The use of brown algae, being a renewable resource, is a promising option with various application options in agricultural systems, mainly in the form of extracts, direct applications, and compost. Brown algae are a source of active biomolecules and minerals that are currently used as agricultural biostimulants, since they increase crop productivity. This type of biostimulants derived from brown algae improve seed germination, increase the accumulation of plant biomass by accelerating cell division and elongation, activating the antioxidant system of plants, making them more resistant to stress, and contributes to the absorption and translocation of nutrients present in the soil. These products are also compatible with other agricultural inputs, such as synthetic fertilizers and pesticides, which makes them ideal for comprehensive applications and maintaining a balance in agroecosystems. This review incorporates fundamental and applied aspects of brown seaweeds that impact yields, biochemical quality, physiology, stress mitigation, and soil properties.
Introduction
The term algae refers to a large and diverse set of organisms that live in water or in very humid environments. They are characterized as photosynthesizing organisms with higher efficiency than vascular plants, where carbon (C), nitrogen (N), phosphorus (P), and potassium (K) are the main elements required for photosynthesis and growth. They are autotrophic organisms with simple structure, no cell differentiation and complex tissues and are therefore considered thallophytes. Marine macroalgae are divided into three groups (green, red, and brown). Brown algae belong to one of the most abundant groups and are used in different areas (biorefinery, food, agriculture, among others); they comprise about 2000 species and 250 genera, including Ascophyllum spp., Fucus spp., Laminaria spp., Sargassum spp., Ecklonia spp., Stoechospermum spp, etc. Taxonomically, brown algae are eukaryotes grouped in the class of Phaeophyceae, in which xanthophylls, pigments that give their characteristic brown coloring, predominate. Xanthophylls, such as fucoxanthin, are carotenoids that play an important role in the adaptation of these organisms to environmental changes. Their cell wall is basically made up of cellulose, alginates, and sulphated polysaccharides (fucoidan) consisting of fucose, mannose, galactose, xylose, and glucose.
Products derived from brown algae contain a large number of bioactive compounds (carbohydrates, phytohormones, vitamins, phenolic compounds, proteins, amino acids, carotenoids, and beneficial and essential elements) and have an important impact on agriculture due to their effectiveness to improve plants growth. Brown algae products improve plants growth and mitigate some stresses by regulating molecular, biochemical, and physiological processes. The brown algae most commonly used in agriculture are Fucus vesiculosus, Ecklonia maxima, Sargassum johnstonii, and Ascophyllum nodosum, the latter being the most studied.
Brown algae products are considered one of the most promising biostimulants, as they contain different effector biomolecules, compared to other biostimulants that act alone. These different biomolecules contained in brown algae act together and potentiate their biostimulant effect, which can cause more marked changes due to their high biological activity. As already mentioned, the function of these products is direct when the biomolecules act directly on the plants and cause changes in the omics levels and is indirect when they modify the soil characteristics. However, these products have biomolecules with antimicrobial, nematicidal, and insecticidal properties against crop pathogens, so they can be used as biopesticides. It is important to differentiate the concept of biostimulant and biostimulation to avoid future confusion. These concepts are recent, and everything stems from biostimulants, which are any substance or microorganism applied to plants that promote nutritional efficiency, stress tolerance, and improved crops quality, regardless of their nutrient content. Now, biostimulation is a biological response triggered by biostimulants, which causes the adaptive modification of metabolic processes, so that the organism makes adjustments that lead to a more efficient use of resources.
Accordingly, and considering the purpose of conserving agroecosystems and the growing demand for food, the application of brown algae in agriculture is feasible, since its use reduces the application of agrochemicals and offers products free of toxic residues to consumers, which is beneficial to the environment. Therefore, the aim of this review is to present the advances published in the literature on brown algae, their derivatives, their composition, and their function in agriculture plants and soil, considering genera and species, application methods, environmental conditions, and crops production systems.
Formulations of Brown Algae
Brown macroalgae can be applied in agriculture in the form of extracts, direct application of fresh or dried stems and in the form of composts. The algae extracts will directly biostimulate the metabolism of the plants, due to their action at low concentrations, while for direct applications and composts, it is advisable to carry out a mineral analysis to the products, soil, and water and thus establish a program of proper application. The agricultural use of these algae today is based on their application forms, which cause varied effects on plants.
2.1. Extracts
It has been more than 60 years since the first seaweed extracts were manufactured for agricultural purposes; these extracts allowed, for the first time, the direct use of the soluble substances contained in seaweeds on specific parts or organs of plants, such as seeds, roots, leaves, and fruits, thus allowing for a more varied use of seaweeds and therefore different plants responses to such applications.
Different institutions and companies use different procedures for the extraction of compounds of interest from brown algae biomass; these extractions are performed under different techniques using different solvents, such as water, ethanol, potassium hydroxide, methanol, chloroform, among others. According to the extraction technique, any of the different solvents can be used; these techniques can be microwave, ultrasound, hydrothermal, and supercritical fluid.
Extractions are also enzymatic, where the use of solvents is null. Enzymatic extraction of bioactive compounds in algae offers the advantage of not using solvents, and the extraction can be more efficient than other methods by degrading complex molecules present in the cell wall or bound with polymers in the cytoplasm, achieving a more effective release and keeping their biological properties intact.
The different methods of extraction, application, and the different genera and species of brown algae make the biological activity of extracts very varied when applied to plants. In agriculture, diluted extracts are applied to promote growth, prevent the incidence of pathogenic organisms, and increase the quality of harvested products. Its efficiency is probably based on the phytohormones, vitamins, phenolic compounds, carbohydrates, proteins, amino acids, and beneficial elements present in the extracts.
There are different conditions to be considered when applying brown algae extracts. One of them is that they have to be used as supplements to increase yields and crops quality and not as nutrient substitutes. It is possible to combine the extracts with inorganic fertilizer to achieve synergy and achieve higher productivity, profitability, and sustainability. Foliar applications, applications to the soil (drench), and applications on seeds can be made, which will show different but positive responses, since the form of application influences the results (Figure 1). Soil applications should be made directly or incorporated into the nutrient solution or irrigation water.
The application of brown algae extracts will also depend on the concentration used, since the use of this type of biostimulant normally works at relatively low doses, as long as an application schedule is established. For the use of this type of biostimulants, different application intervals are normally used, ranging from 7, 10, 15, 20, and 30 days. An important point is that, according to existent studies, it is more common to use foliar extracts, for which it is advisable to do so in the early morning or at dusk to avoid burning the foliage and to make the application more effective.
2.2. Direct Applications
The first uses of brown seaweed were as a fertilizer, and this use was as direct application. This term refers to the practice of incorporating fresh or dried seaweed into the soil as it is obtained. Normally this activity is limited to coastal areas, as transport and availability reduces its use in areas far from the sea. Direct applications of brown seaweed can also be in the form of granules, powder, or the pulp residues remaining after extractions. The direct application of brown algae improves the physical, chemical, and biological characteristics of the soil or substrate. This phenomenon is attributed to the process of incorporation and decomposition of the algae into the soil, as they encourage the multiplication of native soil bacteria. This conditioning action improves the soil structure, making it more porous and stable, and therefore increasing its capacity to retain water, while nutrients are released for assimilation of plants (Figure 1).
An important point that has to be considered in the direct application of brown algae to the soil or substrate is the concentration of salts and sand that may bring the algae, so it is advisable to wash it before application. In addition, at the cellular level, algae contain different heavy metals, which are a point to consider before their application.
The direct application of brown algae represents a potential alternative for soil improvement, due to the gradual decomposition of its compounds that enrich the soils organic matter. The incorporation of fresh or dried algae into the soil can be achieved by first crushing the material to facilitate its decomposition, then leaving it in the surface and incorporation it with a plow or hand equipment, as if it where the incorporation of stubble.
Some authors relate the soil remediation effects to the presence of alginic acid and mannitol, which comprise a large part of the carbohydrate content of algae and their function is related to the complexation of contaminating compounds. It has also been shown that the effect of algae depends to a large extent on the presence of nutrients that are mineralized with the help of soil microorganisms. One benefit of the application of algae to cultivated soils in tropical areas is the reduction in leaching of nutrients during heavy rainfall. This happens thanks to carbohydrates, which form high-molecular-weight complexes with metal ions in the soil; the structure and water retention capacity are improved, and, consequently, the root growth of the plants is increased, which in turn increase the level of exploration for nutrient absorption.
When algae are incorporated into the soil, they undergo a process of decomposition, which is facilitated by fungi and bacteria that metabolize and decompose organic materials. Terrestrial plants and brown algae are mainly composed of cellulose, hemicellulose, lignin, proteins, and other carbohydrates; however, brown algae have a more complex composition of structural sulphated polysaccharides in the cell wall. This variability in the composition of sulfate polysaccharides that is not associated with terrestrial plants require metabolic pathways that are not common in the environment, which makes decomposition difficult. It is mentioned that the current understanding of microbial communities involved in the degradation of brown algae in soil is still poor, which has important considerations for its application in agriculture, as degradation regulates the availability of essential nutrients and bioactive compounds.
Applications and Effects of Brown Algae in Plants
The impact of brown algae on plants depends on factors such as algae species, environmental conditions, cultivar type, and type of application. These effects include improved seeds germination, nutrients uptake, increased crops yield, and quality, as well as increased resistance to biotic and abiotic stresses (Figure 1). Brown algae contain large amounts of metabolites, but carbohydrates and minerals predominate in greater quantities, making them ideal candidates for use in agriculture. Genera such as Ascophyllum, Fucus, and Ecklonia are among the most widely used in agriculture because of the amount of N and K they contain, which are similar to animal manure and organic fertilizers, but with a low P content.
Each of the compounds that make up brown algae has a specific function when applied to plants. The carbohydrates that make up a large part of the content of brown algae are the most important regulators that facilitate many physiological processes, such as photosynthesis, flowering, seeds germination, and tolerance to various abiotic stresses in crop plants. Carbohydrates in plants participate as signaling molecules in response to various environmental and nutritional conditions and are therefore important for maintaining their metabolic homeostasis during stress, as well as providing energy and helping to make signaling more effective. Other important components in brown algae are amino acids, proteins, and fatty acids, which have very specific functions when applied to plants. Proteins are very important metabolites in plants, having diverse functions, such as catalysis, transport, defense, structure, regulation, signaling, and reserve. Amino acids are another coarse group of metabolites in brown algae, and their function is vital when applied to plants, as they are involved in N assimilation, nutrient transport, and environmental stress mitigation. Among the amino acids present in brown algae, proline and phenylalanine stand out, as they are involved in the mitigation of osmotic stress by retaining a greater amount of water in the cytoplasm and in the synthesis of phenolic compounds, which are important metabolites of the antioxidant system of plants. Amino acids are generally considered as precursors and constituents of proteins and play and important role in plants metabolism and development.
Fatty acids in plants, like carbohydrates and proteins, have essential functions not only because they are major components of all cells but also because they are an important source of energy for various metabolic processes and can also function as mediators of signal transduction in stress by acting as intracellular and extracellular signals.
The main biomolecules are not the only ones that make brown algae desirable for agriculture. There are compounds which can regulate different physiological and biochemical processes. Among these compounds are phytohormones, such as auxins, gibberellins, and cytokinins, which act on cells as chemical messengers and are able to regulate various vital phenomena in plants. Studies have showed tha A. nodosum shows contents of up to 50 mg of indole-3-acetic acid (IAA) per gram of dry extract. In addition, brown algae contain considerable concentrations of abscisic acid (ABA), salicylic acid (SA), and jasmonic acid (JA). These three molecules are phytohormones with a well-documented role in plant response to biotic and abiotic stress. The action of these hormones against stress develops through synergistic and antagonistic actions.
There are other substances in brown algae that have a biostimulant effect on plants, such as phenolic compounds, which perform certain defense functions to deal with biotic and abiotic factors, and in addition to this, it fulfills important functions in plants by providing certain colors, flavors, and function as an attractant for pollinators. Brown algae products also contain betaines. This compound plays a very important role in plants, one of which is to mitigate osmotic stress induced by water deficit or salinity, as well as increasing chlorophyll by inhibiting its degradation in treated plants.
Selenium (Se), silicon (Si), and iodine (I) are beneficial elements that brown algae contain and have very important biostimulants functions in plants. It has been shown that Se helps plants to improve their growth and defense system; in addition to this, its electronic configuration is like that of sulfur (S), where it is shown that it has the ability to replace it and perform its functions. The Si has certain benefits in plants, such as greater growth, stronger plants, greater photosynthesis, and increased tolerance to stress. The Si also regulates cuticular water loss due to its accumulation in the epidermis. There are studies that indicate that I was one of the first inorganic antioxidants that allowed organisms to resist oxidative stress. The function of I is widely proven in marine algae, where the element neutralizes the superoxide anion (O2), hydrogen peroxide (H2O2), and singlet oxygen (O2). In addition to this, there are studies that show that in terrestrial plants, I applications increase antioxidant capacity, thus conferring greater resistance to abiotic stress. Brown algae products, applied directly or composted, improve soil health, making it more fertile, benefiting plant nutrition.
3.1. Brown Algae Products on Growth, Yield, Physiology, and Quality of Crops
As already mentioned, brown algae in agriculture have been used as nutritional supplements and as an alternative to chemical products, which has had a satisfactory impact on crops production. Someone applied A. nodosum extracts via foliar application to bell pepper crop and reported increases in agronomic, biochemical, physiological, and mineral variables in fruits and leaves at a dose of 0.5%. The authors attribute the effects to the chemical composition of the extract, since it contains dissolved nutrients and functional organic molecules that promote plant growth and activate the antioxidant system (phytohormones, carbohydrates, and proteins). And others applied a commercial extract of A. nodosum to tomato crop in the form of drench (2.5, 5, and 10 L ha-1), and their results indicate that growth and yield, plant physiology, and fruit quality parameters were improved. The authors attribute the effects to the sulfated polysaccharides contained in the extracts, which stimulate several signaling processes, improving nutrient use efficiency and stimulating N metabolism, thus improving tomato growth, yield, and quality.
The uptake of plants nutrients depends on several factors, and one of them is a function of the roots, where they are normally available in the soil solution; therefore, an extensive root system is a requirement to ensure sufficient nutrients uptake. Several studies have shown that plants biostimulants, such as the brown algal extracts, boost root system development, which is reflected in a higher level of soil exploration, thus allowing for increased crops yield, as mentioned that they treated tomato seeds with 1% Macrocystis pyrifera extracts and indicated that root length, shoot length, and germination percentage increased. They mentioned that according to principal component analysis and hierarchical cluster plots, the improvement in germination was related to the sterol content in the extracts, while shoot and root length were related to the levels of K, Zn, B, Na, N, carbohydrates, and phenolic compounds. Similarly, others indicated that foliar and soil application of A. nodosum extracts to tomato and eggplant seedlings improved growth parameters and biomass of aerial and root parts along with foliar chlorophyll content. It is evaluated the foliar application of Sargassum spp. extracts produced under different conditions of temperature, extraction time, and percentage of ethanol on tomato seedlings at a dose of 1.5%. Their results show that the extract produced at 160 ℃/30 min/50% ethanol increased to a greater extent the growth and biomass of the aerial and root parts and the foliar concentration of pigments and antioxidant metabolites. The authors indicate that these effects were the result of the higher concentration of proteins, glutathione, and amino acids in the extract, which are metabolites capable of stimulating the metabolism of N and C in plants.
The improvement of crops production and yield depends mainly on its genetic characteristics and on the other side by environmental conditions; therefore, the interaction of these factors determines the yield of the crops, and for this reason it has a high variability over time. Considering the conditions that determine yield, there are studies that have shown that the use of biostimulants such as algal extracts have the potential to boost crops production and yield characteristics. It is evaluated seed priming and foliar application of A. nodosum extracts on soybean at doses of 0.25 and 0.5% and showed in their results an increase in leaf and stem biomass, a higher number of pods and seeds, and a higher number of nodules. The authors mentioned that these increases were related to the higher activity of enzymes involved in N metabolism, which also increased N, S, Mg, and K uptake. The better nutrient uptake is possible thanks to the amino acids and sugars contained in the extracts, as they have a complexing function, together with the fact that these extracts are enriched with some nutrients.
The use of macroalgae in general is very extensive, given that different types of brown, green, or red algae can be used, which have varied effects on plants. It is evaluated the effect of the application of brown (S. johnstonii) and green (Ulva lactuca) seaweed extracts on seeds germination and initial growth of eggplant, tomato, and chili seedlings. The findings of the study showed that the brown seaweed extracts gave better results in both germination and initial seedlings growth variables at a dose of 4%. The results are attributed to the considerable content of micronutrients and phytohormones in the extracts. Similarly, others applied foliar extracts of brown (Sargassum swartzii) and red (Kappaphycus alvarezii) seaweeds in cowpea cultivation, and their results show that brown seaweed extracts showed the best effects on yield and nutraceutical quality at a dose of 3%. The authors conclude that the reason why brown seaweed extracts were more effective is due to the higher concentration of macronutrients and micronutrients compared to red seaweed extracts. It is evaluated seeds germination and initial vegetative development of bean seedlings in response to the application of watery extract of brown (Sargassum vulgare) and red algae (Osmundaria obtusiloba). Their results indicated that 25% red algae extract gave the best results. Within the experiment, the concentration of proteins and carbohydrates in the extracts was determined, with the red algae having the highest concentration, which is why it is believed to have produced the best results. All these results are also a product of the conditions in which macroalgae develop, where their biochemical composition is influenced by spatial changes in environmental parameters, so the content of active ingredients varies between and within species, resulting in different responses when applied to crops.
In addition to the above, someone applied seaweed extracts as sources of polysaccharides by collecting 17 species and determining the polysaccharides content and selecting the best six, two red, two green, and two brown seaweed species. Their results indicated that the brown algae extract (Fucus spiralis and Bifurcaria bifurcata) significantly improved seed germination percentage, tomato plant growth, and leaf chlorophyll concentration compared to the other algae and the control, at a dose of 0.1 mg mL–1. Carbohydrates are a group of molecules that have a stimulant effect on crops development, so they applied in wheat and barley laminaran and fucoidan derived from Laminaria cichorioides, whose biopolymers contain carbohydrates. The research shows a stimulant effect at a dose of 10 µg mL–1 on plant height, ear length, number of seeds per ear, and seeds weight per ear, which was reflected in the yield of both crops. Others evaluated different foliar applications of A. nodosum extracts on productive and quality parameters in apples. The applications were made in full bloom, and improvements in fruit yield and quality were observed with the best dose of 0.3%. The authors indicate that this is possible thanks to the compounds contained in the biostimulants derived from A. nodosum, including essential nutrients, carbohydrates, amino acids, and phytohormones.
The use of brown algae in agriculture is normally intended to be used in the form of extracts, but they are also used in compost and direct form. It shows these effects to the increase in organic C and total N in the soil due to the effect of S. polycystum compost, which is richer in nutrients than the compost of plant residues.
3.2. Effect of Brown Algae Products in the Induction of Tolerance to Stress in Crops
Stress in plants is any condition or substance that affects growth, development, or metabolism. This stress can be caused by natural or anthropogenic factors. Some types of stress that plants can experience are extreme temperatures, lack or excess of light, lack or excess of nutrients, salinity, drought, and pathogen attack. All of these stressors are responsible for large production losses worldwide, so the use of products based on brown algae is a feasible option to mitigate their effects, all through the positive regulation of morphological, physiological, genomic, and metabolic parameters, which subsequently leads to the activation of the plants defense system. Someone treated soybean plants under drought stress conditions with A. nodosum extracts (7 mL L-1 via drench). Their results show that plants treated with the extracts had higher relative water content, higher stomatal conductance, and higher antioxidant capacity compared to control treatment. They also indicate that extracts in stressed treatments promoted changes in the expression of stress-progressive genes in leaves: GmCYP707Ala, GmCYP707A3b, GmRD22, GmRD20, GmDREB1B, GmERD1, GmNFYA3, FIB1a, GmPIP1b, GmGST, GmBIP, and GmTp55. Each of these genes has a specific function, coding for certain protection proteins, water transport (aquaporins), signal transduction, osmolyte synthesis, and antioxidants, which provide certain tolerance to plants.
The use of brown algae products has the characteristic of helping plants to use water efficiently in stressful conditions. This level of tolerance related to the efficient use of water is linked to changes in the concentration of osmolytes and the expression of defense genes. It is showed that the tolerance process occurred thanks to the accumulation of osmolytes and the expression of the TAS14 gene in leaves. The TAS14 gene encodes a late embryogenesis abundant protein (LEA) called dehydrin, which is induced by osmotic stress and ABA. The function of this dehydrin is related to the protection of membranes and macromolecules against denaturation, which prevents loss of function. Others foliarly applied A. nodosum extracts (1 L ha–1) in soybeans under water stress (50%) and indicated that there was a decrease in MDA, an increase in relative water content, and an increase in photosynthetic activity.
As mentioned above, products derived from brown algae have the ability to regulate stress in plants through metabolic processes, as indicated, they foliarly applied extracts of Sargassum tenerrimum (10%) on tomato plants to induce resistance to Macrophomina phaseolina. Their results indicate that plants treated with the extracts and the fungus showed the maximum accumulation of SA, ABA, and IAA in the leaves during the vegetative stage. They also show that there was a regulation of O2– and H2O2 mediated by the antioxidant enzymes superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX). These enzymes are the first line of defense against stress in plants and cooperatively reduce the oxidative state.
Another obstacle faced by plants in these times is heat stress, which is caused by high temperatures. This stress causes a series of irreversible damage to crop plants and is usually the cause of low yields. Someone tested the efficiency of extracts (0.106%) of A. nodosum to mitigate long-term moderate heat stress in tomato plants during the reproductive stage. Their results show that foliar applications of the extracts in stressed treatments significantly improved flower development, pollen viability, and fruits production compared to plants that were only stressed. They also indicate that there were important transcriptional changes with increased thermotolerance. Expression analysis of genes encoding for heat shocks proteins (HSPs) was performed in tomato flowers, where it can be observed that HSP101.1, HSP70.9, and HSP17.7C-CI genes were differentially expressed. These HSPs normally increase in concentration under heat stress conditions and protect stress-sensitive proteins from denaturation or misfolding.
Salinity is another stress that causes negative effects on crops growth and yield by causing osmotic and ionic stresses that affect physiological and omics processes. It is evaluated the use of Cystoseira spp. as a soil amendment (15 g of powder seaweed per 5 kg of soil) to mitigate salinity stress (NaCI 75 and 150 mM) in canola. The authors indicate that applications of the algae successfully alleviated the damaging effects of the stress. They mentioned that the tolerance process occurred because the synthesis of antioxidants and osmo-protectants (phenolic compounds, flavonoids, anthocyanins, carbohydrates, and proline) was adequately modulated. Antioxidants help to neutralized stress-synthesized free radicals, and osmo-protectants help cells to retain water in the presence of high salt concentrations. It is also evaluated the effect of extracts (1, 2, and 3 g L–1) of A. nodosum on pepper crop under salinity stress (NaCl 100 mM) in irrigation water. The results indicate that stress negatively affected all growth parameters of the crop. Moreover, the use of the extracts improved plants growth at all concentration levels applied under salinity conditions. The authors indicate that the use of the seaweed extracts on stressed plants increased the activity of antioxidant enzymes in leaves such as SOD, POD, and CAT, and therefore, they suggest that brown algae products are suitable for improving productivity and mitigating the effects of salinity stress in crop plants.
Similarly, others evaluated the use of Lessonia nigrescens polysaccharides in wheat seedlings under salinity stress (NaCl 150 mM). Extraction of the polysaccharides was performed using 100 g of the algae and 2 L of 80% ethanol. After extraction, the polysaccharides were purified and applied to the nutrient solution. The results indicated that the use of the polysaccharides under the stressful conditions promoted seedling growth, increased antioxidant capacity, decreased membrane lipid peroxidation, and improved intracellular ion flux coordination. It is also evaluated the foliar application of extracts of Sargassum spp. in tomato seedlings under salinity stress (100 mM) at a dose of 1.5%. Their results indicate that the extracts activated the enzymatic antioxidant system (CAT, APX, and PAL), non-enzymatic (ascorbic acid, phenols, flavonoids, and glutathione), and the expression of defense genes (NCED1, HSP70, PIP2, P5CS1, ERD15, Fe-SOD, CAT1, cAPX2, and PAL5-3) under stressful and non-stressful conditions. In addition to this, the growth and biomass of the seedlings was improved. The NCED1 gene encodes the enzyme 9-cis-expoxycarotenoid dioxygenase 1, which catalyzes the synthesis of ABA in chloroplasts. The P5CS1 gene encodes the enzyme ∆1-pyrroline-5-carboxylate synthase 1, which catalyzes the synthesis of proline that functions as an osmotic agent, protecting plants from dehydration.
Another limiting factor in crops production is stress caused by nutrients deficiency, which is causing increasing losses in terms of yield and quality of harvested products. It is evaluated the efficacy of extracts (4 g L–1) of A. nodosum on strawberry crop under nutrients deficit stress conditions, the nutrient-limiting condition was imposed by supplying plants with a single fertilization at transplanting and excluding any additional nutrients supply during the experiment. The results show that the foliar application of the extracts induced tolerance in the plants, resulting in higher growth and crop yield. In addition, they obtained fruits with higher content of phenolic compounds, anthocyanins, and antioxidant capacity, and they obtained leaves with higher photosynthetic activity and transpiration. The extracts contained high concentrations of iron (Fe), copper (Cu), and Si. Others applied extracts of A. nodosum and Durvillaea potatorum in Fe-deficient tomato plants, and their results indicate that the A. nodosum extract at a dose of 0.2 mL L-1 increased SOD activity in roots and leaves, the concentration of malondialdehyde in the leaves decreased, and the dry biomass of roots increased. The D. potatorum extract at a dose of 1.1 mL L–1 only increased the activity of CAT in roots. In this study, the concentration of micronutrients, auxins, gibberellins, cytokinins, ABA, SA, and JA in the extracts, compounds responsible for the effects mentioned above, were quantified.
A stress that has been little studied in plants and with the use of brown algae is that of heavy metals. This stress affects plants because they alter their physiological, metabolic, and molecular processes, which affects the yields and quality of the harvested products. Someone treated Brassica chinensis plants with S. polycystum extracts (25, 50, and 100 mL L–1 foliar and drench) contaminated with cadmium (Cd) (100 mg kg–1). The authors mention that there was an increase in biomass and activity of the enzymes CAT, APX, and POD. They also mention that histological characteristics of the leaves such as the size and opening of stomata, mesophyll tissues, and vascular bundles were improved. Regarding the accumulation of Cd, it was demonstrated that as the concentration of the extract increased, the concentration of Cd in the roots and shoots was reduced, which is due to the complexing action of some metabolites of the extracts, such as sulfated polysaccharides. The expression of the rbcL gene was also determined, where an overexpression is observed with the use of the extracts of S. polycystum and Cd. The rbcL gene encodes the RuBisCO enzyme, which catalyzes the assimilation of atmospheric CO2 in the photosynthetic process for the production of photoassimilates and, on the other hand, catalyzes the reaction that initiates the photorespiration process.
Soil Applications of Brown Algae
Soil is the main non-renewable resource and faces the threat of degradation with the growth of agriculture. Intensive agriculture has led to overexploitation of soils, causing erosion problems and ecosystem deterioration. The deficiencies of soils in conjunction with the nutritional need of crops, and the increasing demand for chemical supplies has directed the efforts of the agricultural sector towards the use of available resources. Recently, the use of algae (direct application and composted) as a fertilizer has allowed the gradual replacement of conventional synthetic fertilizers. Brown algae have been widely exploited in the agricultural sector, due to their richness in beneficial trace elements, essential nutrients, and hormones that stimulate plant growth. The application potential of brown algae in soil lies in their ability to compensate for N, P, and K+ deficiency in soils. In addition to activating signaling pathways in the plants and imparting tolerance to biotic and abiotic stresses, thereby improving crops productivity.
4.1. Impact on the Physico-Chemical Characteristics of Soil
Soil fertility is a determining factor for crop production, preservation of ecosystems and cultivable areas. The incorporation of brown algae into the soil is a practice developed since ancient times in coastal areas to improve crops productivity and for the recovery of degraded soils, where nutrients deficiencies are frequent. Brown algae have a great ability to improve the physical and chemical properties of the soil, and they can be applied directly as composts, granules, powders, and extracts; however, the form of application must be considered to avoid problems of salinity, sand residues, and heavy metals. Brown algae also contain a wide range of mineral elements and compounds with complexing functions (sugars and amino acids) that, when applied to the soil, enrich soil fertility, improve soil structure, increase water retention capacity, and total soil porosity. The influence of algae on soil nutrients and aggregated stability is diverse, depending on the organic composition of the algae and the initial nutrients concentrations in the biomass.
Brown algae, when applied in composted or direct form (powders, granules, etc.), contribute to increasing the organic matter in the soil, and this matter influences very important parameters, such as pH, cation exchange capacity (CEC), and nutrient content. On the pH of the soil, humified organic matter has a buffer effect, which reduces the risk of sudden changes in pH, which favors the life of microorganisms, the availability of nutrients, and the elimination of contaminating substances. Microorganisms can slowly adapt to acidic and basic pH values of the soil, but they do not resist the sudden changes that occur with the addition of synthetic fertilizers; for this reason, the use of brown algae products is a promising option. Now, organic matter balances the N in the soil, and thanks to its numerous functional groups, it provides a high capacity for change, which increases the potential for absorption and ionic exchange of the soil, and as a result, increases the retention of nutrients such as calcium (Ca2+), magnesium (Mg2+), K+, etc.
The humified organic matter derived from brown algae has a very marked effect on the physical characteristics of the soil, forming aggregates and giving it structural stability, uniting with the clays and forming the exchange complex, which favors the penetration of water and its retention. When all this is achieved, erosion is reduced, and gas exchange is favored. The humus particles from the organic matter are electrically unbalanced and attract water molecules and retain them, and this facilitates the settlement of the vegetation, making the action of erosive agents difficult. Organic matter, having colloidal properties, due to its charges, in the soil can retain water, swell, contract, fix solutions on the surface, disperse, and flocculate.
The organic matter coming from brown algae, unlike that coming from other plants remains, can have more beneficial effects on the physical-chemical characteristics of the soil; this is because its composition is richer in different biomolecules, mainly alginate, fucoidan, and mannitol. These biomolecules applied to the soil can interact with metal ions (nutrients) and form high molecular weight complexes that absorb water, which improves the structure of the soil, resulting in greater aeration and capillarity of the pores.
The roots frequently breathe carbon dioxide (CO2), which in contact with soil water becomes carbonic acid (H2CO3), which rapidly dissociates into H+ and bicarbonate (HCO3–). H+ ions diffuse into the soil particles and displace other cations that are adsorbed, and thus pass into the soil solution, where they can be absorbed by the roots. The roots can directly diffuse H+ into the soil particles, similarly displacing adsorbed cations into the soil solution. In this way, a cationic exchange phenomenon is generated between the soil and the plants. Now, with the application of brown algae products (organic matter) the CEC is improved, since the colloidal load and complexing compounds in the soil are increased. These compounds can be fucoidan, alginates, mannitol, humic acids, etc., which at the same time improve water absorption, aeration, and the formation of aggregates in the soil. Figure 2 shows schematically those described above. The Figure also illustrates how the OM together with the complexing compounds provide a greater nutrient retention capacity; that is, they have a greater CEC than the soil particles (clays).
4.2. Impact on the Rhizosphere
The use of brown algae or their products has a positive impact on the rhizosphere (Figure 1 and Figure 2), which comprises the interaction zone between plants roots and soil microorganisms. This is related to the increase in beneficial soil organisms, which can solubilize nutrients and produce conditioning substances due to the addition of brown algae.
Soil biota (organisms), including microorganisms, use organic matter (brown algae) as food; therefore, they can increase their colonization in the rhizosphere. By having a good amount and activity of beneficial biota in the rhizosphere due to the application of brown algae, the availability of some nutrients for plants can be improved. The biological fixation of N can be improved by the action of bacteria of the genus Rhizobium, Azotobacter, Azospirillum, etc. Likewise, the solubilization of P (Pseudomonas, Erwinia, Bacillus, etc.) and K+ (Bacillus, Pseudomonas, Arthrobacter, etc.) increases due to the action of their respective bacteria. Now, these bacteria need certain conditions to be able to perform their functions and survive, and the same organic matter from brown algae provides these conditions. In addition to this, there are bacteria (Mycobacterium or Nocardia) that produce siderophores, which have complexing functions and can capture Fe2+ and keep it available for plants. Genera such as Arthrobacter, Azospirillum, Bradyrhizobium, Bacillus, Pseudomonas, and Rhizobium also produce phytohormones, such as auxins and cytokinins, with important functions for plants. Brown algae and their products also improve the development and growth of arbuscular mycorrhizal fungi, where these fungi have a very marked effect on the solubilization of P in the rhizosphere.
The aforementioned tells us about the benefits that brown algae applications provide to the rhizosphere, by improving microbial biomass. These microorganisms also create a protective barrier against fungi and pathogenic bacteria in the roots of the plants. In addition, certain compounds present in brown algae have antifungal, antibacterial, and nematicidal functions when applied to the rhizosphere. These antimicrobial compounds can be mainly phenolic compounds, alginates, laminarin, and fucoidan. The latter is possibly the most effective for controlling pathogens, since it is a sulfur compound with proven antimicrobial action.
As mentioned above, brown algae are mostly composed of carbohydrates, mainly alginates, which stimulate the growth of beneficial microorganisms in the soil. It has been demonstrated that the use of alginate oligosaccharides extracted from brown algae enhanced the growth and development of arbuscular mycorrhizal fungi and improved their infection in orange tree roots.
Likewise, the use of brown algae as soil conditioners has been found to reduce the development of weedy plants and other pathogenic that compete with the crops. Someone evaluated the efficacy of M. pyrifera extracts in combination with A. brasilense in lettuce seedlings with water deficit. Their results indicate that the combination of algae with beneficial bacteria showed a new formula that improved the root development of the seedlings; this is probably due to the synergy between the metabolites of the extracts and the beneficial bacteria. In view of the above, brown algae represent a potential source of exploitation in the agricultural sector, with high importance for the incorporation into the soil.
It is important to keep in mind that the direct use of brown algae sometimes causes problems to the soil and plants, due to the fact that they are not stabilized materials. In addition, algae are characterized by a low C/N ratio and high salinity, which can be solved by composting, a more promising option to avoid these problems. However, another limitation can be the concentration of heavy metals in the algae that can be transferred to the soil and subsequently to agricultural crops, where the concentration can be higher with the direct use or composting of the algae [10,54]. With the use of extracts, heavy metals are not really a problem, since very high dilutions are used to apply them. Currently on the market are different brown algae products that can be applied to all types of crops; however, they are normally products to be applied in the form of extracts. If direct or composted applications are required, large quantities of algae would be needed, and the limitation is that this practice is only viable for producers who are established near the coasts where algae can be obtained.
Mechanism of Action of Algae Products on Plants and Agricultural Soil
When brown algal extracts are applied to plants (foliar, drench, and seeds), they react in different ways through a cell-signaling cascade. All these cellular signaling processes that gives rise to a defense response develop mainly with the binding of biostimulants metabolites to membrane receptors. Said union generates the activation of G proteins, which have the function of inducing the opening of Ca2+ channels so that it enters and can bind to calmodulins proteins. The complex formed between Ca2+ and calmodulins can activate mitogen-activated protein kinases (MAPKs), whose function is to phosphorylate transcription factors. These factors travel to the nucleus and bind to specific DNA sequences and turn on numerous defense genes. Figure 3 shows the process described above.
The other pathway marked in Figure 3 shows signaling by proteins kinases. This MAPKs pathway guides in the signal transduction to downstream transcription factors that produce cellular responses such as proliferation, growth, motility, and the defense response to external stress factors, through differential expression of genes.
This is one of the ways by which the metabolites of the brown algae extracts activate the plants defense system; however, there are others that involve different signaling molecules and second messengers, such as SA, ABA, JA, H2O2, etc.
This signaling process takes place when the cell responds to external substances (biostimulants) or environmental factors (temperature, humidity, and irradiance) through signaling molecules that are on the surface or inside the cell. It is important to mention that the cellular reception mechanisms are still not well understood, and the process involves a very complex network of molecules. In addition to this, biostimulants molecules do not only bind to receptors, since it is also possible that they are transported into the cell by means of membrane transporter proteins and initiate the signaling process directly.
The direct use of seaweed (fresh, dried, or powder) and compost works differently than extracts. Firstly, the physical, chemical, and biological characteristics of the soil improve, such as fertility, CEC, porosity, structure, and microbial biomass. The increase in microbial biomass increases the biological fixation of N, the solubilization of K and P, and the production of siderophores. In addition, there are microorganisms that can synthesize phytohormones. This mode of action that takes place in the rhizosphere brings, as a benefit, crops with better yields, quality, and more tolerance to stress. For this reason, these products are also considered biostimulants, since they can positively modify soil characteristics, thus benefiting plants. In addition, the use of extracts in the form of drench in the root zone is not only used by the roots but can also modify soil characteristics in some way. As a result of these mentioned mechanisms, a new phenotype is obtained, with a higher stress tolerance threshold and higher functional quality of the harvested products, which translates into better crops yields.
Conclusions and Perspectives
Observing the current agricultural panorama, the practices carried out in all production systems are dependent on synthetic chemical products, whether to nourish the crops, eradicate weeds, pathogenic fungi, or insect pests. In accordance with this information, brown algae are a viable option to reduce the use of synthetic chemicals that cause deterioration of the environment and in turn that of the plants. Brown algae products can act as growth stimulants of nutraceutical quality and mitigate biotic an abiotic stress in crop plants due to the content of bioactive compounds they contain.
Most of the research carried out focuses on the use of brown algae foliar extracts, the most studied being A. nodosum, and the direct and composted use of such algae is the least experimented. In general, the use of brown algae in the form of extracts, compost, or direct use has positive effects on the growth and development of crop plants; however, it is important to consider the biological model of study, the concentrations to be used, the form of application (foliar, drench, nutrient solution, seeds or amendment), and the characterization of the product, which will give a broader picture of the effectiveness of brown algae products.
However, all application methods are adequate, since they depend on the objectives sought. If the aim is to produce in soils with problems, it is advisable to apply to the soil to improve its characteristics. Now, if there are no problems in the soil, it is feasible to make applications to the seeds or foliage, to directly stimulate the metabolism of the plants and improve their productivity.
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