Improvement for Sustainable Agriculture Technology

Accepted Manuscript Review Article Role of Marine Macroalgae in Plant Protection & Improvement for Sustainable Agriculture Technology Seham M. Hamed, Amal A. Abdelrhman, Neveen Abdel-Raouf, Ibraheem B.M. Ibraheem PII: DOI: Reference:

S2314-8535(17)30129-4 http://dx.doi.org/10.1016/j.bjbas.2017.08.002 BJBAS 227

To appear in:

Beni-Suef University Journal of Basic and Applied Sciences

Received Date: Revised Date: Accepted Date:

24 March 2017 28 July 2017 12 August 2017

Please cite this article as: S.M. Hamed, A.A. Abdelrhman, N. Abdel-Raouf, I.B.M. Ibraheem, Role of Marine Macroalgae in Plant Protection & Improvement for Sustainable Agriculture Technology, Beni-Suef University Journal of Basic and Applied Sciences (2017), doi: http://dx.doi.org/10.1016/j.bjbas.2017.08.002

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Full title: Role of Marine Macroalgae in Plant Protection & Improvement for Sustainable Agriculture Technology Short title: Marine Macroalgae in Agriculture Management Seham M. Hamed1*, Amal A. Abd elrhman1, Neveen Abdel-Raouf2, Ibraheem B.M. Ibraheem2 1

Soil Microbiology Department, Soils, Water and Environment Institute, Agricultural Research

Center, Giza, Egypt. 2

Botany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef,

Egypt. Seham M. Hamed: 1 Soil Microbiology Department, Soils, Water and Environment Research Institute, Agricultural Research Centre, 12112, Giza, Egypt. Tel.: 002 01019292562 Fax.: (002)35720608 E-mail address: [email protected]

Acknowledgments The authors wish to thank Soils, Water and Environment Research Institute (SWERI), Agriculture Research Center, Giza, Egypt for facilities provided to conduct this research work.

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Full title: Role of Marine Macroalgae in Plant Protection & Improvement for Sustainable Agriculture Technology Short title: Marine Macroalgae in Agriculture Management Abstract Marine macroalgae are plant-like organisms with simple internal structures that generally live in coastal areas. They mainly include different communities of red, brown and green macroalgae. Marine macroalgae commonly occupy intertidal and sublittoral-to-littoral zones on rocks and other hard substrata. They are considered to be an excellent natural biosource in different aspects of agricultural fields. They have great proficiency in improving soil physical and chemical properties. Marine macroalgae are also characterized by producing a large array of biologically active biocidal substances against plant-infecting pathogens. Unfortunately, most available literatures on marine macroalgae and their derivatives mainly focused on their pharmaceutical applications but their potential utilization in sustainable agriculture development is still often regarded as a secondary goal. However, a relatively considerable dataset on marine macroalgae showed that they could play a major role in plant protection and improvement. This review summarizes different aspects of potential macroalgal applications in agriculture. Commercial production and exploitation of specific compounds with interesting biotechnological importance from marine macroalgae including microbicides, nematicides, insecticides, biofertilizers, biostimulators and soil conditioners are highlighted and discussed in detail. Bioactive compounds like fatty acids (in particular polyunsaturated fatty acids (PUFAs), proteins (amino

acids),

bioflavonoids,

sulfated

polysaccharides,

carotenoids,

polyphenols and

carbohydrates are considered to have bactericidal, antiviral and fungicidal effects against some 2

plant-infecting pathogens. These biocontrol agents provide multiple benefits and act as useful pointers for improving cultivation practices in diverse habitats. Marine macroalgae can be generally considered as promising multifunctional bioinoculants and ecofriendly environmental tools in recent trends of organic farming.

Keywords; Marine macroalgae; bioactive compounds; biocontrols; biopesticides; biostimulants; sustainable agriculture.

2. Introduction Management of plant diseases is considered nowadays an important prerequisite for sustainable agricultural development. Although synthetic chemicals are well known to have a fundamental role in suppressing of plant diseases and maintaining high crop yields they have harmful effect on human and environment integrity. The world trade of pesticides in 2005 had been amounted to more than $ 31 billion, of which about 25 % was for insecticides, 48 % for herbicides, 24 % was for fungicides and bactericides, and others as 3 % (Zhang et al., 2011). The persistence of chemical pesticides in top soils, and leaching into groundwater besides their undesired effects on non-target organisms, is of a major environmental concern. On the other hand, natural products are considered to be less harmful to the environment due to their higher biodegradability and influential biocidal activities at lower doses (Saxena and Pandey, 2001). These natural compounds provide novel structures and mechanisms of action for the discovery of more safer microbicidal/pesticides, as well they also may help in development of organic agricultural products integrated with pest management. Man has already exploited the oceans from a long time as a useful resource for producing economically important materials. During the

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last 45 years, several bioactive secondary metabolites have been isolated and characterized from various marine organisms (Elsayed et al., 2012). Macroalgae are commonly found in marine habitats including seas and oceans and known as seaweeds, while a few species could grow and proliferate in other freshwater ecosystems (Ibraheem et al., 2014). Macroalgae are classified into three classes: green algae (Chlorophyta), brown algae (Phaeophyta) and red algae (Rhodophyta). The characteristic green colour of green algae is due to the presence of chlorophyll a and b as in higher plants. The brown pigmentation of phaeophytes is attributed to the dominance of xanthophylls and fucoxanthin pigments which mask other pigments. Phycoerythrin constitutes the major pigment in rhodophytes (red algae) and is mainly responsible for giving the red colour (Abad et al., 2011). Marine macroalgae are considered as excellent source of bioactive compounds that has a broad range of biological activities including antibacterial (Bouhlal et al., 2010; Singh et al., 2010), antifungal (de Felício et al., 2010), and antiviral properties (Bouhlal et al., 2010; Bouhlal et al., 2011). Marine macroalgae extracts also have been used in agricultural trends as soil conditioners to enhance crop productivity (Newton, 1951; Booth, 1969; Abdel-Raouf et al., 2012). Macroalgal-extracted polysaccharides also have been confirmed to be used as perfect metal ion chelators. Furthermore, it has been reported that these polysaccharides are rich in functional groups having the ability to bind to some micro elements of important plant nutritional value (Kaplan et al., 1987). They are also well known as plant stimulators. They have been applied as foliar spray, enhanced plant growth at freezing, drought and salt habitats, showed a noticeable strong resistance to fungi, bacteria and virus and also improved the yield and productivity of several crops (Eris et al., 1995; Norrie and Keathley, 2006; Gajc-Wolska et al., 2013; Sharma et al., 2014). For example, the brown macroalga Ascophyllum nodosum (Linnaeus)

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Le Jolis has been widely investigated and traditionally used as a soil biofertilizer and conditioning agent, animal feed supplement and also as a human nutritional supplement (Fan et al., 2011). In addition, methanolic extract of A. nodosum and to a lesser extent Laminaria digitata, L. hyperborea, and Fucus serratus have been applied for a large-scaled production of biofertilizers due to their high content of betaines, an organic osmolytic compounds that can potentially play a crucial role in effective protection against salts, drought, and extreme temperature stress (Blunden et al., 2010). At the present, one of the main tasks of scientists is to improve the plant productivity using natural alternatives which should be safe and maintain the environment integrity (Nagy and Pintér, 2014). The potential utilizations of marine macroalgae in agriculture is often addressed as a secondary goal and the research in this field is mostly limited to in vitro screening. This review therefore is considered the first of its kind that highlights and summarizes the potentiality of using marine macroalgal biomass and their products in biological controls of some agricultural diseases, integrated pest management, and improving the plant growth for promising sustainable agricultural technology.

3. Utilization of marine macroalgae in the agriculture field 3.1. Biostimulation proficiency on plant growth Marine macroalgae are regarded as valuable resources for plant improvement due to their higher contents of mineral substances, amino acids, vitamins, and plant growth regulators including auxins, cytokinin and gibberellins (Senn, 1987; Stirk and Van Staden, 1997a,b). Brown algal extracts, as well as algae themselves, are widely used in agriculture. They have been shown to increase the productivity of a variety of agricultural plants, including potato, grasses, citrus plants, tomato, beet and legumes. Application of marine macroalgae in plant biotechnology has

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been shown to produce healthy plants, in addition to significant increase the number and weight of fruits. Also, they offer a non-toxic alternative way for disease management (Baloch et al., 2013). It also has been reported that different obtained aqueous algal extracts (e.g. by boiling, autoclaving, or homogenization) showed positive effects on health, growth, and crop yield of many plants. Plant growth regulators mainly differ from fertilizers in several points: (1) they alter and manage the cell division, (2) control of root and shoot elongation, and (3) initiation of flowering and other metabolic functions. While, fertilizers clearly supply nutrients needed for normal plant growth (Allen et al., 2001). For more details, cytokinin is regarded as the most important plant growth regulator in marine algae. Whilst, trace minerals present in marine macroalgal extracts play important roles in plant nutrition and physiology, probably as enzyme activators (Senn, 1987). The exogenous application of the A. nodosum extract on turf and forage grasses increased the antioxidant metabolites in plants such as α-tocopherol, ascorbic acid and β-carotene in tested plants as well as, antioxidant enzyme activities such as superoxide dismutase, GSH reductase and ascorbate peroxidase (Allen et al., 2001). A biostimulant is an organic substance that when applied in small amounts enhances the plant growth and development and such response cannot be achieved by application of traditional plant nutrients (EBIC, 2012). Macroalgal extracts have been utilized as agricultural biostimulants (ABs) (EBIC, 2012). The utilization of macroalgal ABs on crop plants can generate numerous benefits with reported effects including enhanced rooting, higher crop and fruit yields, enhanced photosynthetic activity, and resistance to fungi, bacteria and virus (Sharma et al., 2014). ABs include various formulations of compounds, substances and other products, such as microorganisms, trace elements, enzymes, plant growth regulators (PGRs) and macroalgal

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extracts that are applied to plants or soils to organize and enhance the crop’s physiological processes, therefore making them more efficient. ABs act on the physiology of the plant through diverse pathways to improve crop vigour, yields, quality and post-harvest (EBIC 2012). Macroalgal ABs have been shown to influence respiration, photosynthesis, nucleic acid synthesis and ion uptake (Crouch and Van Staden, 1993; Blunden et al., 1996; Rayorath et al., 2008 a,b; Khan et al., 2009; Craigie, 2011). Consequently, these products can enhance nutrient availability, water-holding capacity, increase antioxidants, enhance metabolism and increase chlorophyll production in plants (Sanderson et al., 1987; Zhang, 1997; Khan et al., 2009).

3.2. Antimicrobial proficiency of marine macroalgae 3.2.1. Antibacterial activity Marine macroalgae produce a wide spectrum of chemically active metabolites including alkaloids, polyketides, cyclic peptides, polysaccharides, phlorotannins, diterpenoids, sterols, quinones, lipids, and glycerols that have a broad range of biological activities against other organisms in their environment (Al-Saif et al., 2014; Abdel-Raouf, et al., 2015). Marine macroalgae have received much attention for their possibility as natural antioxidants, antibacterial and cytotoxic properties (Mayalen et al., 2007; Kayalvizhi et al., 2012; Kosanić et al., 2015; Moubayed et al., 2017). Therefore, it is necessary to test different organic solvents of the algal extracts. This way could provide a potential tool to explore the bioactive compounds responsible for positive effects on plant pathogens and mechanisms of their action (Michalak and Chojnacka, 2015). For example, the methanolic extract of Sargassum wightii, currently identified as S. swartzii C. Agardh, exhibited the highest activity against the phytopathogenic bacterium Pseudomonas syringae which causes leaf spot disease on the valuable medicinal plant Gymnema

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sylvestre (Kumar et al., 2008). Ethyl acetate extract showed less effect. Some other investigated taxa such as Chaetomorpha antennina, Laurencia obtusa , Gracilaria corticata, G. verrucosa (now regarded as Gracilariopsis longissima), Grateloupia lithophila, Padina boergesenii, Turbinaria conoieds, Halimeda tuna, and Ulva lactuca showed less effective bactericidal activity on P. syringae. Nevertheless, the acetonic extracts of the brown macroalga, Sargassum polyceratium (Phaeophyceae) showed also a noticeable treatment against different types of bacteria such as Staphylococcus aureus, Erwinia carotovora (now known as Pectobacterium carotovora), and Escherichia coli using disc diffusion method (Kumar et al., 2008). Meanwhile, the ethanolic extracts of S. polyceratium, Caulerpa racemosa and Gracilaria cervicornis have active effects against Staphylococcus aureus (Borbón et al., 2012). The methanolic extract of S. swartzii has been identified to inhibit the growth of Xanthomonas oryzae pv. oryzae which causes bacterial blight of rice (Arunkumar et al., 2005). Moreover, ethanolic extracts of Cystoseria stricta have been reported to minimize the growth of various bacteria (Pesando et al., 1984). In a greenhouse experiment, spray application of aqueous marine macroalgal extracts from Cystoseira myriophylloides and Fucus spiralis significantly reduced crown gall diseases caused by the bacterial pathogen Agrobacterium tumefaciens in tomato plant (Esserti et al. 2017). It has been showed that the antibacterial properties of marine macroalgae are attributed to different groups of bioactive fatty acids. Contributions of Rosell and Srivastava (1987), Barbosa et al., (2007), Oh et al., (2008), Gerasimenko et al., (2014) and Ibraheem et al., (2017) pointed out that fats and fatty acids extracted from marine algae possess antibacterial activities. Arunkumar et al., (2001) found that predominant fatty acids (palmitic acids) isolated from the green alga Enteromorpha flexuosa, currently accepted taxonomically as Ulva flexuosa, exhibited antibacterial activity against the plant pathogenic bacterium Xanthomonas oryzae pv. oryzae.

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Also, the methanolic extract of Padina gymnospora characterized by a high proportion of plamitic acid showed a high antibacterial activity against the soil-borne pathogenic bacteria Ralstonia solanacearum and P. carotovora (Ibraheem et al., 2017). Active antibacterial extracts from different brown algae have been found to be made up of saturated and unsaturated fatty acids with a predominance of myristic, palmitic, oleic and eicosapentaenoic acids (Bazes et al., 2009; Ibraheem et al., 2017). Therefore, the antibacterial activities could be attributed to the type and amount of these free fatty acids which have a role in the overall defenses against the studied pathogenic Gram-positive and-negative bacteria (Benkendorff et al., 2005). In addition, the phenolic compounds in brown algae have a primary role in the structure of cell walls and are generally considered to be a chemical defender against bacteria (Rao and Parekh, 1981; Le Lann et al., 2008; Plouguerne et al., 2006; Lee and Jeon, 2013). Marine macroalgae-extracted polysaccharides, in particular ulvans from green algae (Chlorophyta), alginates, fucans and laminarin form brown algae (Phaeophyta), and carrageenans and porphyran from red algae (Rhodophyta) and their derived oligosaccharides, have been found to stimulate plant defense responses and protections against a wide spectrum of plant-infecting pathogens (Vera et al., 2011; Kraan, 2012). Furthermore, extracted carotenoids have also some antibacterial activities. It has been assumed that carotenoids could protect plant cells from deleterious oxidative stresses in terms of minimizing damage caused by reactive oxygen species (ROS) through different defense mechanisms (Christaki et al., 2013). The recent contribution of Esserti et al., (2017) highlighted the algal-induced resistance against the crown gall diseases due to their high antioxidants content. In more details, in greenhouse experiment, tomato plants treated with aqueous extracts of the brown algae Cystoseira myriophylloides, Laminaria digitata, and Fucus spiralis showed high

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significant levels of defense enzymes including polyphenol oxidases and peroxidasesas compared to the control (untreated plants).

3.2.2. Antifungal activity Natural algal extracts are nowadays more applicable, instead of synthetic fungicides, for fighting plant-infecting fungi due to their higher safety and relatively negligible impacts on the environmental (Haroun et al., 1995; Brimmer and Boland, 2003; Galal et al., 2011). A considerable number of recent studies showed that the crude and purified algal preparations are able to protect the plants against several pathogenic fungi (Cluzet et al., 2004; Paulert et al., 2009, 2010). For instance, the brown alga L. digitata has been found to induce plant defence mechanism and protect them against several pathogens such as Botrytis cinerea and Plasmopara viticola in grapevine (Aziz et al., 2003). Furthermore, (Baloch et al., 2013) reported that the in vivo utilization of Spatoglossum variabile, Stokeyia indica (currently known as Polycladia indica), and Melanothamnus afaqhusainii have significant suppressive effects against the root rotting fungi Fusarium solani and Macrophomina phaseolina attacking Eggplant (Solanum melongena L.) and watermelon (Citrullus lanatus (Thunb.) Matsum & Nakai). Their study revealed that the application of marine macroalgal powders not only protect the crops from infection by root rotting fungi in naturally infested soil but also they improved the plant growth i.e. vines length of watermelon, shoot lengths of eggplant and fresh shoot weights have been found to be higher in macroalgae-treated plants as compared to the control or the chemical fungicide Topsin-M. Marine macroalgae-treated plants also exhibited earlier fruiting process than control or chemical fungicide-treated plants. Similar findings have also been noticed using different extracts from the brown alga Stoechospormum marginatum (currently accepted

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taxonomically Stoechospermum polypodioides) and the green alga Codium iyengarii to control growth of the root infecting fungi F. solani (Ara et al., 1998). Tuney et al., (2006) also observed positive antifungal activities using varied methanolic, acetone, diethyl ether, and ethanolic extracts of Cystoseira mediterranea and Ulva rigida (currently identified as U.armoricana). Codium fragile has strong fungicidal activities against Alternaria alternata, A. brassicicola, Fusarium oxysporium, Ulocladium botrytis, and Botryotricum piluliferum (Galal et al., 2011). Marine macroalgal extracts sprayed on plants have been reported to reduce the incidence of the grey mold by B. cinerea on strawberries, and the powdery mildew disease caused by Erysiphe polygoni on turnips and damping-off of tomato seedlings (Kulik, 1995). Different concentrations of S. polyceratium acetonic extracts noticeably inhibit the growth of the sour rot-causing plant pathogenic fungus Geotrichum candidum (Borbón et al., 2012). Furthermore, the brown macroalga Padina pavonia, mixed with the plant growth-promoting bacterium Pseudomonas aeruginosa, or used alone, are effective against F. solani and against Rhizoctonia solani (Sultana et al., 2005). Application of the algal U.armoricana extracts reduced foliar disease incidence of three powdery mildew diseases on common bean, grapevine and cucumber plants (Jaulneau et al., 2011). Similar results were also obtained using Ascophyllum nodosum extracts to enhance the foliar resistance against Phytophthora capsici on pepper (Lizzi et al., 1998), Alternaria radicina and B. cinerea foliar blights on carrots, and finally A. cucumerinum, Didymella applanata, F. oxysporum, and B. cinerea on cucumber (Jayaraj et al., 2011). Sultana et al., (2011) reported that application of dry powders of the three marine macroalgae, Spatoglossum variabile, Melanothamnus afaqhusainii and Halimeda tuna have more or similar suppressive effects on plant roots pathogenic fungi infecting tomato and sunflower by reducing percentages of fungal root infection as compared to the fungicide Topsin-M in

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greenhouse and in field conditions. Recent contribution of Ibraheem et al., (2017) revealed that, in vivo application of Padina gymnospora, Sargassum latifolium, and Hydroclathrus clathratus powders, as soil amendments, decreased the percentage of root rotting disease caused by Fusarium solani in Solanum melongena L. (eggplant). Moreover, P. gymnospora enhanced the growth performance of the eggplant in term of shoot length and plant fresh weight in the F. solani infected soils. Additionally, soil-free pathogens treated with the P. gymnospora and S. latifolium powders significantly increased root length and fruits fresh weight as compared to the control. A significant disease resistance was also assessed in the greenhouse experiment of tomato plant against the wilt disease-promoting fungus Verticillium dahlia using aqueous extracts of the brown algae Cystoseira. myriophylloides, Laminaria digitata, and Fucus spiralis either by spraying the whole plant or using seed imbibition techniques (Esserti et al., 2017). Ammar et al., (2017) indicated to the bioactive components of phenolic acids and flavonoids in the methanolic extract of Sargassum vulgare and stated that they might act as strong antifungal factors against Pythium aphanidermatum through inhibiting the pathogen mycelial growth by about 51 % and reducing the disease severity by a value of more than 82%. Raj et al., (2016) also found some fungicidal effects induced by the brown alga Sargassum swartzii where, it can control the rice sheath blight disease caused by Rhizoctonia solani and attributed this defense mechanism to high levels of phenolics and early accumulation of phytoalexin compounds in rice plant. Furthermore, polysaccharides-enriched macroalgal extracts obtained from the green, (e.g., Ulva lactuca and Caulerpa sertularioides), and brown algae (e.g., Padina gymnospora and Sargassum liebmannii) induced the plant protection against the necrotrophic fungus Alternaria solani on tomato (Solanum lycopersicum) (Hernández-Herrera et al., 2014). In addition, the other common storage carbohydrates, mannitol, the sugar alcohol of

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mannose and mannitol might also play an important role in storage of carbon and energy, regulation of coenzymes, osmoregulation, free-radical scavengings, and enhance the overall plant resistance to fungi (Stoop et al., 1996; Bohnert and Jensen, 1996; Prabhavathi and Rajam, 2007). Extracts of Laminaria digitata, Undaria pinnatifida and Porphyra umbilicalis have been documented to strongly suppress the grey mould growing on strawberries, brown rot disease on peaches, and green mould on lemons at a dose of 30 g/L through in vivo experiment on wounded fruits. In addition, fruit decay inhibition and reduction of disease severity have been positively increased in response to the applied dose concentration (de Corato et al., 2017). Recent investigation of de Corato et al., (2017) also demonstrated that high contents of fatty acids in marine macroalgae (e.g. Laminaria digitata, Undaria pinnatifida and Porphyra umbilicalis) may have a role in fungal treatment. In this context, marine macroalgal extract-treated plants have been shown to increase the over expression of some specific genes for defense signaling pathways. For example, Gelidium serrulatum, Sargassum filipendula and Ulva lactuca extracts showed induced jasmonate signaling defense systems (Ramkissoon et al., 2017). In addition, G. serrulatum sequentially induced salicylic acid signaling pathway. In conclusion, the marine macroalgae are an important natural resource that could be used on a large scale to overcome the plant-infecting fungi. 3.2.3. Antiviral Activity. Plant virus diseases, also known as ‘plant cancer’, are the second largest plant diseases and mainly responsible for a great loss in agricultural industry. Although chemotherapeutic management is a direct and effective method for controlling these viruses but it causes a series of side effects including improvement of pathogen-resistance to these drugs with time and accumulation of excessive pesticide residues in the soil. Much great progress has been made for

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discovery of new biogenic anti-virus substances. The structures of these active components largely include proteins, polysaccharides, alkaloids, flavonoids, polyphenols, and oils from plants, proteins and polysaccharides from microorganisms, and micro-and macroalgae (Zhao et al., 2017). Investigations of Pulz et al., (2004), El Gamal, (2010), Mohamed et al., (2012), and Zaid et al., (2016) on marine macroalgae highlighted that they have a wide spectrum of antiviral effects. However, a few studies focused on their applications in agriculture field (Manzo et al., 2009). Polysaccharides, especially sulphated ones separated from brown algae have efficient antiviral activities by blocking viral adsorption at the plant cell membrane (Sano, 1999; Pardee et al., 2004; Jiao et al., 2011). Furthermore, alginates (specific ingredient polysaccharides in brown algae) have been found to inhibit potato virus X (PVX) with a percent of 95% at a concentration of 10 mg/ml (Pardee et al., 2004). Mechanisms of these antiviral-algal interactions were explained based on inhibition of the virus adsorption on host cells through competing with the virus binding (Duarte et al., 2004), or through a synergistic combination between the polysaccharides with the target host cell to block the viral entry (Feldman et al., 1999). Betaines, dictyodial, dictyol C, dicytol H also have been isolated from the marine brown alga, Dictyota ciliolate and in general reported to possess cytotoxic and antiviral activities against some plant viruses (Manzo et al., 2009). For rhodophytes, Nagorskaia et al., (2008) found that kappa/betacarrageenans extracted from Tichocarpus crinitus suppress the infection by TMV in Xanthi-nc tobacco leaves. Significant amounts of vitamin C, amino acids, peptides, omega-3 fatty acids, and proteins have been identified in red marine macroalgae with noticeable antiviral activities (e.g., Dawczynski et al., 2007; MacArtain et al., 2007; Matanjun et al., 2009). Studies of Wang et al., (2004) and Liu et al., (2005) also succeeded to isolate the carbohydrate-binding proteins (lectins) from the marine green alga Ulva pertusa with anti-TMV activity. Pardee et al., (2004)

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investigated the anti-PVX effects using methanol extracts from 30 different species of marine algae, out of which only 6 species (Fucus gardneri Silva, Alaria marginata Postels & Ruprecht, Ralfsia sp. (Berkeley), Codium fragile (Suringar) Hariot, Fragilaria oceanica Cleve, and Egregia menziesii (Turner) J.E. Areschoug) showed inhibition rates by more than 80% at a concentration of 10 mg/ml.

3.3. Antinematodal activity Marine macroalgae are an important source of antinematotal bioactive compounds. Baloch et al., (2013) showed that mixing the soil with marine macroalgal powders of Spatoglossum variabile, Polycladia indica and Melanothamnus afaqhusainii significantly suppressed the infection with the root knot nematode Meloidogyne incognita attacking watermelon and eggplant. Observation of Sultana et al., (2011) supports well the previous conclusion and reported that dry powders of the three marine macroalgae, S. variabile, M. afaqhusainii and Halemida tuna have more or less similar suppressive effects against M. incognita as compared to the toxic chemical nematicide (carbofuran) both in greenhouse and field conditions. Similar findings have also been documented on tomato and sunflower plants through reducing nematode’s galls on roots and nematode’s penetration in root systems (Featonby-Smith and Van Staden, 1983). Wu et al., (1998) demonstrated that soil inoculation with the agricultural algal biostimulants could reduce invasion of tomato plant roots by secondstage juveniles of the root knot nematodes M. javanica and M. incognita. Egg recovery from roots of the treated plants are significantly reduced. In addition, cytokinins and 1aminocyclopropane-1-carboxylic acid, a precursor of ethylene biosynthesis, are present in macroalgae and could improve the resistance/susceptibility of plants to root knot nematodes

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(Kochba and Samish, 1971, 1972; Sawhney and Webster, 1975; Glazer et al., 1985). The recent contribution by Ngala et al., (2016) on in vivo assays against the root-knot nematodes Meloidogyne chitwoodi and M. hapla revealed that the commercially available seaweed extracts derived from the brown macroalgae, Ascophyllum nodosum and Ecklonia maxima have the ability to adversely affect their eggs hatching and sensory perceptions. They also confirmed that continuous exposure of M. chitwoodi egg masses to 50 and 100% of aqueous alkaline extracts of A. nodosum significantly reduced the final percentage of hatching. Moreover, on agar plates, Juveniles2 (J2) of M. chitwoodi pre-exposed to A. nodosum or E. maxima showed less attraction to tomato root diffusate. The 24-h pre-exposure to A. nodosum reduced the infectivity of M. chitwoodi and M. hapla.

3.4. Bioinsecticidal activity It is well known that marine macroalgae have insecticidal activities (Cetin et al., 2010; Sahayaraj and Kalidas, 2011; Asha et al., 2012; Sahayaraj and Mary Jeeva, 2012; Sahayaraj et al., 2012; Ali et al., 2013; Bantoto and Danilo, 2013). Their different extracts provide a novel approach in integrated pest management (Manilal et al., 2009; Rajesh et al., 2011; Sahayaraj and Kalidas, 2011; Sahayaraj and Mary Jeeva, 2012; Asha et al., 2012). Marine macroalgae are natural resources for discovery of ecofriendly environmental and novel botanical insecticidal substances (Isman, 1995). Several crude algal extracts investigated from Caulerpa scalpelliformis (Rajesh et al., 2011; Kombiah and Sahayaraj, 2012), Padina pavonica (Sahayaraj and Kalidas, 2011), Sargassum tenerrimum (Sahayaraj and Mary Jeeva, 2012), Ulva fasciata (Asha et al., 2012; Sahayaraj et al., 2012) and U. lactuca (Asha et al., 2012; Sahayaraj et al., 2012) showed insecticidal activity against the cotton insect pests Dysdercus spp. causing sever crop loss.

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Furthermore, the chloroform extracts of Sargassum swartzii and P. pavonica could cause nymphal mortality of Dysdercus cingulatus after 96 h. In addition, the chloroform and aqueous extracts of S. swartzii could shorten the male and female longevity of D. Cingulatus (Asharaja and Sahayaraj, 2013). The fecundity and hatchability of D. cingulatus have been also found to be reduced using the chloroform and methanolic extracts (800 ppm) of P. pavonica and S. swartzii. Mating period is also highly prolonged by the water extracts. Asharaja and Sahayaraj, (2013) also pointed out that fecundity and hatchability of D. cingulatus are reduced by the hexane extract. The latent effects of S. swartzii and P. pavonica chloroform extracts have been reported to cause mortality of the 3rd instar D. cingulatus nymphs due to the presence of stigmastan-6, 22-dien,3,5dedihydro and hexadecanoic acid methyl ester in S. swartzii and P. pavonica, respectively (Asharaja and Sahayaraj, 2013).

Conclusion Available information on the potential roles of marine macroalgae in plant protection and improvement is still poorly known so far. Certain studies have discussed the antimicrobial activities of marine macroalgae (extracts/biomass) against different plant-infecting pathogens. However, most of these studies were generally performed on a narrow range, i.e. experimental lab conditions. In general, marine macroalgae are mainly characterized by the presence of particular components of a biotechnological interest in integrated pest management such as microbicides, nematicides, insecticides, biofertilizers, biostimulators and soil conditioners. All these substances are considered ecofriendly safe to the environment for organic farming practices. However, many deep investigations on this trend of study are still needed to discover novel substances. Finally, marine macroalgae and their extracts could provide a chance for

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increasing percentage of plant cultivation in harsh habitats and are important bioinoculants in recent trends of organic farming for achieving sustainable agriculture development.

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