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Review

The Use of Microalgae and Cyanobacteria in the Improvement of Agricultural Practices: A Review on Their Biofertilising, Biostimulating and Biopesticide Roles

by
Ana L. Gonçalves
LEPABE—Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, 4200-465 Porto, Portugal
Appl. Sci. 2021, 11(2), 871; https://0-doi-org.brum.beds.ac.uk/10.3390/app11020871
Submission received: 31 December 2020 / Revised: 9 January 2021 / Accepted: 12 January 2021 / Published: 19 January 2021
(This article belongs to the Special Issue New Insight in Microalgae Cultivation and Downstream Processes: Route toward Sustainable and Cost-Effective Production)
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Abstract

:
The increase in worldwide population observed in the last decades has contributed to an increased demand for food supplies, which can only be attained through an improvement in agricultural productivities. Moreover, agricultural practices should become more sustainable, as the use of chemically-based fertilisers, pesticides and growth stimulants can pose serious environmental problems and lead to the scarcity of finite resources, such as phosphorus and potassium, thus increasing the fertilisers’ costs. One possible alternative for the development of a more sustainable and highly effective agriculture is the use of biologically-based compounds with known activity in crops’ nutrition, protection and growth stimulation. Among these products, microalgal and cyanobacterial biomass (or their extracts) are gaining particular attention, due to their undeniable potential as a source of essential nutrients and metabolites with different bioactivities, which can significantly improve crops’ yields. This manuscript highlights the potential of microalgae and cyanobacteria in the improvement of agricultural practices, presenting: (i) how these photosynthetic microorganisms interact with higher plants; (ii) the main bioactive compounds that can be isolated from microalgae and cyanobacteria; and (iii) how microalgae and cyanobacteria can influence plants’ growth at different levels (nutrition, protection and growth stimulation).

1. Introduction

Worldwide population is increasing. According to different studies, this number has raised from six to seven billion between 1999 and 2011, and it is expected to further increase to nine billion by 2050 [1,2]. This increasing trend has resulted in an increased demand for food supplies, with a strong impact on agricultural practices. On the one hand, the increase in the global population results in a higher demand for food products, requiring higher agricultural productivities [1,2,3,4]. On the other hand, the social and economic activities developed by this increasing population have contributed to [1]: (i) a reduction in the area available for the production of food crops; (ii) water resources degradation and scarcity; (iii) accumulation of xenobiotic compounds in the soils; and (iv) degradation of soils’ quality and fertility. To overcome the challenges related to the increase in global population and anthropogenic activities and meet the requirements for food supplies, an improvement in the productivity and sustainability of agricultural practices is required [1,5]. Higher productivities can be achieved in different ways: (i) increasing crops’ yields; or (ii) preventing culture losses under stress conditions (both biotic and abiotic).
Chemically-based products have been widely used in agriculture, either as plant-growth promotors (improving crops’ yields), or as plant protection agents (protecting plants from different stress conditions) [5,6,7,8]. However, most of these agents are toxic and their accumulation in the plants and in the soil can be a threat to humans and to the environment. Moreover, their accumulation has been associated with the development of microbial resistance to several drugs [3,5,7,8]. Considering the negative impacts of these products, current regulations are limiting the use of mineral fertilisers and chemical products in agriculture [5,7]. In the search for more sustainable and environmentally-friendly solutions to improve agricultural productivities, researchers have focused their attentions on biologically-based products, with microalgae and cyanobacteria emerging as a valuable resource for crops’ production and protection due to their biofertilising and biostimulating potential [1,2,3,5,7,9].
The use of algae in agriculture dates from thousands of years ago [5,9]: for example, in coastal areas of Europe, farmers used to apply algae harvested near the shore in their cultures, both directly or after composting, observing positive effects in soil fertilisation. Since this period, algal biomass has been extensively used in agriculture, but in the 20th century, products obtained from algal extracts have attracted the attention of farmers worldwide [5]. In fact, a wide variety of biologically-active compounds extracted from algae and cyanobacteria (e.g., phenols, terpenoids, free fatty acids—FFAs, polysaccharides, and carotenoids) has demonstrated to have promising effects in crops’ production [2,7]. According to the literature, algal metabolites can play an important role in [4,9]: (i) soil decontamination and fertilisation; (ii) plant protection against biotic and abiotic stress factors; and (iii) plant development. In addition, microalgae and cyanobacteria also present phytohormones, which are known for their activity as plant-growth promotors [7,10,11]. Taking into account their potential benefits for the development of a sustainable agriculture, both biomass and extracts from microalgae and cyanobacteria are commercially available [9].
This manuscript presents an overview of how algal biomass and extracts can improve crops’ production, presenting the most recent applications of these microorganisms in the agricultural sector.

2. Microalgae as a Source of Biofertilisers, Biostimulants and Biopesticides

Microalgae and cyanobacteria are an important source of biologically-active compounds, such as phenolic compounds, polysaccharides, hormone-like substances and proteins, known for their benefits as antioxidant agents, plant-growth promotors, among others. Moreover, living organisms, both prokaryotes (e.g., nitrogen-fixing cyanobacteria) and eukaryotes (e.g., microalgae and macroalgae/seaweeds), are broadly recognised for their role in soils’ fertilisation and plant growth stimulation [3]. Besides these important characteristics, the production of microalgal/cyanobacterial biomass can be quite advantageous, when compared to the production of other biological resources [3,4]: (i) production of these photosynthetic organisms can be performed in non-arable areas, thus not competing with the areas intended for food production; (ii) microalgae and cyanobacteria can be grown in low-quality waters, such as wastewaters, thus reducing the requirements for freshwater and nutrients (mainly nitrogen and phosphorus); (iii) the wealth composition of microalgal/cyanobacterial biomass can be fully exploited towards the induction of multiple responses in the same crop; and (iv) when growing autotrophically, microalgae and cyanobacteria uptake CO2 from the atmosphere, thus reducing the carbon footprint of agricultural practices. Although several products can be used in the improvement of crops’ productivities, it is important to understand that different biological compounds may improve the agricultural productivities through different modes of action: (i) soils’ improvement; (ii) crops’ protection against biotic and abiotic stress factors; and (iii) direct growth stimulation. Considering these roles, microalgal/cyanobacterial products and biomass can be classified as biofertilisers, biostimulants and biopesticides. Figure 1 summarises the main activities associated to these biologically-based products in the development of agricultural practices, highlighting their action mode and effect on crops’ production.
Biofertilisers are biologically-based compounds that promote an improvement in crops’ productivities through their activity at the soil level. Typically, these compounds and/or microorganisms are responsible for the improvement of soil properties and soils’ fertility, providing the essential nutrients (e.g., nitrogen, phosphorus and potassium) for plants’ growth [4,8,12,13]. Depending on their beneficial effects and on the microorganisms integrating these formulations, biofertilisers can be classified as [8,14]: (i) plant-growth-promoting bacteria; (ii) compost; (iii) nitrogen-fixators; (iv) phosphate- and potassium-solubilising biofertilisers; and (v) phosphorus-mobilising biofertilisers. The use of biofertilisers in agriculture presents several advantages, such as [14,15]: (i) increased crop productivities per unit of area and time; (ii) reduced energetic requirements; (iii) control and maintenance of adequate soil properties and fertility; (iv) lower risks of soil and water contamination; and (v) crops’ protection against pathogenic organisms.
Biostimulants promote crops’ productivity by acting directly on the plant. These compounds are responsible for improving respiration, photosynthetic activity, nucleic acid synthesis and ion uptake, enhancing plants’ metabolism and, hence, plants’ growth [9]. The stimulatory activity of biostimulants can be observed under both optimal and adverse conditions, meaning that these compounds can play an important role in the improvement of plants’ resistance and tolerance against stress conditions [3,4]. The application of biostimulants in agriculture has, therefore, the following advantages [3,4]: (i) increased crop productivities; (ii) increased nutrients’ utilisation efficiencies; and (iii) enhanced crops’ quality. Characterisation and categorisation of biostimulants can be quite complex, as a wide variety of compounds (e.g., polysaccharides, phenolic compounds, hormone-like compounds, vitamins, etc.) have been identified for their biostimulating activity in crops.
Biopesticides are known for their activity against plant pathogens. These compounds, typically presenting antimicrobial, antioxidant, antiviral or antifungal properties, promote crops’ development by protecting plants from pathogenic organisms.

3. Microalgal/Cyanobacterial Metabolites and Phytohormones with Potential Interest for Agriculture

Microalgae and cyanobacteria produce a wide variety of metabolites that, due to their biological activity, can be used in agriculture as biofertilisers, biostimulants or biopesticides. Among these metabolites, phenolic compounds, terpenoids, FFAs, polysaccharides, carotenoids and phytohormones are of particular interest, as they have already been identified as plant-growth promotors [2,7,12]. Table 1 presents the main biologically-active compounds that can be extracted from microalgae and cyanobacteria for their benefits in agricultural practices.

3.1. Phenolic Compounds

Phenolic compounds correspond to aromatic hydrocarbons bonded to a hydroxyl group. These compounds can be broadly categorised into phenols and polyphenols, with phenols being sub-divided into phenolic acids, flavonoids and phenylpropanoids [2,7,19,21]. In microalgae, phenols are considered secondary metabolites and their production and release is determined by several physical, chemical and environmental conditions. Phenolic compounds present in microalgae and cynobacteria are associated with their antioxidant properties [18,55], playing an important role in the growth, reproduction and protection against several stress conditions [55]. Goiris, et al. [18] assessed the antioxidant activity of 32 microalgal strains and compared the obtained results with total phenolics and carotenoids contents, concluding that, after carotenoids, phenolic compounds had a significant contribute to the antioxidant capacity of the studied microalgae. Among the studied microalgal species, Tetraselmis suecica, Botryococcus braunii, Neochloris oleoabundans, Isochrysis sp., Chlorella vulgaris and Phaeodactylum tricornutum presented the highest antioxidant capacities, and the highest phenolic contents (between 1.70 and 4.57 mg g−1 DW, dry weight basis). More recently, Foo, et al. [17] evaluated the relationship between the antioxidant activity of six algal species (five microalgae and one macroalga) and the presence of bioactive compounds (e.g., carotenoids, phenolic acids, fucoxanthin and fatty acids profile). In this study, the authors concluded that Chaetoceros calcitrans and Isochrysis galbana presented the highest antioxidant activity, followed by Odontella sinensis and Skeletonema costatum, with moderate antioxidant activity, and P. tricornutum and Saccharina japonica with the lowest antioxidant properties. Regarding the influence of bioactive compounds in the antioxidant activity of these algal species, through Pearson correlation and multiple linear regression analyses, the authors concluded that the main contributors to the antioxidant capacity of the studied algae were carotenoids (representing 0.05–6.13 mg g−1 DW) and phenolic acids (representing 0.02–12.24 mg g−1 DW). For agricultural purposes, phenolic compounds act mainly on crop protection against pathogens or other biotic and abiotic stress conditions, due to their antimicrobial, fungicide and antioxidant properties [7,16,20].

3.2. Terpenoids

Terpenoids are organic compounds that derive from the inclusion of methyl- or oxygen-based functional groups to terpenes. Based on the number of five-carbon isoprene units that constitute them, terpenoids can be classified into: hemiterpenoids (one isoprene unit, C5), monoterpenoids (two isoprene units, C10), sesquiterpenoids (three isoprene units, C15), diterpenoids (four isoprene units, C20), triterpenoids (six isoprene units, C30), tetraterpenoids (eight isoprene units, C40) and polyterpenoids (more than eight isoprene units, >C40) [2,7]. Moreover, terpenoids can be classified according to the number of cyclic structures that constitute them, being the main categories monocyclic, bicyclic, rearranged and linear [7]. These compounds are secondary metabolites of several algal and cyanobacterial species. Among algae, red algae (Rhodophyta) are the richest source of secondary metabolites, with many genera known for their ability to produce terpenoids [28]. For example, 512 sesquiterpenes and 133 diterpenes with different structures have been extracted from the genus Laurentia [56]. Other red algae species that produce terpenoids include Chondrococcus hornemanni, Hypnea pannosa, Sphaerococcus coronopifolius, Plocamium cornutum, Plocamium leptophyllum and Portieria hornemannii [28]. In the case of cyanobacte ria, genes encoding the enzymes involved in the terpenoid biosynthetic pathway were identified in Synechocystis sp. PCC 6714 and Thermosynechococcus elongatus. Similarly, ma- rine cyanobacteria, such as those from the genera Prochlorococcus, Synechococcus and Trich-odesmium are known for their ability to produce isoprene. Finally, some filamentous cyanobacteria (e.g., Pseudanabaena sp., Pseudanabaena articulate, Planktothricoids raciborskii and Oscillatoria perornata) were also reported as a source for terpenoids [25]. Due to their bioactivity, especially in terms of antibacterial, antioxidant and anticancer properties, terpenoids are widely used in pharmaceutical and cosmetic formulations [22,23,27]. As precursors of linear terpenes, terpenoids are also being explored as potential candidates to replace fossil fuels [25,57]. In agriculture, the antimicrobial, allelochemical and antioxidant properties of terpenoids make them valuable resources for use as biopesticides, with major impact on crops’ protection against bacteria, insects and other organisms [26]. In addition, it has been reported that terpenoids can play an important role during the preliminary growth and development of plants, as well as on the attraction of pollinators [24].

3.3. Free Fatty Acids

FFAs are non-esterified fatty acids typically found in microalgal and cyanobacterial crude extracts. According to the length of the hydrocarbon chain, FFAs can be classified as short, medium, long and very long chain fatty acids. Moreover, they can be divided into unsaturated (e.g., lignoceric, palmitic, capric, behenic, cerotic, caprylic, lauric, stearic, myristic and arachidic acids) and saturated (e.g., cis- and trans-fatty acids) fatty acids [7]. FFAs were identified in microalgal biomass from different genera (e.g., Anabaena, Chlorella, Dunaliella, Porphyridium, Scenedesmus and Spirulina), which include green, red and blue-green algae [29,33]. In addition, several studies have reported that microalgae and cyanobacteria can accumulate up to 70% of fatty acids per dry weight [2]. For example, in the study performed by Feller, et al. [32], extracts from the marine microalgae P. tricornutum, Nannochloropsis oculata and Porphyridium cruentum presented 37.3–82.4% of saturated fatty acids and 27.5–38.5% of polyunsaturated fatty acids. Due to current demands for renewable energy resources, FFAs from microalgae and cyanobacteria have been extensively explored as a resource for biodiesel production, as it can be obtained from the transesterification of fatty acids [58]. In addition to their potential use as a renewable energy resource, FFAs are also recognised for their anticarcinogenic, antibiotic, antifungal, antioxidant and antiviral activities, which make them promising candidates for the development of pharmaceutical, nutraceutical and cosmetic products [2,7,30,31]. Biological activity, namely antimicrobial, antifungal and antioxidant properties, is also an important advantage for agriculture, as application of FFAs extracts can act on crops’ protection.

3.4. Polysaccharides

Polysaccharides are polymers of carbohydrate molecules, which correspond to monosaccharide chains bonded by glycosidic interactions. A great diversity of polysaccharides can be obtained, being their characteristics determined by the building blocks, that is, the monosaccharides (e.g., hexose, pentose, uronic acid and methyl pentose) [2,7]. These polysaccharides are used by other organisms as carbon and energy sources, being excreted by algae under both normal and stress conditions. Production of a great diversity of extracellular polysaccharides has been reported for microalgae of different genera, such as Cylindrotheca, Navicula, Phaeodactylum, Chlamydomonas, Chlorella, Dunaliella, Aphanothece, Arthrospira, Nostoc, Scytonema, Porphyridium and Rhodella, being the production yields comprised between 0.01 and 2.9 g L−1 [37]. Other polysaccharides have structural functions in the cell walls of different organisms. These include arabinoxylans, cellulose, chitin and pectins, and their production has been associated with marine and freshwater algae, including brown, red, green and blue-green algae [7]. In addition, some polysaccharides (e.g., starch and glycogen) act as energy storage molecules. Starch is typically produced by red and green algae, whereas glycogen is mainly accumulated by species of Porphyridium and blue-green algae [7]. Polysaccharides’ synthesis by microalgae and cyanobacteria accounts for 0.5–20 g L−1 [37]. These polymers have been widely applied as thickening, gelling, stabiliser and emulsifier agents [45]. Moreover, antibacterial, anticoagulant, antioxidant, anticancer and anti-inflammatory properties have been described for these compounds [38,43,44]. In agriculture, polysaccharides have a preponderant role in the improvement of soil quality, with major activities as soil conditioners, nutrient carriers and as safe release systems for agrochemicals [35,36,41,42]. Despite their impact on soils, some studies have also demonstrated that polysaccharides can act on plant growth stimulation and on plant defence against biotic and abiotic factors [34,36,39,40,46].

3.5. Carotenoids

Carotenoids are accessory pigments used by algae during photoautotrophic growth. These compounds are obtained through polymerisation of five-carbon isoprene units [51,59]. Although they are essential for photosynthetic organisms, production of these compounds has also been described for bacteria and fungi [48,60]. Their role in algae is associated with light harvesting, protein assembly in photosystems and protection against photo-induced free radicals exposure [49]. The main carotenoids obtained from microalgae include alpha- and beta-carotene, lutein, lycopene, astaxanthin and zeaxanthin. Spirulina and Dunaliella species are the major sources of alpha- and beta-carotene (up to 10% DW), respectively. Lutein is typically obtained from Chlorella protothecoides, Scenedesmus almeriensis and Muriellopsis species, which can accumulate between 4.3 and 5.4 mg g−1 DW. Lycopene, in turn, can be found in several green algae, such as Chlorella marina, Chlorella regularis and Dunaliella salina. Similarly, astaxanthin is mainly produced by green algae, such as Haematococcus pluvialis and Chlorella zofingiensis, being H. pluvialis the major source of this compound, accumulating up to 3% DW. Finally, zeaxanthin is obtained from red and green microalgae, such as P. cruentum and Chlorella ellipsoidea. According to several studies, zeaxanthin in P. cruentum accounts for 97.4% of the total carotenoids content of this microalga. On the other hand, C. ellipsoidea can accumulate up to 4.26 mg g−1 DW of zeaxanthin [47,49,51,52]. Carotenoids from microalgae have been extensively used in food, feed, cosmetics, nutraceutical and pharmaceutical applications, due to the antioxidant, anti-inflammatory and anticancer properties exhibited by these compounds [47,48,49,52]. Regarding agricultural practices, carotenoids have been applied in soils’ bioremediation and also as antioxidants, fertilisers and biopesticides, with major impacts on soil improvement and crops’ protection. They are also applied to increase the availability of provitamin A, contributing to the development of biofortified crops [50,53].

3.6. Phytohormones

Phytohormones are considered signal molecules that are responsible for the regulation of several cellular processes in plants. Typically, these molecules are produced in small amounts and their presence has been firstly identified in higher plants [11]. However, the booming in algal research in the last decades, especially microalgal genomic studies, has demonstrated that these signalling molecules are also produced by a wide diversity of microalgae and cyanobacteria. In fact, the most popular phytohormones (i.e., auxins, abscisic acid, cytokinins, ethylene and gibberellins) have already been identified in multiple algal lineages, such as brown, red and green algae, cyanobacteria and diatoms [10,11]. Although research studies on the physiological responses promoted by microalgal phytohormones are still very scarce, the similarities found between phytohormones profiles in higher plants and algae suggest that their roles may be very similar. In higher plants, auxins, especially indole-3-acetic acid, are responsible for the regulation of growth and development [11]. In microalgae, these molecules also act as growth regulators, as auxins from C. vulgaris, D. salina, Nannochloropsis oceanica, Scenedesmus obliquus and Scenedesmus quadricauda have promoted an increase in cell size and chlorophyll and protein contents, as well as cell division, which resulted in higher biomass productivities [61,62,63,64,65]. Abscisic acid is commonly associated with the cellular response to environmental stress factors, such as high salinity levels, drought and nutrients scarcity [10,11]. Typically, this molecule induces cellular mechanisms to increase the plants’ tolerance to these stress conditions and avoid their harmful effects. In higher plants, it has been demonstrated that abscisic acid can improve the tolerance to temperature and salt stresses through the control of water and ions uptake [66]. In microalgae and cyanobacteria, this molecule is quite effective in the control of cells’ response to salt, osmotic, oxidative, drought and nutrients’ stresses [67,68]. Common responses induced by the activation of the abscisic acid pathway include the production of carotenoids, which typically act as protecting agents against oxidative stress [62]. Regarding cytokinins, these molecules mediate several processes in higher plants, namely cell division, growth, biogenesis, chloroplasts differentiation, regulation of seed dormancy, among others [10]. Therefore, the role of these hormones in plants’ growth and development is crucial. Besides these activities, cytokinins also improve the plants’ tolerance to adverse environmental conditions [10,11]. In microalgae and cyanobacteria, the role of these hormones is very similar, as they also stimulate cell division and photosynthetic activity and protect cells from environmental stress conditions [69]. For example, cytokinins from Acutodesmus obliquus, C. vulgaris and Gracilaria caudata have been associated with increased pigments’ contents in these organisms, which resulted in higher photosynthetic rates and, hence, higher biomass productivities [70,71,72]. Additionally, a cytokinin produced by D. salina, kinetin, induced the accumulation of the photo-protective pigment beta-carotene in this microalga [62]. Ethylene is known for its multiple responses in plants, which range from the regulation of plants’ growth and ageing, to the improvement of plants’ tolerance to both biotic and abiotic stress factors [10]. In microalgae and cyanobacteria, the role of ethylene is not well documented. However, some studies have evidenced that this molecule may act as a growth stimulation agent in Chlamydomonas reinhardtii, Chlorella sp. and Spirogyra platensis [73,74,75]. Gibberellins from plants and microalgae/cyanobacteria have similar functions, which are mainly related with growth stimulation and induction of pigments and proteins accumulation [10,11]. In the case of microalgae and cyanobacteria, gibberellins from C. ellipsoidea, Chlorella pyrenoidosa, C. vulgaris and Microcystis aeruginosa have been associated with increased cell number and size and higher growth rates [76,77,78,79]. The regulation activities promoted by phytohormones extracted from microalgae and cyanobacteria highlight additional benefits of using these organisms (or their extracts) in agricultural fields, especially in what concerns growth stimulation and plants’ protection against biotic and abiotic factors.

4. The Impacts of Microalgae/Cyanobacteria and Their Extracts on Crops’ Production

As reported in Section 3, microalgae and cyanobacteria are an important source of biologically-active compounds that can significantly improve agricultural productivities. The wide diversity of compounds found in microalgae/cyanobacteria, together with their multiple functions in crops’ production, allow their use as pure extracts or as a crude algal compost. Moreover, this diversity of metabolites impacts crops’ production at different levels: (i) some extracts and microorganisms induce higher crops’ productivities through an improvement in the soil quality; (ii) others enhance crops’ development through the protection against biotic and abiotic stress conditions; and (iii) some metabolites act directly on plant growth stimulation. The next sections present how different metabolites can improve crops’ production at these three levels, focusing on specific application examples.

4.1. Soil Improvement

Some algal and cyanobacterial species and their extracts are known for their positive effect at the soil level. Well-known activities include their ability to (i) fix atmospheric nitrogen into nitrogen species that can be easily assimilated by plants; (ii) provide essential nutrients for plants; and (iii) improve soil physical and chemical properties. Table 2 presents some application examples where microalgae and cyanobacteria (and their extracts) have contributed to an improvement in crops’ productivities by action at the soil level.

4.1.1. Nitrogen Fixation

Blue-green algae (or cyanobacteria) are able to fix atmospheric nitrogen (N2), converting it into organic nitrogen forms, which are more easily assimilated by higher plants. Therefore, the use of cyanobacteria in soils increase the availability of nitrogen, which is one of the essential nutrients for plants’ growth [6,8,96,97]. The beneficial effects of cyano-bacteria in agricultural soils (for the production of different crops) has already been demonstrated [90]. For example, using a cyanobacterial inoculum in a rice paddle, Jha and Prasad [80] concluded that this inoculum improved the grain and straw yields and increased the availability of nitrogen in the soil. Similarly, using Anabaena variabilis strains in a rice field, Singh and Datta [81] demonstrated that the used strains promoted an overall improvement in the rice crops (e.g., increase in plant height and leaf length, and improvement of seeds, grain and straw productivities). When applying Nostoc sp. vegetative cells to a rice field, Innok, et al. [82] obtained an increase in grain yields comparable to the one obtained with a chemically-based nitrogen fertiliser. Although the majority of the studies refer to the use of cyanobacteria in rice fields, recent studies have also referred the positive effect of cyanobacteria in other cultures. Osman, et al. [83] inoculated the soil intended for pea plant production with the cyanobacterial species Nostoc entophytum and Oscillatoria angustissima, observing a significant increase in the germination percentage, photosynthetic pigments and growth parameters of this plant. In addition, the authors observed that this increase was associated with a higher N2 fixation activity by both cyanobacteria. In the study performed by Swarnalakshmi, et al. [84], the use of a biofilm composed by the cyanobacterium Anabaena torulosa in a wheat crop significantly increased the availability of nitrogen in the soil. Prasanna, et al. [85] evaluated the potential of several cyanobacterial-bacterial consortia as fertilisers for soybean and mungbean production, presenting positive results in terms of nitrogen availability in the soil and plant fresh weight. Considering the improvements observed in terms of nitrogen availability, it is possible to conclude that cyanobacteria could be used in replacement of chemical nitrogen fertilisers, which can reduce crops’ production costs by 25–40%. The use of these microorganisms also promotes nitrogen recycling, avoiding the continuous production of chemically-based nitrogen fertilisers. Finally, cyanobacteria are known for their ability to form soil crusts that avoid nitrogen leaching/runoff and, therefore, the risks of water contamination with nitrogen [96].

4.1.2. Nutrients’ Availability in Soils

The use of microalgae and cyanobacteria in soils can also increase the availability of other essential nutrients for plants. As photosynthetic microorganisms, microalgae and cyanobacteria uptake nitrogen and phosphorus from different environments (even from sites where these nutrients are limiting) and store them in their biomass. As these nutrients are essential for the development of higher plants, microalgal/cyanobacterial biomass can be considered as an important source of these nutrients, avoiding the use of the traditional chemical fertilisers [4,8,97]. Other essential microelements for plants’ growth and development (e.g., potassium, magnesium, sulphur and iron) can also be found in microalgal/cyanobacterial biomass. These elements are typically involved in redox reactions, playing an important role in plants’ metabolism. Therefore, the use of microalgae and cyanobacteria in soils can improve the availability of both macro- and micronutrients for plants’ growth. This improvement in nutrients’ availability has already been reported in the literature [88,89,91,92]. Coppens, et al. [88] applied microalgal-bacterial flocs and N. oculata biomass to a tomato culture and evaluated their impact on soil composition and fruit development. The authors concluded that the presence of the photosynthetic organisms increased the availability of nitrogen, phosphorus and potassium in the soil and improved the fruit quality, by an increase in the sugar and carotenoids contents. However, a lower tomato yield was obtained when compared to the one achieved using an inorganic fertiliser. In the study performed by Manjunath, et al. [89], the use of cyanobacterial-bacterial biofilms and consortia to okra crops resulted in an increase in zinc and iron contents in the soil and contributed to an increased root yield and weight. More recently, Marks, et al. [92] evaluated the influence of applying a Chlorella sorokiniana culture in a vineyard soil on its composition, concluding that the presence of this microalga increased the concentration of nitrogen in the referred soil.
Microalgae and cyanobacteria can also act as a source of organic matter to higher plants, which should be supplied in adequate concentrations for a proper plants’ growth [96,97]. Firstly, these photosynthetic microorganisms fix atmospheric CO2, converting it into organic biomass. Moreover, these organisms tend to excrete extracellular polymeric substances, increasing the organic carbon levels in soils and promoting the growth of other microorganisms. Finally, microalgal and cyanobacterial biomass present in agricultural fields may be degraded by other organisms and grazers, which also increases the organic carbon content in the soils. The increase of organic carbon contents in soils using microalgae and/or cyanobacteria has already been described in the literature [86,87,91]. For example, Karthikeyan, et al. [86] demonstrated that the use of cyanobacterial suspensions (Calothrix ghosei, Hapalosiphon intricatus and Nostoc sp.) in wheat production increased organic carbon concentration in the soil, while promoting higher grain yields. More recently, Renuka, et al. [91] evaluated the effect of unicellular and filamentous microalgal-cyanobacterial consortia on soil composition and grain quality of a wheat crop. Besides an increase in micronutrient availability in the soil (mainly zinc, iron, copper and manganese), the studied consortia also enhanced its organic carbon content. This improvement in soil quality resulted in an increased grain yield and in a higher quality product, as the obtained grains presented an improved nutritional composition.

4.1.3. Soil Physical and Chemical Amendments

Microalgae and cyanobacteria also play an important role in the recovery of damaged soils, as they are able to: (i) modulate soils’ pH; (ii) control soils’ salinity or protect plants from high salinity levels; and (iii) remove heavy metals and other contaminants from soils [7,85,97,98]. Regarding the pH control, several studies have reported either an increase or decrease in soils’ pH when using microalgal/cyanobacterial biomass. However, it is important to highlight the beneficial effect of this biomass in controlling the acidic/basic nature of different soils [7,99]. In terms of soils’ salinity, several studies have reported an improvement in plants’ growth in soils presenting high salinities [97]. This improvement may be a result of (i) a reduction in the soils’ salinity (by increasing the water retention capacity of soils); or (ii) an increase in plants’ tolerance to high salinity levels (which may be achieved by gibberellic acid, a phytohormone commonly found in microalgae and cyanobacteria). Finally, microalgae and cyanobacteria are able to sequester trace elements (e.g., iron, zinc, copper and manganese), heavy metals (e.g., cadmium, lead and chromium), hydrocarbons and other compounds from the surrounding environment. Therefore, when applied to soils, microalgae and cyanobacteria may contribute to its remediation and to an increase in soils’ quality and fertility [7,8,98,100]. Decesaro, et al. [95] evaluated the potential of inactive Spirulina platensis cells and phycocyanin extracts from the same species on hydrocarbons removal from a soil contaminated with diesel and biodiesel. Compared to the control, phycocyanin extracts and inactive cells have effectively removed hydrocarbons from the contaminated soils, with the extracts being more effective in biodiesel removal (88.8%) and S. platensis inactive cells in diesel removal (63.9%).
Besides their importance in the enrichment of soils with essential nutrients and in the reclamation of soil properties, microalgae and cyanobacteria can also improve some soil characteristics, such as aggregation, porosity, permeability, ventilation and humidity level [6,7,97,101]. Typically, the improvement of these characteristics is associated with the polysaccharides excreted by several microalgal/cyanobacterial species [6,97]. When excreted to the soils, these polysaccharides tend to form an adhesive and gelatinous sheath that contributes to soils’ aggregation and prevents them from erosion [6]. These polysaccharides also play an important role in soils’ aeration and in their ability for water retention, which is crucial to maintain soils’ temperature, pH and salinity [6,7,97,101]. The improvement of these soil properties significantly enhances crops’ productivities, as they stimulate root growth and boost the soil microbial activity. Therefore, microalgae and cyanobacteria have been widely used in the restoration of soils’ properties and in the improvement of soils’ fertility. Hu, et al. [93] demonstrated that the resistance to wind erosion of unconsolidated sand was increased in the presence of desert soil algae, such as Microcoleus vaginatus, Phormidium tenue, Scytonema javanicum, Nostoc sp. and Desmococcus olivaceus, concluding that this increase was associated with higher crusts’ cohesion in the samples treated with the referred algae. Similarly, Issa, et al. [94] inoculated a poorly aggregated soil with Nostoc strains, achieving a higher degree of aggregation in the inoculated soil when compared to the non-inoculated one.

4.2. Crops’ Protection

Crops protection against biotic and abiotic factors is crucial for the improvement of agricultural productivities. Some plants have their defence and resistance mechanisms, but to achieve the ambitious target productivities, external protection agents should be employed on food crops. Considering the wide variety of bioactive compounds that can be found in microalgae and cyanobacteria, the use of these microorganisms (or their extracts) can promote an adequate crops’ protection against both biotic and abiotic factors. Table 3 presents some examples of the application of microalgae and cyanobacteria (biomass and/or extracts) on crops’ protection and productivity.

4.2.1. Protection against Biotic Factors

Biotic factors that can negatively impact crops’ productivities include the presence of organisms, such as insects, nematodes, bacteria and fungi [7,36,119]. Protection against these pathogenic organisms is commonly addressed by polysaccharides, which recognise the signalling molecules present in the pathogenic organism cell wall, and induce several defence responses [36]. Common defence responses include the regulation of signalling pathways, gene expression and induction of specific biosynthetic pathways, which typically result in the production secondary metabolites with antioxidant, antimicrobial and fungicidal properties (e.g., phenolic compounds, terpenoids and other compounds) [7,36,40,96,120]. When applied in agricultural crops, microalgae and cyanobacteria may promote these defence mechanisms, as these microorganisms are a great source of polysaccharides [36,121]. In fact, induction of plant defence mechanisms in the presence of microalgae and cyanobacteria has already been described in the literature. For example, in the study performed by Kumar, et al. [109], inoculation of spice crops’ seeds with the cyanobacteria Anabaena laxa and Calothrix elenkinii significantly improved the activity of the enzyme β-1,3-endoglucanase in shoots and roots, which is responsible for the breakdown of the cell wall components of pathogens. Moreover, the authors reported an increase in the fungicidal activity, plant dry weight and shoot and root length. Similarly, Priya, et al. [111] demonstrated an increase in the activity of plant defence enzymes, namely peroxidase, polyphenol oxidase and phenylalanine ammonia lyase, in shoots and roots of rice plants treated with C. elenkinii. Increased activity of these enzymes is associated with the up-regulation of metabolic pathways that induce the production of thousands of metabolites, such as phenolic compounds, that have a toxic effect against pathogenic organisms. For example, phenylalanine ammonia lyase results in the up-regulation of the phenylpropanoid pathway, which is responsible for the production of phytoalexins, phenolic substances known for their antimicrobial and antioxidant properties [36]. More recently, Farid, et al. [40] demonstrated that elicitation of plant defence mechanisms may be a result of algal polysaccharides’ activity. In this study, the authors concluded that: (i) polysaccharides extracted from C. vulgaris and C. sorokiniana promoted an increase in β-1,3-endoglucanase activity of tomato plants; (ii) polysaccharides extracted from C. sorokiniana induced an increased activity of phenylalanine ammonia lyase; and (iii) polysaccharides extracted from C. vulgaris and C. reinhardtii induced an increased activity of peroxidase and ascorbate peroxidase.
Although the majority of plant defence mechanisms may be promoted by microalgal/cyanobacterial polysaccharides, several metabolites presenting antioxidant, antimicrobial and cytotoxic properties are commonly found in microalgal/cyanobacterial biomass [119]. For example, the fatty acids’ contents, especially the type and amount of myristic, palmitic, oleic and eicosapentaenoic acids, are the major contributors to the antimicrobial properties commonly associated to microalgae and cyanobacteria [122,123]. Due to their antioxidant nature, carotenoids may also have antibacterial activity [112]. Phenolic compounds, in turn, are responsible for the degradation of pathogenic organisms’ cell walls [119]. Therefore, the use of microalgae and/or cyanobacteria in food crops can induce plants’ defence mechanisms not only through the activity of their polysaccharides, but also through the activity of these biologically-active compounds, as it has already been documented in the literature. Arunkumar, et al. [103] demonstrated that a methanolic extract from the brown seaweed Sargassum wightii exhibited activity against Xanthomonas oryzae, which is a common bacterial blight of rice. More recently, Baloch, et al. [108] reported a significant suppressive effect of the seaweeds Spatoglossum variabile, Stokeyia indica and Melanothamnus afaqhusainii against eggplant and watermelon pathogens (e.g., the root rotting fungi, Fusarium solani, Fusarium oxysporum and Macrophomina phaseolina, and the root knot nematode, Meloidogyne spp.). Besides the inhibitory effect against these organisms, the authors reported an improved plant growth (increased fresh weight of shoots, increased length of vines in watermelon and increased shoot lengths in eggplant).

4.2.2. Protection against Abiotic Factors

Besides biotic factors, plants’ exposure to extreme environmental conditions (e.g., very cold and hot temperatures, high salinity conditions and drought) can negatively impact crops’ production and development [9,124]. In the case of extreme temperatures, low temperatures may reduce the metabolic activity of higher plants and damage the cell membranes, as the phospholipidic layer that constitutes these membranes become unstable. Exposure to high temperatures may also be harmful for cell membranes and influence the synthesis and activity of plants’ proteins and enzymes [124]. High salinity levels are commonly associated with the osmotic stress in plants, which affects the nutritional composition of plants (typically, salt-stressed plants exhibit lower chlorophyll contents than the non-stressed ones) and, hence, plants’ metabolism and growth [9,124,125]. Drought is also responsible for the osmotic stress in plants. However, it also affects plants’ ability for gas exchange, significantly influencing the photosynthetic and transpiration rates and, therefore, the plants’ yield [9,124]. Considering the negative impacts of extreme environmental conditions on plants’ growth and development, increasing the tolerance of higher plants to these harsh conditions is crucial for the improvement of agricultural productivities. For this purpose, the use of biostimulants can be a very promising option, as these compounds are able to [124,126]: (i) promote the accumulation of antioxidant compounds, thus increasing the plants’ tolerance to stress conditions; and (ii) improve the overall performance of higher plants, thus stimulating their growth. Although several biological compounds are known for their stimulatory activity, the use of secondary metabolites produced by microalgae and cyanobacteria has attracted researchers worldwide, due to their wide variety and to their ability to induce several plant response mechanisms and metabolic pathways. In fact, the use of algal-based products as biostimulants has been successfully applied in food crops under temperature, salt and drought stress conditions [34,113,114,115,116,117,118]. In the study performed by Arroussi, et al. [34], the polysaccharides excreted by D. salina induced the jasmonic acid pathway, a metabolic pathway involved in plants’ response to stress, reducing the salt stress damages in tomato cultures. Moreover, this algal-based treatment promoted an improvement in roots and shoots’ length. Similarly, the use of seaweed extracts from Ulva rigida and Fucus spiralis in bean plants under drought stress increased the tolerance of this plant to drought and improved its growth [116].

4.3. Direct Growth Stimulation

Apart from their beneficial effects at the soil level and on plants’ protection, the use of microalgae and cyanobacteria (and/or their extracts) can directly stimulate plants’ growth and development, through an improvement in germination rates and plant characteristics (e.g., increased shoot and root length, increased leaf area and higher nutritional contents). These improvements are achieved as a result of the activity of microalgal/cyanobacterial metabolites, which are able to trigger several metabolic responses, such as respiration, photosynthesis, nucleic acid synthesis, chlorophyll production and ions uptake [9]. Table 4 presents some examples where microalgae and cyanobacteria (biomass and/or extracts) have been successfully applied in direct growth stimulation of higher plants.
Commonly involved metabolites include plant growth promoting factors, such as phytohormones, but also some amino acids, vitamins (e.g., vitamin B12 and biotin), polysaccharides and polypeptides [97]. Treatment of a paddy field with Anabaena isolates resulted in an overall increase in seeds’ germination rate and in an improvement of plant properties, such as plant height, root length and fresh and dry weights of leaves, stems and roots [127]. In addition, an improvement of soil properties, namely moisture and porosity, was observed. In the study performed by Omar, et al. [130], aqueous extracts of Gracilaria corticata and Enteromorpha flexuosa were applied to maize and sunflower seeds. Although extracts from both species resulted in increased root and shoot lengths and dry weights, these effects were more pronounced in plants treated with E. flexuosa extracts. After evaluating the composition of both extracts, the authors attributed the most promising effects of E. flexuosa extracts to the higher contents of phytohormones (indole-3-acetic acid, gibberellins and cytokinins) determined for this organism. Elarroussia, et al. [39] evaluated the effect of applying a solution of total polysaccharides extracts obtained from S. platensis in tomato and pepper cultures. With this study, the authors demonstrated that application of the extracts’ solution resulted in an increase in the size of both tomato and pepper plants. In addition, increased root weight, size and number of nodes was registered for the treated plants.

5. Major Limitations to the Use of Microalgae and Cyanobacteria in Agriculture

Although the beneficial effects of microalgae and cyanobacteria (or their extracts) in agricultural practices is undeniable, one of the major limitations to the use of these microorganisms or compounds is the high costs typically associated with microalgal/cyanobacterial biomass production and compounds’ extraction. For example, autotrophic growth of microalgae and cyanobacteria can be quite expensive and biomass productivities achieved are not very high. Moreover, biomass recovery after the production process can be costly and energetic-demanding, representing a large fraction of the overall biomass production costs. On the other hand, application of microalgal/cyanobacterial extracts requires the extraction of the interest metabolites, being the most commonly used methods very expensive [7,96]. The high costs associated with microalgal biomass production and processing contribute to an increase in the biofertilisers/biostimulants/biopesticides cost to values that cannot compete with the actual price of chemically-based compounds. For these reasons, applications with higher revenues (e.g., obtention of bioactive compounds for the nutraceutical, pharmaceutical and cosmetics’ industries) are typically preferred for microalgal/cyanobacterial biomass.
Another problem arising from the use of microalgal and cyanobacterial extracts is related with the sustainability of the most commonly used extraction procedures. Usually, extraction of the bioactive compounds requires and disposes large amounts of organic solvents.
Finally, the use of microalgal/cyanobacterial products is not broadly applied in agriculture because little is known about the interactions established between microalgae/cyanobacteria (and their extracts), plants and the environment. Although a lot of studies have been carried out in this area, the great diversity of photosynthetic organisms already isolated and identified and the infinite number of metabolites that can be extracted from them difficult a deep understanding of these interactions and, hence, their application in agriculture [7].

6. Conclusions

This manuscript presents a detailed review on the potential benefits of using microalgae and cyanobacteria in the improvement of agricultural productivities in a sustainable and effective way. Microalgae and cyanobacteria are an important source of a wide variety of bioactive compounds that can regulate several plant response mechanisms: (i) the improvement of soil quality and plants’ nutrition; (ii) plants’ protection against biotic and abiotic factors; and (iii) growth stimulation. Therefore, the use of microalgal/cyanobacterial biomass (or their extracts) can be a sustainable and viable alternative to the chemically-based fertilisers, pesticides and growth stimulants. Additionally, the use of these biologically-based substances/organisms constitutes an important step towards the improvement of agricultural productivities, which is essential to meet the continuously increasing targets for food products determined by the world population increase. Despite all the benefits, the use of these photosynthetic microorganisms in agriculture is still limited because: (i) biomass production and processing costs are still quite expensive; and (ii) the wide diversity of microalgae/cyanobacteria and their products difficult a deep understanding of the interactions between these microorganisms (or their extracts) and higher plants. To use microalgal and cyanobacterial biomass in the agricultural field and avoid the high process costs, one possible way is to promote the biorefinery concept, in which the obtained biomass should be fully exploited, towards the obtention of different products, for different applications, at the same time. Additionally, for a better definition of the most adequate substances for agricultural activities, more research studies focusing on the effect of each metabolite/biomass on crops are required.

Funding

This work was financially supported by: (i) Base Funding—UIDB/00511/2020 of the Laboratory for Process Engineering, Environment, Biotechnology and Energy—LEPABE—funded by national funds through the FCT/MCTES (PIDDAC); and (ii) Project POCI-01-0145-FEDER-031736—PIV4Algae—Process Intensification for microalgal production and Valorisation, funded by FEDER funds through COMPETE2020—Programa Operacional Competitividade e Internacionalização (POCI) and by national funds (PIDDAC) through FCT/MCTES.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Conflicts of Interest

The author declares no conflict of interest.

References

  1. Pathak, J.; Rajneesh; Maurya, P.K.; Singh, S.P.; Häder, D.-P.; Sinha, R.P. Cyanobacterial Farming for Environment Friendly Sustainable Agriculture Practices: Innovations and Perspectives. Front. Environ. Sci. 2018, 6, 7–19. [Google Scholar] [CrossRef]
  2. Singh, R.; Parihar, P.; Singh, M.; Bajguz, A.; Kumar, J.; Singh, S.; Singh, V.P.; Prasad, S.M. Uncovering Potential Applications of Cyanobacteria and Algal Metabolites in Biology, Agriculture and Medicine: Current Status and Future Prospects. Front. Microbiol. 2017, 8, 515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Chiaiese, P.; Corrado, G.; Colla, G.; Kyriacou, M.C.; Rouphael, Y. Renewable Sources of Plant Biostimulation: Microalgae as a Sustainable Means to Improve Crop Performance. Front. Plant Sci. 2018, 9, 1782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Ronga, D.; Biazzi, E.; Parati, K.; Carminati, D.; Carminati, E.; Tava, A. Microalgal Biostimulants and Biofertilisers in Crop Productions. Agronomy 2019, 9, 192. [Google Scholar] [CrossRef] [Green Version]
  5. Dmytryk, A.; Chojnacka, K. Algae as fertilizers, biostimulants, and regulators of plant growth. In Algae Biomass: Characteristics and Applications; Chojnacka, K., Wieczorek, P.P., Schroeder, G., Michalak, I., Eds.; Springer: Cham, Switzerland, 2018; pp. 115–122. [Google Scholar]
  6. Baweja, P.; Kumar, S.; Kumar, G. Organic fertilizer from algae: A novel approach towards sustainable agriculture. In Biofertilizers for Sustainable Agriculture and Environment; Giri, B., Prasad, R., Wu, Q.-S., Varma, A., Eds.; Springer: Cham, Switzerland, 2019; pp. 353–370. [Google Scholar]
  7. Pan, S.; Jeevanandam, J.; Danquah, M.K. Benefits of Algal Extracts in Sustainable Agriculture. In Grand Challenges in Marine Biotechnology; Springer Science and Business Media LLC: Berlin, Germany, 2019; pp. 501–534. [Google Scholar]
  8. Win, T.T.; Barone, G.D.; Secundo, F.; Fu, P. Algal Biofertilizers and Plant Growth Stimulants for Sustainable Agriculture. Ind. Biotechnol. 2018, 14, 203–211. [Google Scholar] [CrossRef]
  9. Górka, B.; Korzeniowska, K.; Lipok, J.; Wieczorek, P.P. The Biomass of Algae and Algal Extracts in Agricultural Production. In Algae Biomass: Characteristics and Applications; Springer Science and Business Media LLC: Berlin, Germany, 2018; pp. 103–114. [Google Scholar]
  10. Han, X.; Zeng, H.; Bartocci, P.; Fantozzi, F.; Yan, Y. Phytohormones and Effects on Growth and Metabolites of Microalgae: A Review. Fermentation 2018, 4, 25. [Google Scholar] [CrossRef] [Green Version]
  11. Lu, Y.; Xu, J. Phytohormones in microalgae: A new opportunity for microalgal biotechnology? Trends Plant Sci. 2015, 20, 273–282. [Google Scholar] [CrossRef]
  12. Kusvuran, A.; Kusvuran, S. Using of microbial fertilizer as biostimulant alleviates damage from drought stress in guar (Cyamopsis Tetragonoloba (L.) Taub.) seedlings. Int. Lett. Nat. Sci. 2019, 76, 147–157. [Google Scholar] [CrossRef] [Green Version]
  13. Reddy, C.A.; Saravanan, R.S. Polymicrobial multi-functional approach for enhancement of crop productivity. In Advances in Applied Microbiology; Sariaslani, S., Gadd, G.M., Eds.; Academic Press: Cambridge, MA, USA, 2013; Volume 82, pp. 53–113. [Google Scholar]
  14. Vessey, J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 2003, 255, 571–586. [Google Scholar] [CrossRef]
  15. Carvajal-Muñoz, J.; Carmona-Garcia, C. Benefits and limitations of biofertilization in agricultural practices. Livest. Res. Rural Dev. 2012, 24, 1–8. [Google Scholar]
  16. Esquivel-Hernández, D.A.; Ibarra-Garza, I.P.; Rodríguez-Rodríguez, J.; Cuéllar-Bermúdez, S.P.; Rostro-Alanis, M.D.J.; Alemán-Nava, G.S.; García-Pérez, J.S.; Parra-Saldívar, R. Green extraction technologies for high-value metabolites from algae: A review. Biofuels Bioprod. Biorefining 2017, 11, 215–231. [Google Scholar] [CrossRef]
  17. Foo, S.C.; Yusoff, F.M.; Ismail, M.; Basri, M.; Yau, S.K.; Khong, N.M.; Chan, K.W.; Ebrahimi, M. Antioxidant capacities of fucoxanthin-producing algae as influenced by their carotenoid and phenolic contents. J. Biotechnol. 2017, 241, 175–183. [Google Scholar] [CrossRef] [PubMed]
  18. Goiris, K.; Muylaert, K.; Fraeye, I.; Foubert, I.; De Brabanter, J.; De Cooman, L. Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. Environ. Boil. Fishes 2012, 24, 1477–1486. [Google Scholar] [CrossRef]
  19. Khoddami, A.; Wilkes, M.A.; Roberts, T.H. Techniques for Analysis of Plant Phenolic Compounds. Molecules 2013, 18, 2328–2375. [Google Scholar] [CrossRef]
  20. Michalak, I.; Chojnacka, K.; Saeid, A. Plant Growth Biostimulants, Dietary Feed Supplements and Cosmetics Formulated with Supercritical CO2 Algal Extracts. Molecules 2017, 22, 66. [Google Scholar] [CrossRef]
  21. Oksana, S. Plant phenolic compounds for food, pharmaceutical and cosmetics production. J. Med. Plants Res. 2012, 6, 2526–2539. [Google Scholar] [CrossRef]
  22. Awasthi, M.; Upadhyay, A.K.; Singh, S.; Pandey, V.P.; Dwivedi, U.N. Terpenoids as promising therapeutic molecules against Alzheimer’s disease: Amyloid beta- and acetylcholinesterase-directed pharmacokinetic and molecular docking analyses. Mol. Simul. 2018, 44, 1–11. [Google Scholar] [CrossRef]
  23. Betterle, N.; Melis, A. Photosynthetic generation of heterologous terpenoids in cyanobacteria. Biotechnol. Bioeng. 2019, 116, 2041–2051. [Google Scholar] [CrossRef]
  24. Gershenzon, J.; Dudareva, N. The function of terpene natural products in the natural world. Nat. Chem. Biol. 2007, 3, 408–414. [Google Scholar] [CrossRef]
  25. Pattanaik, B.; Lindberg, P. Terpenoids and Their Biosynthesis in Cyanobacteria. Life 2015, 5, 269–293. [Google Scholar] [CrossRef] [Green Version]
  26. Pavela, R.; Benelli, G. Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints. Trends Plant Sci. 2016, 21, 1000–1007. [Google Scholar] [CrossRef] [PubMed]
  27. Rodríguez-García, A.; Hosseini, S.; Martinez-Chapa, S.O.; Cordell, G.A. Multi-target Activities of Selected Alkaloids and Terpenoids. Mini-Reviews Org. Chem. 2017, 14, 272–279. [Google Scholar] [CrossRef]
  28. Wei, G.; Jia, Q.; Chen, X.; Köllner, T.G.; Bhattacharya, D.; Wong, G.K.; Gershenzon, J.; Chen, F. Terpene Biosynthesis in Red Algae Is Catalyzed by Microbial Type But Not Typical Plant Terpene Synthases. Plant Physiol. 2019, 179, 382–390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Demirbas, A.; Demirbas, M.F. Importance of algae oil as a source of biodiesel. Energy Convers. Manag. 2011, 52, 163–170. [Google Scholar] [CrossRef]
  30. Desbois, A.P.; Smith, V.J. Antibacterial free fatty acids: Activities, mechanisms of action and biotechnological potential. Appl. Microbiol. Biotechnol. 2010, 85, 1629–1642. [Google Scholar] [CrossRef] [Green Version]
  31. El-Baz, F.; El-Senousy, W.; El-Sayed, A.; Kamel, M. In vitro antiviral and antimicrobial activities of Spirulina platensis extract. J. Appl. Pharm. Sci. 2013, 3, 52–56. [Google Scholar] [CrossRef]
  32. Feller, R.; Matos, Â.P.; Mazzutti, S.; Moecke, E.H.; Tres, M.V.; Derner, R.B.; Oliveira, J.V.; Agenor, F., Jr. Polyunsaturated ω-3 and ω-6 fatty acids, total carotenoids and antioxidant activity of three marine microalgae extracts obtained by supercritical CO2 and subcritical n-butane. J. Supercrit. Fluids 2018, 133, 437–443. [Google Scholar] [CrossRef]
  33. Lam, M.K.; Lee, K.T. Microalgae biofuels: A critical review of issues, problems and the way forward. Biotechnol. Adv. 2012, 30, 673–690. [Google Scholar] [CrossRef]
  34. El Arroussi, H.; Benhima, R.; Elbaouchi, A.; Sijilmassi, B.; El Mernissi, N.; Aafsar, A.; Meftah-Kadmiri, I.; Bendaou, N.; Smouni, A. Dunaliella salina exopolysaccharides: A promising biostimulant for salt stress tolerance in tomato (Solanum lycopersicum). Environ. Boil. Fishes 2018, 30, 2929–2941. [Google Scholar] [CrossRef]
  35. Campos, E.V.R.; De Oliveira, J.L.; Fraceto, L.F.; Singh, B. Polysaccharides as safer release systems for agrochemicals. Agron. Sustain. Dev. 2015, 35, 47–66. [Google Scholar] [CrossRef]
  36. Chanda, M.-J.; Merghoub, N.; Hicham, E.A. Microalgae polysaccharides: The new sustainable bioactive products for the development of plant bio-stimulants? World J. Microbiol. Biotechnol. 2019, 35, 177. [Google Scholar] [CrossRef] [PubMed]
  37. Delattre, C.; Pierre, G.; Laroche, C.; Michaud, P. Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol. Adv. 2016, 34, 1159–1179. [Google Scholar] [CrossRef] [PubMed]
  38. Dvir, I.; Stark, A.H.; Chayoth, R.; Madar, Z.; Arad, S. Hypocholesterolemic Effects of Nutraceuticals Produced from the Red Microalga Porphyridium sp. in Rats. Nutrients 2009, 1, 156–167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Elarroussia, H.; Elmernissia, N.; Benhimaa, R.; El Kadmiria, I.M.; Bendaou, N.; Smouni, A.; Wahbya, I. Microalgae polysac-charides a promising plant growth biostimulant. J. Algal Biomass Util. 2016, 7, 55–63. [Google Scholar]
  40. Farid, R.; Mutale-Joan, C.; Redouane, B.; Najib, E.M.; Abderahime, A.; Laila, S.; Hicham, E.A. Effect of Microalgae Polysaccharides on Biochemical and Metabolomics Pathways Related to Plant Defense in Solanum lycopersicum. Appl. Biochem. Biotechnol. 2018, 188, 225–240. [Google Scholar] [CrossRef]
  41. González, A.; Castro, J.; Vera, J.; Moenne, A. Seaweed Oligosaccharides Stimulate Plant Growth by Enhancing Carbon and Nitrogen Assimilation, Basal Metabolism, and Cell Division. J. Plant Growth Regul. 2012, 32, 443–448. [Google Scholar] [CrossRef] [Green Version]
  42. Guilherme, M.R.; Aouada, F.A.; Fajardo, A.R.; Martins, A.F.; Paulino, A.T.; Davi, M.F.; Rubira, A.F.; Muniz, E.C. Superabsorbent hydrogels based on polysaccharides for application in agriculture as soil conditioner and nutrient carrier: A review. Eur. Polym. J. 2015, 72, 365–385. [Google Scholar] [CrossRef] [Green Version]
  43. Guzmán, S.; Gato, A.; Lamela, M.; Freire-Garabal, M.; Calleja, J.M. Anti-inflammatory and immunomodulatory activities of polysaccharide from Chlorella stigmatophora and Phaeodactylum tricornutum. Phytother. Res. 2003, 17, 665–670. [Google Scholar] [CrossRef]
  44. Rechter, S.; König, T.; Auerochs, S.; Thulke, S.; Walter, H.; Dörnenburg, H.; Walter, C.; Marschall, M. Antiviral activity of Arthrospira-derived spirulan-like substances. Antivir. Res. 2006, 72, 197–206. [Google Scholar] [CrossRef]
  45. Usman, A.; Khalid, S.; Usman, A.; Hussain, Z.; Wang, Y. Algal polysaccharides, novel application, and outlook. In Algae Based Polymers, Blends, and Composites; Zia, K.M., Zuber, M., Ali, M., Eds.; Elsevier: Amsterdam, The Netherlands, 2017; pp. 115–153. [Google Scholar]
  46. Vera, J.; Castro, J.; Figueroa, A.G.; Moenne, A. Seaweed Polysaccharides and Derived Oligosaccharides Stimulate Defense Responses and Protection against Pathogens in Plants. Mar. Drugs 2011, 9, 2514–2525. [Google Scholar] [CrossRef]
  47. Cezare-Gomes, E.A.; Mejia-Da-Silva, L.D.C.; Pérez-Mora, L.S.; Matsudo, M.C.; Ferreira-Camargo, L.S.; Singh, A.K.; De Carvalho, J.C.M. Potential of Microalgae Carotenoids for Industrial Application. Appl. Biochem. Biotechnol. 2019, 188, 602–634. [Google Scholar] [CrossRef] [PubMed]
  48. Galasso, C.; Corinaldesi, C.; Sansone, C. Carotenoids from Marine Organisms: Biological Functions and Industrial Applications. Antioxidants 2017, 6, 96. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Guedes, A.C.; Amaro, H.M.; Malcata, F.X. Microalgae as Sources of Carotenoids. Mar. Drugs 2011, 9, 625–644. [Google Scholar] [CrossRef] [PubMed]
  50. Han, T.; Zhao, Z.; Wang, Y. The effect of ryegrass and fertilizer on the petroleum contaminated soil remediation. Fresenius Environ. Bull. 2016, 25, 2243–2250. [Google Scholar]
  51. Rajesh, K.; Rohit, M.V.; Venkata Mohan, S. Microalgae-based carotenoids production. In Algal Green Chemistry; Rastogi, R.P., Madamwar, D., Pandey, A., Eds.; Elsevier: Amsterdam, The Netherlands, 2017; pp. 139–147. [Google Scholar]
  52. Raposo, M.F.D.J.; De Morais, R.M.S.C.; De Morais, R.M.S.C. Carotenoids from Marine Microalgae: A Valuable Natural Source for the Prevention of Chronic Diseases. Mar. Drugs 2015, 13, 5128–5155. [Google Scholar] [CrossRef] [PubMed]
  53. Sakamoto, Y.; Mori, K.; Matsuo, Y.; Mukojima, N.; Watanabe, W.; Sobaru, N.; Tamiya, S.; Nakao, T.; Hayashi, K.; Watanuki, H.; et al. Breeding of a new potato variety ‘Nagasaki Kogane’ with high eating quality, high carotenoid content, and resistance to diseases and pests. Breed. Sci. 2017, 67, 320–326. [Google Scholar] [CrossRef] [Green Version]
  54. Ördög, V.; Stirk, W.A.; Van Staden, J.; Novák, O.; Strnad, M. Endogenous cytokinins in three genera of microalgae from the Chlorophyta. J. Phycol. 2004, 40, 88–95. [Google Scholar] [CrossRef]
  55. Freile-Pelegrín, Y.; Robledo, D. Bioactive phenolic compounds from algae. In Bioactive Compounds from Marine Foods: Plant and Animal Sources; Hernández-Ledesma, B., Herrero, M., Eds.; Wiley: Chichester, UK, 2013; pp. 113–129. [Google Scholar]
  56. Harizani, M.; Ioannou, E.; Roussis, V. The Laurencia paradox: An endless source of chemodiversity. In Progress in the Chemistry of Organic Natural Products; Kinghorn, A.D., Falk, H., Gibbons, S., Kobayashi, J.I., Eds.; Springer International Publishing: Cham, Switzerland, 2016; pp. 91–252. [Google Scholar]
  57. Hellier, P.; Al-Haj, L.; Talibi, M.; Purton, S.; Ladommatos, N. Combustion and emissions characterization of terpenes with a view to their biological production in cyanobacteria. Fuel 2013, 111, 670–688. [Google Scholar] [CrossRef] [Green Version]
  58. Veillette, M.; Giroir-Fendler, A.; Faucheux, N.; Heitz, M. Esterification of free fatty acids with methanol to biodiesel using heterogeneous catalysts: From model acid oil to microalgae lipids. Chem. Eng. J. 2017, 308, 101–109. [Google Scholar] [CrossRef]
  59. Gong, M.; Bassi, A.S. Carotenoids from microalgae: A review of recent developments. Biotechnol. Adv. 2016, 34, 1396–1412. [Google Scholar] [CrossRef]
  60. Zhang, Y.; Liu, Z.; Sun, J.; Xue, C.; Mao, X. Biotechnological production of zeaxanthin by microorganisms. Trends Food Sci. Technol. 2018, 71, 225–234. [Google Scholar] [CrossRef]
  61. Kozlova, T.A.; Hardy, B.P.; Krishna, P.; Levin, D.B. Effect of phytohormones on growth and accumulation of pigments and fatty acids in the microalgae Scenedesmus quadricauda. Algal Res. 2017, 27, 325–334. [Google Scholar] [CrossRef]
  62. Mousavi, P.; Montazeri-Najafabady, N.; Abolhasanzadeh, Z.; Mohagheghzadeh, A.; Hamidi, M.; Niazi, A.; Morowvat, M.H.; Ghasemi, Y. Investigating the effects of phytohormones on growth and beta-carotene production in a naturally isolates stain of Dunaliella salina. J. Appl. Pharm. Sci. 2016, 6, 164–171. [Google Scholar] [CrossRef] [Green Version]
  63. Piotrowska-Niczyporuk, A.; Bajguz, A. The effect of natural and synthetic auxins on the growth, metabolite content and antioxidant response of green alga Chlorella vulgaris (Trebouxiophyceae). Plant Growth Regul. 2014, 73, 57–66. [Google Scholar] [CrossRef] [Green Version]
  64. Salama, E.-S.; Kabra, A.N.; Ji, M.-K.; Kim, J.R.; Min, B.; Jeon, B.-H. Enhancement of microalgae growth and fatty acid content under the influence of phytohormones. Bioresour. Technol. 2014, 172, 97–103. [Google Scholar] [CrossRef]
  65. Udayan, A.; Arumugam, M. Selective enrichment of Eicosapentaenoic acid (20:5n-3) in N. oceanica CASA CC201 by natural auxin supplementation. Bioresour. Technol. 2017, 242, 329–333. [Google Scholar] [CrossRef]
  66. George, E.F.; Hall, M.A.; De Klerk, G.-J. Plant Growth Regulators III: Gibberellins, Ethylene, Abscisic Acid, their Analogues and Inhibitors; Miscellaneous Compounds. In Plant Propagation by Tissue Culture; Springer Science and Business Media LLC: Berlin, Germany, 2007; Volume 1, pp. 227–281. [Google Scholar]
  67. Maršálek, B.; Zahradníčková, H.; Hronková, M. Extracellular Abscisic Acid Produced by Cyanobacteria under Salt Stress. J. Plant Physiol. 1992, 139, 506–508. [Google Scholar] [CrossRef]
  68. Yoshida, K.; Igarashi, E.; Wakatsuki, E.; Miyamoto, K.; Hirata, K. Mitigation of osmotic and salt stresses by abscisic acid through reduction of stress-derived oxidative damage in Chlamydomonas reinhardtii. Plant Sci. 2004, 167, 1335–1341. [Google Scholar] [CrossRef]
  69. Romanenko, E.; Kosakovskaya, I.; Romanenko, P. Phytohormones of microalgae: Biological role and involvement in the regulation of physiological processes. Pt II. Cytokinins and gibberellins. Algologia 2016, 26, 203–229. [Google Scholar] [CrossRef] [Green Version]
  70. Piotrowska-Niczyporuk, A.; Czerpak, R. Cellular response of light/dark-grown green alga Chlorella vulgaris Beijerinck (Chlorophyceae) to exogenous adenine- and phenylurea-type cytokinins. Acta Physiol. Plant. 2009, 31, 573–585. [Google Scholar] [CrossRef]
  71. Renuka, N.; Guldhe, A.; Singh, P.; Ansari, F.A.; Rawat, I.; Bux, F. Evaluating the potential of cytokinins for biomass and lipid enhancement in microalga Acutodesmus obliquus under nitrogen stress. Energy Convers. Manag. 2017, 140, 14–23. [Google Scholar] [CrossRef]
  72. Souza, J.M.C.; Yokoya, N.S. Effects of cytokinins on physiological and biochemical responses of the agar-producing red alga Gracilaria caudata (Gracilariales, Rhodophyta). Environ. Boil. Fishes 2016, 28, 3491–3499. [Google Scholar] [CrossRef]
  73. Ju, C.; Van De Poel, B.; Cooper, E.D.; Thierer, J.H.; Gibbons, T.R.; Delwiche, C.F.; Chang, C. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants 2015, 1, 14004. [Google Scholar] [CrossRef] [PubMed]
  74. Tate, J.J.; Gutierrez-Wing, M.T.; Rusch, K.A.; Benton, M.G. The Effects of Plant Growth Substances and Mixed Cultures on Growth and Metabolite Production of Green Algae Chlorella sp.: A Review. J. Plant Growth Regul. 2012, 32, 417–428. [Google Scholar] [CrossRef]
  75. Yordanova, Z.P.; Iakimova, E.T.; Cristescu, S.M.; Harren, F.J.M.; Kapchina-Toteva, V.M.; Witkowska, E.W.I. Involvement of ethylene and nitric oxide in cell death in mastoparan-treated unicellular alga Chlamydomonas reinhardtii. Cell Biol. Int. 2010, 34, 301–308. [Google Scholar] [CrossRef] [Green Version]
  76. Du, K.; Tao, H.; Wen, X.; Geng, Y.; Li, Y. Enhanced growth and lipid production of Chlorella pyrenoidosa by plant growth regulator GA3. Fresenius Environ. Bull. 2015, 24, 3414–3419. [Google Scholar]
  77. Falkowska, M.; Pietryczuk, A.; Piotrowska, A.; Bajguz, A.; Grygoruk, A.; Czerpak, R. The effect of gibberellic acid (GA3) on growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (Chlorophyceae) Beijerinck exposed to cad-mium and lead stress. Pol. J. Environ. Stud. 2011, 20, 53–59. [Google Scholar]
  78. González-Garcinuño, Á.; Sánchez-Álvarez, J.M.; Galán, M.A.; Del Valle, E.M.M. Understanding and optimizing the addition of phytohormones in the culture of microalgae for lipid production. Biotechnol. Prog. 2016, 32, 1203–1211. [Google Scholar] [CrossRef]
  79. Pan, X.; Chang, F.; Kang, L.; Liu, Y.; Li, G.; Li, D. Effects of gibberellin A3 on growth and microcystin production in Microcystis aeruginosa (cyanophyta). J. Plant Physiol. 2008, 165, 1691–1697. [Google Scholar] [CrossRef]
  80. Jha, M.N.; Prasad, A.N. Efficacy of New Inexpensive Cyanobacterial Biofertilizer Including its Shelf-life. World J. Microbiol. Biotechnol. 2006, 22, 73–79. [Google Scholar] [CrossRef]
  81. Singh, S.; Datta, P. Outdoor evaluation of herbicide resistant strains of Anabaena variabilis as biofertilizer for rice plants. Plant Soil 2007, 296, 95–102. [Google Scholar] [CrossRef]
  82. Innok, S.; Chunleuchanon, S.; Boonkerd, N.; Teaumroong, N. Cyanobacterial akinete induction and its application as biofertilizer for rice cultivation. Environ. Boil. Fishes 2009, 21, 737–744. [Google Scholar] [CrossRef]
  83. Osman, M.E.H.; El-Sheekh, M.M.; El-Naggar, A.H.; Gheda, S.F. Effect of two species of cyanobacteria as biofertilizers on some metabolic activities, growth, and yield of pea plant. Biol. Fertil. Soils 2010, 46, 861–875. [Google Scholar] [CrossRef]
  84. Swarnalakshmi, K.; Prasanna, R.; Kumar, A.; Pattnaik, S.; Chakravarty, K.; Shivay, Y.S.; Singh, R.; Saxena, A.K. Evaluating the influence of novel cyanobacterial biofilmed biofertilizers on soil fertility and plant nutrition in wheat. Eur. J. Soil Biol. 2013, 55, 107–116. [Google Scholar] [CrossRef]
  85. Prasanna, R.; Triveni, S.; Bidyarani, N.; Babu, S.; Yadav, K.; Adak, A.; Khetarpal, S.; Pal, M.; Shivay, Y.S.; Saxena, A.K. Evaluating the efficacy of cyanobacterial formulations and biofilmed inoculants for leguminous crops. Arch. Agron. Soil Sci. 2013, 60, 349–366. [Google Scholar] [CrossRef]
  86. Karthikeyan, N.; Prasanna, R.; Nain, L.; Kaushik, B.D. Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur. J. Soil Biol. 2007, 43, 23–30. [Google Scholar] [CrossRef]
  87. Nisha, R.; Kaushik, A.; Kaushik, C. Effect of indigenous cyanobacterial application on structural stability and productivity of an organically poor semi-arid soil. Geoderma 2007, 138, 49–56. [Google Scholar] [CrossRef]
  88. Coppens, J.; Grunert, O.; Hende, S.V.D.; Vanhoutte, I.; Boon, N.; Haesaert, G.; De Gelder, L. The use of microalgae as a high-value organic slow-release fertilizer results in tomatoes with increased carotenoid and sugar levels. J. Appl. Phycol. 2016, 28, 2367–2377. [Google Scholar] [CrossRef]
  89. Manjunath, M.; Kanchan, A.; Ranjan, K.; Venkatachalam, S.; Prasanna, R.; Ramakrishnan, B.; Hossain, F.; Nain, L.; Shivay, Y.S.; Rai, A.B.; et al. Beneficial cyanobacteria and eubacteria synergistically enhance bioavailability of soil nutrients and yield of okra. Heliyon 2016, 2, e00066. [Google Scholar] [CrossRef] [Green Version]
  90. Renuka, N.; Prasanna, R.; Sood, A.; Ahluwalia, A.S.; Bansal, R.; Babu, S.; Singh, R.; Shivay, Y.S.; Nain, L. Exploring the efficacy of wastewater-grown microalgal biomass as a biofertilizer for wheat. Environ. Sci. Pollut. Res. 2016, 23, 6608–6620. [Google Scholar] [CrossRef]
  91. Renuka, N.; Prasanna, R.; Sood, A.; Bansal, R.; Bidyarani, N.; Singh, R.; Shivay, Y.S.; Nain, L.; Ahluwalia, A.S. Wastewater grown microalgal biomass as inoculants for improving micronutrient availability in wheat. Rhizosphere 2017, 3, 150–159. [Google Scholar] [CrossRef]
  92. Marks, E.A.; Montero, O.; Rad, J.C. The biostimulating effects of viable microalgal cells applied to a calcareous soil: Increases in bacterial biomass, phosphorus scavenging, and precipitation of carbonates. Sci. Total. Environ. 2019, 692, 784–790. [Google Scholar] [CrossRef]
  93. Hu, C.; Liu, Y.; Song, L.; Zhang, D. Effect of desert soil algae on the stabilization of fine sands. Environ. Boil. Fishes 2002, 14, 281–292. [Google Scholar] [CrossRef]
  94. Issa, O.M.; Défarge, C.; Le Bissonnais, Y.; Marin, B.; Duval, O.; Bruand, A.; D’Acqui, L.P.; Nordenberg, S.; Annerman, M. Effects of the inoculation of cyanobacteria on the microstructure and the structural stability of a tropical soil. Plant Soil 2007, 290, 209–219. [Google Scholar] [CrossRef] [Green Version]
  95. DeCesaro, A.; Rampel, A.; Machado, T.S.; Thomé, A.; Reddy, K.; Margarites, A.C.; Colla, L.M. Bioremediation of Soil Contaminated with Diesel and Biodiesel Fuel Using Biostimulation with Microalgae Biomass. J. Environ. Eng. 2017, 143, 04016091. [Google Scholar] [CrossRef]
  96. Renuka, N.; Guldhe, A.; Prasanna, R.; Singh, P.; Bux, F. Microalgae as multi-functional options in modern agriculture: Current trends, prospects and challenges. Biotechnol. Adv. 2018, 36, 1255–1273. [Google Scholar] [CrossRef]
  97. Sharma, R.; Khokhar, M.; Jat, R.; Khandelwal, S. Role of algae and cyanobacteria in sustainable agriculture system. Wud Pecker J. Agric. Res. 2012, 1, 381–388. [Google Scholar]
  98. Priya, M.; Gurung, N.; Mukherjee, K.; Bose, S. Microalgae in removal of heavy metal and organic pollutants from soil. In Microbial Biodegradation and Bioremediation; Das, S., Ed.; Elsevier: Oxford, UK, 2014; pp. 519–537. [Google Scholar]
  99. Chatterjee, A.; Singh, S.; Agrawal, C.; Yadav, S.; Rai, R.; Rai, L. Role of Algae as a Biofertilizer. In Algal Green Chemistry; Elsevier BV: Amsterdam, The Netherlands, 2017; pp. 189–200. [Google Scholar]
  100. Kumar, K.S.; Dahms, H.-U.; Won, E.-J.; Lee, J.-S.; Shin, K.-H. Microalgae—A promising tool for heavy metal remediation. Ecotoxicology and Environmental Safety 2015, 113, 329–352. [Google Scholar] [CrossRef]
  101. Chatzissavvidis, C.; Therios, I. Role of algae in agriculture. In Seaweeds: Agricultural Uses, Biological and Antioxidant Agents; Pomin, V.H., Ed.; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2014; pp. 1–37. [Google Scholar]
  102. Aziz, A.; Poinssot, B.; Daire, X.; Adrian, M.; Bézier, A.; Lambert, B.; Joubert, J.-M.; Pugin, A. Laminarin Elicits Defense Responses in Grapevine and Induces Protection Against Botrytis cinerea and Plasmopara viticola. Mol. Plant Microbe Interact. 2003, 16, 1118–1128. [Google Scholar] [CrossRef] [Green Version]
  103. Arunkumar, K.; Selvapalam, N.; Rengasamy, R. The antibacterial compound sulphoglycerolipid 1-0 palmitoyl-3-0(6′-sulpho-α-quinovopyranosyl)-glycerol from Sargassum wightii Greville (Phaeophyceae). Bot. Mar. 2005, 48, 441–445. [Google Scholar] [CrossRef] [Green Version]
  104. Kim, J.-D. Screening of Cyanobacteria (Blue-Green algae) from Rice Paddy Soil for Antifungal Activity against Plant Pathogenic Fungi. Mycobiology 2006, 34, 138–142. [Google Scholar] [CrossRef] [Green Version]
  105. Khan, Z.; Kim, Y.H.; Kim, S.; Kim, H. Observations on the suppression of root-knot nematode (Meloidogyne arenaria) on tomato by incorporation of cyanobacterial powder (Oscillatoria chlorina) into potting field soil. Bioresour. Technol. 2007, 98, 69–73. [Google Scholar] [CrossRef]
  106. Jaulneau, V.; Lafitte, C.; Corio-Costet, M.-F.; Stadnik, M.J.; Salamagne, S.; Briand, X.; Esquerré-Tugayé, M.-T.; Dumas, B. An Ulva armoricana extract protects plants against three powdery mildew pathogens. Eur. J. Plant Pathol. 2011, 131, 393–401. [Google Scholar] [CrossRef]
  107. Chaudhary, V.; Prasanna, R.; Nain, L.; Dubey, S.C.; Gupta, V.; Singh, R.; Jaggi, S.; Bhatnagar, A.K. Bioefficacy of novel cyanobacteria-amended formulations in suppressing damping off disease in tomato seedlings. World J. Microbiol. Biotechnol. 2012, 28, 3301–3310. [Google Scholar] [CrossRef]
  108. Baloch, G.N.; Tariq, S.; Ehteshamul-Haque, S.; Athar, M.; Sultana, V.; Ara, J. Management of root diseases of eggplant and watermelon with the application of asafoetida and seaweeds. J. Appl. Bot. Food Qual. 2013, 86, 138–142. [Google Scholar] [CrossRef]
  109. Kumar, M.; Prasanna, R.; Bidyarani, N.; Babu, S.; Mishra, B.K.; Kumar, A.; Adak, A.; Jauhari, S.; Yadav, K.; Singh, R.; et al. Evaluating the plant growth promoting ability of thermotolerant bacteria and cyanobacteria and their interactions with seed spice crops. Sci. Hortic. 2013, 164, 94–101. [Google Scholar] [CrossRef]
  110. Babu, S.; Prasanna, R.; Bidyarani, N.; Singh, R. Analysing the colonisation of inoculated cyanobacteria in wheat plants using biochemical and molecular tools. Environ. Boil. Fishes 2014, 27, 327–338. [Google Scholar] [CrossRef]
  111. Priya, H.; Prasanna, R.; Ramakrishnan, B.; Bidyarani, N.; Babu, S.; Thapa, S.; Renuka, N. Influence of cyanobacterial inoculation on the culturable microbiome and growth of rice. Microbiol. Res. 2015, 171, 78–89. [Google Scholar] [CrossRef]
  112. Esserti, S.; Smaili, A.; Rifai, L.A.; Koussa, T.; Makroum, K.; Belfaiza, M.; Kabil, E.M.; Faize, L.; Burgos, L.; Alburquerque, N.; et al. Protective effect of three brown seaweed extracts against fungal and bacterial diseases of tomato. Environ. Boil. Fishes 2016, 29, 1081–1093. [Google Scholar] [CrossRef]
  113. Rodriguez, A.A.; Stella, A.M.; Storni, M.M.; Zulpa, G.; Zaccaro, M.C. Effects of cyanobacterial extracellular products and gibberellic acid on salinity tolerance in Oryza sativa L. Saline Syst. 2006, 2, 7. [Google Scholar] [CrossRef] [Green Version]
  114. Sarhan, T.Z.; Ismael, S.F. Effect of Low Temperature and Seaweed Extracts on Flowering and Yield of Two Cucumber Cultivars (Cucumis sativus L.). Int. J. Agric. Food Res. 2014, 3, 41–54. [Google Scholar] [CrossRef]
  115. Stamatiadis, S.; Evangelou, L.; Yvin, J.-C.; Tsadilas, C.; Mina, J.M.G.; Cruz, F. Responses of winter wheat to Ascophyllum nodosum (L.) Le Jol. extract application under the effect of N fertilization and water supply. Environ. Boil. Fishes 2014, 27, 589–600. [Google Scholar] [CrossRef]
  116. Mansori, M.; Chernane, H.; Latique, S.; Benaliat, A.; Hsissou, D.; El Kaoua, M. Seaweed extract effect on water deficit and antioxidative mechanisms in bean plants (Phaseolus vulgaris L.). Environ. Boil. Fishes 2014, 27, 1689–1698. [Google Scholar] [CrossRef]
  117. Latef, A.A.H.A.; Srivastava, A.K.; Saber, H.; Alwaleed, E.A.; Tran, L.-S.P. Sargassum muticum and Jania rubens regulate amino acid metabolism to improve growth and alleviate salinity in chickpea. Sci. Rep. 2017, 7, 1–12. [Google Scholar] [CrossRef] [Green Version]
  118. Haggag, W.; Hoballah, M.; Ali, R. Applications of nano biotechnological microalgae product for improve wheat productiv-ity in semai aird areas. Int. J. Agric. Technol. 2018, 14, 675–692. [Google Scholar]
  119. Hamed, S.M.; El-Rhman, A.A.A.; Abdel-Raouf, N.; Ibraheem, I.B. Role of marine macroalgae in plant protection & improvement for sustainable agriculture technology. Beni Suef Univ. J. Basic Appl. Sci. 2018, 7, 104–110. [Google Scholar] [CrossRef]
  120. Mercier, L.; Lafitte, C.; Borderies, G.; Briand, X.; Esquerré-Tugayé, M.T.; Fournier, J. The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol. 2001, 149, 43–51. [Google Scholar] [CrossRef]
  121. I Pardee, K.; Ellis, P.; Bouthillier, M.; Towers, G.H.; French, C.J. Plant virus inhibitors from marine algae. Can. J. Bot. 2004, 82, 304–309. [Google Scholar] [CrossRef] [Green Version]
  122. Benkendorff, K.; Davis, A.R.; Rogers, C.N.; Bremner, J.B. Free fatty acids and sterols in the benthic spawn of aquatic molluscs, and their associated antimicrobial properties. J. Exp. Mar. Biol. Ecol. 2005, 316, 29–44. [Google Scholar] [CrossRef]
  123. Gerasimenko, N.I.; Martyyas, E.A.; Logvinov, S.V.; Busarova, N.G. Biological activity of lipids and photosynthetic pigments of Sargassum pallidum C. Agardh. Appl. Biochem. Microbiol. 2013, 50, 73–81. [Google Scholar] [CrossRef]
  124. Bulgari, R.; Franzoni, G.; Ferrante, A. Biostimulants Application in Horticultural Crops under Abiotic Stress Conditions. Agronomy 2019, 9, 306. [Google Scholar] [CrossRef] [Green Version]
  125. Kaya, C.; Higgs, D.; Sakar, E. Response of two leafy vegetables grown at high salinity to supplementary potassium and phosphorus during different growth stages. J. Plant Nutr. 2002, 25, 2663–2676. [Google Scholar] [CrossRef]
  126. Du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Sci. Hortic. 2015, 196, 3–14. [Google Scholar] [CrossRef] [Green Version]
  127. Saadatnia, H.; Riahi, H. Cyanobacteria from paddy fields in Iran as a biofertilizer in rice plants. Plant Soil Environ. 2009, 55, 207–212. [Google Scholar] [CrossRef] [Green Version]
  128. Safinaz, A.; Ragaa, A. Effect of some red marine algae as biofertilizers on growth of maize (Zea mayz L.) plants. Int. Food Res. J. 2013, 20, 1629–1632. [Google Scholar]
  129. El Arroussi, H.; Elbaouchi, A.; Benhima, R.; Bendaou, N.; Smouni, A.; Wahby, I. Halophilic microalgae Dunaliella salina extracts improve seed germination and seedling growth of Triticum aestivum L. under salt stress. Acta Hortic. 2016, 1148, 13–26. [Google Scholar] [CrossRef]
  130. Omar, H.H.; Abdullatif, B.M.; Al-Kazan, M.M.; El-Gendy, A.M. Various Applications of Seaweed Improves Growth and Biochemical Constituents ofZea MaysL. andHelianthus AnnuusL. J. Plant Nutr. 2014, 38, 28–40. [Google Scholar] [CrossRef]
  131. Ramya, S.S.; Vijayanand, N.; Rathinavel, S. Foliar application of liquid biofertilizer of brown alga Stoechospermum marginatum on growth, biochemical and yield of Solanum melongena. Int. J. Recycl. Org. Waste Agric. 2015, 4, 167–173. [Google Scholar] [CrossRef] [Green Version]
  132. El-din, S.M.M.; Hassan, S.M. The promotive effect of different concentrations of marine algae on spinach plants (Spinacia oleracea L.). Egypt. J. Hortic. 2016, 43, 109–122. [Google Scholar] [CrossRef]
  133. Mógor, Á.F.; Ördög, V.; Lima, G.P.P.; Molnár, Z.; Mógor, G. Biostimulant properties of cyanobacterial hydrolysate related to polyamines. Environ. Boil. Fishes 2018, 30, 453–460. [Google Scholar] [CrossRef]
  134. Dineshkumar, R.; Subramanian, J.; Gopalsamy, J.; Jayasingam, P.; Arumugam, A.; Kannadasan, S.; Sampathkumar, P. The Impact of Using Microalgae as Biofertilizer in Maize (Zea mays L.). Waste Biomass Valorization 2017, 10, 1101–1110. [Google Scholar] [CrossRef]
Applsci 11 00871 g001 550
Figure 1. Categorisation of the main activities attributed to algal/cyanobacterial biomass and extracts in crops’ production.
Figure 1. Categorisation of the main activities attributed to algal/cyanobacterial biomass and extracts in crops’ production.
Applsci 11 00871 g001
Table
Table 1. Microalgal and cyanobacterial metabolites with potential interest for agriculture.
Table 1. Microalgal and cyanobacterial metabolites with potential interest for agriculture.
MetabolitesExamplesMicroalgal/Cyanobacterial SourcesBiological
Activity		Role in
Agriculture		Refs.
Phenolic
compounds		Polyphenols; phenolic acids; flavonoids; phenylpropanoidsBotryococcus braunii; Chaetoceros calcitrans; Chlorella vulgaris; Isochrysis galbana; Isochrysis sp.; Neochloris oleoabundans; Odontella sinensis; Phaeodactylum tricornutum; Saccharina japonica; Skeletonema costatum; Tetraselmis suecicaAntibacterial; antioxidant; antifungalCrops’ protection against pathogens or other biotic and abiotic stress conditions[2,7,16,17,18,19,20,21]
TerpenoidsHemiterpenes; monoterpenes; sesquiterpenes; diterpenes; triterpenes; polyterpenesChondrococcus hornemanni; Hypnea pannosa; Oscillatoria perornata; Planktothricoids raciborskii; Plocamium cornutum; Plocamium leptophyllum; Portieria hornemann; Pseudanabaena articulate; Pseudanabaena sp.; Sphaerococcus coronopifolius; Synechocystis sp.; Thermosynechococcus elongatusAntibacterial; anticarcinogenic; antioxidantCrops’ protection against bacteria, insects and other organisms
Stimulation of preliminary growth and development of plants
Attraction of pollinators		[2,7,22,23,24,25,26,27,28]
Free fatty acidsSaturated and unsaturated fatty acidsAnabaena; Chlorella; Dunaliella; Nannochloropsis; Porphyridium; Scenedesmus; SpirulinaAntibiotic; anticarcinogenic; antifungal; antioxidant; antiviralCrops’ protection against pathogens or other biotic and abiotic stress conditions[2,7,29,30,31,32,33]
PolysaccharidesExtracellular polysaccharides; structural polysaccharides; energy-storage polysaccharidesAphanothece; Arthrospira; Chlamydomonas; Chlorella; Cylindrotheca; Dunaliella; Navicula; Nostoc; Phaeodactylum; Porphyridium; Rhodella; ScytonemaAntibacterial; anticancer; anticoagulant; anti-inflammatory; antioxidantImprovement of soil quality
Plant growth stimulation
Crops’ protection against biotic and abiotic stress conditions		[2,7,34,35,36,37,38,39,40,41,42,43,44,45,46]
CarotenoidsAlpha-carotene; beta-carotene; lutein; lycopene; astaxanthin; zeaxanthinChlorella protothecoides; Chlorella pyrenoidosa; Chlorella zofingiensis; Dunaliella salina; Haematococcus pluvialis; Muriellopsis sp.; Phaeodactylum tricornutum; Spirulina sp.Anticancer; anti-inflammatory; antioxidantSoil bioremediation and fertilisation
Crops’ protection against bacteria, insects and other biotic and abiotic stress conditions
Crops’ fortification		[7,47,48,49,50,51,52,53]
PhytohormonesAuxins; abscisic acid; cytokinins; ethylene; gibberellinsArthrospira; Chlamydomonas; Chlorella; Phormidium; Protococcus; ScenedesmusChemical messengersPlant growth stimulation
Regulation of cellular activities in crops
Crops’ response to stress conditions		[2,4,7,10,11,54]
Table
Table 2. Impacts of microalgae and cyanobacteria (and their metabolites) on soils’ improvement.
Table 2. Impacts of microalgae and cyanobacteria (and their metabolites) on soils’ improvement.
Mode of ActionAlgae/Algal ExtractsTarget Crop/SoilObserved ImprovementsRef.
Nitrogen fixationCyanobacterial inoculum composed by Aulosira fertilissima, Anabaena sphaerica, Nostoc hatei, Cylindrospermum majus and Westiellopsis prolificaRiceIncrease in nitrogen availability in the soil
Increase in grain and straw yields		[80]
Wild type and herbicide-resistant strains of Anabaena variabilisRiceIncrease in grain, straw and seeds yields
Increase in plant height and leaf length		[81]
Nostoc sp. vegetative cellsRiceIncrease in grain yields comparable to those obtained with a chemical fertiliser[82]
Nostoc entophytum and Oscillatoria angustissimaPeaIncrease in nitrogen fixation
Increase in growth parameters, germination percentage and photosynthetic pigments
Increase in nutritional value of pea seeds		[83]
Anabaena torulosa biofilmWheatIncrease in nitrogen availability in the soil[84]
Cyanobacterial-bacterial biofilms including the species: Calothrix sp., Anabaena laxa, Anabaena torulosa, Anabaena doliolum, Nostoc carneum, Nostoc piscinale, Trichoderma viride, Pseudomonas fluorescens and Azotobacter chroococcumSoybean and mungbeanIncrease in nitrogen availability in the soil
Increase in plant fresh weight		[85]
Nutrients’ availability in soilsCalothrix ghosei, Hapalosiphon intricatus and Nostoc sp.WheatIncrease in organic carbon content in the soil
Increase in grain yield		[86]
Cyanobacterial consortia including the species: Anabaena doliolum, Cylindrospermum sphaerica and Nostoc calcicolaWheat and milletIncrease in nitrogen and phosphorus availability in the soil
Decrease in soil density
Improvement of water retention capacity
Increase in grain yields
Improvement of nutritional properties (increase in protein content of grain and leaves)		[87]
Microalgal-bacterial flocs and Nannochloropsis oculataTomatoIncrease in ammonium, phosphorus and potassium availability in the soil
Improvement of fruit quality (increase in sugar and carotenoids contents)		[88]
Consortia and biofilms including the species: Azotobacter sp., Anabaena sp., Providencia sp. and Calothrix sp.OkraIncrease in zinc and iron availability in the soil
Beneficial changes in the microbiome
Increase in root yield and weight		[89]
Microalgal-cyanobacterial unicellular and filamentous consortia including species of: Chlorella, Scenedesmus, Chlorococcum, Chroococcus, Phormidium, Anabaena, Fischerella and SpirogyraWheatIncrease in nitrogen, phosphorus and potassium availability in the soil
Increase in organic carbon content in the soil
Improvement of product quality (increase in nitrogen, phosphorus and potassium contents in roots, shoots and grains)		[90]
Microalgal-cyanobacterial unicellular and filamentous consortia including species of: Chlorella, Scenedesmus, Chlorococcum, Chroococcus, Phormidium, Anabaena, Fischerella and SpirogyraWheatIncrease in zinc, iron, copper and manganese availability in the soil
Increase in organic carbon content in the soil
Increase in grain yield
Improvement of plant nutritional value (increase in grain micronutrient contents)		[91]
Chlorella sorokinianaSoil from a vineyardIncrease in nitrogen availability in the soil[92]
Soil physical and chemical amendmentsMicrocoleus vaginatus, Phormidium tenue, Scytonema javanicum, Nostoc sp. and Desmococcus olivaceusUnconsolidated sandIncrease in crust cohesion
Increase in the resistance to wind erosion		[93]
Nostoc strainsPoorly aggregated tropical soilsIncrease in aggregates’ stability[94]
Phycocyanin extract from Spirulina platensis and inactive biomass of Spirulina platensisSoil contaminated with diesel and biodieselReduction in diesel and biodiesel concentration using S. platensis and phycocyanin, respectively[95]
Table
Table 3. Impacts of microalgae and cyanobacteria (and their metabolites) on crops’ protection.
Table 3. Impacts of microalgae and cyanobacteria (and their metabolites) on crops’ protection.
Mode of ActionAlgae/Algal ExtractsTarget CropObserved ImprovementsRef.
Protection against biotic factorsLaminaria digitataGrapevineFungicidal activity against Botrytis cinerea and Plasmopara viticola[102]
Methanolic extract from Sargassum wightiiRiceAntibacterial activity against Xanthomonas oryzae[103]
Oscillatoria, Anabaena, Nostoc, Nodularia and Calothrix speciesPepperFungicidal activity against Alternaria alternate and Botrytis cinerea[104]
Oscillatoria chlorinaTomatoFungicidal activity against Meloidogyne arenaria
Improved plant growth		[105]
Extracts from Ulva armoricanaBean, grapevine and cucumberFungicidal activity against Erysiphe polygoni, Erysiphe necator and Sphareotheca fuliginea
Reduced foliar disease		[106]
Anabaena variabilis and Anabaena oscillarioidesTomatoReduction in fungal disease severity
Improved plant growth (increased height and fresh weight of plants)		[107]
Spatoglossum variabile, Stokeyia indica and Melanothamnus afaqhusainiiWatermelon and eggplantFungicidal activity against the root rotting fungi, Fusarium solani, Fusarium oxysporum and Macrophomina phaseolina
Antinematodal activity against Meloidogyne spp.
Improved plant growth (increased fresh weight of shoots, increased length of vines in watermelon and increased shoot length in eggplant)		[108]
Anabaena laxa and Calothrix elenkiniiCoriander, cumin and fennelIncrease in the activity of β-1,3 endoglucanase in shoots and roots
Increase in fungicidal activity
Increase in germination rates
Increase in shoot and root length
Increase in plant dry weight		[109]
Anabaena torulosa, Anabaena laxa, Anabaena azollae, Anabaena oscillarioides and Calothrix sp.WheatIncrease in nitrogen fixation
Increase in the activity of hydrolytic and defence enzymes (endoglucanase, peroxidase, polyphenol oxidase and phenylalanine ammonia lyase)
Increase in fresh and dry weight of plant		[110]
Calothrix elenkiniiRiceIncrease in the activity of hydrolytic and defence enzymes (peroxidase, polyphenol oxidase and phenylalanine ammonia lyase)
Increase in nitrogenase activity and indole acetic acid production
Increase in plant growth		[111]
Aqueous extract from Cystoseira myriophylloides and Fucus spiralisTomatoAntibacterial activity against Agrobacterium tumefaciens[112]
Polysaccharides’ extract from Chlorella vulgaris, Chlorella sorokiniana and Chlamydomonas reinhardtiiTomatoIncrease in the activity of hydrolytic and defence enzymes (β-1,3 endoglucanase, peroxidase, ascorbate peroxidase and phenylalanine ammonia lyase)
Improvement of plant nutritional value (increase in polyunsaturated fatty acids contents)		[40]
Protection against abiotic factorsScytonema hofmanniRiceAlleviation of salt stress comparable to the one obtained with gibberellic acid[113]
Seaweed extractsCucumberLow temperature stress was not observed in treated plants
Improvement of plant productivity (increase in the number of fruit per plant, fruit weight and total yield)		[114]
Extracts from Ascophyllum nodosumWheatAlleviation of drought stress
Increase in growth, yield and nutrients uptake		[115]
Extracts from Ulva rigida and Fucus spiralisBeansAlleviation of drought stress
Increase in the activity of antioxidant enzymes and in the polyphenol content (mediators of plants’ protection mechanisms)
Improvement of plant growth		[116]
Sargassum muticum and Jania rubensChickpeaAlleviation of salt stress
Increase in the activity of enzymes (superoxide dismutase and peroxidase) and amino acids (serine, threonine, proline and aspartic acid) associated with plants’ stress responses
Improvement of plant growth		[117]
Polysaccharides extracted from Dunaliella salinaTomatoAlleviation of salt stress
Activation of metabolic pathways involved in plants’ tolerance to stress
Mitigation of the decrease in length and dry weight of shoots and roots		[34]
Oscillatoria agardhiiWheatAlleviation of drought stress
Increase in the activity of hydrolytic and defence enzymes (catalase, superoxide dismutase and peroxidase)
Increase in grain yield
Improvement of plant quality parameters		[118]
Table
Table 4. Impacts of microalgae and cyanobacteria (and their metabolites) on direct growth stimulation of plants.
Table 4. Impacts of microalgae and cyanobacteria (and their metabolites) on direct growth stimulation of plants.
Algae/Algal ExtractsTarget CropObserved ImprovementsRef.
Anabaena strains (Anabaena spiroides, Anabaena osillarioides, Anabaena torulosa and Anabaena variabilis)RiceIncrease in germination rate
Increase in plant height and shoots length
Increase in fresh and dry weights of leaf, stem and root
Improvement of soil properties (increase in soil moisture and porosity)		[127]
Laurencia obtusa, Corallina elongata and Jania rubensMaizeIncrease in plant length and fresh and dry weight
Increase in the number of leaves
Improvement of plant nutritional value (increase in potassium, phosphorus and nitrogen contents)		[128]
Exopolysaccharides extracts from Dunaliella salinaWheatIncrease in germination rate and seedling growth
Increase in root and coleoptiles height
Increase in tolerance to salt stress		[129]
Aqueous extracts from Gracilaria corticata and Enteromorpha flexuosaMaize and sunflowerIncrease in shoot and root length and dry weight
Improvement of plant nutritional value (increase in photosynthetic pigments, carbohydrate, proteins and nutrients contents)		[130]
Liquid extracts from Stoechospermum marginatumBrinjalIncrease in shoot and root length
Increase in fresh and dry weight of leaves
Increase in leaf area
Improvement of leaves nutritional value (increase in moisture, photosynthetic pigments, protein, amino acids, reducing sugars and ascorbic acid contents)		[131]
Total polysaccharides extract from Spirulina platensisTomato and pepperIncrease in plants’ size
Increase in roots’ weight
Increase in size and number of nodes		[39]
Ulva lactuca and Jania rubensSpinachIncrease in plant yield and height
Improvement of plant nutritional value (increase in chlorophyll and nitrogen contents)		[132]
Arthrospira platensisLettuceIncrease in seedling growth
Increase in spermine content in leaves		[133]
Chlorella vulgaris and Spirulina platensisMaizeIncrease in germination rate and plant yield
Increase in fresh and dry weights of shoot, root and whole plant
Increase in shoot length and in the number of leaves		[134]
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Gonçalves, A.L. The Use of Microalgae and Cyanobacteria in the Improvement of Agricultural Practices: A Review on Their Biofertilising, Biostimulating and Biopesticide Roles. Appl. Sci. 2021, 11, 871. https://0-doi-org.brum.beds.ac.uk/10.3390/app11020871

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Gonçalves AL. The Use of Microalgae and Cyanobacteria in the Improvement of Agricultural Practices: A Review on Their Biofertilising, Biostimulating and Biopesticide Roles. Applied Sciences. 2021; 11(2):871. https://0-doi-org.brum.beds.ac.uk/10.3390/app11020871

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Gonçalves, Ana L. 2021. "The Use of Microalgae and Cyanobacteria in the Improvement of Agricultural Practices: A Review on Their Biofertilising, Biostimulating and Biopesticide Roles" Applied Sciences 11, no. 2: 871. https://0-doi-org.brum.beds.ac.uk/10.3390/app11020871

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