Potential Use of Extracts of Seaweeds Against Plant Pathogens 183
in cucumbers. Most recently, Ramikissoon et al. (2017) produced extracts of three Caribbean seaweeds
(i.e., green—Ulva lactuca, brown—Sargassum filipendula, and red—Gracilaria serrulata) to suppress
pathogenic infections (i.e., Alternaria solani and Xanthomonas campestris pv vesicatoria) in tomatoes.
A discussion on salicylic and jasmonic acid pathways is included in their modes of action discussion.
Paulert et al. (2009) tested a crude seaweed extract and the polysaccharide ulvan (at rates of 0.1; 1;
and 10 mg ml
–1
), against conidial germination and mycelial growth of Colletotrichum lindemuthianum. The
authors reported inhibition of mycelial growth in vitro with a soluble methanolic extract. However, mycelial
growth and conidial germination of the fungus was increased in vitro with ulvan, whereas greenhouse
plants sprayed with 10 mg ml
−1
ulvan reduced the anthracnose severity by 38%. In addition, Cluzet et al.
(2004) reported that polysaccharides from Ulva armoricana had no effect, in vitro, on Colletotrichum
trifolii development, although it protected alfalfa (Medicago truncatula) against the fungus. Borsato et al.
(2010) showed that the polysaccharide ulvan did not inhibit germination of the fungus on leaf discs, nor
alter the activity of peroxidases, but still protected the plants, suggesting induced plant resistance. The
extracts of S. zonale, L. dendroidea, P. canaliculata, S. muticum, A. nodosum, and F. spiralis significantly
inhibited Colletotrichum lagenarium, whereas the same extracts did not inhibit Aspergillus flavus growth
in vitro. Similar results were reported by Sangha et al. (2010) who also demonstrated that various red algal
polysaccharides had no direct effects on the fungus Sclerotinia sclerotiorum, in vitro, but it was effective
through induced plant resistance.
It is interesting to note that many of the seaweed extracts tested have also shown variations in
bioactivity, simply due to seasonal effects (Arunkumar and Rangasamy 2000). Moreau et al. (1988) identified
anti-fungal substances from some members of the Dictyotales (brown algae) collected around the French
Mediterranean coast and reported that seasonal variations were found in the bioactivity of the extracts.
Manilal et al. (2009) investigated in vitro anti-microbial activity against four species of plant pathogenic
fungi using extracts of 15 seaweeds, belonging to 13 families and six orders of the Rhodophyta, sampled
for a year between April 2007 and March 2008, along the southwest coast of India. The crude extracts of
both fresh and dried samples, prepared from different polar and non-polar solvents, were used. Four species
of red algae (e.g., Asparagopsis taxiformis, Laurencia ceylanica, L. brandenii, and Hypnea valentiae) were
found to be highly active, although a seasonal variation was observed for antimicrobial activity which
was most prominent in the green coenocyte A. taxiformis between December and January. Jiménez et al.
(2011) demonstrated potential anti-phytopathogenic activities of aqueous and ethanolic extracts obtained
from nine Chilean marine macroalgae, collected at different seasons, in in vitro conditions, and showed
differential suppression of microbes with the extracts.
Virii: Various seaweed extracts have been shown to have broad spectrum viral suppression (Shi et al.
2017). In particular, algal oligosaccharides have been shown to stimulate plant defence responses against
tobacco mosaic virus (TMV) in whole plants, or suspension cell cultures (Klarzynski et al. 2003; Laporte
et al. 2007; Fu et al. 2011). The oligosaccharides, especially laminarin or chemically sulphated laminarin
(PS3), can prime or activate defence mechanisms, increase the expression of genes, promote oxidative
bursts and other defense mechanisms in cell suspensions, indicating that plant defense activity may be
induced against viral pathogens (also discussed in a later section). For example, tobacco cell suspensions,
treated with laminarin or PS3, increased molecular and biochemical defense response that was directly
related to the induction of resistance in treated plants, when challenged with pathogens (Menard et al.
2005). Reunov et al. (2011) also reported that fucoidan (extracted from Fucus evanescens) treatment, to
detached Datura stramonium leaves, resulted in reduced accumulation of potato virus X (PVX) in the
mesophyll cells, as compared to the control.
Indirect bioactivity of seaweed extracts against microbes
In addition to in vitro activities against plant pathogens, seaweed extracts have also been shown to
enhance plant resistance to various pests and diseases (Allen et al. 2001; Sangha et al. 2010; Jiménez et al.
2011). Such effects could be effected indirectly through altering plant-pathogen interactions, activating
plant defence pathways, as well as promoting plant health by modulation of the rhizosphere microbial
community, or by improving the soil environment by direct antagonism to the pathogen (see Mercier
in cucumbers. Most recently, Ramikissoon et al. (2017) produced extracts of three Caribbean seaweeds
(i.e., green—Ulva lactuca, brown—Sargassum filipendula, and red—Gracilaria serrulata) to suppress
pathogenic infections (i.e., Alternaria solani and Xanthomonas campestris pv vesicatoria) in tomatoes.
A discussion on salicylic and jasmonic acid pathways is included in their modes of action discussion.
Paulert et al. (2009) tested a crude seaweed extract and the polysaccharide ulvan (at rates of 0.1; 1;
and 10 mg ml
–1
), against conidial germination and mycelial growth of Colletotrichum lindemuthianum. The
authors reported inhibition of mycelial growth in vitro with a soluble methanolic extract. However, mycelial
growth and conidial germination of the fungus was increased in vitro with ulvan, whereas greenhouse
plants sprayed with 10 mg ml
−1
ulvan reduced the anthracnose severity by 38%. In addition, Cluzet et al.
(2004) reported that polysaccharides from Ulva armoricana had no effect, in vitro, on Colletotrichum
trifolii development, although it protected alfalfa (Medicago truncatula) against the fungus. Borsato et al.
(2010) showed that the polysaccharide ulvan did not inhibit germination of the fungus on leaf discs, nor
alter the activity of peroxidases, but still protected the plants, suggesting induced plant resistance. The
extracts of S. zonale, L. dendroidea, P. canaliculata, S. muticum, A. nodosum, and F. spiralis significantly
inhibited Colletotrichum lagenarium, whereas the same extracts did not inhibit Aspergillus flavus growth
in vitro. Similar results were reported by Sangha et al. (2010) who also demonstrated that various red algal
polysaccharides had no direct effects on the fungus Sclerotinia sclerotiorum, in vitro, but it was effective
through induced plant resistance.
It is interesting to note that many of the seaweed extracts tested have also shown variations in
bioactivity, simply due to seasonal effects (Arunkumar and Rangasamy 2000). Moreau et al. (1988) identified
anti-fungal substances from some members of the Dictyotales (brown algae) collected around the French
Mediterranean coast and reported that seasonal variations were found in the bioactivity of the extracts.
Manilal et al. (2009) investigated in vitro anti-microbial activity against four species of plant pathogenic
fungi using extracts of 15 seaweeds, belonging to 13 families and six orders of the Rhodophyta, sampled
for a year between April 2007 and March 2008, along the southwest coast of India. The crude extracts of
both fresh and dried samples, prepared from different polar and non-polar solvents, were used. Four species
of red algae (e.g., Asparagopsis taxiformis, Laurencia ceylanica, L. brandenii, and Hypnea valentiae) were
found to be highly active, although a seasonal variation was observed for antimicrobial activity which
was most prominent in the green coenocyte A. taxiformis between December and January. Jiménez et al.
(2011) demonstrated potential anti-phytopathogenic activities of aqueous and ethanolic extracts obtained
from nine Chilean marine macroalgae, collected at different seasons, in in vitro conditions, and showed
differential suppression of microbes with the extracts.
Virii: Various seaweed extracts have been shown to have broad spectrum viral suppression (Shi et al.
2017). In particular, algal oligosaccharides have been shown to stimulate plant defence responses against
tobacco mosaic virus (TMV) in whole plants, or suspension cell cultures (Klarzynski et al. 2003; Laporte
et al. 2007; Fu et al. 2011). The oligosaccharides, especially laminarin or chemically sulphated laminarin
(PS3), can prime or activate defence mechanisms, increase the expression of genes, promote oxidative
bursts and other defense mechanisms in cell suspensions, indicating that plant defense activity may be
induced against viral pathogens (also discussed in a later section). For example, tobacco cell suspensions,
treated with laminarin or PS3, increased molecular and biochemical defense response that was directly
related to the induction of resistance in treated plants, when challenged with pathogens (Menard et al.
2005). Reunov et al. (2011) also reported that fucoidan (extracted from Fucus evanescens) treatment, to
detached Datura stramonium leaves, resulted in reduced accumulation of potato virus X (PVX) in the
mesophyll cells, as compared to the control.
Indirect bioactivity of seaweed extracts against microbes
In addition to in vitro activities against plant pathogens, seaweed extracts have also been shown to
enhance plant resistance to various pests and diseases (Allen et al. 2001; Sangha et al. 2010; Jiménez et al.
2011). Such effects could be effected indirectly through altering plant-pathogen interactions, activating
plant defence pathways, as well as promoting plant health by modulation of the rhizosphere microbial
community, or by improving the soil environment by direct antagonism to the pathogen (see Mercier