE (seaweed extract) derived from A. nodosum on different plants under abiotic stress.
Ascophyllum products may assist in stress alteration because of betaines’ presence in the seaweed. Betaines serve as osmotic-compatible solutes under stress conditions [5]. Ascophyllum also contains mannitol, which facilitates osmotic adaptation [166]. AnE application alleviates drought stress in growing plants [140,141]. Several reports prove that the drought-stressed Arabidopsis thaliana plants can sustain strong stomatal conductance, water use efficiency (WUE), and mesophyll conductance after the application of AnE. The pre-treatment of A. thaliana plants with seaweed extract induced stomatal closure and changed the gene expression level involved in abscisic acid (ABA) response and antioxidant system pathways [151]. Shukla et al. [153] found that plants treated with AnE had a greater RWC, high stomatal conductance, and antioxidant activity under drought stress. Commercial seaweed extracts significantly improve the drought stress tolerance in grasses [167] crops, vegetables, ornamental plants [137], and container-grown “Hamlin” sweet orange trees [140]. Seaweed AnE has been applied to ornamental plants, such as Spiraea nipponica (Snow mound) and Pittosporum eugenioides (Variegatum), to increase drought stress tolerance. Under drought conditions, AnE improved the leaf gas exchange parameters, leaf water potential, and the RWC and increased the number of leaves and the dry weight and height of plants in Spiraea nipponica and Pittosporum eugenioides [147]. According to Elansary et al. [15], seaweed extract increases the turfgrass quality, the photochemical efficiency of leaves, root length, dry weight, and the total carbohydrates, potassium, calcium, and proline contents in supplemented Paspalum vaginatum (turfgrass) plants under extended irrigation and salt stress conditions. AnE alleviated the effect of salt stress on the growth and efficiency of Persea americana Mill. (avocado) by improving nutrient absorption and showing higher Ca+ and K+ ion contents [156]. Used as a biostimulant, seaweed AnE alleviated the water stress effect and improved the yield and nutrient content of Phaseolus vulgaris [158]. AnE also improved heat stress tolerance as it enhanced CO2 assimilation, rate of transpiration, and stomatal conductance and reduced the leaf temperature [168].
The application of alkaline AnE, Acadian (a commercial product), in drought-stressed Glycine max L. (soybean) altered the expression of GmCYP707A1a and GmCYP707A3b, genes that are implicated in the catabolism of ABA [153]. It was also noticed that the AnE-treated plants changed their expression of the “GmRD22, GmRD20, GmDREB1B, GmERD1, GmNFYA3, FIB1a, GmPIP1b, GmGST, GmBIP, and GmTp55” stress-responsive genes [153]. AnE improved the expression of diverse miRNAs related to nutrient uptake and enhanced salt stress tolerance in A. thaliana [169]. Bioactive organic compounds of AnE have been reported to regulate the union and communication of different transcription factors such as “DREB/CBF, COR47, NF-YA, COR15A, AGF2, CCA1, and LHY1,” which improve stress tolerance in plants [170,171]. Rayirath et al. [50] observed that AnE application in A. thaliana stimulated the cold-responsive genes “COR15A, RD29A, and CBF3” and improved the plant’s cold stress tolerance. Stimplex, an AnE-based commercial product, upregulated 635 genes and downregulated 456 genes and strongly influenced the expression of genes involved in CO2 fixation, glutathione, phenyl propanoid, stilbenoid metabolism, and plant–pathogen interactions [172]. In AnE, the upregulation of defense pathway genes such as PinII (jasmonic acid), Etr1 (ethylene), and PR-1a (salicylic acid) enhanced the auxin-responsive proteins such as SAUR21 and indole-3-acetic acid-amido synthetase in AnE-treated tomatoes [172]. It was observed that the AnE alleviated the effect of heat stress by activating heat shock proteins (HPS), which mainly influenced the AtHSP17 family, particularly AtHPS17.4 and AtHPS17.6A and B, confirming the most significant changes [173].

6. Ascophyllum nodosum Extract (AnE) Reduced Oxidative Stress

Stress causes the production of reactive oxygen species (ROS), which damage the structures of proteins, lipids, carbohydrates, and DNA, impairing plant growth and development [174]. Under stress, enzymatic and non-enzymatic mechanisms such as superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione reductase (GR), and glutathione peroxidase (GPX) play critical roles in ROS scavenging. The application of AnE to bean (P. vulgaris) improved drought tolerance by reducing ROS, inducing lipid peroxidation (MDA content), improving CAT activity, and enhancing proline biosynthesis [157]. AnE increases flavonoid content, and flavonoids protect the roundworm Caenorhabditis elegans from oxidative and heat stress [175]. It was found that there was an increase in root growth of 58% and enhanced freezing tolerance in A. thaliana while using A. nodosum extract [63,143]. Burchett et al. [176] observed that using AnE increased barley’s winter toughness and cold tolerance. It was reported that AnE improved the leaf water relations, maintained the cell turgor pressure, and enhanced the growth of spinach by reducing stomatal limitations under drought stress conditions [145]. The expression of glutathione-S transferase was elicited by bioactive substances of AnE, resulting in the reduction of salinity-induced oxidative damage in A. thaliana [177]. AnE reduces oxidative stress damage by altering the expression of miRNAs and targeting the copper–zinc SOD1 gene, AtCSD1, which is essential in superoxide radical detoxification [169]. Increases in the activities of antioxidant enzymes such as superoxide dismutase, catalase, ascorbate peroxidase, peroxidase, and reductase nitrate, as well as proline concentration, were observed following AnE concentration treatment [168]. The spray application of 0.3% AnE enhanced the chlorophyll content and the activities of anthocyanin, proline, and antioxidant enzymes [172].

7. Ascophyllum nodosum Extract (AnE) Induced Defense Enzymatic Activity

A. nodosum contains laminarans with low and high molecular weights. Laminarans are intracellular water-soluble β-D-(1--3) glucan and β-D-(1--3) oligoglucans known as elicitors of phytoalexins. Laminarans are competent in eliciting D-glycanase activities such as “laminaranase, α-amylase” in Rubus fruticosus suspended cell cultures [178]. Applying seaweed extract induced peroxidase activity in the Capsicum annuum plant [179]. Laminaran and fucoidan exhibit a sample array of elicitor and growth-development activities [45]. Carrot and cucumber plants accumulated high levels of defense-related gene transcripts, received higher activity from defense-related enzymes, and showed increased levels of phenols when treated with AnE. Seaweed extract significantly increased chitinase, glucanase, peroxidase (PO), polyphenol oxidase (PPO), phenylalanine ammonia-lyase (PAL), and lipoxygenase enzyme activities [16,17,18]. The AnE treatment of postharvest plums increased polygalacturonase (PG) activity [180].

8. Ascophyllum nodosum Extract (AnE) Improves Disease Resistance in Plants

In recent years, environmental conditions and exhaustive agricultural practices have increased the occurrences of highly infectious diseases in plants, reducing crop productivity [181]. Due to their effectiveness in controlling microbial infections in crop plants, the use of chemical-based fungicides in cultivation has become limited over time. As a result, researchers must explore alternatives to improve crop health that involve priming the defense systems of plants to enhance their resistance levels against microbial or pathogenic infections. Modern-day crop protection strategies and signaling biomolecules or elicitors are promising biological and eco-friendly practices [182]. Bioactive organic molecules present in AnE elicit defense reactions against the pathogens that cause plant diseases [60]. AnE has been formerly reported to decrease the severity of pathogens, including viruses [183], bacteria [184], and fungi [185].
Seaweed extracts are used in plants to protect them from pathogenic infections, either directly or indirectly. A. nodosum has the potential to act as a protectant to control plant diseases. Both foliar (spray) and soil applications of seaweed extract were found to be effective in reducing foliar and soil-borne pathogens against a variety of crops [16,17]. Cucumber plants sprayed with an A. nodosum commercial seaweed extract (StimplexTM) showed significant reductions in fungal pathogen inoculation levels with Alternaria cucumerinum, Didymella applanata, Fusarium oxysporum, and Botrytis cinerea [17]. Comparable results were obtained when carrot plants treated with AnE demonstrated prominently lower rates of infection from Alternaria radicina and B. cinerea fungi compared with control plants [16]. In Capsicum annuum, treatment with AnE increased foliar resistance to Phytophthora capsici [179]. The application of AnE to greenhouse cucumber plants revealed a considerable decline in damping-off disease caused by Phytophthora melonis [18]. The use of a commercial AnE significantly suppressed the infection of broccoli by Plasmodiophora brassicae [186]. Seaweed-supplemented A. thaliana plants elicited defense responses against the necrotrophic pathogen Sclerotinia sclerotiorum, and jasmonic-acid-dependent systemic resistance in the leaves was induced against the hemibiotrophic pathogen Pseudomonas syringae [187]. Radwan et al. [188] observed the consequences of algae (A. nodosum) on the root-nematode M. incognita in a tomato crop, finding a reduced number of root galls and a better growth of infected plants. Drenching Brassica oleracea with AnE stimulated microbes more than Pythium ultimum, resulting in a lower frequency of damping-off disease in seedlings [189]. In tropical tomato plants, using AnE via foliar application increased disease suppression frequency caused by Alternaria solani and Xanthomonas campteris and subsequently increased the fruit yield [190]. Ajah [191] found that A. nodosum possesses an antifungal activity against Candida albicans. Ali et al. [14] discovered that a 0.5% concentration of seaweed extract reduced the severity of bacterial spot disease and the early blight of tomato and sweet pepper in tropical conditions as an AnE biostimulant induced plant growth and a defense mechanism against foliar diseases caused by X. campestris pv. vesicatoria and A. solani [14]. The rigorousness of Fusarium head blight, which is caused by Fusarium graminearum (Gibberella zeae), was decreased by the application of AnE to Triticum aestivum (wheat) [89]. Similarly, at a concentration of 0.4 mL/L, AnE reduced brown rot disease in the plum fruits by 50%, a disease which is caused by members of the Monilinia genus: M. fructicola, M. laxa, and M. frutigena [180]. Paiva et al. [192] reported that at a concentration of 40 mL/L of AnE, the mycelia growth of the fungus Rhizopus stolonifer was significantly reduced, ultimately decreasing the incidence of soft rot by up to 22.3% in postharvest Fragaria ananassa (strawberry). Islam et al. [193] reported that the pretreatment of A. thaliana roots with alkaline AnE reduced the extent of Phytophthora cinnamomi colonization.

9. Ascophyllum nodosum Extract (AnE) Has Antimicrobial Activity

A. nodosum has anti-microbial activity: it reduces the growth of Escherichia coli, Streptococci, and Lactobacilli [194]. The soil application of AnE enhanced the antifungal activities of Calibrachoa × hybrida against Aspergillus flavus, Candida albicans, Penicillium funiculosum, and Penicillium ochrochloron [64]. A. nodosum has anti-microbial activity against pathogens such as E. coli, Murococcus pyogenes var. aureus, Streptococcus pyogenes, and Salmonella typhosa [195]. Laminarin shows antibacterial activity, and it inhibits the activities of E. coli, Listeria monocytogenes, Salmonella typhimurium, and Staphylococcus aureus [196]. Ascophyllan, an organic compound present in AnE, showed antibacterial [197] and antiviral [198] activities. The acetone extract of A. nodosum demonstrated significant antibacterial activity and was more effective against Gram-positive bacteria such as Micrococcus luteus and Staphylococcus aureus than against Gram-negative bacteria such as E. coli and Enterococcus aerogenes [199]. In another study, Frazzini et al. [200] reported that AnE inhibited the activity of E. coli more significantly in comparison to other seaweed extracts.

10. Ascophyllum nodosum Extract (AnE) Stimulates the Production and Antioxidant Activities of Secondary Metabolites

Secondary metabolites are phenolic compounds that play a vital role in plants as they have antioxidant potential. Flavonoids comprise an essential group of polyphenolic compounds in plants and demonstrate more potent antioxidant activities [201]. The use of the commercial product “Tasco-Forage”, a feed supplement derived from dried A. nodosum, increased the activities of the antioxidant enzymes SOD, GR, and APX and non-enzymatic antioxidants such as ascorbic acid, α-tocopherol, and β-carotene, in forage grasses and turf [202]. A. nodosum (AnE) stimulates flavonoid synthesis and increases the total phenolic content (TPC), total flavonoid contents (TFCs), and total antioxidant activities in Spinacia oleracea, thus enhancing its nutritional value [175]. In A. nodosum-treated plants of Calibrachoa, Elansary et al. [64] found enhanced phytochemical compositions. Similarly, the regular application of seaweed can potentially improve phytochemicals and significantly increase the TPC and TFC in cabbage [103]. Frioni et al. [125] observed that the application of seaweed extract significantly increased anthocyanin in the three most crucial grapevine cultivars. Spiraea nipponica and Pittosporum eugenioides showed higher phenolic and proline concentrations and flavonoid contents under drought stress when treated with AnE [147]. Under the conditions of prolonged irrigation gaps and salt stress, seaweed-treated turfgrass increased CAT, SOD, and APX activities and non-enzymatic antioxidants and also reduced lipid peroxidation [15]. Phlorotannins are central antioxidant molecules in the hydroalcoholic extracts of Ascophyllum [203]. Phlorotannins are important polyphenols for the biological activity of an organism [37,38,39]. Polymeric phlorotannins inhibit enzymes such as phospholipase, lipoxygenase, cyclooxygenase-1 [204] and hyaluronidase [205]. Phlorotannins isolated from A. nodosum with molecular weights ranging from 30 to 100 kDa inhibited α-amylase and trypsin in a noncompetitive manner [206]. Fucoidan from A. nodosum inhibited α-amylase and α-glucosidase enzymes effectively [207]. Chrysargyris et al. [159] observed that the foliar application of 1% biopost-AG200 biweekly for up to five weeks increased the comparative growth and postharvest quality of lettuce in a potassium-deficient condition by enhancing antioxidant activity. Applying Ascophyllum nodosum to postharvest plums increased the total phenolic content (TPC) in “Irati” plums [180]. The treatment of broccoli florets with A. nodosum and amino acid-based filtrate increased the TPC, sinapic acid, and quercetin levels [208]. AnE-treated okra plants showed significantly increased carotenoid contents under drought stress [172].

11. Ascophyllum nodosum Extract (AnE) Regulates the Biosynthesis of Growth Hormones in Plants

Growth hormones, also known as “phytohormones”, are low-molecular-weight compounds formed in very minute quantities. They regulate several physiological, morphological, and growth-developmental processes in plants [209]. Auxins, gibberellins, cytokinins, abscisic acid, ethylene, jasmonic acid, salicylic acid, brassinosteroids, and strigolactones are the major plant hormones [210]. Growth and development-supporting results of AnE in plants were recognized due to the different types of “phytohormone-like substances” present in A. nodosum [5,22,60,166]. Khan et al. [5] reported about a dry extract concentration of about 50 mg/g of indole-acetic acid (IAA) in A. nodosum. According to the results presented by Castaings et al. [211] and Krouk et al. [212], AnE upregulates the expression of the nitrate transporter gene (NRT1.1), which induces nitrogen (N2) sensing and the transport of auxins; consequently, the development of lateral roots improved, and nitrogen assimilation was enhanced. The findings of Rayorath et al. [63] proposed that the organic fraction of AnE regulates the auxins’ responsive promoter elements (AuxRE), which help in the regulation of the auxin activity of A. thaliana. At a concentration of 0.2%, the foliar application of neutral and alkaline-based AnE upregulated the expression of SAUR33, SAUR59, and SAUR71, whereas SAUR1 and SAUR50 were downregulated [213]. Small, auxin-induced RNAs, also called small auxin-up RNAs (SAURs), play a significant role in growth, physiological, morphological, and developmental procedures in plants [214]. A commercial product of AnE, Seamac, induced maximum callus formation in soybean, which indicates that AnE has cytokinin activity [215]. The root application of alkaline AnE triggered the cytokinin-responsive promoter ARR5 [209]. According to Wally et al. [209], AnE stimulated the expression of the IPT3, IPT4, and IPT5 genes, which regulate the activities of isopentenyl transferases (IPTs), which are involved in the biosynthesis of cytokinin in A. thaliana. Similarly, AnE stimulated the regulation of the gene involved in the synthesis of gibberellic acid (GA) when applied to roots [209]. The expressions of gibberellic-acid-responsive genes, GASA1 and GASA4, in A. thaliana were regulated by the foliar spray of AnE at a concentration of 0.2% [213].

12. Ascophyllum nodosum Extract (AnE) Improves the Soil Health and Rhizospheric Microbial Population

Soil health is the capability of the soil to function as an essential, living ecosystem that maintains animals, plants, and humans. The alginic acid and poly-uronides in AnE improve soil water retention, crumb organization, aeration, and capillary action, stimulating plant root systems, increasing soil microbial activity, and improving mineral accessibility and assimilation [216]. They also increase the movement of carbohydrates and other organic compounds inside the plant [217]. A commercial seaweed extract from A. nodosum applied to the roots of hydroponically grown Hordeum vulgare increased plant growth by 56–63% over the control [99]. It was found that the bioactive substances and organic sub-fractions reported in A. nodosum affected the rhizobia–legume signaling process, resulting in more functional, healthy nodules and enhancing the growth of the Medicago sativa plant [26]. A commercial product of AnE, Active, was used as a natural iron chelator, which increased the rhizospheric microbial population and productivity in the strawberry crop [218]. A. nodosum’s commercial product Acadian increased the number of microbes in the rhizosphere of a ten-day-old alfalfa plant prior to inoculation with Sinorhizobium meliloti [26]. A. nodosum increased soil microbial activity in treated strawberries and carrot roots, and the alginates in AnE improved the soil’s physical condition by binding with metal ions in the soil and forming high-molecular-weight polymers that took up moisture from the soil and increased soil aeration and water-holding capacity [5,166,218,219] (Table 5).
Table 5. Effects of commercial products and Ascophyllum nodosum seaweed extract (AnE) derived from different plants under biotic stress.

13. Conclusions

The world’s population is increasing every day, and food demands are also increasing. Therefore, to maintain the increasing population, agriculture must be supplementary and more fruitful than ever. In modern agricultural practices, the cultivation of crops is dependent on synthetic fertilizers. To combat abiotic and biotic stresses and improve plant health, chemical fertilizers and pesticides are constantly used. To decrease dependence on elementary fertilizers and pesticides, it is essential to include natural resources and compounds in agricultural practices that promote the growth of crop plants under apparently poor growing conditions without adverse side effects on the surrounding ecosystems.
This review emphasized the significant role of AnE in various crops, vegetables, fruits, pulses, etc. The application of AnE significantly improved the germination rate, increased the growth of lateral roots, enhanced water and nutrient use efficiencies, increased antioxidant activity, increased phenolic and flavonoid contents, increased chlorophyll and nutrient contents, alleviated the effects of abiotic as well as biotic stresses in different crop plants, and even improved the postharvest quality of different fruits and vegetables. The applications of A. nodosum-based commercial products as plant biostimulants are diverse, as they promote plant growth while reducing the negative effects of biotic and abiotic stresses. In addition, AnE has been observed to perform as a biocontrol mediator and improve soil health and the rhizospheric bacterial population. Although the present situation for AnE as a biostimulator in agriculture shows potential and affects forward progress toward achieving goal of sustainability, it is essential to thoroughly focus the research on the saturation of these commercial AnE extracts in agricultural practices. Further identification of the mechanism of action of AnE on the plants will enhance the extension of AnE applications into many other fields of agriculture.

Author Contributions

Methodology design, draft preparation, and writing—original review, A.R.S.; data curation and investigation, S.K.; editing, K.D.S., A.R.S., D.P., R.C., S.N.S., V.D.R., M.S.V., R.A.M., A.N.S. and S.S.S. All authors have read and agreed to the published version of the manuscript.

Funding

The research was financially supported by the project of the Ministry of Science and Higher Education of Russia on the Young Scientist Laboratory (no. LabNOTs-21-01AB, FENW-2021-0014) and the Strategic Academic Leadership Program of the Southern Federal University (“Priority 2030”).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data, tables, figures, and results in this article are our own and original.

Acknowledgments

The authors are thankful to the Department of Botany, M. D. University, Rohtak for proving all supports for the said research.

Conflicts of Interest

The authors declare no conflict of interest.

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Screening and Prioritization of Pesticide Application for Potential Human Health and Environmental Risks in Largescale Farms in Western Kenya
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