2024 年 12 巻 p. 295-312
Abiotic stress is one of the major perils in agriculture that reduces crop yield at an alarming rate. Hence, exploring an important plant stress-mitigating technique is critical. Seaweeds are extensively used as plant biostimulants and their biostimulatory properties are due to bioactive compounds such as polysaccharides, pigments, phenolic compounds, proteins, phytohormones, and numerous micro and macro nutrients. Foliar applications of seaweed extracts (SWEs) exhibit promising outcomes for plants’ stress alleviation. Seaweed, namely Ascophyllum spp., Sargassum spp., Kappaphycus spp., and Ulva spp. are the best candidates evaluated to improve plant growth and development under various abiotic stress conditions. Foliar sprays of SWEs improve crop growth, boost final yield, and product quality. Furthermore, the mechanisms activated in response to stress when SWEs are used are largely unknown. However, existing phytostimulatory components could affect plant metabolism by activating numerous enzymes in the phenylpropanoid pathway, and their antioxidant properties could lessen the degenerative effects of reactive oxygen species that accumulate in plant tissues during a stressful environment. Noticeably, SWEs regulate the expression of phytohormone-responsive genes, which in turn control endogenous phytohormone levels, thereby improving plant growth and development. This review explores seaweed taxonomy, biostimulatory properties, and the impact of foliar applications of SWEs on crop production under abiotic stresses, including the way SWEs attenuate the deleterious effect, highlighting limitations, areas requiring further investigation, and potential developments.
Crops’ sessile nature makes them vulnerable [1] to abiotic stresses such as drought, salt, extreme temperatures, nutritional deficiencies, and heavy metals [2, 3, 4]. These stressors pose a serious threat to crop growth and development, resulting in substantial crop losses [5, 6] and questions about food security worldwide. The likelihood of yield reduction due to severe drought conditions could increase to 68% and 64% for wheat and rice, respectively [7]. Salt stress on crops causes 10% to 50% of the yield, and the losses vary with the salt concentration present [8]. Even though breeding and genetically engineered and genome-edited crops have produced a number of varieties with increased abiotic stress tolerance, their practical application is dependent on lengthy processes such as biological cycles and legal considerations. Therefore, searching for an alternative and strategic approach to tackling extreme abiotic stresses is crucial [9].
Exogenous application of natural chemicals namely, phyto and biostimulants are emerging as a promising and environmentally sound option for improving crop performance under stress conditions [10]. Extracts derived from marine natural resources (e.g; seaweeds), are gaining impetus in agriculture due to their biostimulatory properties that are directly associated with their spectacular bioactive components [11]. Seaweed extracts (SWEs) account for over 33% of the total biostimulant market, globally and are projected to be worth €894 million in 2022 [12]. Plenty of seaweeds have been documented to exhibit plant-growth-promoting and yield-boosting actions when applied to crops as foliar sprays or to the roots [13, 14, 15, 16, 17]. Interestingly, seaweed-based formulations combat major fungal, viral, and bacterial phytopathogens as extracts contain an array of bioelicitors that potentially elicits systemic acquired resistance (SAR) or induced systemic resistance (ISR) in infected plants [18, 19].
Furthermore, the application of seaweeds has demonstrated beneficial effects against abiotic stresses [20, 21]. The approach represents a potentially novel solution in plant protection to modify the physiological process of antioxidant defense mechanism and improve plant tolerance under abiotic stress-induced conditions [22, 23]. This article highlights the recent findings that give tantalizing prospects for foliar applications of SWEs to minimize the effect of major abiotic stresses on crop production and focuses on seaweed taxonomy and biostimulatory capabilities, as well as how the application of SWEs mitigates the negative impacts and outlines the challenges and constraints, as well as possible advancements in the sector.
Seaweeds or marine macroalgae are multicellular, plant-like, and photoautotrophic organisms that are generally called “the ocean’s living bioresources” [24]. The abundance and the distribution of these marine resources depend upon a multitude of physical properties, including light quality and intensity, substrate, tidal activity, water temperature, wind and storms, chemical factors viz., pH, gases, nutrients, salinity, and biological factors such as microbes, herbivores, symbionts, endophytes, etc. [25]. Seaweed distribution is highly limited by a few factors like light intensity, nutrient concentration, and substrate. Although Seaweeds are conspicuous in tropical regions, seaweeds can be found all around the world. Around 9600 species of seaweed have been reported so far. Further, different physiological conditions of diverse species control their distribution [26]. These form widespread and prolific benthic marine vegetation along the world’s offshore rocky shores, coral reefs, mangrove forests, or seagrass meadows, and their niches cover approximately 3.4 million km2 area [27].
Algae classification is chiefly based on their pigmentation. The three broad groups of algal clades include red (Rhodophyta), green (Chlorophyta) and brown (Phaeophyta) [28]. Although each group uses different pigments to collect photosynthetically active radiation (400–700 nm), chlorophyll is found in all seaweeds. Green seaweeds are photophilic, contain high levels of chlorophyll a and b and are often found in shallow subtidal or intertidal environments [29]. Because of their accessory pigments, brown (xanthophylls) and red seaweed (phycoerythrin and phycocyanin) may endure poor light levels, while red seaweed is known to have a tolerance to very low light levels. Therefore, red seaweeds are dominated in benthic environments and high-light attenuation areas [30]. Laminariales and fucales are larger seaweeds with high nutritional demands that commonly dominate beaches in higher latitudes where temperatures are cold and nutrient concentrations are rich [31].
SWEs are rich in a myriad of bioactive compounds such as minerals (macro and microelements), organic compounds (osmolytes, amino acids, polysaccharides, vitamins and vitamin precursors), phenolic substances (galloyl, catechol), phytohormones (auxins, cytokinins, gibberellins, etc.) and antioxidants (catechin, ascorbic acid) are highly abundant [32]. SWEs would be applied to the plants as soil applications or as foliar sprays [33]. However, foliar application SWEs seemed to be the most effective application type, and application in the morning resulted in better results since the stomata are fully activated in leaves. When SWEs are used as foliar applications, nutrients present in SWEs are freely absorbed by leaves, mainly via stomata and cuticle hydrophilic pores (Fig. 1). However, nutrient absorption through stomata is highly affected by environmental factors (e.g; temperature, relative humidity, light intensity, and wind velocity), which manage the stomata and cuticle permeability [32]. To be activated by these mineral nutrients, SWE should enter the cytoplasm of the cell and perform interactions with respective compounds (Fig. 1).
Previous experiments on biostimulant activities of SWEs ensured the stimulation of SWEs on plant growth and development through the activation of enzymatic reactions [13]. This was achieved through enhanced nutrient absorption by roots and inspiring plant defense mechanisms even under biotic and abiotic stresses [34]. These stimulatory reactions are governed by numerous bioactive compounds contained in the SWEs [34]. Furthermore, it has been reported that biostimulatory reactions of SWEs occur due to combined interactions of molecules existing in the SWEs; thus, the overall result of these reactions is considered a holistic approach for plant growth and development. The modes of biostimulatory responses of SWEs both under stress and non-stress conditions in advance are depicted in Fig. 2.
Plants treated with various SWEs have enhanced the nutrition absorption rate compared to non-treated plants in most experiments [34]. Generally, plants absorb nutrients through roots or the surface of foliage; whereas SWEs would change the physicochemical and biological properties of soil, leading to modification of the root architecture to facilitate nutrient uptake in an efficient manner [32]. For instance, alginic acid presence in brown seaweed indicated soil conditioning properties and chelated some metal ions, creating high molecular weight polymers [35]. These polymers improved the soil water retention capability of the soil, thereby promoting root growth and microbial activities in the soil [36]. Alginic acid existing in the brown SEWs induces hyphal growth and elongation of arbuscular mycorrhizal fungi (AMF); improves the phosphorus uptake of plants [37]. Studies further reported that genes involved in phytohormones secretion were unregulated by seaweed extract and would enhance plant growth and development [38]. Furthermore, vitamin K1 compound found in Kahydrin SWE induced rhizosphere acidification via the alternation of plasma membrane protein pumps and H+ ions released into the rhizosphere [39].
Moreover, Almaroai and Eissa [40] suggest that Mg in SWEs acts as a key ingredient in the chlorophyll synthesis process. Numerous biostimulant compounds present in SWEs elicit the gene responsible for nutrient uptake [32, 34]. For instance, Ascophyllum nodosum extract unregulated the expression of a nitrate transporter gene in roots; BnNRT1.1 and BnNRT2.1 enhanced the nitrogen assimilation and auxin transport [41] through enhancing of lateral roots. Simultaneously, overexpression of BnSultr4.1 and BnSultr4.2 genes stimulate sulfur absorption [41]. Moreover, A. nodosum extracts further enhanced biomass, antioxidant, chlorophyll, flavonoids and phenolic content in plants through stimulation of genes (e.g; GS1) related to phenylpropanoid and flavonoid pathways to activate several enzymes namely chitinase, betaine aldehyde dehydrogenase, glutathione reductase (GR), ascorbate peroxidase (APX), RuBisCO and carbonic anhydrase; thus, enhancing the overall growth of plants [42]. In addition, correlation analysis between overexpressed genes and their impacts exhibited a positive relationship since SWE increased the number of chloroplasts, chlorophyll content, and starch assimilation [42]. Interestingly, A. nodosum extract’s effect on root nodule formation in alfalfa plants showed activation of the Nodc gene of bacteria significantly maintained the bacteria-plant signaling process while increasing the number of nodules [43].
3.2 Mechanism and mode of biostimulatory activities under stress conditionsSWEs have been effectively evaluated under stress conditions, especially aiming at drought mitigation. However, the absolute mechanisms behind these actions are still unknown [34]. When plants are subjected to drought stress, a variety of management strategies are implemented to maintain water equilibrium within the plant, including stomatal closure, wilting, hormonal signaling, antioxidant species production, lower levels of sugar deposition, and defense metabolites [44]. Stomatal closure reduces CO2 availability, electron transport capability, RuBisCO activity, and has consequences in the Calvin cycle, resulting in excessive reactive oxygen species (ROS) production [45]. The accumulation of ROS in the cytosol results in cellular level disruptions. Hydrogen peroxide (H2O2), singlet oxygen (1O2), superoxide radicals (O2-), and hydroxyl radicals (HO•) are the major ROS compounds that function as secondary messengers at lower concentrations [46]. However, at higher concentration results in denaturation of proteins, lipid peroxidation, and lower nutrient uptake [47]. As a result of lipid peroxidation, free radicals and malondialdehyde (MDA) are being produced in the cells. Free radical compounds create cellular damage, including in chloroplasts and mitochondria [48]. Moreover, when drought stress intensifies; proline-like osmo-protectant production and accumulation extensively increases [46]. Figure 2 illustrates the several biostimulatory reactions of SWEs under non-stress and stress.
The application of SWEs stimulates the antioxidant enzymes (e.g.; superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD)) and accelerates the activities of several molecules (e.g; α-tocopherol, ascorbate, and β-carotene; [49]. SOD catalyzes both 1O2 and O2- radicals’ presence in the cytosol and concurrently reduces the synthesis of HO• [50]. CAT and POD catalyze H2O2 and detoxify into H2O. The absence of H2O2 encourages balanced redox stability of the cytosol by mitigating drought stress [51]. In addition, some phenolic compounds (e.g; flavonoids, tannins, lignin, and hydroxycinnamate esters) present in the cytosol could take part in plant defense mechanisms against stress; thus, the phenolic concentration would decrease [52]. SWEs application stimulates starch metabolism by mobilizing carbohydrate reserve into sugars; thus, promoting growth even under drought situations [53]. Besides, SWEs convert starch reserves into leaves, resulting in an enhancement of the glucose level in the cytosol [54]. Simultaneously, metabolites produced from starch degradation act as osmo-protectants which maintain the osmotic equilibrium of cells [53]. In addition, SWEs affect enzyme activities which involve controlling oxygen levels in photosystems I and II and maintaining the ROS concentration [55].
Like non-stress conditions, several genes would activate to mitigate drought stress conditions after the application of SWEs. For instance, abscisic acid (ABA) responsive genes namely At5g66400 and At5g52310 are overexpressed and maintain the functions of photosystem II [34]. On the contrary, overexpression of antioxidant coding genes (e.g; At5g42800 and At1g8830) averts oxidative damage in photosystem II [34]. Furthermore, ROS detoxification processes are upregulated by several genes including GmGST, GmBIP, and GmTP55 [56]. As a result of gene activation, lipid peroxidation would become lower and glucose, proline, and sucrose concentration could be enhanced [34].
In addition to drought stress, salinity also has a high impact on growth and final yield [57, 58] stated that treating saline stressed plants with Ulva rigida extracts could restore the photosynthetic activity of pigments which is attributed to the betaines in the SWEs. The great quantities of antioxidant components in the SWEs exhibited a positive correlation with the augmented photosynthetic pigments under saline conditions. Further, the chlorophylls found in the photosynthetic membranes could be protected by the photosynthetic apparatus from extreme ROS by quenching of 1O2 and other radicals. Similar to drought stress, salinity induces ROS production in the cytosol and disturbs the cell’s functions [57]. Through a similar process explained under drought stress; enzymatic and non-enzymatic (e.g; phenolic compounds) antioxidants activate and alleviate the ROS concentration in the cytosol [59]. For instance, APX and CAT antioxidant enzyme activities increased after the application of A. nodosum extract treated plants [60]. Additionally, glycine betaine is involved in extenuating the salt stress through upregulating ROS scavenging and osmotic adjusting mechanisms [61]. Salinity stress causes overexpression of genes, including ABA signaling genes, glutathione S-transferase encoding genes, and dehydration-responsive protein transcripts [62]. Simultaneously, microRNA (miRNA) also plays a massive role in stress mitigation, both in salinity and drought conditions [34]. For instance, Shukla et al. [63] discussed the diminishing of the NaCl-induced up or downregulation trend in miRNAs including ath-miR396a-5p, ath-miR399, ath-miR2111b, and ath-miR827 after application of A. nodosum extract. Furthermore, the SEW modified the expression of ath-miR399 and several genes such as AtUBC24, AtWAK2, AtSYG1 and At3g27150 ensuring A. nodasum is involved in phosphate homeostasis.
In temperate countries, cold stress is also considered abiotic stress in the plant development process. Like other abiotic stresses, freezing stress also disturbs plant growth and development. Proline and other compounds such as soluble sugar and unsaturated fatty acid content are enhanced significantly due to cold stress. Proline synthesis occurs when the 5CS1 and 5CS2 genes upregulation and 9SEX1 and SEX4 genes’ overexpression enhance soluble sugar content. Furthermore, upregulation of DGD1 engages in the synthesis of galactolipids, which are considered a key substance in cold stress mitigation [34]. The use of SWEs shows that the chlorophyll content of cold-affected plants increases due to the downregulation of chlorophyll degradation genes, namely AtCLH1 and AtCLH2. In addition, DREB1A and COR78/ RD29A gene activation results in cryoprotection of chloroplast stomatal proteins; thus, tolerance to cold stress [64].
Compared with freezing stress, heat stress has momentous implications for vegetative and reproductive growth [65]. Since global temperatures have been rising during the past few decades, it might frequently result in severe heat waves; thus, creating a negative impact on plants [66]. Heat stress results in malfunctioning of physiological reactions including photosynthesis and carbohydrate portioning processes, membrane disruptions, and protein denaturation [65, 67]. To overcome heat stress, plants would synthesize heat shock proteins (HSP) which are considered the first defense mechanism of plants’ cells and prevent protein denaturation [68, 69]. Furthermore, McLoughlin [70] reported HSP70 and showed orchestrate mechanism between HSP101 and sHPSs for reversing the permanent accumulation of heat-sensitive proteins. Apart from gene expression regulated activities; antioxidant protection mechanisms, and enzymatic or non-enzymatic detoxification mechanisms, which are explained under drought, salinity, and cold stress, occur similar ways to mitigate heat stress [71].
Abiotic stress amelioration with the foliar sprays of SWEs is well documented in different crop production systems. Recent findings that give tantalizing prospects for foliar applications of SWEs to minimize the effect of major abiotic stresses are listed in Table 1.
| Crop | Name of the seaweed/s | Findings | Reference |
|---|---|---|---|
| Drought stress | |||
| Grapevine (Vitis vinifera) | Ascophyllum nodosum | Foliar applications preserved photosystems integrity and vineyard resilience and improved water use efficiency under water deficit conditions | [72] |
| Potato (Solanum tuberosum) | Ascophyllum nodosum/Ecklonia maxima | Foliar sprays with Bio-algeen S90 (A. nodosum) and Kelpak (E. maxima), along with humic and fulvic acids, improved drought tolerance and increased potato tuber yield by 2.15 tons/ha | [73] |
| Tomato (Solanum lycopersicum) | Ascophyllum nodosum | Foliar sprays of SWEs showed lower lipid peroxidation levels and greater expression of tas14 that encode dehydrin proteins associated with long-term drought tolerance | [74] |
| Soybean (Glycine max) | Ascophyllum nodosum | SWE and fulvic acid boosted photosynthetic activity, improved energy dissipation efficiency, and increased antioxidant enzyme activity, leading to enhanced recovery from water deficit. | [51] |
| Gracilaria tenuistipitata | Foliar application of 10% seaweed extracts increased grain yield by 54.87% and 23.97% | [75] | |
| Sugarcane (Saccharum spp) | Ascophyllum nodosum | SWE enhanced stalk sucrose accumulation, increasing sugar and stalk yield. Elevated antioxidant enzyme activity and reduced malondialdehyde levels indicated improved metabolic activity and biomass production | [76] |
| Spinach (Spinacia oleracea) | Ascophyllum nodosum | The SWE improved spinach growth by enhancing foliage water relations, maintaining cell turgor pressure and decreasing stomatal limitation | [77] |
| Sweet orange (Citrus sinensis) | Ascophyllum nodosum | The crop biostimulant Stimplex® (5 mlL-1) treated to both drought-stressed rootstock and trees boosted growth and drought tolerance compared to untreated ones | [78] |
| Bean (Phaseolus vulgaris) | Fucus spiralis Ulva rigida |
Both SWEs improved vegetative parameters and increased stress tolerance | [79] |
| Sage (Salvia officinalis) | Ulva rigida | Under the water stress conditions, the SWE enhanced the antioxidant potential and drought tolerance | [80] |
| Canola (Brassica napus) | Sargassum angustifolium | Foliar sprays of extract improved canola plant shoot height, dry weight, and enhanced photosynthesis, free radical scavenging, and superoxide dismutase activity under water-deficit stress. Real-time PCR showed increased proline content likely due to P5CS overexpression, crucial for proline biosynthesis, and reduced PRODH | [81] |
| Wheat (Triticum aestivum L.) | Sargassum denticulatum | The foliar application of SWEs 2% enhanced all growth and yield parameters while accumulation of the organic solutes in leaves and increased compatible osmolytes and antioxidants | [82] |
| Faba bean (Vicia faba L.) | Fucus spiralis and Ascophyllum nodosum | Foliar application of SWEs accumulation of osmo-protectants and osmo-regulators as proline and soluble sugars, the improvement of relative water content in plant tissues as well as phenols, and the reduction of lipid peroxidation | [84] |
| Mustard (Brassica juncea) | Ascophyllum nodosum | SWE combined with ortho silicic acid increased photosynthetic rate, stomatal conductance, transpiration rate, relative water content, water potential ad osmotic potential, decreased canopy temperature depression, proline, glycine-betaine, H2O2 and MDA and improved the yield | [85] |
| Salinity stress | |||
| Eggplant (Solanum melongena) | Ascophyllum nodosum | Foliar application of 5 mlL-1 of SWE was highly effective and it significantly increased SOD and APX | [86] |
| Durum wheat (Triticum durum) | Fucus spiralis | Seedlings treated with the water extracts of F. spiralis increased shoot length and the foliar application increased CAT, SOD, APX and GR in salt-stressed plants in greenhouse | [87] |
| Amaranthus (Amaranthus tricolor) | Ascophyllum nodosum | Spraying A. nodosum extract at a rate of 2.5 mlL-1 increased morphometric parameters of inflorescence and enhances the potted Amaranthus tolerance against salinity | [88] |
| Sugarcane (Saccharum spp) | Laminaria japonica | In the soil at a depth of 20–40 cm, root dry weight and root length density rose by 45.0% and 9.8%, respectively, and 38.3% and 8.9%. Decreased the oxidative damage to roots brought on by drought stress and increased the activity of antioxidant enzymes, viz., SOD, CAT, and POD, in roots | [89] |
| Rice (Oryza sativa) | Ascophyllum nodosum | Enhanced shoot and root biomass, maintained ionic balance, improved gas exchange and antioxidant mechanism, increased chlorophyll and carotenoid contents by spraying of 2 mlL-1 concentration | [90] |
| Okra (Abelmoschus esculentus L.) | Sargassum wightii | SWE effectively increased growth-promoting metabolites and hormones, enhancing plant vegetative and reproductive development and reduced H2O2 and ABA levels while increasing lipids, proteins, carotenoids, and proline | [91] |
| Tomato (Solanum lycopersicum) | Jania rubens | Liquid SEWs from both the fresh and dried J. rubens not only enhanced total chlorophylls, soluble sugar and total free amino acids but also increased enzymatic and non-enzymatic antioxidant activities and improved salt tolerance of tomatoes | [92] |
| Heat stress | |||
| Grapevine (Vitis vinifera) | Ascophyllum nodosum | The foliar application of A. nodosum extract increased stomatal conductance, transpiration, and leaf thermoregulation and facilitated vine recovery after temperature stress | [93] |
Growing impacts from climate change recorded an unprecedented increase in the occurrence and severity of the drought. It arises as a result of the cumulative effects of temperature dynamics, light intensity, and low rainfall and its’ multidimensional characteristics have a harsh influence on morphological, physiological, biochemical, and molecular attributes of crops that ultimately impact photosynthetic capacity and reduce the yield [94]. A plethora of findings shed light on how the foliar sprays of different SWEs function as biostimulants to counteract the deleterious impacts caused by the drought (Table 1).
Freshly produced and commercially accessible seaweed products have proven effectiveness in reducing water-deficit stress in a variety of crops. In a pot experiment, treating drought-stressed okra with 0.3% of a commercial extract of A. nodosum significantly replenished chlorophyll content, increased the activities of anthocyanin, proline, and antioxidants namely, APX, POD, and CAT and improved biochemical and physiological functions [83]. In another study, a biostimulant, ERANTHIS® (a seaweed product made with A. nodosum and Laminaria digitata and yeast extracts), alleviated water-deficit stress on tomatoes. Spectrophotometric determination of the biostimulant showed that the formulation had bioactive substances including phenolic components, flavonoids, flavan-3-ol, and flavanol families. Antioxidant capacity assays exhibited that the commercial product had strong radical scavenging activity, and the foliar application reduced the levels of stress indicators ABA and MDA and proline content associated with the lower activities of ROS compared to those in control [95]. In addition, Ecklonia maxima-derived SWE enhanced total chlorophyll, proline, and ascorbic acid in both drought-stressed and non-stressed leafy vegetable chicory (Cichorium intybus) [96]. Kappaphycus alvarezi seaweed extract (KSWE) is well known for its bioactive components, namely glycine betaine (GB), choline chloride (Ch), and zeatin, and their individual role in soil moisture stress alleviation on maize revealed elevated antioxidant enzymes and yield responses in the 10% KSWE-treated or 10% equivalent titer of GBCh application [97].
Drought stress instigates membrane lipid peroxidation in plants. MDA is a biochemical marker for lipid peroxidation. Higher levels of MDA indicate more lipid peroxidation and membrane permeability, and the plants are attributed to being more susceptible to water-deficit conditions. Jacomassi [76] found that the foliar sprays of A. nodosum boosted stalk and sugar yield by 3.08 tha-1 and 3.4 tha-1, respectively, in drought-stressed sugarcane, and decreased the levels of MDA, which further contributed to the lessening of the membrane damage induced by the drought stress in the plants. In addition, leaf analysis revealed that the biostimulant application decreased carbohydrate reserves and increased total sugars, resulting in an enhancement in metabolic activity in the plants.
Foliar applications of SWE not only induce growth and yield but also modify the physiology of the plants and regulate the expression of drought tolerance-related genes under stress conditions. For instance, a commercial extract of A. nodosum can mitigate the drought stress impacts on the soybean. Drought-stressed soybeans given SWE exhibited higher physiological attributes in relative water content, stomatal conductance, and antioxidant activity. Furthermore, quantitative real-time PCR analysis revealed the changes in the stress-related genes, viz., FIB1a, GmBIP, GmCYP707A1a, GmCYP707A3b, GmDREB1B, GmERD1, GmGST, GmNFYA3, GmPIP1b, GmRD20 and GmTp55 responsible for ABA biosynthesis and ROS detoxification [56]. The mechanisms of action of foliar application of KSWE on maize leaves were investigated using a transcriptomic analysis. To combat drought stress, genes involved in nitrate transport, signal transmission, photosynthesis, trans-membrane transport, and starch biosynthesis were upregulated, while genes involved in the catabolism of polysaccharides were downregulated [98].
4.2 Foliar application of seaweed extracts to alleviate salinity stress in cropsSalinity is one of the most destructive abiotic stresses, impacting crop growth and metabolism because of osmotic stress generated by salt [99]. Sodium chloride is the most common salt in saline areas, which is toxic to plants in higher amounts [100]. Several investigations (Table 1) found the mitigating effect of SWEs applied under saline conditions. For instance, potted rosemary plants treated with foliar sprays of 0.2% of Sargassum latifolium seaweed extract significantly augmented growth and oil yield attributes, photosynthetic pigments, antioxidant related enzymes POD, POP, and ascorbate oxidase, while the treatment decreased the activities of CAT and indole acetic acid oxidase compared to those untreated controls [101].
In another study, foliar application of water extracts of 12.5% of U. rigida improved growth and photosynthetic pigments in salt-stressed durum wheat. The application significantly improved antioxidant activity-related compounds viz., SOD, isocitrate dehydrogenase, glutathione peroxidase, and GR in stressed plants [58]. In NaCl stressed chickpeas (Cicer arietinum), foliar applications of S. muticum and Jania rubens extract enhanced photosynthetic pigments. A critical defensive mechanism against salinity stress is the Na+ extrusion, which was also observed in the seaweed extract-treated plants. Further, comparative analysis revealed that the amino acids for example serine, threonine, proline, and aspartic acids in the roots were responsible for the seaweed-mediated NaCl stress amelioration. Furthermore, the treatment resulted in enhanced levels of enzymatic antioxidants including SOD, CAT, APX, and POD [102].
4.3 Foliar application of seaweed extracts to alleviate temperature stress in cropsTemperature changes due to climatic fluctuations are already a global concern [103, 104] and could harm crops irreversibly by disrupting physiological and biochemical pathways [105, 106]. SWEs give better solutions for both the crops that are affected by the low or cold temperature stress or the heat stress. The applications of A. nodosum exhibited significant effects on flower development, pollen viability, and fruit production. In addition, examination of floral tissues revealed the expression of heat shock protein genes namely HSP 101.1, HSP70.9, and HSP17.7C-Cl under heat-stressed conditions. Similarly, overexpression of small heat shock-protein in tomato anthers and young fruits has been given a significant contribution to heat tolerance [66].
In general, the beneficial effects of SWEs-based biostimulants on crop production and the eco-system rationalize their usage in many crops. So far, existing field data of SWEs in various cropping systems has demonstrated the positive effects on plant growth, vigor, resistance to pests, diseases, and abiotic stresses, and an overall increase in plant productivity. The positive outcomes of the SWEs are primarily depended on numerous factors namely seaweed types, quality of the raw material, extracts’ composition and method, frequency and the concentration of application. Furthermore, all the improved growth responses were only detected with the whole extract, revealing the highly interactive nature and synergistic action of the seaweed extract components on plant growth and behavior. However, due to their complexity, the synergistic activities, and interactions of biomolecules, as well as their molecular roles on plants, remain largely unclear. The next section covers the limitations of using SWEs as a biostimulant for abiotic stress alleviation in three categories: seaweed collection, extraction techniques, and applications.
5.1 Seaweed collectionDespite the fact that seaweeds are a sustainable natural resource, collecting, processing, and storing seaweed biomass poses major obstacles. Furthermore, seasonal growth and input of seaweed feedstock encourage industries to rely on effective cultivation practices, rapid processing, and storage technologies [34]. Appropriate harvesting approaches for a few seaweed species have been proposed and adopted successfully, for instance, brown kelp. However, harvesting knowledge of most of the key seaweed is not known. Problems in wet and dry processing and preservation methods, storage, extraction, and biotransformation occur due to a lack of understanding of the seaweed harvesting process [107]. Another barrier is obtaining high-quality biomass on a consistent basis because environmental conditions alter both the chemical content and its activity [108]. Until recently, most seaweed production has been directed towards human food, the phycocolloids sector, and biostimulant production [109].
5.2 Extraction methodsThe extraction procedures used are crucial in order to extract as many bioactive compounds as possible. The procedure included source material pretreatment, extraction stages, separation, and concentration [110]. Additional pre-treatments are required to increase the recovery time and ultimate outcomes in many circumstances [111]. Conventional methods have significant constraints for industry, most notably time consumption, high energy requirement, and solvent. Furthermore, rigorous techniques using high temperatures and long extraction times may have deleterious effects on the compounds and their functionalities, stressing the need for new extraction strategies to be developed and used. Convection via the solvent and conduction from the surfaces to the core of the matrix particles are both important heating mechanisms for efficient extraction in traditional extractions [112]. Furthermore, bioactive compound extraction is challenging to optimize since it is extremely dependent on seaweed origins, geographical position, harvesting season, solvent concentrations, temperature, pH, raw material size, and time [113]. Also, a higher volume of hazardous waste generation resulted from the conventional extraction technique due to the toxic organic solvents used. It further increases the carbon footprint in the environment. There are a variety of sustainable technologies and procedures that enable the efficient recovery of diverse compounds via various extraction processes while keeping fascinating functional characteristics. However, each new technique has a set of constraints to limit its adoption in the mass-scale production of SWE.
Most advanced approaches, namely microwave-assisted extraction (MAE), ultrasound-assisted extraction (UAE), enzyme-assisted extraction (EAE), supercritical fluid extraction (SFE), pressurized solvent extraction (PSE), and electro technologies (ET), necessitate a one-of-a-kind technology as well as significant upfront capital and equipment expenditures. Furthermore, a continuous process necessitates the use of skilled human resources. For instance, while the MAE approach has the potential for commercial scale-up, the effectiveness of wave penetration into feedstock matrices is restricted [110, 113]. Even though the UAE requires a significant initial investment owing to the energy requirement and equipment costs, its utilization is still restricted [110, 113, 114]. In the EAE method, terrestrial biomass enzymes are used. However, it shows slow enzymatic kinetics due to the lower amount of specificity for substrate [110]. Further studies on innovative extraction methods should be reconsidered [115].
5.3 ApplicationsThe application of the proper SWEs can boost root and shoot vigour; however, the selection of the suitable SWEs is crucial since the benefits vary significantly between species. SWEs are often employed in agriculture as either pure or complete extracts [112]. Currently, only liquid, dispersible, and soluble solid formulations are available. There have not been many recorded successful attempts to develop unique commercial formulations for use in conventional and protected crop production systems using SWES [41]. While there is a plethora of beneficial effects of SWE-based foliar and seed priming applications, there are also some unwanted side effects posed by seaweed-based products that must be addressed in advance. For example, heavy metal and persistent organic pollutant contamination of seaweed bio-resources threatens its broad usage in agricultural applications [116]. SWEs elicit an array of biostimulatory effects in plants against abiotic stresses, however, their genetic, physiological, and biochemical mode of mechanisms are largely unraveled.
Moreover, the majority of the SWEs’ impacts on abiotic stress mitigation findings are based on greenhouse and controlled environment research; the same results may not be anticipated for field level applications. SWE delivery is now mostly restricted to foliar and soil application, which is typically costly due to the high levels and repeated sprays required, which is a restriction for sustainable use.
An extensive range of SWEs based formulations are available for agricultural purposes, as a result, the foundation for widespread usage of SWEs has already been laid. Although the efficacy of many of these extracts has been demonstrated, particularly under experimentally controlled environments, mechanisms of action need to be identified in-depth. Similarly, more field research should be undertaken to find the optimal application rate and frequency of extracts for different crops and soil conditions. Such experiments must address the question of what the return on investment in order is to disclose the true value of adoption. Although a lot of studies on the use of SWEs and their integral bioactive chemicals is encouraging, a deeper knowledge of holistic modes of action and abiotic responses, particularly in enhancing plant immunity, is required.
Field crops are genuinely subjected to multiple stressors at about the same time. Using numerous SWEs simultaneously, or at specified times, may help to mitigate the effects of several stressors on crops. Furthermore, the functional versatility of SWEs should be considered because a single extract often activates many plants stress signaling pathways [117, 118]. Hence, more study is needed to determine whether the positive benefits of SWEs are enhanced under abiotic stress conditions when mixed with other biostimulants, including microbial biostimulants, or even fertilizers and organic manures.
Extraction techniques for some of the potential seaweed must be refined. In terms of formulations, a successful initiative to produce innovative commercial formulations to use under abiotic stresses needs to be fast-forwarded. Instead of trying to extract as many bioactive chemicals as possible, the extraction process should be tailored to the seaweed species, application mode, crop type, and expected physiological impact (e.g., abiotic stress tolerance, improving soil fertility, improving fruit quality, etc). Because various interactions may occur within the bioactive compounds that are available in a SWE, resulting in both synergistic and antagonistic effects. Finally, to fully use the algal biomass, integrated extraction systems that combine methodologies need to be explored.
Abiotic stressors such as drought, salt, high temperatures, and cold cause physiological, biochemical, and molecular changes in crops, resulting in lower relative water content, increased ROS production, increased relative stress injury, cell electrolyte leakage, decreased photosynthetic pigment count, shorter root and shoot length, and lower yield. Seaweeds are plentiful marine resources with numerous bioactive molecules, have recently attracted interest to mitigate the detrimental effects of abiotic stresses on agricultural productivity. Foliar application of SWEs seems to be the most effective treatment form, with morning applications yielding greater benefits since the stomata are fully engaged. Seaweed species such as Ascophyllum spp., Ulva spp., Sargassum spp., and Kappaphycus spp. have been extensively studied in crop production as foliar applications under non-stress and abiotic stress conditions. Under stress environments, foliar sprays of SWE not only increase crop growth and yield but also change its physiology via increasing stomatal closure, production of photosynthetic pigments, water use and nutrient use efficiency, modulating gas exchange and regulating the osmolytes, and affecting the expression of abiotic stress tolerance-related genes. In stressed plants, the SWE application increased enzymatic and non-enzymatic antioxidant activities and reduced the damage caused by ROS. However, the exact mechanisms behind these stimulatory actions are still unknown.
