Abstract
The indiscriminate or non-strategic use of chemical fertilizers in agriculture can potentially have adverse effects on natural ecosystems due to their harmful impacts. As a cleaner, more sustainable supplementary treatment to minimize the need for synthetic nutrient inputs, seaweed-based biostimulants (phyco[bio]stimulants) are being widely studied to increase agricultural productivity for the burgeoning global population. Kappaphycus alvarezii, a fast-growing, tropical red alga widely cultivated for its hydrocolloid content, is a promising source of bioactive compounds that improve plant growth, including imparted tolerance to some levels of abiotic and biotic stressors in harsh environmental conditions. The alga also contains protein, carbohydrates, fatty acids, fibres, algal hormones, polyphenols, and various macro- and microelements. The polysaccharide κ-carrageenan, a major constituent of this particular seaweed, also has known plant growth-stimulating effects. Thus, various K. alvarezii-based biostimulants are used in agriculture, including liquid extracts and solid formulations which are applied as: drenches, foliarly and seed coatings, or seed soaking. These groups of biostimulants are reported to increase growth, yield, nutrient uptake, and biotic and abiotic resilience, depending on the type of extraction method, concentration of the applied extract, and also timing of the application within the treated plant’s growth cycle. This review summarizes various K. alvarezii-based products used in agriculture for plant biostimulation, their extraction procedures, application modes, and proposed mechanisms of action. We reviewed the scientific data supporting the use of Kappaphycus extracts as biostimulants to enhance crop productivity and quality. Additionally, the beneficial impacts of using Kappaphycus extracts on soil health and their potential as a sustainable, adaptive strategy for addressing climate variability is discussed. Several research gaps have been identified to understand the current limitations of the existing knowledge base, and a way forward has been presented to prioritize areas for further investigation.
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Introduction
The 2030 Agenda for Sustainable Development adopted by United Nations, identified 17 goals aimed at maintaining peace and prosperity for humanity. Key amongst these goals: "responsible consumption and production," "zero hunger," and "climate action" need to be achieved while ensuring food security for the growing population. To meet this challenge, it is essential to increase agricultural production while minimizing environmental impacts. Sustainable production techniques such as conservation agriculture, to increase resilience, integrated plant nutrient management, natural resource management, and the use of agricultural inputs with low carbon footprints, have been suggested as requirements to responsibly increase crop productivity.
Biostimulants are gaining prominence globally as one method to meet these challenges. The US 2018 Farm Bill defined biostimulants (Sible et al. 2021), while the EU included them as a distinct category under the regulation of fertilizer products (Ricci et al. 2019). India's Gazette publication in Feb. 2021 spelled out categories, including seaweed extracts. Such regulatory frameworks encourage biostimulant use in agriculture and boost their need for manufacture. Seaweed-based biostimulants (phyco[bio]stimulants) are the most researched members of the biostimulant category and improve plant growth, defense, and nutrient-use-efficiency (Shukla et al. 2019, 2022). Various seaweeds have long been used as an amendment for soil (Buschmann et al. 2017). The red, tropical seaweed, Kappaphycus alvarezii has gained increasing importance in recent years as a source of various types of biostimulant extracts (da Costa et al. 2017; Begum et al. 2018; Carillo et al. 2020; Del Buono 2020; El Boukhari et al. 2020; Wozniak et al. 2020).
Ghosh et al. (2015) and Singh et al. (2018) showed that Kappaphycus-based biostimulants can play a significant role in crop intensification with limited environmental trade-offs. Members of this seaweed genus have a high growth rate and can be relatively easily cultivated leading to their being responsible for significant carbon assimilation (Mantri et al. 2017b). Biostimulants made from biomass of this genus and in particular the species K. alvarezii have lower carbon and fresh water footprints than fertilizers (Singh et al. 2018) and are also reported to enhance crop yields (Pramanick et al. 2014a; Raverkar et al. 2016; Mantri et al. 2022). Their use ultimately reduces the units of carbon and water associated with each unit of food production, contributing to the reduction of greenhouse gas emissions to the atmosphere (Ghosh et al. 2015; Sharma et al. 2017; Singh et al. 2018). Climate change can exacerbate environmental stress, drastically diminishing crop productivity and adversely affecting rhizospheric soil microbes (Trivedi et al. 2022b). Kappaphycus-based biostimulants have been demonstrated to ameliorate soil moisture stress by modulating biochemical and microbiological parameters (Trivedi et al. 2022b). The implementation of biostimulants sourced from this economically important, cultivatable alga can yield positive socio-economic results throughout the entire value-chain, leading to the betterment of seaweed growers' livelihoods (i.e., the marine farmers) and the associated industry employees, as well as an increase in terrestrial farmers' income upon the application of these products to crops (Mantri et al. 2017b, 2022). As such, it is imperative to provide a thorough review of the diverse categories of available biostimulants derived from K. alvarezii and the advantages for crop quality and productivity that can be gained from their use. This review emphasizes essential research that has established the basis for comprehending the active components of this red seaweed and their functions in treated plants, such as their mechanisms of action, as well as the optimal application frequency and dosage for achieving the maximum benefits. Furthermore, this review aims to shed light on required areas for future research and development.
Kappaphycus alvarezii cultivation and biomass valorization for various applications, including biostimulants
Kappaphycus alvarezii (Doty) L.M. Liao, is a red alga also known by its commercial names of ‘cottonii’ and ‘Elkhorn sea moss’, that is widely cultivated in tropical waters since the early 1970s. It is especially cultivated in Asian countries such as Indonesia, the Philippines, Vietnam, Zanzibar and Malaysia. It is mainly cultivated for its cell wall polysaccharides i.e., predominantly κ-carrageenan (κ-Cg) (Hayashi and Reis 2012) for use in many applications such as highly processed food. Figure 1 shows the structure of κ-Cg along with ι- and λ- carrageenans. Other significant uses of cultivated K. alvarezii biomass are its commercial-scale application for non-rheological purposes, such as the production of reduced graphene oxide (Sharma et al. 2014), chemicals (i.e., potassium sulfate fertilizer and hydroxymethyl furfural), water purification (Mondal et al. 2013), bioethanol (Khambhaty et al. 2012; Meinita et al 2012), food supplements (Wanyonyi et al. 2017), animal feeds (Sharma and Datt 2020) and health supplements (Sharma et al. 2019), etc. (Fig. 2). However, since the development of an integrated carrageenan and plant biostimulant technology (Eswaran et al. 2005), the use of its raw material as a biomass for the industrial production of plant biostimulants has increased considerably (Hurtado et al. 2021). Dried cultivated Kappaphycus biomass is known as RDS (i.e., Raw Dried Seaweed) and has a moisture content of around 35%.
The first successful cultivation of K. alvarezii was achieved in the Philippines in the 1970s (Mantri et al. 2017b). Since then, the global fresh weight production of K. alvarezii reached 1.6 million tonnes, valued at US$ 215 million in 2018 (FAO 2020). These values are provided here for comparative purposes only and recently the veracity of these values was questioned (See Steven Herman’s http://www.phyconomy.net and Hatch Blue’s http://www.seaweedinsights.com/. for evolving details; accessed July 2023). Southeast Asian countries have almost 60% of the world’s cultivation sites (Hurtado et al. 2019). This is mainly because of the favourable geographical area for cultivation within ± 10° latitude (Hayashi et al. 2010). A series of videos on eucheumatoid seaweeds amongst which K. alvarezii is a member were made available by the Tropical Seaweed Coalition Development workshop which is maintained at www.phyconomy.org (accessed July 2023).
Kappaphycus alvarezii has a high average daily growth rate (DGR) of up to 10.7% when cultivated using the bamboo raft technique (Hayashi et al. 2010), yielding up to 150–200 kg fresh biomass, in a 45-day cycle, from a 3 × 3 m bamboo raft (Ghosh et al. 2015; Mantri et al. 2017b). Various cultivation methods have been used, including fixed off-bottom (for shallow areas), hanging long-line fixed and swing (for deeper areas), monoline, tube-net, multiple-raft long-line (such as bamboo raft, PVC pipe rafts) (Hayashi et al. 2010; Mantri et al. 2017a). The average DGR reported was 0.2–5.3% day−1 and 0.5–10.7% day−1 for fixed off-bottom and raft methods, respectively (Hayashi et al. 2010). Growth rates, biomass, yield, and carrageenan quality greatly depend on the water quality (Simatupang et al. 2021) variety/strain, cultivation technique, period of growth (i.e., 30, 45, and 60 days), and water depth (Hurtado et al. 2021).
In 1984, CSIR—Central Salt & Marine Chemicals Research Institute (CSMCRI) introduced a strain of K. alvarezii of Philippine origin into quarantine in Indian waters and employed floating bamboo rafts with nets laid out at the bottom to reduce losses due to grazing by herbivorous fish. Tube-net methods were also adopted in waters with a high current, allowing the thalli to grow in open water (Mantri et al. 2017b).
Globally, a number of commercial seaweed products derived from K. alvarezii biomass are used in agriculture (Table 1) and have a known significant impact on crops. Whilst the un-processed RDS biomass, when added to the soil, can act as a soil conditioner due to its water binding nature, its various liquid and κ-Cg extracts are effective as biostimulants and primers of plant biotic responses. In particular, κ-Cg and its oligo-saccharides are known to improve the growth of treated plants by modulating physiological and biochemical processes involved in stress tolerance and nutrient-use-efficiency (Shukla et al. 2016; Deolu-Ajayi et al. 2022).
Kappaphycus alvarezii biostimulants: Extraction methods and formulations
There are several methods available to extract Kappaphycus biomass, including simple liquefaction by crushing it while still wet, hydrolysing it with acid or alkali, or using hot and/or cold water-based extraction methods. These individual or combined extraction methods are utilized to produce different types of biostimulatory products.
Strained Seaweed Extract (SSE)
A process for the production of κ-Cg (a hydrocolloid) along with liquid biostimulant from fresh K. alvarezii biomass was described by Eswaran et al. (2005), henceforth referred to as SSE. The process requires homogenization of fresh thalli and filtering them through a muslin cloth. The liquid has been beneficially applied at various dilutions to different crops the remnant fibrous material is dried and used for carrageenan extraction.
Boiled Seaweed Extract (BSE)
BSE of K. alvarezii was produced by boiling fresh seaweed in water (1:100 w/v) for 15 min at 100 °C, filtering, and cooling the resulting filtrate at room temperature (Banu et al. 2020).
Lyophilized Seaweed Extract (LSE)
Fresh seaweed was lyophilized, powdered, and mixed in deionized water at a ratio of 1 g per 10 mL. The resulting suspension was centrifuged, and the supernatant was lyophilized and powdered again (de Araújo Amatuzzi et al. 2020). The resulting extract is referred to as LSE in this article and has been used at various dilution levels.
Strained Seaweed Extract Acid Hydrolysate (SSEAH)
In a patent (Nori et al. 2019), the SSE obtained as described previously was mixed with concentrated acid hydrolysate of the pulp, which contained soluble oligo-sulfated galactans, resulting in a mixed extract known as strained seaweed extract acid hydrolysate (SSEAH). AgroGain® is a formulation made using SSEAH, along with suitable carriers, diluents, and excipients that improve plant growth and stress tolerance (Nori et al. 2019; Sahana et al. 2022).
Girish et al. (2020) reported a method to prepare a Kappaphycus-based biostimulant rich in sulfated galactose and de-polymerized polysaccharides using acid hydrolysis. The low molecular weight fractions from SSEAH has been reported to induce natural immunity against different pathogens in plants (Banakar et al. 2022; Roy et al. 2022). Different biostimulant formulations (i.e., LBD1, LBD3, and LBD12) have been prepared using SSEAH. The products LBD3 (Tomatough®) and LBD12 (AgFort®) contain molecular weight fractions of sulfated galacto-oligosaccharides that are less than 5 kDa and less than 1 kDa, respectively (Roy et al. 2022). SSEAH-based formulations have been commercialized by Sea6 Energy Private Limited (Bangalore, India).
Minimally Processed Homogenate (MPH)
An extract of dry K. alvarezii (RDS) was prepared by homogenizing it with water in a ratio of 1:6 (w/v) for 30 min. The resulting slurry was filtered through a 200 mesh sieve and the filtrate was dried to a water-soluble powder using a triple-effect evaporator, yielding the extract in powdered form and henceforth called MPH (Vaghela et al. 2023).
Composite Seaweed Extract (CSE)
Shinde and Madathil (2018) from Heliae Development LLC (Arizona, USA) reported the production of bioactive formulations by lysing seaweed thalli. They subjected the harvested Kappaphycus thalli to a solvent-based extraction process (utilizing alkali such as NaOH or KOH, acid, and ethanol) at an elevated temperature (i.e., 90–95 °C). The extracts obtained were combined and concentrated and henceforth reported as CSE and formulated as a biostimulant.
Kappaphycus alvarezii SSE has been widely studied and reported. It is utilized in a commercial formulation, as a blend of red seaweed K. alvarezii and brown seaweed, by M/s AquAgri Processing Private Limited (Manamadurai, India) and marketed under the brand name "Sagarika" in high volumes by the Indian Farmers Fertilizer Cooperative Limited (IFFCO), New Delhi, India (Annual report 2021). Kappaphycus alvarezii is a rich source of κ-Cg, which is also a biostimulant. It can be extracted through a hot alkali extraction method (Eswaran et al. 2005).
Components of Kappaphycus alvarezii and their activities
Until approximately 15 years ago (i.e., 2005), there was only one need for estimating the chemical composition of K. alvarezii, which was its primary use as a source of κ-Cg (Reddy et al. 2003). However, applications of the cultivated biomass emerged for the purpose of manufacturing various types of biostimulatory extracts for agriculture. Even though K. alvarezii is a tropical seaweed, the chemical composition of the biomass is known to vary widely based on the geographic location of the cultivation sites and even seasonally, at the same site of cultivation (Kumar et al. 2015; Araújo et al 2022) (Table 2). Seawater temperature, salinity and nitrate concentration are some of the major environmental and physical factors that significantly influence the chemical composition of this type of seaweed (Kumar et al. 2015).
The macro- micronutrients and proximate composition of whole, dried K. alvarezii cultivated at selected Indian and Malaysian sites (Table 2) varied by 9.8–19.3% between the study sites. Similarly, the lipid and ash contents varied between 0.6–2.1 and 27–38.9%, respectively. Carbohydrate and fibre contents were reported at approximately 25.9 and 14.5% (Kumar et al. 2015; Yong et al. 2015). A high ash content indicated the efficiency of K. alvarezii in absorbing various elements from surrounding seawater, e.g., potassium (Yong et al. 2015). Kappaphycus alvarezii is rich in macroelements, having high sulfur (11.24%), sodium (2.23%) and potassium (4.10%). Among microelements, iron was reported to have a maximum level of up to 659 ppm (Kumar et al. 2015).
Kappaphycus alvarezii has also been found to be rich in fatty acids. The powder of whole, dried K. alvarezii was reported to have a 2.1% lipid content, of which 59.3% was saturated, 13.8% was monounsaturated and 17.6% was polyunsaturated fatty acids (Yong et al. 2015). Palmitic acid (36.4%), palmitelaidic acid (8.6%), and eicosapentaenoic acid (10.3%) are the major fatty acids reported among saturated, monounsaturated and polyunsaturated fatty acids (Yong et al. 2015).
Other constituents, such as glycine betaine and choline chloride, have been reported in the SSE of K. alvarezii at 78.5 and 60.7 ppm, respectively, and have been shown to have beneficial roles in crop production (Mondal et al. 2015). Rathore et al. (2009) also reported the chemical composition of K. alvarezii SSE (Table 2). The alga was reported to possess a higher affinity for potassium over sodium absorption (Mondal et al. 2013), which explains the relatively high levels of potassium in virtually all of its extracts. Additionally, high-performance liquid chromatography (HPLC) and tandem mass spectrometry (MS–MS) revealed the presence of algal phytohormones such as indole-3-acetic acid (IAA), gibberellic acid 3 (GA3), and zeatin in the SSE, with concentrations of 21.1, 25.7, and 18.6 ppm, respectively (Mondal et al. 2015).
Vaghela et al. (2022) found that the lyophilized SSE of K. alvarezii contained 0.4% calcium and 0.2% magnesium, as well as significant amounts of Fe, Cu, Mn, Mo, and Zn (i.e., 37.4, 10.6, 3.9, 2.1, and 12.4 mg kg−1, respectively). On a dry weight basis, the lyophilized powder of SSE was reported to have 22.4% and 1.7% potassium and sodium, respectively (Vaghela et al. 2022). Recently, several bioactive compounds were identified in the lyophilized SSE of K. alvarezii that have significant, positive impacts on plants (Vaghela et al. 2022). These compounds include sulfabenzamide, kinetin, 1-phosphatidyl-1D-myo-inositol, C-16 sphinganine, and dodecanamide. More recently, several biologically active compounds, such as catechin hydrate, naringenin, cinnamic acid, cysteine, proline, methionine, phenylalanine, lysine, glutamic acid, glycine, leucine, putrescine and IAA, were identified in the MPH of K. alvarezii (Vaghela et al. 2023). Table 3 summarizes the specific beneficial bioactivities of these compounds when individually applied exogenously. Additionally, κ-Cg of K. alvarezii stands out as a particularly noteworthy ingredient that has been extensively studied, and its bioactive properties are well-documented (Shukla et al. 2016). A positive response of maize was found by application of kappa-oligocarrageenan with molecular weights of 42, 17 and 4 kDa that were derived from K. alvarezii (San et al. 2020).
Beneficial effects of Kappaphycus alvarezii extracts/formulations on plants and soil
Effects on seed germination and vigour
Babu and Rengasamy (2012) studied the effects of SSE on seed germination potential. Chilli, rice, and peanut seeds in a 1–2% extract, for 6 or 24 h, resulted in significantly higher radicle and plumule lengths and increased fresh weight of the treated seedlings. Similarly, the highest germination percentage of chilli seeds was achieved by priming for 72 h in a 1:25 SSE-water solution. Additionally, primed seeds stored for 12 months at room temperature in a sealed plastic bag, under dark conditions, exhibited lower electrolyte leakage and higher levels of total phenol, 2,2-diphenyl-1-picryl-hydrazyl-hydrate (DPPH), and 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid (ABTS) activity, compared to non-primed seeds. The same extract, used at the same concentration, also induced early flowering and increased the number of chilli fruits per plant in comparison to the control (Dutta et al. 2019). Maize seeds soaked in 0.3, 0.5, and 0.7% solutions of SSE for one hour exhibited a higher germination potential, germination energy, and seed vigour than the control (Shanmugam and Seth 2018). The application of SSE to rice seed germination was also found to be very effective and resulted in an approximately 20% increase in overall germination. A 0.03% solution of a spray-dried powder of SSE was also effective for improved germination in pigeon pea (Karthikeyan and Shanmugam 2016a). The effect of SSEAH extracts, prepared by mixing SSE and acid hydrolysate of the carrageenan containing leftover biomass in a ratio of 25:75 or 75:25, was evaluated on the germination and growth of soybean seedlings at various concentrations.
Soybean seed priming with SSEAH improved the aerial shoot length by up to 28% and primary root length by up to 19%, as compared to the negative control (da Costa et al. 2017). Similarly, orchid seed germination was shown to be significantly improved by LSE, with treated seedlings displaying increased rooting, shoot development, and taller plantlet growth (de Araújo Amatuzzi et al. 2020) (Table 4). These findings clearly demonstrated that the bioactive compounds present in K. alvarezii stimulated seed germination and thus positively influenced plant growth and development.
Effects on plant growth, yield, and produce quality
In 335 multi-locational and multicrop trials, the use of SSE, along with recommended fertilizer rates, resulted in an average significant yield increase in cereals (13–23.5%), pulses (14–36.9%), sugarcane (13–16.7%), potato (14–16.9%), and oilseeds (19–26.8%) when compared to the control of normal, recommended fertilizer rates (Mantri et al. 2022). The effects of K. alvarezii extracts on several crops, including vegetables, cereals, pulses, legumes, oil crops, flowers, fruits, and perennial grasses, are compiled in Table 4, indicating the potential benefits of these extracts at different concentrations and through various application methods.
SSE, applied at concentrations ranging from 0.5—15% of applied solution prepared in water by drench or foliar spray to different crops, significantly increased yields by 13—61% and promoted growth by enhancing height, dry matter accumulation, nutrient uptake, fruit or grain quality parameters, and root attributes (Babu and Rengasamy 2012; Singh et al. 2015b; Dwivedi et al. 2016; Deb and Singh 2022; Layek et al. 2023). SSE improved crop quality by augmenting biochemical parameters such as carbohydrate, protein, and lipid content in grains and leaves, lycopene content in fruits such as tomatoes, and oil content in groundnut (Babu and Rengasamy 2012; Karthikeyan and Shanmugam 2015; Layek et al. 2018; Pramanick et al. 2020; Chaudhari et al. 2023). In legumes, SSE was shown to increase the number of root nodules (Raverkar et al. 2016). Furthermore, it regulated genes associated with stress, defense, phytohormones, nitrogen metabolism, signal transduction, photosynthesis, ion transport, antioxidant pathways, and polysaccharide metabolism in plants such as tomato, wheat, and maize (Agarwal et al. 2016; Patel et al. 2018; Kumar et al. 2020; Trivedi et al. 2021). Additionally, a 7.5% SSE was found to reduce the required chemical fertilizer dose by 25% (Pramanick et al. 2017). SSE also contributed to a positive nitrogen balance when applied in cropping systems (Pramanick et al. 2020). Additionally, the foliar application of a 0.2% solution of AquAsap powder, which is commercially available and prepared by using SSE, resulted in a significant improvement in the total soluble solid, moisture content, ash content, and pyruvic acid, as well as the yield of onion bulbs (Karthikeyan and Shanmugam 2016b).
The performance of SSE is deemed to rely on the presence of nutrients and plant growth regulators (19.65–26.52 ppm) (Layek et al. 2015). In potato, these compounds were hypothesized to facilitate the translocation of greater amounts of photosynthates and nutrients into the tubers, leading to an increase in both the number and size of tubers (Pramanick et al. 2017). SSE also helped rice plants to take up more nutrients (Pramanick et al. 2014a) resulting in higher growth and yield. Zeatin (19.6 ppm) was found to reduce leaf drop in soybean (Lodhi et al. 2015).
For a better understanding of the mechanisms of action of SSE, diethyl ether and ethyl acetate were used to selectively eliminate IAA and GA3 from the original SSE. The selective elimination of GA3 from the SSE resulted in a higher photosynthetic rate and yield and increased CO2 uptake in treated plants, as compared to those treated with basally applied SSE (Mondal et al. 2015; Layek et al. 2023). These results were hypothesized to be due to the prevention of negative interactions between GA3 and cytokinins in this particular study. It was also reported that choline chloride and glycine betaine present in SSE were positively correlated with yield (Mondal et al. 2015). The findings suggested that each component of the extract played specific roles, which may interact either synergistically or antagonistically. The ratio of these components was the critical factor influencing their effectiveness in improving plant growth and productivity, as well as providing tolerance to various stresses.
For plantation crops such as banana, three applications of a 5% solution of the commercial form of SSE 'AquAsap' resulted in a higher yield (i.e., up to 56.6% over the control) as well as increased nutritional content (Karthikeyan and Shanmugam 2014). Sugarcane plants treated with a 1% SSE of that proprietary extract had a higher sugar brix, purity and polarity (Karthikeyan and Shanmugam 2017). In sugarcane, SSE (5%) applied three times as a foliar spray increased productivity by 12.5% and reduced chemical fertilizer use. A life-cycle impact assessment indicated a positive sustainability impact, with 5% SSE having the highest reduction in greenhouse gas emissions (260 kg CO2 equivalent ha−1) (Singh et al. 2018). Sharma et al. (2017) have reported a 11.4% reduction in climate change impact category while using SSE at 15% in rice. Further they also showed that at least 35 kg CO2 equivalents per tonne of rice could be saved while using SSE with 50% recommended rate of fertilizers.
A bio-formulation (i.e. LBS6) prepared using SSEAH of K. alvarezii was found to increase the chlorophyll content of rice leaves when treated three times at a concentration of 1 mL L−1 (Banakar and Kumar 2020). The bioactive compounds present in LBS6 induced the expansion of cucumber cotyledons by regulating the expression of the genes involved in cell division, expansion and proliferation and phytohormone metabolism (Shukla et al. 2023). Additionally, LBS6-treated cotyledons differentially modulated carbohydrate metabolism to provide energy to expanding cotyledons (Shukla et al. 2023). The same study showed that the foliar spray of LBS6 regulated photosynthesis and improved plant growth with higher foliage growth (Shukla et al. 2023). Similarly, de Castro et al. (2023) showed that the organic fragments of κ-Cg, lipids and peptides present in an aqueous extract of K. alvarezii, enriched with a potassium-rich inorganic fraction from K. alvarezii, improved the growth and nutrient-uptake-efficiency of rice. Furthermore, the application of 0.8% MPH on tomato plants was found to increase the yield by 31% under normal conditions and by 19% under drought conditions, in comparison to the control groups. The applied solution of 0.8% contained several physiologically relevant bioactive compounds as detailed in the section "Components of Kappaphycus alvarezii and their activities" (Vaghela et al. 2023). In another experiment, coating tomato fruits with 1, 2, and 3% concentrations of BSE was found to exhibit anti-bacterial and anti-fungal properties, ultimately resulting in enhanced quality and prolonged shelf-life of tomato fruits by up to 28 days (Banu et al. 2020).
Soaking greengram seeds in a 0.1% solution in water for 30 min, followed by two foliar sprays on the crop at 25 and 35 days after sowing, using a 0.25% solution containing a mixture of K. alvarezii (red alga), Sargassum sp. (brown alga), and select, microbial bio-fertilizers (e.g., Rhizobium, Azotobacter, Acetobacter, phosphorus-solubilizing bacteria, and potassium-mobilizing bacteria) resulted in improved plant and root growth, increased leaf chlorophyll content, higher grain yield, and enhanced nutrient levels in the grains (Iswarya et al. 2019).
Stress resilience
Given the variability in climate conditions, seaweed biostimulants enable and prime crops to endure and even thrive under unfavorable environmental circumstances. In general, seaweed extracts help plants achieve this through various strategies, such as improving nutrient-uptake-efficiency (NUE), enhancing root growth, and activating stress-responsive genes. Several studies reported on the ability of K. alvarezii-based extracts to provide tolerance to plants against both abiotic and biotic stressors and improve the growth, yield, and nutritional quality of various crops. For instance, 10% and 15% SSE increased drought stress tolerance in maize, when applied three times (i.e., at 25, 59, and 78 days after sowing) by elevating antioxidant enzyme activity, such as catalase, ascorbate peroxidase, glutathione reductase, and superoxide dismutase, and reducing malondialdehyde (MDA) and reactive oxidant species levels. These concentrations of SSE also purportedly protected cell organelles, chlorophyll, and macromolecules during stress conditions (Trivedi et al. 2018a). Alleviation of moderate soil moisture stress in maize was achieved with 10% SSE, while a higher concentration (15%) was required for an alleviatory response to severe stress at the V5 or V15 stages (Trivedi et al. 2018a). These studies contributed significantly to a better understanding of all extracts of seaweed, highlighting the importance of a dose dependent, stress alleviation responses in plants generally.
In another study, foliar application of 10% SSE, carried out only once, at the grain filling stage of maize increased growth and yield under normally irrigated conditions, but not under drought stress conditions. Here, the authors proposed that the quaternary ammonium compounds and other bioactive compounds present in the SSE might have assisted the plants in tolerating soil moisture stress during brief dry spells (Trivedi et al. 2018b). Similarly, maize yield was enhanced up to 31.5% under drought-stressed conditions and up to 20.4% under well-watered conditions through drench application of 2.5% SSE (Kumar et al. 2020).
Plants experience negative effects on their chlorophyll and carotenoid contents due to drought and salinity stress. Applying 7.5% SSE to 25-day-old wheat seedlings significantly increased photosynthetic pigment concentrations, providing relief from both drought and salt stress (Patel et al. 2018). Kappaphycus extract-treated wheat plants were found to have the highest internal levels of the plant hormones cytokinin and ABA, known to be involved in protecting photosynthetic pigments during stressful conditions (Rivero et al. 2009). Patel et al. (2018) reported that after applying 7.5% SSE, reactive oxygen species (ROS) levels were reduced, along with lower lipid peroxidation and electrolyte leakage. Salinity stress impairs the Na+/K+ ratio in leaves (Shukla et al. 2015), which hampers transpiration due to stomatal guard cell effects and negatively affects ion transporter activity (Patel et al. 2018). SSE helped maintain a balanced Na+/K+ ratio and a higher Ca++ ion content, which together provided an improved osmotic balance to treated plants under abiotic stress conditions. It also maintained the turgor pressure of cells in treated plants, reducing extreme water loss under stressful conditions and reducing damage to various cell membranes. Applying the extract on wheat triggered the levels of many other osmo-protectants, suggesting its role in osmotic balance and stress tolerance. Upon application of the extract to wheat plants, stress-responsive genes such as WCK-1 and the wheat-specific mitogen-activated protein (MAP) kinase gene were upregulated. WCK-1 was reported to increase up to 1.2 – 1.4-fold higher in salt- and drought-stressed wheat plants when treated with SSE. These MAP kinase cascade genes play significant roles in the regulation of cellular processes under normal and abiotic stress conditions (Patel et al. 2018).
Role in plant defence against biotic stress
κ-Cg can prime and elicit plant defence mechanisms (Vera et al. 2011; Shukla et al. 2016; Paulert and Stadnik 2019). Specifically, κ-Cg has been found to increase the activity of phenylalanine ammonia-lyase, leading to the production of antimicrobial phenylpropanoid compounds that can protect tobacco plants against various pathogens such as tobacco mosaic virus (TMV), Botrytis cinerea, and Pectobacterium carotovorum (Vera et al. 2012). Additionally, carrageenans and oligo-carrageenans, which contain κ-Cg, have been shown to modulate the salicylate, jasmonate, and ethylene signalling pathways, eliciting plant defence responses against a range of pathogens, including viruses, bacteria, viroids, fungi, and insects (Shukla et al. 2016). A 5% SSE was found to regulate plant hormones and defence-related genes in tomato plants related to alleviating biotic stress due to infection by the fungus Macrophomina phaseolina, a causative agent of charcoal rot disease (Agarwal et al. 2016). Thus, Kappaphycus-based, carrageenan-containing biostimulants can support the induction of systemic resistance in plants against different pathogens. They increase the endogenous levels of abscisic, indole acetic and salicylic acids (ABA, IAA and salicylic acid (SA), respectively) and zeatin. Up-regulation of some defense-related genes, such as PR-1b1, PR-3, and PR-5, and the transcription factor Pti4 to alleviate biotic stress caused by M. phaseolina was also demonstrated. Elevated endogenous phytohormone levels in plants were hypothesized to be due to their presence either in extracts or due to increased endogenous biosynthesis in treated plants (Agarwal et al. 2016). It was demonstrated that the Pti4 transcription factor participated in the enhancement of LeMPK2, one of the components of MAP kinase cascade proteins, responsible for Pto-mediated resistance in tomato plants and provided mitigation towards applied biotic stress (Pedley and Martin 2004; Agarwal et al. 2016). Similarly, Sahana et al. (2022) showed that a formulation (i.e., LBD1) rich in fractions of bioactive sulfated galacto-oligosaccharides (SSEAH), elicited immunity of rice against Magnaporthe oryzae by regulating the expression of defence-related genes and enzymes. LBD1 induced immunity in rice by up-regulating the transcription of defense-related genes (Banakar et al. 2023). Interestingly, LBD1 showed up-regulation of beta-D-xylosidase, a gene involved in secondary cell wall formation (Banakar et al. 2023). Roy et al. (2022) deciphered the mode of action of Tomatough® (LBD3) and AgFort® (LBD12), a commercial formulation of Sea6 Energy Private Limited as prepared using SSEAH (Girish et al. 2020), which elicited a systemic immune response in Arabidopsis thaliana and Oryza sativa against Pseudomonas syringae pv. tomato (PstDC3000) and Xanthomonas oryzae pv. oryzae, respectively. Tomatough® and AgFort®-treated plants showed a higher abundance of transcripts of disease-related genes and higher accumulation of SA. The expression of FLG22-induced receptor-like kinase 1 (FRK1) and PR1a genes involved in SA-mediated signalling pathways was significantly up-regulated in the treated plants. In addition, SA, ABA, IAA, and trans-zeatin levels were higher in Tomatough®- and AgFort®-treated plants, suggesting induced response cross-talk between different phytohormone signalling pathways to induce innate immunity in plants (Roy et al. 2022). The K. alvarezii-derived commercial formulation Biostimul® enriched with amino acids improved the chlorophyll content and stimulated defense against powdery mildew in lettuce (Rover et al. 2022).
Effects on root physiology and soil properties
Various seaweed extracts can have significant impacts on belowground microbial ecosystems due to their ability to improve root growth and stimulate beneficial microbiome activity, which in turn secrete beneficial secondary compounds. This, in turn, can improve nutrient cycling and overall soil health, leading to higher crop productivity. SSE has been reported to stimulate root growth when applied as a soil drench in maize plants (Kumar et al. 2020). A soil application of 2.5% SSE, at the V5 stage of maize, caused up-regulation of genes involved in root growth, GA3 and IAA signalling, seed development, nitrogen metabolism, and antioxidant activity. The nitrogen, phosphorus and magnesium contents in SSE-treated roots of maize were improved by the extract applied under field capacity, as well as drought-stressed conditions (Kumar et al. 2020). Higher root length and volume were reported in treated maize under drought stress, which ensured better nutrient uptake and transport. Uptake of nitrogen, phosphorus, copper and iron, by the treated roots, was enhanced due to the application. Better nitrate reductase, a rate-limiting enzyme for protein metabolism, was reported in the roots of treated maize and was found to be responsible for more efficient nitrogen assimilation. It is important to note that the SSE, when applied at the effective dose, does not contain enough nutrients to meet the crop's demands. Therefore, the best results are obtained when the soil already contains sufficient amounts of macro- and micronutrients or has sufficient fertilizers applied. The possibility of reduced nutrient requirements upon application of SSE is due to the higher efficiency of nutrient uptake and assimilation, as evident in the case of nitrogen. Kumar et al. (2020) also reported increased expression of the cysteine synthase gene in SSE-treated roots under drought, which is key to producing reduced and oxidized forms of glutathione, GSH and GSSG, respectively. These antioxidants are required for quenching ROS generated during stress conditions. Key enzymes in plants responsible for fatty acid synthesis were also found to be up-regulated in treated plants. SSE modulated starch metabolism in maize roots by positively regulating the expression of genes involved in biosynthesis and negatively regulating the expression of genes involved in degradation (Kumar et al. 2020). These observations suggest that the application of SSE to plants might have a positive effect on enhancing carbohydrate storage and partitioning, leading to an increase in maize grain yield. Modulations in the genes of treated plants were related to enhanced cell wall synthesis that could lead to protection against osmotic imbalances during water shortage (Kumar et al. 2020). The presence of IAA, at approximately 21.1 ppm in the SSE may have contributed to the promotion of root growth in potato plants, ultimately increasing their nutrient uptake capacity and water-use-efficiency (Pramanick et al. 2017).
Foliar applications of SSE, applied at 10%, not only improved maize productivity under soil moisture stress conditions but also had a favourable influence on the soil bacterial community (Trivedi et al. 2022b). Under soil-moisture stress, imposed at the V5, 10, and 15 stages of maize, there was a decreased abundance (by 49–79%) of the genera Alicyclobacillus, Anaerolinea, Bacillus, Balneimonas, Nitrospira, Rubrobacter, and Steroidobacter compared to the irrigated control. However, the application of SSE improved the abundance of these soil bacteria. Several bacterial genera, e.g., Flavobacterium, Nitrosomonas, Nitrosovibrio, and Rubrobacter, which are known to be positively related to plant growth promotion and nutrient cycling, were also reported to be enriched by run-off from the extract. The SSE of K. alvarezii also showed favourable effects on the activities of soil enzymes. The application of SSE led to significantly higher activities of alkaline and acid phosphomonoesterases, aryl sulfatase, glucosidase, and fluorescein diacetate (FDA) hydrolysis in comparison to the control (Trivedi et al. 2022b).
Figure 3 summarises the positive effects of the Kappaphycus-derived formulations on plants as well as the current known mechanism behind these effects.
Research gaps and the way forward
The current literature review on a variety of Kappaphycus alvarezii extracts has highlighted their potential to significantly enhance crop productivity, quality, and soil properties, both under conditions for optimal growth and abiotic or biotic stresses. Many of the reviewed studies are supported by positive findings on the active ingredients and underlying mechanisms that contribute to these beneficial effects on crop productivity. Despite this, there are key research gaps that require further investigation to fully understand and optimize the use of K. alvarezii extracts in agriculture.
It is important to note that significant variations in the application timings, dosages, and frequencies of K. alvarezii extracts have been reported. There is a need for standardization of treatments across experiments, or else a justification for why such non-standard treatments were applied. Since reports suggest that this group of red seaweed extracts can alleviate biotic stress, a systematic comparison with commercial pesticides is lacking and should be pursued with vigour, since the needs in agriculture are great.
One common feature of contention is that few of these studies have reported the levels of soluble solids in their extracts, which makes it difficult, if not impossible to compare results across different formulations (liquid to powder). Sometimes the citation of a percent solution really does not mean anything, as the percentage is dependent on the processing, which is itself a major variable. This factor may primarily explain the variations in responses observed across the studies. To account for such variations, it is advisable to present the outcomes of diverse extracts on a dry weight, soluble solids basis. As extraction techniques vary, the constituents within the K. alvarezii extracts also differ and that may be a considerable variation that needs to be standardised. This criticism could be applied to virtually all types of extracts of all types of seaweeds. Identification of the active constituents within the extracts and their specific roles in plant metabolism should be investigated to ascertain the application doses at which they are physiologically relevant. One has to acknowledge that it is not a simple relationship to presence and concentration but with some compounds, the plants respond to various ratios of constituents. It is equally important to identify whether the active constituents produce the same effect when present in a mixture. This aspect should be carefully examined to determine if the presence of other components in the mixture influence the overall effects of the active constituent. By investigating this, we can gain a deeper understanding of how the interaction between extracts of seaweeds may affect the desired outcome or efficacy within the targeted plants they are applied to.
Information is also completely lacking on the proportion of the applied active ingredients that are absorbed by the plants and the mechanism of their uptake through foliage or roots. The interaction of seaweed extracts/formulations with the soil and leaf microbiome is yet another, largely unexplored area that is important because it can influence the production of secondary metabolites by microbes, which may affect plant growth and health. Similarly, the composition of K. alvarezii extracts, even though of tropical origin, are highly likely to vary over season and location; thus, it would be necessary to understand how crops respond to these variations. Such a study would also be important to generate data towards standardization of specifications of Kappaphycus-based biostimulants, which is currently an area of limited understanding.
Overall, this review shows that Kappaphycus extracts play a role in improving plant resilience to stress and therefore could be considered as an adaptive strategy for crops to environmental variability under climate change scenarios.
Conclusions
In conclusion, Kappaphycus alvarezii, a red macroalga known principally for its hydrocolloid content, is increasingly being used in the agriculture sector for its biostimulatory effects on crops. Various K. alvarezii-based well-characterized commercial products are available on the market, globally and their chemical composition and modes of application have been extensively studied. The bioactive compounds in K. alvarezii extracts have been shown to positively influence plant growth and development, including seed germination, nutrient uptake, dry matter accumulation, photosynthetic efficiency, and modulation of gene expression. This collective of seaweed-derived compounds can also impart tolerance against biotic and abiotic stresses. Additionally, the use of these sustainably produced red seaweed-based products can help increase soil health and reduce the need for chemical fertilizers, leading to better yields and higher quality crops. All the literature reviewed shows no negative effects of Kappaphycus-extracts on the yield or growth of crops, thus allaying any such concerns. However, further studies are needed to fully characterize these extracts and optimize their efficacy, including the identification of individual active compounds, the comparison of extraction methods, and the standardization of application rates and timings. Extracts of K. alvarezii have the potential to contribute to sustainable and economically viable agriculture, which is increasingly under considerable pressure to perform for the benefits of society.
Data availability
Data/material can be available from the corresponding author on reasonable request.
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Acknowledgements
The authors thank all the workers working in this domain, whose work forms the basis of this review. More particularly, the three anonymous reviewers are acknowledged who, through their constructive suggestions, improved the manuscript significantly. This manuscript possesses CSIR-CSMCRI communication no. 191/2022.
Funding
The Council of Scientific and Industrial Research (CSIR), New Delhi, India, greatly acknowledges providing funding under the projects MLP-0016, MLP 0049(1) and HCP 0024.
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Arup Ghosh: Conceptualization, review and editing. K G Vijay Anand: Resource validation, review and editing. Pradipkumar Vaghela: Data curation and formal analysis. Alan T Critchley: Conceptualization, review and editing. Pushp Sheel Shukla: Review and editing. Khanjan Trivedi: Conceptualization, Literature collection, and writing original draft. All the authors have read and approved the final manuscript.
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Trivedi, K., Anand, K.G.V., Vaghela, P. et al. A review of the current status of Kappaphycus alvarezii-based biostimulants in sustainable agriculture. J Appl Phycol 35, 3087–3111 (2023). https://doi.org/10.1007/s10811-023-03054-4
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DOI: https://doi.org/10.1007/s10811-023-03054-4