Abstract
Plant biostimulants are defined as materials containing microorganisms or substances whose function when applied to plants or the rhizosphere is to stimulate natural mechanisms to enhance plant growth, nutrient use efficiency, tolerance to abiotic stressors and crop quality, independent of their nutrient content. In agriculture, seaweeds (Macroalgae) have been used in the production of plant biostimulants while microalgae still remain unexploited. Microalgae are single cell microscopic organisms (prokaryotic or eukaryotic) that grow in a range of aquatic habitats, including, wastewaters, pounds, lakes, rivers, oceans, and even humid soils. These photosynthetic microorganisms are widely described as renewable sources of biofuels, bioingredients and biologically active compounds, such as polyunsaturated fatty acids (PUFAs), carotenoids, phycobiliproteins, sterols, vitamins and polysaccharides, which attract considerable interest in both scientific and industrial communities. Microalgae polysaccharides have so far proved to have several important biological activities, making them biomaterials and bioactive products of increasing importance for a wide range of applications. The present review describes microalgae polysaccharides, their biological activities and their possible application in agriculture as a potential sustainable alternative for enhanced crop performance, nutrient uptake and resilience to environmental stress. This review does not only present a comprehensive and systematic study of Microalgae polysaccharides as plant biostimulants but considers the fundamental and innovative principles underlying this technology.
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Introduction
Microalgae are photosynthetic microscopic organisms (prokaryotic or eukaryotic) that grow in a range of aquatic habitats, including ponds, rivers, lakes, oceans, wastewaters and even humid soils. Microalgae are an economical, renewable and sustainable bioresource that are exploited in different fields as biofuels, bioactive products and food ingredients. Several microalgae species have been investigated for their potential as value-added products with remarkable pharmacological and biological qualities, which come from their significant ability to convert atmospheric CO2 to useful products such as carbohydrates, lipids, and other bioactive metabolites (Almomani et al. 2019; Bhagea et al. 2019; Khan et al. 2018; Molazadeh et al. 2019; Nie et al. 2018; Shakibaie et al. 2010; Villarruel-López et al. 2017). In agriculture, microalgae can be used for different applications, such as soil amendments or plant biostimulants. (Chiaiese et al. 2018; Renuka et al. 2018; Ronga et al. 2019).
Plant biostimulants are defined as microorganisms or substances which when applied to plants in finite quantities, are able to improve plant growth, nutrient use efficiency, tolerance to abiotic stressors and crop quality. This definition entails diverse organic and inorganic substances and/or microorganisms including algal extracts (Calvo et al. 2014; Chiaiese et al. 2018; du-Jardin 2015; Rouphael and Colla 2018). Today, seaweeds more than microalgae, have been largely exploited for the production of plant growth biostimulants and represent an important category of organic biostimulants (Battacharyya et al. 2015; Colla et al. 2017; Khan et al. 2011). However, microalgae could also be largely exploited in agriculture as a renewable bioresource for plant biostimulants, considering their capacity to produce a remarkable diversity of biologically active molecules including fatty acids, osmolytes, phytohormones, polysaccharides and phenolics (Cuellar-Bermudez et al. 2015; Renuka et al. 2018; Ronga et al. 2019). In addition, other studies have reported that microalgae can also produce plant growth-promoting substances such as auxins, cytokinins, betaines, amino acids, vitamins, polyamines and gibberellins (Stirk et al. 2013a, b; Tate et al. 2013; Plaza et al. 2018). Nevertheless, carbohydrates, including polysaccharides are usually one of the major components of microalgal extracts, accounting for up to 46% of the dry weight (DW) in certain species such as Chlorella spp., Chlamydomonas spp., Dunaliella spp. and Spirulina spp., (Pinzón et al. 2014; Spolaore et al. 2006; Tibbetts et al. 2015).
In recent years, an increasing amount of research has been undertaken to study the effect of microalgae-based products (proteins hydrolysates, polysaccharides/exopolysaccharides and cell wall extracts) on the growth and development of several crops such as tomato, wheat, lettuce and pepper, under optimal and stressful conditions (Barone et al. 2018; Chiaiese et al. 2018; El Arroussi et al. 2016, 2018; Garcia and Sommerfeld 2016). The objective of this review is to report an overview of the current status of microalgae polysaccharide use and their potential as biostimulants of plant growth, nutrient uptake and tolerance to both biotic and abiotic stresses. Comparison of the biological activities between microalgae total extracts and purified or total microalgae polysaccharide extracts is also highlighted and briefly discussed.
Biochemical composition and functional groups of Microalgae polysaccharides
Polysaccharides are polymeric carbohydrate macromolecules with complex structures, and have various functional activities (Nie et al. 2018). Both biochemically and structurally, polysaccharides greatly differ from one specie to another. These complex differences are also reflected in the high number of enzymes involved in polysaccharide synthesis and modification (Rossi and Philippis 2016). With the exception of Gyrodinium impudicum and Chlorella vulgaris that produce homopolymer polysaccharides of galactose (Yim et al. 2007) and B-(1,3)-glucan respectively, microalgae polysaccharides are heteropolymers of mainly galactose, xylose and glucose in different proportions, linked together by glycosidic bonds (Raposo et al. 2015). This proportion difference in constituent neutral sugars can modify the polysaccharide’s bio stimulant properties, although other biostimulatory properties are also largely attributed to the polysaccharide’s sufation, uronic acid content and molecular weight (MW) (Farid et al. 2019; Mishra and Jha 2013; Ponce et al. 2003;Sangha et al. 2010; Qi et al. 2005; Zha et al. 2016). Other sugars such as rhamnose, fucose, fructose and methyl sugars can also be constituents of microalgae polysaccharides (Raposo et al. 2015). Table 1 illustrates some strains of microalgae/blue-green algae producing polysaccharides and their main neutral sugars.
There are few studies on microalgae polysaccharides exhibiting biostimulant and plant- protector properties. Hence, the direct relationship between the molecular structure of polysaccharides and their bio-stimulant activity is yet to be understood. However, the knowledge of seaweed-extracted polysaccharides and their effects on plant mechanisms (Michalak et al. 2017; Michalak and Chojnacka 2015), could help predict microalgae polysaccharides and their possible elicitor effects on plant mechanisms. For instance, recent research had unraveled that molecular mechanisms by which carrageenan polysaccharides from seaweed can mediate plant growth and plant defense responses is by modulating various metabolic processes such as photosynthesis, nitrogen and sulfur assimilation and plant defense pathways (Shukla et al. 2016). Nevertheless, the functional activities of polysaccharides differ according to their constituent monosaccharides, molecular weight and degree of sulfation, thus, a study of the molecular structure of microalgae polysaccharides and their specific elicitor effects on plant growth and defense mechanism might be a helpful tool in plant biotechnology.
Microalgae polysaccharides as plant bio stimulants
With an ever-increasing global population estimated to expand to more than 9.7 billion by 2050, modern agriculture is compelled to become increasingly efficient by producing more food in a sustainable and eco-friendly way. One of the innovative technologies addressing these challenges involves the development of novel plant biostimulants and effective methods for their application (Bulgari et al. 2015; Calvo et al. 2014; Yakhin et al. 2017). Plant biostimulants including algal polysaccharides have been described since the beginning of modern agriculture, and could be considered as a good production strategy for obtaining high yields of nutritionally valuable food with lower impact on the environment.
The definition of plant biostimulants is based on scientific principles as microorganisms or substances which when applied to plants are able to stimulate nutrient uptake, promote seed germination, improve crop’s yield and tolerance to abiotic stress. Some important concepts have been proposed so far to define and classify plant biostimulants. For instance (Basak 2008) proposed that biostimulants could be classified depending on the mode of action and the origin of the active ingredient. However, years later (du-Jardin 2015), suggested that “any definition of biostimulants should focus on the agricultural functions of biostimulants, which is improvement in plant yield or quality or increased efficiency of plant productivity, and not on the nature of their constituents nor on their modes of action”. Similarly, (Bulgari et al. 2015) highlighted that “biostimulants should be classified on the basis of their action on plants or on the physiological plant responses rather than on their composition.” Today, microlgae can be classed among seaweed extracts and botanicals. But compared with seaweeds, the practical applications of microalgae in agriculture is still very limited and much less is known regarding their biostimulant mechanisms in plants, the attention being much focused on their functional activities in Nutraceutical, pharmaceutical and cosmetic products. However, there seems to be opportunities to largely exploit them as plant biostimulants. In recent years, researchers have pushed the barrier by looking into exploiting microalgae total extracts and/or Polysaccharides as potential plant bio-elicitors and/or bio stimulants in agriculture. So far, Microalgae polysaccharides have demonstrated a broad range of biological activities on higher plants (El Arroussi et al. 2016, 2018; Farid et al. 2019) and could have multi-functional properties in agriculture, facilitating nutrient uptake, improving crop performance, physiological status and tolerance to abiotic stress (Barone et al. 2018, 2019; Borowitzka 2016; de Morais et al. 2015; Faheed and Fattah 2008; Garcia and Sommerfeld 2016; Renuka et al. 2018; Stadnik and Freitas 2014).
The outstanding challenge in promoting microalgae polysaccharide as plant biostimulants in agriculture is understanding their specific structure–function bioactivities on plants. Some studies demonstrated that besides neutral sugars and sulfate content, low (MW) polysaccharides exhibit greater effects on plant mechanisms (Stasio et al. 2018; Zha et al. 2016). This can be explained by the fact that a lower (MW) is generally important for the permeability of compounds. Therefore, it is not only the bioactivity of molecules or their specific target/function, but their permeability and capacity to reach the target also remains essential.
Some studies have also unraveled the molecular mechanisms by which seaweed polysaccharides such as carrageenans and their oligomeric forms mediate plant growth and plant defense responses; by regulating photosynthesis and carbon fixation in plants, enhancing ribulose 1, 5 bisphosphate carboxylase/oxygenase (Rubisco) activity, ancillary pathways, cell division, purine and pyrimidine synthetic pathways as well as metabolic pathways involved in nitrogen and sulfur assimilation. It was also observed that carrageenans and their oligomeric forms modulate the activity of different defense pathways, including jasmonate, salicylate and ethylene signaling pathways (González et al. 2013; Mercier et al. 2001; Shukla et al. 2016; Jiang et al. 2012).
Today, significant advancements including, the application of the omics strategies; transcriptomics (Goñi et al. 2016; Wilson et al. 2015), and metabolomics (Ertani et al. 2014) or other molecular (Petrozza et al. 2014) studies, have been proposed in order to shed light on the modes of action of plant biostimulants. In addition, (Conan et al. 2015) at the 2nd World Congress on the use of Biostimulants in Agriculture also highlighted the identification of the bioactive compounds responsible for plant growth responses using metabolomic profiling of biostimulant products and analysis of their physiological effects on plants through transcriptomic and metabolomic strategies. This methodology would allow the determination of metabolite pathways in plants, modulated by biostimulants and could provide insight into gene regulations. Figure 1 depicts the bio-stimulant property of algal polysaccharides on some of the key mechanism related to plant growth.
Microalgae polysaccharides on plant growth and Nutrient uptake
Microalgae Polysaccharides can stimulate plant growth and nutrient uptake by modulating various physiological and biochemical processes. Some studies have demonstrated that microalgae extracts, tested both under open-field and greenhouse conditions are able to stimulate germination, seedling growth, shoot, and root biomass in plants.
In his study, El Arroussi et al. (2016) showed that polysaccharides extracted from S. platensis significantly promoted plant growth in Capsicum annuum and Solanum lycopersicum, which was demonstrated in terms of plant weight, plant size, and size/number of leaves. In the same way, seaweed polysaccharides have demonstrated a number of biological activities on plant growth (Castro et al. 2012; González et al. 2013; Khan et al. 2011; Sarfaraz et al. 2011; Sharma et al. 2012, 2014; Vera et al. 2012). It was speculated by González et al. (2013) that oligo-alginate and oligo-carrageenan may interact with plasma membrane receptors that use a co-receptor involved in signal transduction leading to simultaneous activation of plant growth. In addition, macroalgal-extracted polysaccharides have been confirmed to be used as perfect metal ion chelators. However, without in-depth study of polysaccharide mechanisms on nutrient uptake, it is possible to assume that the increased nutrient uptake might not be directly modulated by polysaccharides but could be a result of improved root surface of treated plants, which may automatically improve nutrient accessibility and uptake. It has also been reported that polysaccharides are rich in functional groups having the ability to bind to some micro elements with important plant nutritional value (Kaplan et al. 1987), hence improving the roots’ nutrient availability. Therefore, there is need to study microalgae polysaccharides and their specific effects on nutrient uptake by plants and soil nutrient availability.
Microalgae polysaccharides on abiotic stress
Algal compounds exhibit great potential to enhance not only plant growth and nutrient uptake but resistance to abiotic and biotic stresses. During their entire life cycle, plants are exposed to several environmental stresses, which negatively affect their productivity and survival (Shaik and Ramakrishna 2014). One of the most common indication of stress is the production of reactive oxygen species (ROS). ROS are constantly produced from metabolic processes such as photosynthesis and respiration but are also formed in plant cells as a consequence of myriad stimuli ranging from abiotic and biotic stress. ROS constitute an ambiguous role during stress responses. Being toxic molecules, they are able to oxidatively injure cells (Mittler et al. 2004). To enable them to tolerate stress factors and survive, plants have developed a range of morphological, physiological and biochemical mechanisms such as the production of ROS scavenging enzymes in order to mitigate ROS potential toxic effects. (Gill and Tuteja 2010; Potters et al. 2004; You and Chan 2015). Interestingly, it has been demonstrated that Microalgae Polysaccharides can mitigate ROS toxicity in plants by enhancing the production of ROS antioxidant enzyme activities.
This mechanism can be explained by the fact that Polysaccharides contain neutral sugars which may interact with plasma membrane receptors as signal molecules and thereby leading to the activation of a series of biochemical reactions. But more importantly, algal polysaccharides could be perceived by membrane receptors as microbial-associated molecular patterns (MAMPs) and thereby inducing the MAMPs-dependent signaling pathways which involves the activation of Ca2+ influx, ROS production, Octadecanoid and Phenylpropanoid pathways with Lipoxygenase (LOX) and Phenylalanine ammonia lyase (PAL) respectively as key enzymes, and consequently ROS scavenging enzymes (Farid et al. 2019; Kemmerling et al. 2011). In his study, El Arroussi et al. (2016) demonstrated that the application of microalgae sulfated exopolysaccharides derived from D. salina enhanced the accumulation of proline and ROS antioxidant enzyme activities of Catalase (CAT), Peroxidase (POD) and Superoxide dismutase (SOD) in plants subjected to saline stress. Farid et al. (2019) also reported that treatment with C. vulgaris polysaccharides stimulated the enzymatic activity of Ascorbate Peroxidase (APX) in tomato plants. In the same study, microalgae polysaccharides extracted from C. reinhardtii and C. sorokiniana significantly enhanced POD activity. The ability of Algae polysaccharides to enhance ROS scavenging was also reported by Zou et al. (2019), who demonstrated that Lessonia nigressens polysaccharides (LPNs) effectively induced ROS scavenging in wheat seedlings by modulating their antioxidant enzyme activities under salt stress. Figure 2 illustrates the possible cellular mechanisms triggered by algal polysaccharides.
The activation of the MAMPs-dependent signaling pathways also trigger other mechanisms such as wax formation on the cuticle and synthesis of lignin, leading to the thickening of the cell walls (Fujita et al. 2006; Rejeb et al. 2014), which may reduce water loss through trans-evaporation and alleviate drought stress in plants.
Microalgae polysaccharides on biotic stress
As described in Fig. 2, plants deploy a wide range of defense mechanisms induced by elicitors from pathogen’s cell wall components including chitin, lipo-polysaccharides, proteins such as bacterial flagellin and other chemicals of natural and synthetic origin.
Microalgae could be a promising source of polysaccharide elicitors. Molecules of polysaccharides perceived by plants’ membrane receptors may trigger a series of defense mechanisms. Farid et al. (2019) indicated that microalgae crude polysaccharide extracts can induce plant innate immunity, depending on the microalgae strain. In his study, polysaccharides extracted from C. vulgaris and C. sorokiniana exhibited a significant increase in β-1,3-glucanase activity, which is one of the pathogenesis-related (PR) proteins, grouped in the PR-2 family that break down the cell wall components of pathogens. Induction of PR proteins is a consequence of the activation of plant defensive pathways, which limit the entry, or the further spread of the pathogen (Gupta et al. 2013). In the same study, C. sorokiniana crude polysaccharides had a significant stimulatory effect on Phenylalanine ammonia lyase (PAL) activity, indicating an up-regulation of the phenylpropanoid pathway.
The products of phenylpropanoid pathway in plants are thousands of compounds, that may end up in the composition of phenolic substances such as phytoalexins, which are toxic molecules against pathogens (Fesel and Zuccaro 2016). Moreover, sulfated polysaccharides from seaweed exhibited similar effects on phytoalexin accumulation and on the expression of genes involved in Salicylic acid (SA) and Jasmonic acid (JA) signaling pathways that induce plants’ resistance against pathogens (Ghannam et al. 2013; Klarzynski et al. 2003). The activation of these signaling pathways leads to an increased expression of genes encoding PR proteins, PAL, lipoxygenase (LOX) and ROS Scavenging enzymes and other enzymes involved in synthesis of terpenoids and/or alkaloids having antimicrobial activities (Vera et al. 2011, 2012).
Comparison of the biological activity of Microalgae total crude extracts and purified polysaccharides extracts
The biostimulant properties of total algae extracts have generally been attributed to the presence of many bioactive ingredients such as phytohormones, phenolic compounds, amino acids organic molecules, and bioactive secondary metabolites (Di Stasio et al. 2018). Nonetheless, it is difficult to determine the active compounds of total extracts and their mode of action due to their diversity and complexity. On the other hand, polysaccharides are purified compounds and much easier to exploit, their biostimulant properties usually being attributed to constituent neutral sugars, sulfate content and MW (Ponce et al. 2003; Qi et al. 2005; Sangha et al. 2010; Zha et al. 2016). Moreover, polysaccharides are one of the major components of total algal extracts that contribute to the observed beneficial effects of total extracts on plants (Di Stasio et al. 2018). However, the application of total crude microalgae extracts may prove more effective in stimulating plant growth as compared to their purified polysaccharides, attributing to the fact that total crude extracts contain several other bioactive molecules that may work in synergy to promote plant growth (Rouphael and Colla 2018). But while several bioactive molecules might exhibit greater effects, we cannot annul the possibility for their contrarious and antagonistic interactions, which could result in less effect on plant growth as compared to purified compounds. Thus, an in-depth comparative study of microalgae extracts and their purified polysaccharides is necessary to shed more light on this hypothesis. The comparison of total algae extracts and their purified compounds is summarized in Table 2.
Future perspective
Studies on microalgae polysaccharides in agriculture have so far highlighted their biostimulant properties on plants in laboratory conditions. However, On-farm trials and whole-field studies are needed to provide support information for practical microalgae polysaccharide applications and valorize the studies conducted so far. There is also need to study the effect of microalgae polysaccharides on a broader range of plant species to understand their biostimulant effects on different plant types.
Conclusion
Microalgae could be the new sustainable bioproducts for the development of plant biostimulants. These photosynthetic microorganisms are not only renewable but sustainable and economical sources of bioactive products and food ingredients. Microalgae polysaccharides have so far exhibited bio-stimulant properties that have proven useful for diverse industrial applications, although only a few studies have demonstrated their potential as plant bio-elicitors and/or biostimulants in agriculture. The modes of action of Microalgae polysaccharides have also been poorly studied. Understanding their specific elicitor effects on plant growth and defense mechanism might not only be a helpful tool in plant biotechnology but a big step in addressing modern agriculture challenges faced with an ever-increasing food demand and a changing climate.
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Chanda, Mj., Merghoub, N. & EL Arroussi, H. Microalgae polysaccharides: the new sustainable bioactive products for the development of plant bio-stimulants?. World J Microbiol Biotechnol 35, 177 (2019). https://doi.org/10.1007/s11274-019-2745-3
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DOI: https://doi.org/10.1007/s11274-019-2745-3