Beni-Suef University Journal of Basic and Applied Sciences 7 (2018) 104–110

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Beni-Suef University
Journal of Basic and Applied Sciences
journal homepage: www.elsevier.com/locate/bjbas

Review Article

Role of marine macroalgae in plant protection & improvement for

sustainable agriculture technology
Seham M. Hamed a,⇑, Amal A. Abd El-Rhman a, Neveen Abdel-Raouf b, Ibraheem B.M. Ibraheem b
a
Soil Microbiology Department, Soils, Water and Environment Research Institute, Agricultural Research Center, Giza, Egypt
b
Botany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt

a r t i c l e i n f o a b s t r a c t

Article history: Marine macroalgae are plant-like organisms with simple internal structures that generally live in coastal
Received 24 March 2017 areas. They mainly include different communities of red, brown and green macroalgae. Marine macroal-
Received in revised form 28 July 2017 gae commonly occupy intertidal and sublittoral-to-littoral zones on rocks and other hard substrata. They
Accepted 12 August 2017
are considered to be an excellent natural biosource in different aspects of agricultural fields. They have
Available online 14 August 2017
great proficiency in improving soil physical and chemical properties. Marine macroalgae are also charac-
terized by producing a large array of biologically active biocidal substances against plant-infecting patho-
Keywords:
gens. Unfortunately, most available literatures on marine macroalgae and their derivatives mainly
Marine macroalgae
Bioactive compounds
focused on their pharmaceutical applications but their potential utilization in sustainable agriculture
Biocontrols development is still often regarded as a secondary goal. However, a relatively considerable dataset on
Biopesticides marine macroalgae showed that they could play a major role in plant protection and improvement.
Biostimulants This review summarizes different aspects of potential macroalgal applications in agriculture.
Sustainable agriculture Commercial production and exploitation of specific compounds with interesting biotechnological impor-
tance from marine macroalgae including microbicides, nematicides, insecticides, biofertilizers, biostimu-
lators 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, antivi-
ral and fungicidal effects against some plant-infecting pathogens. These biocontrol agents provide mul-
tiple 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 envi-
ronmental tools in recent trends of organic farming.
Ó 2017 Beni-Suef University. Production and hosting by Elsevier B.V. This is an open access article under
the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
2. Utilization of marine macroalgae in the agriculture field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
2.1. Biostimulation proficiency on plant growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
2.2. Antimicrobial proficiency of marine macroalgae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
2.2.1. Antibacterial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
2.2.2. Antifungal activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
2.2.3. Antiviral activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
2.3. Antinematodal activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
2.4. Bioinsecticidal activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
3. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108

⇑ Corresponding author at: Soil Microbiology Department, Soils, Water and Environment Research Institute, Agricultural Research Centre, 12112 Giza, Egypt.
E-mail address: seham_moussa939@yahoo.com (S.M. Hamed).

http://dx.doi.org/10.1016/j.bjbas.2017.08.002
2314-8535/Ó 2017 Beni-Suef University. Production and hosting by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
 S.M. Hamed et al. / Beni-Suef Univ. J. Basic Appl. Sci. 7 (2018) 104–110
1. Introduction
Management of plant diseases is considered nowadays an
important prerequisite for sustainable agricultural development.
Although synthetic chemicals are well known to have a fundamen-
tal role in suppressing of plant diseases and maintaining high crop
yields they have harmful effect on human and environment integ-
rity. 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 pes-
ticides in top soils, and leaching into groundwater besides their
undesired effects on non-target organisms are of major environ-
mental concerns. On the other hand, natural products are consid-
ered 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 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 bioac-
tive compounds that has a broad range of biological activities
including antibacterial (Bouhlal et al., 2010; Singh and
Chaudhary, 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 with important plant nutritional
value (Kaplan et al., 1987). They are also well known as plant stim-
ulators. They have been applied as foliar spray, enhanced plant
growth at freezing, drought and in salt habitats, showed a notice-
able 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 Ascophyl-
lum nodosum (Linnaeus) Le Jolis has been widely investigated and
traditionally used as a soil biofertilizer and conditioning agent, ani-
mal 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 serra-
tus have been applied for a large-scaled production of biofertilizers
due to their high content of betaines, an organic osmolytic com-
pounds that can potentially play a crucial role in effective protec-
tion against salts, drought, and extreme temperature stress
(Blunden et al., 2010). At the present, one of the main tasks of sci-
105
entists is to improve the plant productivity using natural alterna-
tives which should be safe to 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 high-
lights and summarizes the potentiality of using marine macroalgal
biomass and their products in biological controls of some agricul-
tural diseases, integrated pest management, and improving the
plant growth for promising sustainable agricultural technology.
2. Utilization of marine macroalgae in the agriculture field
2.1. 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 aux-
ins, 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 been shown to pro-
duce 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, auto-
claving, 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 a-
tocopherol, ascorbic acid and b-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 uti-
lized as agricultural biostimulants (ABs) (EBIC, 2012). The utiliza-
tion 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 resis-
tance to fungi, bacteria and virus (Sharma et al., 2014). ABs include
various formulations of compounds, substances and other prod-
ucts, such as microorganisms, trace elements, enzymes, plant
growth regulators (PGRs) and macroalgal 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., 2008a,b; Khan et al.,
2009; Craigie, 2011). Consequently, these products can enhance
106 S.M. Hamed et al. / Beni-Suef Univ. J. Basic Appl. Sci. 7 (2018) 104–110
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).
2.2. Antimicrobial proficiency of marine macroalgae
2.2.1. 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, cur-
rently identified as S. swartzii C. Agardh, exhibited the highest
activity against the phytopathogenic bacterium Pseudomonas syrin-
gae which causes leaf spot disease on the valuable medicinal plant
Gymnema sylvestre (Kumar et al., 2008). However, 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 macro-
alga, Sargassum polyceratium (Phaeophyceae) showed also a notice-
able activity against different types of bacteria such as
Staphylococcus aureus, Erwinia carotovora (now known as Pectobac-
terium carotovora), and Escherichia coli using disc diffusion method
(Kumar et al., 2008). Meanwhile, the ethanolic extracts of S. polyc-
eratium, 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 and Caram, 1984). In a green-
house experiment, spray application of aqueous marine macroalgal
extracts from Cystoseira myriophylloides and Fucus spiralis signifi-
cantly reduced crown gall diseases caused by the bacterial patho-
gen 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 had antibacterial activities.
Arunkumar et al., (2001) found that predominant fatty acids (pal-
mitic acids) isolated from the green alga Enteromorpha flexuosa,
currently accepted taxonomically as Ulva flexuosa exhibited
antibacterial activity against the plant pathogenic bacterium Xan-
thomonas oryzae pv. oryzae. Also, the methanolic extract of Padina
gymnospora characterized by a high proportion of plamitic acid
showed a high antibacterial activity against the soil-borne patho-
genic 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 addi-
tion, 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). Mar-
ine 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 protec-
tions 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 carote-
noids 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 significant levels of defense enzymes
including polyphenol oxidases and peroxidasesas compared to
the control (untreated plants).
2.2.2. Antifungal activity
Natural algal extracts are nowadays more applicable, instead of
synthetic fungicides, in controlling of plant-infecting fungi due to
their higher safety and relatively negligible impacts on the envi-
ronment (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 Plas-
mopara 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 Polycla-
dia indica), and Melanothamnus afaqhusainii have significant sup-
pressive 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 chem-
ical 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 taxonomically as 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 iden-
tified as U. armoricana). Codium fragile has strong fungicidal activity
against Alternaria alternata, A. brassicicola, Fusarium oxysporium,
Ulocladium botrytis, and Botryotricum piluliferum (Galal et al.,
 S.M. Hamed et al. / Beni-Suef Univ. J. Basic Appl. Sci. 7 (2018) 104–110
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 Ery-
siphe 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). Fur-
thermore, the brown macroalga Padina pavonia, mixed with the
plant growth-promoting bacterium Pseudomonas aeruginosa, or
used alone, are effective against F. solani and 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 nodo-
sum 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, Didy-
mella 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, Melanoth-
amnus afaqhusainii and Halimeda tuna have more or similar sup-
pressive 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 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 Fusar-
ium solani in Solanum melongena L. (eggplant). Moreover, P. gym-
nospora 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. gym-
nospora and S. latifolium powders significantly increased root
length and fruits fresh weight as compared to the control. A signif-
icant disease resistance was also assessed in the greenhouse exper-
iment of tomato plant against the wilt disease-promoting fungus
Verticillium dahlia using aqueous extracts of the brown algae Cysto-
seira. 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 Sargas-
sum vulgare and stated that they might act as strong antifungal fac-
tors 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 gym-
nospora and Sargassum liebmannii) induced the plant protection
against the necrotrophic fungus Alternaria solani on tomato (Sola-
num lycopersicum) (Hernández-Herrera et al., 2014). In addition,
the other common storage carbohydrates, mannitol, the sugar
alcohol of 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
107
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 con-
centration (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 pinnat-
ifida 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, Sar-
gassum filipendula and Ulva lactuca extracts showed induced jas-
monate 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 control
the plant-infecting fungi.
2.2.3. 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 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
and Gross (2004), El Gamal, (2010), Mohamed et al. (2012), and
Zaid et al., (2016) on marine macroalgae highlighted the wide
spectrum of their 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 polysac-
charides 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 interac-
tions 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/beta-carrageenans
extracted from Tichocarpus crinitus suppressed 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) 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 mar-
ginata 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.
108 S.M. Hamed et al. / Beni-Suef Univ. J. Basic Appl. Sci. 7 (2018) 104–110
2.3. 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 sup-
pressed 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. vari-
abile, 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 inocu-
lation with the agricultural algal biostimulants could reduce inva-
sion of tomato plant roots by second-stage 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 1-aminocyclopropane-1-carboxylic acid, a precur-
sor of ethylene biosynthesis, are present in macroalgae and could
improve the resistance/susceptibility of plants to root knot nema-
todes (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 Meloidog-
yne chitwoodi and M. hapla revealed that the commercially avail-
able 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 dif-
fusate. The 24-h pre-exposure to A. nodosum reduced the infectiv-
ity of M. chitwoodi and M. hapla.
2.4. Bioinsecticidal activity
It is well known that marine macroalgae have insecticidal activ-
ities (Cetin et al., 2010; Sahayaraj and Kalidas, 2011; Asha et al.,
2012; Sahayaraj and MaryJeeva, 2012; Sahayaraj et al., 2012; Ali
et al., 2013; Bantoto and Danilo, 2013). Their different extracts pro-
vide a novel approach in integrated pest management (Manilal
et al., 2009; Rajesh et al., 2011; Sahayaraj and Kalidas, 2011;
Asha et al., 2012). Marine macroalgae are natural resources for dis-
covery of ecofriendly environmental and novel botanical insectici-
dal 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 MaryJeeva,
2012), Ulva fasciata (Asha et al., 2012; Sahayaraj et al., 2012) and
U. lactuca (Asha et al., 2012; Sahayaraj et al., 2012) showed insec-
ticidal activity against the cotton insect pests Dysdercus spp. caus-
ing sever crop loss. 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. cingu-
latus 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,3,5-dedihydro and hexade-
canoic acid methyl ester in S. swartzii and P. pavonica, respectively
(Asharaja and Sahayaraj, 2013).
3. Conclusion
Available information on the potential roles of marine macroal-
gae 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 gener-
ally 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 environ-
ment for organic farming practices. However, many deep investi-
gations on this trend of study are still needed to discover novel
substances. Finally, marine macroalgae and their extracts could
provide a chance for increasing percentage of plant cultivation in
harsh habitats and are important bioinoculants in recent trends
of organic farming for achieving sustainable agriculture
development.
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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