Content uploaded by Wajahatullah Khan
Author content
All content in this area was uploaded by Wajahatullah Khan
Content may be subject to copyright.
REVIEWS
Seaweed Extracts as Biostimulants of Plant Growth
and Development
Wajahatullah Khan ÆUsha P. Rayirath ÆSowmyalakshmi Subramanian Æ
Mundaya N. Jithesh ÆPrasanth Rayorath ÆD. Mark Hodges Æ
Alan T. Critchley ÆJames S. Craigie ÆJeff Norrie Æ
Balakrishan Prithiviraj
Received: 24 October 2008 / Accepted: 18 March 2009 / Published online: 8 May 2009
Springer Science+Business Media, LLC 2009
Abstract Marine algal seaweed species are often regar-
ded as an underutilized bioresource, many have been used
as a source of food, industrial raw materials, and in ther-
apeutic and botanical applications for centuries. Moreover,
seaweed and seaweed-derived products have been widely
used as amendments in crop production systems due to the
presence of a number of plant growth-stimulating com-
pounds. However, the biostimulatory potential of many of
these products has not been fully exploited due to the lack
of scientific data on growth factors present in seaweeds and
their mode of action in affecting plant growth. This article
provides a comprehensive review of the effect of various
seaweed species and seaweed products on plant growth and
development with an emphasis on the use of this renewable
bioresource in sustainable agricultural systems.
Keywords Seaweed Biostimulants Plant growth
Plant development Biotic and abiotic stresses
Plant-microbe interactions
Introduction
Seaweeds form an integral part of marine coastal ecosys-
tems. They include the macroscopic, multicellular marine
algae that commonly inhabit the coastal regions of the
world’s oceans where suitable substrata exist. It has been
estimated that there are about 9,000 species of macroalgae
broadly classified into three main groups based on their
pigmentation (for example, Phaeophyta, Rhodophyta, and
Chlorophyta; or the brown, red, and green algae, respec-
tively). Brown seaweeds are the second most abundant
group comprising about 2,000 species which reach their
maximum biomass levels on the rocky shores of the tem-
perate zones. They are the type most commonly used in
agriculture (Blunden and Gordon 1986) and, among them,
Ascophyllum nodosum (L.) Le Jolis is the most researched
(Ugarte and others 2006). Besides A. nodosum, other brown
algae such as Fucus spp., Laminaria spp., Sargassum spp.,
and Turbinaria spp. are used as biofertilizers in agriculture
(Hong and others 2007).
The benefits of seaweeds as sources of organic matter
and fertilizer nutrients have led to their use as soil condi-
tioners for centuries (Blunden and Gordon 1986; Metting
and others 1988; Temple and Bomke 1988). Some
15 million metric tonnes of seaweed products are produced
annually (FAO 2006), a considerable portion of which is
W. Khan U. P. Rayirath S. Subramanian
M. N. Jithesh P. Rayorath B. Prithiviraj (&)
Department of Plant and Animal Sciences, Nova Scotia
Agricultural College, P.O. Box 550, 58 River Road,
Truro, NS B2N 5E3, Canada
e-mail: bprithiviraj@nsac.ca
D. M. Hodges
Atlantic Food and Horticulture Research Centre,
Agriculture and Agri-Food Canada, 32 Main Street,
Kentville, NS B4N 1J5, Canada
A. T. Critchley J. S. Craigie J. Norrie
Acadian Seaplants Limited, 30 Brown Avenue,
Dartmouth, NS B3B 1X8, Canada
J. S. Craigie
Institute for Marine Biosciences, National Research Council of
Canada, 1411 Oxford Street, Halifax, NS B3H 3Z1, Canada
Present Address:
W. Khan
Department of Biochemistry, College of Science,
King Saud University, P.O. Box 2455, Riyadh 11451, Kingdom
of Saudi Arabia
123
J Plant Growth Regul (2009) 28:386–399
DOI 10.1007/s00344-009-9103-x
used for nutrient supplements and as biostimulants or
biofertilizers to increase plant growth and yield. A number
of commercial seaweed extract products are available for
use in agriculture and horticulture (Table 1).
Numerous studies have revealed a wide range of bene-
ficial effects of seaweed extract applications on plants, such
as early seed germination and establishment, improved
crop performance and yield, elevated resistance to biotic
and abiotic stress, and enhanced postharvest shelf-life of
perishable products (Beckett and van Staden 1989; Hankins
and Hockey 1990; Blunden 1991; Norrie and Keathley
2006) (Fig. 1).
Modes of Action of Growth Stimulatory Factors
in Seaweed Extracts
Seaweed products exhibit growth-stimulating activities,
and the use of seaweed formulations as biostimulants in
crop production is well established. Biostimulants are
defined as ‘‘materials, other than fertilizers, that promote
plant growth when applied in small quantities’’ and are also
referred to as ‘‘metabolic enhancers’’ (Zhang and Schmidt
1997). Seaweed components such as macro- and microel-
ement nutrients, amino acids, vitamins, cytokinins, auxins,
and abscisic acid (ABA)-like growth substances affect
cellular metabolism in treated plants leading to enhanced
growth and crop yield (Crouch and others 1992; Crouch
and van Staden 1993a; Reitz and Trumble 1996; Durand
and others 2003; Stirk and others 2003;O
¨rdo
¨g and others
2004). Seaweed extracts are bioactive at low concentra-
tions (diluted as 1:1000 or more) (Crouch and van Staden
1993a). Although many of the various chemical compo-
nents of seaweed extracts and their modes of action remain
unknown, it is plausible that these components exhibit
synergistic activity (Fornes and others 2002; Vernieri and
others 2005).
Chemical Components of Seaweed that Affect Plant
Growth
Carbohydrates, Minerals, and Trace Elements
Seaweeds, particularly the red and brown algae, are a
source of unusual and complex polysaccharides not present
Table 1 Commercial seaweed products used in the agriculture and horticulture industries
Product name Seaweed name Company Application
Acadian
Ascophyllum nodosum Acadian Agritech Plant growth stimulant
Acid Buf Lithothamnium calcareum Chance & Hunt Limited Animal feed
Agri-Gro Ultra Ascophyllum nodosum Agri Gro Marketing Inc. Plant growth stimulant
AgroKelp Macrocystis pyrifera Algas y Bioderivados Marinos, S.A. de C.V. Plant growth stimulant
Alg-A-Mic Ascophyllum nodosum BioBizz Worldwide N.V. Plant growth stimulant
Bio-Genesis
TM
High Tide
TM
Ascophyllum nodosum Green Air Products, Inc. Plant growth stimulant
Biovita Ascophyllum nodosum PI Industries Ltd Plant growth stimulant
Emerald RMA Red marine algae Dolphin Sea Vegetable Company Health product
Espoma Ascophyllum nodosum The Espoma Company Plant growth stimulant
Fartum
Unspecified Inversiones Patagonia S.A. Biofertilizer
Guarantee
Ascophyllum nodosum MaineStream Organics Plant growth stimulant
Kelp Meal Ascophyllum nodosum Acadian Seaplants Ltd Plant growth stimulant
Kelpak Ecklonia maxima BASF Plant growth stimulant
Kelpro Ascophyllum nodosum Tecniprocesos Biologicos, S.A. de C.V. Plant growth stimulant
Kelprosoil Ascophyllum nodosum Productos del Pacifico, S.A. deC.V. Plant growth stimulant
Maxicrop Ascophyllum nodosum Maxicrop USA, Inc. Plant growth stimulant
Nitrozime Ascophyllum nodosum Hydrodynamics International Inc. Plant growth stimulant
ProfertDurvillea antarctica BASF Plant biostimulant
Sea Winner Unspecified China Ocean University Product Development Co., Ltd Plant biostimulant
Seanure Unspecified Farmura Ltd. Plant growth stimulant
Seasol
Durvillea potatorum Seasol International Pty Ltd Plant growth stimulant
Soluble Seaweed Extract Ascophyllum nodosum Technaflora Plant Products, LTD Plant growth stimulant
Stimplex
Ascophyllum nodosum Acadian Agritech Plant growth stimulant
Synergy Ascophyllum nodosum Green Air Products, Inc. Plant growth stimulant
Tasco
Ascophyllum nodosum Acadian Agritech Animal feed
J Plant Growth Regul (2009) 28:386–399 387
123
in land plants (Siegel and Siegel 1973; Painter 1983;
Blunden and Gordon 1986; Craigie 1990; Chizhov and
others 1998; Duarte and others 2001) (Table 2). For
example, the brown seaweeds Ascophyllum nodosum,
Fucus vesiculosus, and Saccharina longicruris contain the
polysaccharides laminaran, fucoidan, and alginate (Painter
1983; Lane and others 2006). Laminaran is a (1,3)-b-D-
glucan with b-(1,6) branching (Nelson and Lewis 1973;
Zvyagintseva and others 1999). Although the precise
structures of fucoidans are not fully established, fucoidan
from A. nodosum consists primarily of sulfated fucose
linked in a-(1,3) and a-(1,4) configuration (Chevolot and
others 1999; Chevolot and others 2001; Daniel and others
2001; Marais and Joseleau 2001). Alginate is a block
copolymer structure composed of D-mannuronic and L-
guluronic acids with b-(1,4)-glycosidic linkages. The
properties of the various alginates differ depending on the
position of each monomeric unit in the chain, the average
molecular weight of the polymer, and the nature of its
associated counter ions. The monomers may alternate in
some regions of the alginate (heteropolymeric), or they
may occur in contiguous groups to produce homopolymeric
sections with either monomer within the alginate molecule
(Painter 1983; Rioux and others 2007). Of these three
polysaccharides, laminaran and fucoidan exhibit a wide
range of biological activities (Rioux and others 2007).
Direct effects of fucoidan on plants have not yet been
reported but sulfated fucoidans from brown algae have
evinced biological activities in mammalian systems
(McClure and others 1992; Angstwurm and others 1995;
Mauray and others 1995). Laminarin has been shown to
stimulate natural defense responses in plants and is
involved in the induction of genes encoding various path-
ogenesis–related (PR) proteins with antimicrobial proper-
ties (Fritig and others 1998; van Loon and van Strien
1999).
Growth Hormones
The concentration of mineral nutrient elements present in
commercial seaweed concentrates (SWCs) alone cannot
account for the growth responses elicited by seaweed
extracts (Blunden 1972,1991). Beneficial effects observed
in various plant growth bioassays have led to speculation
that SWCs contain plant growth-regulatory substances
(Williams and others 1981; Tay and others 1985; Mooney
and van Staden 1986). Furthermore, the wide range of
growth responses induced by seaweed extracts implies the
presence of more than one group of plant growth-promot-
ing substances/hormones (Tay and others 1985; Crouch
and van Staden 1993a).
Cytokinins have been detected in fresh seaweeds (Hus-
sein and Boney 1969) and seaweed extracts (Brain and
others 1973). The cytokinins present in seaweed formula-
tions include trans-zeatin, trans-zeatin riboside, and dihy-
dro derivatives of these two forms (Stirk and van Staden
1997). Liquid chromatography/mass spectroscopy
(LC/MS) analysis of 31 seaweed species representing
various groups revealed that zeatin (Z) and isopentenyl (IP)
conjugates of cytokinins are the predominant cytokinins
Fig. 1 Schematic
representation of physiological
effects elicited by seaweed
extracts and possible
mechanism(s) of bioactivity
388 J Plant Growth Regul (2009) 28:386–399
123
(Stirk and others 2003). Seaweed concentrates also con-
tained aromatic cytokinins BAP (benzyl amino purine) and
topolin (6-[3-hydroxybenzyl-amino] purine) derivatives)
(Stirk and others 2004).
Marine algae are also reportedly rich in auxins and
auxin-like compounds (Crouch and van Staden 1993a). An
A. nodosum extract had as high as 50 mg IAA (indole
acetic acid) per gram of dry extract (Kingman and Moore
1982). Similarly, an extract of Ecklonia maxima exhibited
a remarkable root-promoting activity on mung bean, an
effect reminiscent of auxins (Crouch and van Staden 1991).
Gas chromatography/mass spectroscopy (GC/MS) analysis
of the extract revealed the presence of indole compounds,
including IAA in SWC (Crouch and others 1992).
Auxins have been detected in other algal species like
Porphyra perforata, but the levels found were low (Zhang
and others 1993). In higher plants IAA occurs as an inac-
tive conjugate with carboxyl groups, glycans, amino acids,
and peptides, which, upon hydrolysis, are converted to free
active IAA (Bartel 1997). Stirk and others (2004) found
four amino acid and three indole conjugates of IAA in the
extracts of two seaweeds, E. maxima and Macrocystis
pyrifera. Biologically active auxin-like compounds other
than IAA were reported in alkaline hydrolyzates of
A. nodosum,Fucus vesiculosus, and other seaweeds
(Buggeln and Craigie 1971).
The water-soluble growth inhibitors extracted from
Laminaria digitata and A. nodosum resulted in marked
inhibition of lettuce hypocotyl growth (Hussain and Boney
1973). One of these substances seemed to be similar to
ABA as revealed by bioassay, thin-layer, and gas-liquid
chromatography analysis. Presence of ABA in seaweeds
has also been reported by others such Tietz and others
(1989) (green algae) and Kingman and Moore (1982)
(A. nodosum).
Betaines
Ascophyllum nodosum extracts contain various betaines
and betaine-like compounds (Blunden and others 1986). In
plants, betaines serve as a compatible solute that alleviates
osmotic stress induced by salinity and drought stress;
however, other roles have also been suggested (Blunden
and Gordon 1986), such as enhancing leaf chlorophyll
content of plants following their treatment with seaweed
extracts (Blunden and others 1997). This increase in
chlorophyll content may be due to a decrease in chloro-
phyll degradation (Whapham and others 1993). Yield
enhancement effects due to improved chlorophyll content
in leaves of various crop plants have been attributed to the
betaines present in the seaweed (Genard and others 1991;
Whapham and others 1993; Blunden and others 1997). It
has been indicated that betaine may work as a nitrogen
source when provided in low concentration and serve as an
osmolyte at higher concentrations (Naidu and others 1987).
Betaines have been shown to play a part in successful
formation of somatic embryos from cotyledonary tissues
and mature seeds of tea (Wachira and Ogada 1995; Akula
and others 2000).
Sterols
As with many other eukaryotic cells, sterols are an essen-
tial group of lipids. Generally, a plant cell contains a
mixture of sterols, such as b-sitosterol, stigmasterol,
24-methylenecholesterol, and cholesterol (Nabil and Cos-
son 1996). Brown seaweed chiefly contains fucosterol and
fucosterol derivatives, whereas red seaweeds primarily
contain cholesterol and cholesterol derivatives. Green
seaweed accumulates mainly ergosterol and 24-methylen-
echolesterol (Ragan and Chapman 1978; Hamdy and
Dawes 1988; Govindan and others 1993; Nabil and Cosson
1996) (Table 3).
Table 2 Selected polysaccharide constituents of green, red, and
brown seaweeds
Seaweed Polysaccharides
Chlorophyceae
(Green)
Amylose, amylopectin
Cellulose
Complex hemicellulose
Glucomannans
Mannans
Inulin
Laminaran
Pectin
Sulfated mucilages
(glucuronoxylorhamnans)
Xylans
Rhodophyceae (Red) Agars, agaroids
Carrageenans
Cellulose
Complex mucilages
Furcellaran
Glycogen (floridean starch)
Mannans
Xylans, rhodymenan
Phaeophyceae
(Brown)
Alginates
Cellulose
Complex sulfated heteroglucans
Fucose containing glycans
Fucoidans
Glucuronoxylofucans
Laminarans
Lichenan-like glucan
J Plant Growth Regul (2009) 28:386–399 389
123
Effect on Soil Health
Soil Structure and Moisture Retention
Besides eliciting a growth-promoting effect on plants,
seaweeds also affect the physical, chemical, and bio-
logical properties of soil which in turn influence plant
growth. Seaweeds and seaweed extracts enhance soil
health by improving moisture-holding capacity and by
promoting the growth of beneficial soil microbes.
Brown seaweeds are rich in polyuronides such as algi-
nates and fucoidans. The gelling and chelating abilities
of these polysaccharides coupled with their hydrophilic
properties make these compounds important in food
processing and in the agricultural and pharmaceutical
industries (Cardozo and others 2007). Alginate occurs
in the cell walls of seaweeds as a mixed salt with the
major cations being Na, Ca, Mg, and K together with a
number of minor metal counterions. The molecular
mass of alginate isolated from A. nodosum,F. vesicu-
losus,andS. longicruris varies between 106.6 and
177.3 kDa (Rioux and others 2007). Alginates possess
unique and valuable properties attributable to the
varying proportions of their two monomeric units
(D-mannuronic acid and L-guluronic acid) that are
arranged in block copolymer structures. The free acid
form, alginic acid, is insoluble in water, as are alginates
of certain divalent and polyvalent metal ions. Knowl-
edge of these properties together with that of chain
lengths and copolymer composition are used to control
the gel structure and porosity of alginates for agricul-
tural, pharmaceutical, and industrial uses (Lewis and
others 1988; Skjak-Braek and others 1989). For exam-
ple, alginates are widely used in formulating slow-
release pharmaceuticals (Kim and others 2005;Chan
and Heng 2002; Wong and others 2002)andpesticides
(Vollner 1990; Davis and others 1996; Gonzalez-Pradas
and others 1999; Kumbar and others 2003). The wide-
spread interest in alginate is due in part to its biode-
gradable nature and the relatively non toxic nature of
this natural compound.
Salts of alginic acid combine with the metallic ions in
the soil to form high-molecular-weight complexes that
absorb moisture, swell, retain soil moisture, and improve
crumb structure. This results in better soil aeration and
capillary activity of soil pores which in turn stimulate
the growth of the plant root system as well as boost soil
microbial activity (Eyras and others 1998; Gandhiyappan
and Perumal 2001; Moore 2004). The polyanionic
properties of seaweeds and unicellular algae have proved
valuable in remediation of soils, especially those con-
taminated with heavy metals (Metting and others 1988;
Blunden 1991).
Table 3 Common sterol constituents of green, red, and brown
seaweeds
Seaweed Type of sterol
Chlorophyceae (Green) 22-Dehydrocholesterol
24-Methylenecholesterol
24-Methylenecycloartanol
28-Isofucosterol
Brassicasterol
Cholesterol
Clerosterol
Clionasterol
Codisterol
Cycloartannol
Cycloartenol
Decortinol
Decortinone
Ergosterol
Fucosterol
Isodecortinol
Ostreasterol
ß-Stitosterol
Zymosterol
Chondrillasterol
D
5
- Ergostenol
D
7
- Ergostenol
Poriferastenol
24-Methylenophenol
Rhodophyceae (Red) 22-Dehydrocholesterol
24-Methylenecholesterol
Campesterol
Cholesterol
Cycloartenol
Desmosterol
Fucosterol
Stigmasterol
Brassicasterol
5-Dihydroergosterol
D
5
- Ergostenol
Obusifoliol
D
4,5
- Ketosteroids
Sitosterol
Phaeophyceae (Brown) 22-Dehydrocholesterol
Cycloartenol
24-Methylenecycloartenol
24-Methylenecholesterol
Fucosterol
Cholesterol
Campesterol
Stigmasterol
Brassicasterol
Clionasterol
Porifasterol
390 J Plant Growth Regul (2009) 28:386–399
123
Effect on Rhizosphere Microbes
Application of seaweeds and seaweed extracts triggers the
growth of beneficial soil microbes and secretion of soil-
conditioning substances by these microbes. As mentioned,
alginates affect soil properties and encourage growth of
beneficial fungi. Ishii and others (2000) observed that
alginate oligosaccharides, produced by enzymatic degra-
dation of alginic acid mainly extracted from brown algae,
significantly stimulated hyphal growth and elongation of
arbuscular mycorrhizal (AM) fungi and triggered their
infectivity on trifoliate orange seedlings. Extracts of vari-
ous marine brown algae [Laminaria japonica Areschoug
and Undaria pinnatifida (Harvey) Suringar] could be used
as an AM fungus growth promoter (Kuwada and others
2006). Kuwada and others (1999) previously showed that
methanol extracts of brown algae fractionated by flash
chromatography promoted in vitro AM hyphal growth as
well as improved root colonization by AM fungi on trifo-
liate orange, Poncirus trifoliate (Linn.) Raf., seedlings.
Indigenous AM fungi demonstrated a 27% improvement in
root colonization, while spore number was increased about
21% over the controls when liquid fertilizer containing
tangle (L. japonica) extracts was applied via a sprinkler
system in a citrus orchard (Kuwada and others 2000).
Kuwada and others (2006) reported that organic fractions
(25% MeOH eluates) of red and green algae considerably
improved in vitro hyphal growth of AM fungi. Their results
showed that application of the 25% MeOH eluates of red
and green algal extracts to roots of papaya (Carica papaya
Linn.) and passion fruit (Passiflora edulis Sims.) improved
mycorrhizal development more than the control treatment.
Kuwada and others (2006) implied that both red and green
algae have AM stimulatory compounds which play a part
in mycorrhizal development in higher plants.
Limited research has been conducted on the effects of
seaweed extracts on other beneficial AM fungi.
Effect on Plant Growth and Health
Root Development and Mineral Absorption
Seaweed products promote root growth and development
(Metting and others 1990; Jeannin and others 1991). The
root-growth stimulatory effect was more pronounced when
extracts were applied at an early growth stage in maize, and
the response was similar to that of auxin, an important root-
growth-promoting hormone (Jeannin and others 1991).
SWC applications reduce transplant shock in seedlings of
marigold, cabbage (Aldworth and van Staden 1987), and
tomato (Crouch and van Staden 1992) by increasing root
size and vigor. SWC treatment enhanced both root:shoot
ratios and biomass accumulation in tomato seedlings by
stimulating root growth (Crouch and van Staden 1992).
Similarly, wheat plants treated with SWC Kelpak
(Table 3) exhibited an increase in root:shoot dry mass
ratio, indicating that the components in the seaweed had a
considerable effect on root development (Nelson and van
Staden 1986). This stimulatory activity was lost on ashing,
suggesting that the active principles in the seaweed extract
were organic in nature (Finnie and van Staden 1985). The
root-growth-promoting activity was observed when the
seaweed extracts were applied either to the roots or as a
foliar spray (Biddington and Dearman 1983; Finnie and
van Staden 1985). The concentration of kelp extract is a
critical factor in its effectiveness as Finnie and van Staden
(1985) showed for tomato plants in which high concen-
trations (1:100 seaweed extract:water) inhibited root
growth but stimulatory effects were found at a lower
concentration (1:600). Biostimulants in general are capable
of affecting root development by both improving lateral
root formation (Atzmon and van Staden 1994; Vernieri and
others 2005) and increasing total volume of the root system
(Thompson 2004; Sla
`vik 2005; Mancuso and others 2006).
An improved root system could be influenced by
endogenous auxins as well as other compounds in the
extracts (Crouch and others 1992). Seaweed extracts
improve nutrient uptake by roots (Crouch and others 1990),
resulting in root systems with improved water and nutrient
efficiency, thereby causing enhanced general plant growth
and vigor.
Effect on Shoot Growth and Photosynthesis
Seaweeds and seaweed products enhance plant chlorophyll
content (Blunden and others 1997). Application of a low
concentration of Ascophyllum nodosum extract to soil or on
foliage of tomatoes produced leaves with higher chlorophyll
content than those of untreated controls. This increase in
chlorophyll content was a result of reduction in chlorophyll
degradation, which might be caused in part by betaines in the
seaweed extract (Whapham and others 1993). Glycine
betaine delays the loss of photosynthetic activity by inhib-
iting chlorophyll degradation during storage conditions in
isolated chloroplasts (Genard and others 1991).
In a recent study (Rayorath and others 2008), extracts of
A. nodosum have been shown to affect the root growth of
Arabidopsis at very low concentrations (0.1 g L
-1
),
whereas plant height and number of leaves were affected at
concentrations of 1 g L
-1
. Plants treated with extracts
showed growth enhancement effects over control plants;
for example, plants treated with A. nodosum extract were at
a more advanced developmental stage when compared with
untreated plants and the effect was concentration depen-
dent (Fig. 2; unpublished results).
J Plant Growth Regul (2009) 28:386–399 391
123
Although they may contain different levels of minerals,
biostimulants are unable to provide all the nutrients needed
by a plant in required quantities (Schmidt and others 2003);
however, their main benefit is to improve plant mineral
uptake by the roots (Vernieri and others 2005) and in the
leaves (Mancuso and others 2006).
Effect on Crop Yield
Seaweed concentrate triggers early flowering and fruit set
in a number of crop plants (Abetz and Young 1983;
Featonby-Smith and van Staden 1987; Arthur and others
2003). For example, tomato seedlings treated with SWC set
more flowers earlier than the control plants and this was not
considered to be a stress response (Crouch and van Staden
1992). In many crops yield is associated with the number of
flowers at maturity. As the onset and development of
flowering and the number of flowers produced are linked to
the developmental stage of plants, seaweed extracts prob-
ably encourage flowering by initiating robust plant growth.
Yield increases in seaweed-treated plants are thought to be
associated with the hormonal substances present in the
extracts, especially cytokinins (Featonby-Smith and van
Staden 1983a,b,1984). Cytokinins in vegetative plant
organs are associated with nutrient partitioning, whereas in
reproductive organs, high levels of cytokinins may be
linked with nutrient mobilization. Fruit ripening generally
causes an increase in transport of nutrient resources within
the developing plant (Hutton and van Staden 1984, Adams-
Phillips and others 2004) and the fruits have the capacity to
serve as strong sinks for nutrients (Varga and Bruinsma
1974; Adams-Phillips and others 2004). Photosynthate
distribution could be shifted, perhaps markedly, moving
from vegetative parts (roots, stem, and young leaves) to the
developing fruit, to be utilized in fruit development
(Nooden and Leopold 1978). Fruit treated with seaweed
extracts had higher concentrations of cytokinins compared
to untreated fruit in tomato (Featonby-Smith and van Sta-
den 1984). Cytokinins have been implicated in nutrient
mobilization in vegetative plant organs (Gersani and Kende
1982) as well as reproductive organs (Davey and van
Staden 1978). Such a response indicates that seaweed
extracts are involved either in enhancing the mobilization
of cytokinins from the roots to the developing fruit, or,
more likely, by improving the amount or synthesis of
endogenous fruit cytokinins (Hahn and others 1974).
Higher root cytokinin levels have also been found in sea-
weed extract-treated plants (Featonby-Smith 1984). This
increase in cytokinin availability will eventually result in a
greater supply of cytokinins to the maturing fruit. Devel-
oping fruits and seeds demonstrated increased endogenous
cytokinin levels (Crane 1964; Nitsch 1970; Letham 1994).
It has been reported that the increased cytokinin concen-
tration is associated with translocation of cytokinin from
roots to other plant parts (Stevens and Westwood 1984;
Carlson and others 1987).
Seaweed extract increased fruit yield when sprayed on
tomato plants during the vegetative stage, producing large-
sized fruits (30% increase in fresh fruit weight over the
controls) with superior quality (Crouch and van Staden
1992). The number of flowers and seeds per flower head
increased (as much as 50% over the control) (van Staden
and others 1994) when marigold seedlings were treated
with SWC Kelpak immediately after transplanting (Ald-
worth and van Staden 1987). Application of Maxicrop
enhanced harvestable yield in lettuce, whereas an increase
in the heart size of the florets and curd diameter was
observed in cauliflower (Abetz and Young 1983). Simi-
larly, a substantial increase in yield was achieved in barley
(Featon-Smith and van Staden 1987) and peppers (Arthur
and others 2003) after treatment with Kelpak.
Foliar application of seaweed liquid extract (Kelpak 66)
enhanced bean yield by 24% (Nelson and van Staden
1984). Kelpak 66 also had a similar effect on the yield of
wheat under potassium stress, although its application had
no significant effect on the plants receiving an adequate K
supplement (Beckett and van Staden 1989). Norrie and
Keathley (2006) have reported that A. nodosum extracts
showed positive effects on the yield of ‘Thompson seed-
less’ grape (Vitis vinifera L.) consistently over a 3-year
period. They observed that the A. nodosum-treated plants
always outperformed (in terms of berries per bunch, berry
size, berry weight, rachis length, and the number of pri-
mary bunches per plant) the controls maintained under the
regular crop management program, and resulted in
improved fruit size (13% increase), weight (39% increase),
and yields (60.4% increase over the control).
Vegetative Propagation
Seaweed products are exploited in conventional vegetative
propagation in many crop species (Crouch and van Staden
1991; Atzmon and van Staden 1994; Kowalski and others
1999). It is common practice to apply auxins exogenously
to enhance rooting in cuttings in certain species that are
difficult to root. It has been observed that treating cuttings
Fig. 2 Arabidopsis thaliana plants treated with different A. nodosum
extracts (1 g L
-1
) showed growth enhancement effects over the
control plants 3 weeks after treatment
392 J Plant Growth Regul (2009) 28:386–399
123
of some flowering plants like marigold (Tagetus patula) for
about 18 h with 10% SWC Kelpak increased the number
and dry weight of roots (Crouch and van Staden 1991).
Similarly, Kelpak, when applied at a 1:100 dilution,
increased the number of rooted cuttings and improved the
vigor of the roots in difficult-to-root cuttings of Pinus pinea
(Atzmon and van Staden 1994). In another study, Leclerc
and others (2006) observed that foliar application of
commercial liquid seaweed extract from Ascophyllum
nodosum (Acadian Seaplants Limited), supplemented with
BA and IBA, enhanced the number of propagules (crown
divisions) per plant in the ornamental herbaceous perennial
Hemerocallis sp.
Resistance to Environmental Stresses
Effects of SWCs in Alleviating Abiotic Stress in Crop
Plants
Abiotic stresses such as drought, salinity, and temperature
extremes can reduce the yield of major crops (Wang and
others 2003) and limit agricultural production worldwide.
For example, salinity and drought are becoming wide-
spread in many regions of the world, with an estimated
50% of all arable lands possibly being salinized by 2050
(Flowers and Yeo 1995). Many abiotic factors such as
drought, salinity, and temperature are manifested as
osmotic stress and cause secondary effects like oxidative
stress, leading to an accumulation of reactive oxygen
species (ROS) such as the superoxide anion (O
2
•-
) and
hydrogen peroxide (H
2
O
2
) (Mittler 2002). These are known
to damage DNA, lipids, carbohydrates, and proteins and
also cause aberrant cell signaling (Arora and others 2002).
Seaweed extracts from Ascophyllum nodosum have been
shown to contain betaines, including gamma-aminobutyric
acid betaine, 6-aminovaleric acid betaine, and glycine
betaine (Blunden and others 1986). To test whether the
increased chlorophyll content in leaves caused by seaweed
extract treatment may be due in part to the betaines present
in the extract, the effects of Algifert 25, an alkaline extract
of A. nodosum, were compared with those of a mixture of
known betaine constituents of A. nodosum (Blunden and
others 1997). Blunden and others (1986) used a betaine
mixture in the same concentrations as those present in
the diluted seaweed extract (gamma-aminobutyric
acid betaine, 0.96 mg L
-1
; 6-aminovaleric acid betaine,
0.43 mg L
-1
; glycine betaine, 0.34 mg L
-l
). Results
showed that similar leaf chlorophyll levels were recorded
in both seaweed- and betaine-treated plants. Sixty-three
and 69 days after application of SWC, leaf chlorophyll
contents, as expressed in SPAD (soil-plant analysis
development; Minolta Corporation, Japan) units, were
27.70 and 26.48, respectively, for seaweed extract and
27.30 and 23.60, respectively, for the betaine treatment.
Both treatments resulted in higher chlorophyll levels versus
controls measured on both days. The results imply that the
enhanced leaf chlorophyll content of plants treated with
SWC might depend on betaines present in the extract
(Blunden and others 1997).
Plants sprayed with seaweed extracts also exhibit
enhanced salt and freezing tolerance (Mancuso and others
2006). Commercial formulations of Ascophyllum extracts
(Seasol
) improved freezing tolerance in grapes. Grape-
vines sprayed with Seasol (0.8%) showed a reduction in
leaf osmotic potential, a key indicator of osmotic tolerance.
The treated plants showed an average osmotic potential of
-1.57 MPa after 9 days of seaweed extract treatment,
whereas it was -1.51 MPa in untreated controls (Wilson
2001). Field studies on winter barley (Hordeum vulgare cv
Igri) have shown that application of seaweed extract
(Maxicrop) improves winter hardiness and increases frost
resistance (Burchett and others 1998).
Taken collectively, these studies suggest that seaweed
products elicit abiotic stress tolerance in plants and that the
bioactive substances derived from seaweeds impart stress
tolerance and enhance plant performance. The chemistry of
bioactive compounds in the seaweed and the physiologic
mechanism of action of the compounds that impart this
tolerance are largely unknown. However, a number of
reports suggest that the beneficial antistress effects of
seaweed extracts may be related to cytokinin activity. For
example, Zhang and Ervin (2004) conducted experiments
to confirm the action of seaweed extracts (Ascophyllum
nodosum) on drought tolerance in creeping bentgrass.
Drought-stressed plants treated with a combination of
humic acid and seaweed extract had root mass enhanced by
21–68%, foliar tocopherol by 110%, and endogenous
zeatin riboside (ZR) by 38%. A systematic analysis of
cytokinins, namely, ZR and isopentenyl adenosine (iPA),
was then performed on A. nodosum extract using enzyme-
linked immunosorbent assay (ELISA). Seaweed extract
contained substantial amounts of cytokinins amounting to
66 lgg
-1
as zeatin riboside. Ashing of the seaweed extract
reduced the effectiveness of the treatments suggesting the
organic nature of the bioactive compound (Zhang and Er-
vin 2004). Cytokinins mitigate stress-induced free radicals
by direct scavenging and by preventing reactive oxygen
species (ROS) formation by inhibiting xanthine oxidation
(McKersie and Leshem 1994; Fike and others 2001). It was
hypothesized that seaweed extract-induced heat tolerance
in creeping bent grass might be attributed largely to the
cytokinin components in the seaweed extracts (Ervin and
others 2004; Zhang and Ervin 2008). However, it has also
been reported that Kelpak seems to mediate stress tolerance
by enhancing K
?
uptake, although synthetic
J Plant Growth Regul (2009) 28:386–399 393
123
benzylaminopurine (BA), at a similar concentration to
natural cytokinin present in Kelpak, showed no effect on
yield, irrespective of the K
?
supply. Hence, the beneficial
effects of seaweed extract against abiotic stress could also
be partly elicited by bioactive chemicals other than cyto-
kinin (Beckett and van Staden 1989).
Reactive oxygen species (ROS) are a common factor in
many abiotic stresses such as salinity, ozone exposure, UV
irradiation, temperature extremes, and drought (Hodges
2001). Application of an A. nodosum extract (Tasco
)to
unstressed turf grasses increased the activity of the anti-
oxidant enzyme superoxide dismutase (SOD), which
scavenges superoxide (Fike and others 2001). In another
study, tall fescue (Festuca arundinacea) treated with 0, 1.7,
or 3.4 kg ha
_1
of A. nodosum extract exhibited increased
SOD activity in all 3 years of the study by an average of
approximately 30% (Zhang 1997). Similarly, Ayad (1998)
reported an increase in SOD, glutathione reductase (GR),
and ascorbate peroxidase (AsPX) activities in genetically
similar endophyte-infected and endophyte-free tall fescue
in response to 3.4 kg Tasco ha
-1
. Thus, the primary effect
of Tasco application to tall fescue in these experiments
seems to be through an increase in antioxidant capacity
(Fike and others 2001).
Effect of SWC in Alleviating Biotic Stress
Seaweed extracts have been shown to enhance plant
defense against pest and diseases (Allen and others 2001).
Besides influencing the physiology and metabolism of
plants, seaweed products promote plant health by affecting
the rhizosphere microbial community.
Nematodes Seaweed extracts were found to have an
impact on the population of nematodes in the soil (Wu and
others 1997). Plants treated with seaweed extracts caused a
reduction in nematode infestation (Featonby-Smith and van
Staden 1983a; Wu and others 1997). Root knot nematode
infestation in tomato was reduced in soil amended with
commercial seaweed extracts from Ecklonia maxima (Feat-
onby-Smith and van Staden 1983a; Crouch and van Staden
1993b). Interestingly, seaweed extract treatment did not
affect the nematode population in the rhizosphere (Featonby-
Smith and van Staden 1983a) and did not show a direct
nematicidal effect. Taken together, these results suggest that
seaweed extract imparts nematode resistance possibly by
altering the auxin:cytokinin ratio in the plant. An in vitro
experiment in which excised maize roots were treated with
seaweed extract showed reduction in the reproduction of the
nematode Pratylenchus zeae by 47–63%. However, in a pot
experiment, the reproduction of P. zeae was not influenced
by seaweed extracts (De Waele and others 1988).
Fungal and bacterial pathogens Marine algae can serve
as an important source of plant defense elicitors (Cluzet and
others 2004). Plants protect themselves against pathogen
invasion by the perception of signal molecules called elici-
tors which include a wide variety of molecules such as oligo-
and polysaccharides, peptides, proteins, and lipids, often
found in the cell wall of attacking pathogens (Boller 1995;
Co
ˆte
´and others 1998). A variety of polysaccharides present
in algal extracts include effective elicitors of plant defense
against plant diseases (Kloareg and Quatrano 1988).
Although red algae typically contain agars and carrageenans
in their cell walls, extracts of brown algae contain alginates,
laminarans, sulfated fucans, and other complex mucilages,
and green algae (e.g., Ulva spp.) contain mucilages com-
posed of units such as rhamnose, uronic acid, and xylose
(Cluzet and others 2004). Laminaran, a linear b-(1,3)-glu-
can, and sulfated fucans from brown algae elicit multiple
defense responses in alfalfa and tobacco (Kobayashi and
others 1993; Klarzynski and others 2000,2003). Similarly,
carrageenans, a family of sulfated linear galactans, are
effective elicitors of defense in tobacco plants (Mercier and
others 2001). Foliar sprays of A. nodosum extract reduced
Phytophthora capsici infection in Capsicum and Plasmo-
para viticola in grape (Lizzy and others 1998). Soil appli-
cation of liquid seaweed extracts to cabbage stimulated the
growth and activity of microbes that were antagonistic to
Pythium ultimum, a serious fungal pathogen that causes
damping-off disease of seedlings (Dixon and Walsh 2002).
Seaweeds are a rich source of antioxidant polyphenols with
bactericidal properties (Zhang and others 2006). The
application of A. nodosum extract and humic acid to bent-
grass (Agrostis stolonifera) increased SOD activity, which
in turn significantly decreased dollar spot disease caused by
Sclerotinia homoeocarpa.
A study using extracts of Ulva spp. against Colletotri-
chum trifolii in Medicago truncatula showed disease
resistance without the elicitation of necrotic lesions (Cluzet
and others 2004). Ulva extract elicited the expression of the
PR-10 gene. The PR-10 gene belongs to the group of
pathogenesis-related genes (PR) important for active
defense against diseases following pathogen attack (van
Loon and others 2006). Treatment of alfalfa with the algal
extracts prior to pathogen challenge resulted in an
increased resistance to Colletotrichum. cDNA array
revealed that the algal extract caused upregulation of 152
genes, mostly plant defense genes such as those involved in
phytoalexin, PR proteins, cell wall proteins, and oxylipin
pathways (Cluzet and others 2004).
Bacterial quorum sensing and effect of seaweed on
quorum sensing Quorum sensing (QS) is a communication
mechanism used by bacterial populations that are depen-
dent on cell density which, in turn, triggers and controls
gene expression that regulates various physiologic func-
tions and responses (Brelles-Marino and Bedmar 2001;
Winzer and Williams 2001; Dong and Zhang 2005). This
394 J Plant Growth Regul (2009) 28:386–399
123
response is mediated by low-molecular-weight signal
molecules called acylated-homoserine lactones (acyl-
HSL).
The virulence of pathogenic bacteria is under the control
of the QS system. Agents that affect the QS system can
potentially alter pathogenicity. The marine red alga Delisea
pulchra synthesizes halogenated furanones and enones that
are homologous to acyl-HSL. They bind to the LuxR in the
acyl-HSL binding site and prevent the binding of acyl-HSL
autoinducers, thereby inhibiting the process of QS. These
furanones in nature seem to interfere with QS in marine
bacteria such as Serratia liquefaciens,Vibrio fischeri, and
Vibrio harveyi (Rasmussen and others 2000; Manefield and
others 2002).
Other pests Aphids and other sap-feeding insects gen-
erally avoid plants treated with seaweed extracts (Ste-
phenson 1966; Hankins and Hockey 1990). Hydrolyzed
seaweed extracts sprayed onto apple trees reduced red
spider mite populations (Stephenson 1966), and 2–3 years
of seaweed extract application resulted in a level of control
similar to that of acaricides (Stephenson 1966). Futher-
more, it was observed that the use of Maxicrop on straw-
berry plants (Fragaria sp.) greatly reduced the two-spotted
red spider mite (Tetranychus urticae) population (Hankins
and Hockey 1990). It has been suggested that seaweed
extracts might contain chelated metals that have been
shown to reduce the population of red spider mites (Ter-
riere and Rajadhyaksha 1964; Abetz 1980).
Conclusions and Future Perspectives
Seaweeds and seaweed products are increasingly used in
crop production. However, the mechanism(s) of actions of
seaweed extract-elicited physiological responses are lar-
gely unknown. As genomes of a number of plants are now
completely sequenced or nearing completion, it is possible
to look at the effects of seaweed extracts and components
of the seaweeds on the whole genome/transcriptome of
plants to better understand the mechanisms of action of
seaweed-induced growth response and stress alleviation.
For example, the use of model plants Arabidopsis thaliana
and Medicago truncatula could potentially unravel the
molecular mechanism(s) of action of seaweed extracts
(Rayorath and others 2008). The recent challenges to food
production due to the increasing occurrence of biotic and
abiotic stresses is likely due to climate change and will
further reduce yields and/or will have an impact on crops in
the 21st century (IPCC 2007). Therefore, research into
developing sustainable methods to alleviate these stresses
should be a priority. Recent studies have shown that sea-
weed extracts protect plants against a number of biotic and
abiotic stresses and offers potential for field application.
Further, seaweed extracts are considered an organic farm
input as they are environmentally benign and safe for the
health of animals and humans.
References
Abetz P (1980) Seaweed extracts: have they a place in Australian
agriculture or horticulture? J Austral Inst Agric Sci 46:23–29
Abetz P, Young CL (1983) The effect of seaweed extract sprays
derived from Ascophyllum nodosum on lettuce and cauliflower
crops. Bot Mar 26:487–492
Adams-Phillips L, Barry C, Giovannoni J (2004) Signal transduction
systems regulating fruit ripening. Trends Plant Sci 9:331–338
Akula A, Akula C, Bateson M (2000) Betaine: a novel candidate for
rapid induction of somatic embryogenesis in tea (Camellia
sinensis [L.] O. Kuntze). Plant Growth Regul 30:241–246
Aldworth SJ, van Staden J (1987) The effect of seaweed concentrate
on seedling transplants. S Afr J Bot 53:187–189
Allen VG, Pond KR, Saker KE, Fontenot JP, Bagley CP, Ivy RL, Evans
RR, Schmidt RE, Fike JH, Zhang X, Ayad JY, Brown CP, Miller
MF, Montgomery JL, Mahan J, Wester DB, Melton C (2001)
Tasco: influence of a brown seaweed on antioxidants in forages
and livestock—a review. J Anim Sci 79(E Suppl):E21–E31
Angstwurm K, Weber JR, Segert A, Bu
¨rger W, Weih M, Freyer D,
Einha
¨upl KM, Dirnagl U (1995) Fucoidin, a polysaccharide
inhibiting leukocyte rolling, attenuates inflammatory responses
in experimental pneumococcal meningitis in rats. Neurosci Lett
191:1–4
Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and
antioxidative systems in plants. Curr Sci 82:1227–1238
Arthur GD, Stirk WA, van Staden J (2003) Effect of a seaweed
concentrate on the growth and yield of three varieties of
Capsicum annuum. S Afr J Bot 69:207–211
Atzmon N, van Staden J (1994) The effect of seaweed concentrate on
the growth of Pinus pinea seedlings. New For 8:279–288
Ayad JY (1998) The effect of seaweed extract (Ascophyllum
nodosum) extract on antioxidant activities and drought tolerance
of tall fescue (Festuca arundinacea Schreb.). Ph.D. dissertation,
Texas Tech University, Lubbock
Bartel B (1997) Auxin biosynthesis. Annu Rev Plant Physiol Plant
Mol Biol 48:51–66
Beckett RP, van Staden J (1989) The effect of seaweed concentrate on
the growth and yield of potassium stressed wheat. Plant Soil
116:29–36
Biddington NL, Dearman AS (1983) The involvement of the root
apex and cytokinins in the control of lateral root emergence in
lettuce seedlings. Plant Growth Regul 1:183–193
Blunden G (1972) The effects of aqueous seaweed extract as a
fertilizer additive. Proc Int Seaweed Symp 7:584–589
Blunden G (1991) Agricultural uses of seaweeds and seaweed
extracts. In: Guiry MD, Blunden G (eds) Seaweed resources in
Europe: uses and potential. Wiley, Chicester, pp 65–81
Blunden G, Gordon SM (1986) Betaines and their sulphono analogues
in marine algae. In: Round FE, Chapman DJ (eds) Progress in
phycological research, vol 4. Biopress Ltd, Bristol, pp 39–80
Blunden G, Cripps AL, Gordon SM, Mason TG, Turner CH (1986)
The characterisation and quantitative estimation of betaines in
commercial seaweed extracts. Bot Mar 29:155–160
Blunden G, Jenkins T, Liu Y (1997) Enhanced leaf chlorophyll levels
in plants treated with seaweed extract. J Appl Phycol 8:535–543
Boller T (1995) Chemoperception of microbial signals in plant cells.
Annu Rev Plant Physiol Plant Mol Biol 46:189–214
J Plant Growth Regul (2009) 28:386–399 395
123
Brain KR, Chalopin MC, Turner TD, Blunden G, Wildgoose PB
(1973) Cytokinin activity of commercial aqueous seaweed
extract. Plant Sci Lett 1:241–245
Brelles-Marin
˜o G, Bedmar EJ (2001) Detection, purification and
characterisation of quorum-sensing signal molecules in plant-
associated bacteria. J Biotechnol 91:197–209
Buggeln RG, Craigie JS (1971) Evaluation of evidence for the
presence of indole-3-acetic acid in marine algae. Planta 97:
173–178
Burchett S, Fuller MP Jellings AJ (1998) Application of seaweed
extract improves winter hardiness of winter barley cv Igri. The
Society for Experimental Biology, Annual Meeting, The York
University, March 22–27, 1998. Experimental Biology Online.
Springer ISSN 1430-34-8
Cardozo KHM, Guaratini T, Barros MP, Falca
˜o VR, Tonon AP,
Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P,
Pinto E (2007) Metabolites from algae with economical impact.
Comp Biochem Physiol C Toxicol Pharmacol 146:60–78
Carlson DR, Dyer DJ, Cotterman CD, Durley RC (1987) The
physiological basis for cytokinin induced increases in pod set in
IX93–100 soybeans. Plant Physiol 84:233–239
Chan LW, Heng PWS (2002) Effects of aldehydes and methods of
cross-linking on properties of calcium alginate microspheres
prepared by emulsification. Biomaterials 23:1319–1326
Chevolot L, Foucault A, Kervarec N, Sinquin C, Fischer AM,
Boisson-Vidal C (1999) Further data on the structure of brown
seaweed fucans: relationships with anticoagulant activity. Car-
bohydrate Res 319:154–165
Chevolot L, Mulloy B, Ratiskol J, Foucault A, Colliec-Jouault S
(2001) A disaccharide repeat unit is the major structure in
fucoidans from two species of brown algae. Carbohydrate Res
330:529–535
Chizhov AO, Dell A, Morris HR, Reason AJ, Haslam SM, McDowell
RA (1998) Structural analysis of laminaran by MALDI and FAB
mass spectrometry. Carbohydrate Res 310:203–210
Cluzet S, Torregrosa C, Jacquet C, Lafitte C, Fournier J, Mercier L,
Salamagne S, Briand X, Esquerre
´-Tugaye
´MT, Dumas B (2004)
Gene expression profiling and protection of Medicago truncatula
against a fungal infection in response to an elicitor from the
green alga Ulva spp. Plant Cell Environ 27:917–928
Co
ˆte
´F, Ham KS, Hahn MG, Bergmann CW, Biswas Das (eds) (1998)
Oligosaccharide elicitors in host-pathogen interactions: genera-
tion, perception, and signal transduction. In: Subcellular bio-
chemistry: plant–microbe interactions, vol 29. Plenum Press,
New York, pp 385–432
Craigie JS (1990) Cell walls. In: Cole KM, Sheath RG (eds) Biology
of the red algae. Cambridge University Press, Cambridge, pp
221–257
Crane JC (1964) Growth substances in fruit setting and development.
Annu Rev Plant Physiol 15:303–326
Crouch IJ, van Staden J (1991) Evidence for rooting factors in a
seaweed concentrate prepared from Ecklonia maxima. J Plant
Physiol 137:319–322
Crouch IJ, van Staden J (1992) Effect of seaweed concentrate on the
establishment and yield of greenhouse tomato plants. J Appl
Phycol 4:291–296
Crouch IJ, van Staden J (1993a) Evidence for the presence of plant
growth regulators in commercial seaweed products. Plant
Growth Regul 13:21–29
Crouch IJ, van Staden J (1993b) Effect of seaweed concentrate from
Ecklonia maxima (Osbeck) Papenfuss on Meloidogyne incognita
infestation on tomato. J Appl Phycol 5:37–43
Crouch IJ, Beckett RP, van Staden J (1990) Effect of seaweed
concentrate on the growth and mineral nutrition of nutrient
stressed lettuce. J Appl Phycol 2:269–272
Crouch IJ, Smith MT, van Staden J, Lewis MJ, Hoad GV (1992)
Identification of auxins in a commercial seaweed concentrates. J
Plant Physiol 139:590–594
Daniel R, Berteau O, Chevolot L, Varenne A, Gareil P, Goasdoue N
(2001) Regioselective desulfation of sulfated L-fucopyranoside
by a new sulfoesterase from marine mollusc Pecten maximus:
application to the structural study of algal fucoidan (Ascophyl-
lum nodosum). Eur J Biochem 268:5617–5628
Davey JE, van Staden J (1978) Cytokinin activity in Lupinus albus.
III. Distribution in fruits. Physiol Plant 43:87–93
Davis RF, Wauchope RD, Johnson AW, Burgoa B, Pepperman AB
(1996) Release of fenamiphos, atrazine, and alachlor into flowing
water from granules and spray deposits of conventional and
controlled-release formulations. J Agric Food Chem 44:2900–2907
De Waele D, McDonald AH, De Waele E (1988) Influence of
seaweed concentrate on the reproduction of Pratylenchus zeae
(Nematoda) on maize. Nematologica 34:71–77
Dixon GR, Walsh UF (2002) Suppressing Pythium ultimum induced
damping-off in cabbage seedlings by biostimulation with
proprietary liquid seaweed extracts managing soil-borne patho-
gens: a sound rhizosphere to improve productivity in intensive
horticultural systems. Proceedings of the XXVIth International
Horticultural Congress, Toronto, Canada, 11–17 August 2002,
pp 11–17
Dong Y, Zhang L (2005) Quorum sensing and quorum-quenching
enzymes. J Microbiol 43(Suppl):101–109
Duarte MER, Cardoso MA, Noseda MD, Cerezo AS (2001) Structural
studies on fucoidan from brown seaweed Sagassum stenophyl-
lum. Carbohydrate Res 333:281–293
Durand N, Briand X, Meyer C (2003) The effect of marine bioactive
substances (NPRO) and exogenous cytokinins on nitrate reduc-
tase activity in Arabidopsis thaliana. Physiol Plant 119:489–493
Ervin EH, Zhang X, Fike J (2004) Alleviating ultraviolet radiation
damage on Poa pratensis: II. Hormone and hormone containing
substance treatments. Hortic Sci 39:1471–1474
Eyras MC, Rostagno CM, Defosse GE (1998) Biological evaluation
of seaweed composting. Comp Sci Util 6:74–81
FAO (2006) Yearbook of fishery statistics, vol 98(1–2). Food and
Agricultural Organisation of the United Nations, Rome
Featonby-Smith BC (1984) Cytokinins in Ecklonia maxima and the
effect of seaweed concentrate on plant growth. Ph.D. thesis,
University of Natal, Pietermaritzburg
Featonby-Smith BC, van Staden J (1983a) The effect of seaweed
concentrate on the growth of tomato plants in nematode-infested
soil. Sci Hortic 20:137–146
Featonby-Smith BC, van Staden J (1983b) The effect of seaweed
concentrate and fertilizer on the growth of Beta vulgaris.Z
Pflanzenphysiol 112:155–162
Featonby-Smith BC, van Staden J (1984) The effect of seaweed
concentrate and fertilizer on growth and the endogenous
cytokinin content of Phaseolus vulgaris. S Afr J Bot 3:375–379
Featonby-Smith BC, van Staden J (1987) Effects of seaweed
concentrate on grain yield in barley. S Afr J Bot 53:125–128
Fike JH, Allen VG, Schmidt RE, Zhang X, Fontenot JP, Bagley CP,
Ivy RL, Evans RR, Coelho RW, Wester DB (2001) Tasco-
Forage: I. Influence of a seaweed extract on antioxidant activity
in tall fescue and in ruminants. J Anim Sci 79:1011–1021
Finnie JF, van Staden J (1985) Effect of seaweed concentrate and
applied hormones on in vitro cultured tomato roots. J Plant
Physiol 120:215–222
Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop
plants—where next? Aust J Plant Physiol 22:875–884
Fornes F, Sa
`nchez-Perales M, Guadiola JL (2002) Effect of a seaweed
extract on the productivity of ‘de Nules’ clementine mandarin
and navelina orange. Bot Mar 45:486–489
396 J Plant Growth Regul (2009) 28:386–399
123
Fritig B, Heitz T, Legrand M (1998) Antimicrobial proteins in
induced plant defense. Curr Opin Immunol 10:16–22
Gandhiyappan K, Perumal P (2001) Growth promoting effect of
seaweed liquid fertilizer (Enteromorpha intestinalis) on the
sesame crop plant. Seaweed Resource Util 23:23–25
Genard H, Le Saos J, Billard J-P, Tremolieres A, Boucaud J (1991)
Effect of salinity on lipid composition, glycine betaine content
and photosynthetic activity in chloroplasts of Suaeda maritima.
Plant Physiol Biochem 29:421–427
Gersani M, Kende H (1982) Studies on cytokinin-stimulated trans-
location in isolated bean leaves. J Plant Growth Regul 1:161–171
Gonzalez-Pradas E, Fernandez-Perez M, Villafranca-Sanchez M,
Martinez-Lopez F, Flores-Cespedes F (1999) Use of bentonite
and humic acid as modifying agents in alginate-based controlled-
release formulations of imidacloprid. Pest Sci 55:546–552
Govindan M, Hodge JD, Brown KA, Nun
˜ez-Smith M (1993)
Distribution of cholesterol in Caribbean marine algae. Steroids
58:178–180
Hahn H, de Zacks R, Kende H (1974) Cytokinin formation in pea
seeds. Naturwissenschaften 61:170–171
Hamdy AEA, Dawes CJ (1988) Proximate constituents and lipid
chemistry in two species of Sargassum from the west coast
Florida. Bot Mar 31:79–81
Hankins SD, Hockey HP (1990) The effect of a liquid seaweed extract
from Ascophyllum nodosum (Fucales, Phaeophyta) on the two-
spotted red spider mite Tetranychus urticae. Hydrobiologia
204(205):555–559
Hodges DM (2001) Chilling effects on active oxygen species and
their scavenging systems in plants. In: Basra A (ed) Crop
responses and adaptations to temperature stress. Food Products
Press, Binghamton, NY, pp 53–78
Hong DD, Hien HM, Son PN (2007) Seaweeds from Vietnam used
for functional food, medicine and biofertilizer. J Appl Phycol
19:817–826
Hussain A, Boney AD (1969) Isolation of kinin-like substances from
Laminaria digitata. Nature 223:504–505
Hussain A, Boney AD (1973) Hydrophilic growth inhibitors from
Laminaria and Ascophyllum. New Phytol 72:403–410
Hutton MJ, van Staden J (1984) Transport and metabolism of labeled
zeatin applied to the stems of Phaseolus vulgaris at different
stages of development. Z Pflanzenphysiol 114:331–339
IPCC (Intergovernmental Panel on Climate Change) (2007) Summary
for policymakers. In: Parry ML, Canziani OF, Palutikot JP, van
der Linden PJ, Hanson CE (eds) Climate change 2007: impacts,
adaptation and vulnerability. Contribution of Working Group II to
the Fourth Assessment Report of the Intergovernmental Panel on
Climate Change. Cambridge University Press, Cambridge, UK
Ishii T, Aikawa J, Kirino S, Kitabayashi H, Matsumoto I, Kadoya K
(2000) Effects of alginate oligosaccharide and polyamines on
hyphal growth of vesicular-arbuscular mycorrhizal fungi and
their infectivity of citrus roots. In: Proceedings of the 9th
International Society of Citriculture Congress, Orlando, FL, 3–7
December 2000, pp 1030–1032
Jeannin I, Lescure JC, Morot-Gaudry JF (1991) The effects of
aqueous seaweed sprays on the growth of maize. Bot Mar
34:469–473
Kim MS, Park GD, Jun SW, Lee S, Park JS, Hwang SJ (2005)
Controlled release tamsulosin hydrochloride from alginate beads
with waxy materials. J Pharm Pharmacol 57:1521–1528
Kingman AR, Moore J (1982) Isolation, purification and quantifica-
tion of several growth regulating substances in Ascophyllum
nodosum (Phaeophyta). Bot Mar 25:149–153
Klarzynski O, Plesse B, Joubert JM, Yvin JC, Kopp M, Kloareg B,
Fritig B (2000) Linear beta-1, 3 glucans are elicitors of defense
responses in tobacco. Plant Physiol 124:1027–1038
Klarzynski O, Descamps V, Plesse B, Jean-Claude Yvin, Kloareg B,
Fritig B (2003) Sulfated fucan oligosaccharides elicit defense
responses in tobacco and local and systemic resistance against
tobacco mosaic virus. Mol Plant Microbe Interact 16:115–122
Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine
algae and ecophysiological functions of the matrix polysaccha-
rides. Oceanogr Mar Biol Annu Rev 26:259–315
Kobayashi A, Tai A, Kanzaki H, Kawazu K (1993) Elicitor-active
oligosaccharides from algal laminaran stimulate the production
of antifungal compounds in alfalfa. Z Naturforsch 48c:575–579
Kowalski B, Jager AK, van Staden J (1999) The effect of a seaweed
concentrate on the in vitro growth and acclimatization of potato
plantlets. Potato Res 42:131–139
Kumbar SG, Dave AM, Aminabhavi TM (2003) Release kinetics and
diffusion coefficients of solid and liquid pesticides through
interpenetrating polymer network beads of polyacrylamide-g-
guar gum with sodium alginate. J Appl Polym Sci 90:451–457
Kuwada K, Ishii T, Matsushita I, Matsumoto I, Kadoya K (1999)
Effect of seaweed extracts on hyphal growth of vesicular–
arbuscular mycorrhizal fungi and their infectivity on trifoliate
orange roots. J Jpn Soc Hortic Sci 68:321–326
Kuwada K, Utamura M, Matsushita I, Ishii T (2000) Effect of tangle
stock ground extracts on in vitro hyphal growth of vesicular-
arbuscular mycorrhizal fungi and their in vivo infections of
citrus roots. In: Proceedings of the 9th International Society of
Citriculture Congress, Orlando, FL, 3–7 December 2000, pp
1034–1037
Kuwada K, Wamocho LS, Utamura M, Matsushita I, Ishii T (2006)
Effect of red and green algal extracts on hyphal growth of
arbuscular fungi, and on mycorrhizal development and growth of
papaya and passionfruit. Agron J 98:1340–1344
Lane CE, Mayes C, Druehl LD, Saunders GW (2006) A multi-gene
molecular investigation of the kelp (Laminariales, Phaeophy-
ceae) supports substantial taxonomic re-organization. J Phycol
42:493–512
Leclerc M, Caldwell CD, Lada RR, Norrie J (2006) Effect of plant
growth regulators on propagule formation in Hemerocallis spp.
and Hosta spp. Hortic Sci 41:651–653
Letham DS (1994) Cytokinins as phytohormones: sites of biosynthe-
sis, translocation, and function of translocated cytokinins. In:
Mok DWS, Mok MC (eds) Cytokinins: chemistry, activity and
functions. CRC Press, Boca Raton, FL, pp 57–80
Lewis JG, Stanley NF, Guist GG (1988) Commercial production and
applications of algal hydrocolloids. In: Lembi CA, Waaland JR
(eds) Algae and human affairs. Cambridge University Press,
Cambridge, UK, pp 205–236
Lizzi Y, Coulomb C, Polian C, Coulomb PJ, Coulomb PO (1998)
Seaweed and mildew: what does the future hold? Laboratory
tests have produced encouraging results [L’algue face au
mildiou: quel avenir? Des resultats de laboratoire tres encoura-
geants]. Phytoma 508:29–30
Mancuso S, Azzarello E, Mugnai S, Briand X (2006) Marine
bioactive substances (IPA extract) improve ion fluxes and water
stress tolerance in potted Vitis vinifera plants. Adv Hortic Sci
20:156–161
Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P,
Kjelleberg S, Givskov M (2002) Halogenated furanones inhibit
quorum sensing through accelerated LuxR turnover. Microbiol-
ogy 148:1119–1127
Marais MF, Joseleau JP (2001) A fucoidan fraction from Ascophyllum
nodosum. Carbohydrate Res 336:155–159
Mauray S, Sternberg C, Theveniaux J, Millet J, Sinquin C, Tapon-
Bretaudie
`re J, Fischer AM (1995) Venous antithrombotic and
anticoagulant activities of a fucoidan Fraction. Thromb Haemost
74:1280–1285
J Plant Growth Regul (2009) 28:386–399 397
123
McClure MO, Moore JP, Blanc DF, Scotting P, Cook GMW, Keynes
RJ, Weber JN, Davies D, Weiss RA (1992) Investigations into
the mechanism by which sulfated polysaccharides inhibit HIV
infection in vitro. AIDS Res Hum Retroviruses 8:19–26
McKersie BD, Leshem YY (1994) Stress and stress coping in
cultivated plants. Kluwer Academic Publishers, Dordrecht
Mercier L, Lafitte C, Borderies G, Briand X, Esquerre
´-Tugaye
´MT,
Fournier J (2001) The algal polysaccharide carrageenans can act
as an elicitor of plant defence. New Phytol 149:43–51
Metting B, Rayburn WR, Reynaud PA (1988) Algae and agriculture.
In: Lembi CA, Waaland JR (eds) Algae and human affairs.
Cambridge University Press, Cambridge, UK, pp 335–370
Metting B, Zimmerman WJ, Crouch IJ, van Staden J (1990)
Agronomic uses of seaweed and microalgae. In: Akatsuka I
(ed) Introduction to applied phycology. SPB Academic Publish-
ing, The Hague, Netherlands, pp 269–627
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance.
Trends Plant Sci 7:405–410
Mooney PA, van Staden J (1986) Algae and cytokinins. J Plant
Physiol 123:1–21
Moore KK (2004) Using seaweed compost to grow bedding plants.
BioCycle 45:43–44
Nabil S, Cosson J (1996) Seasonal variations in sterol composition of
Delesseria sanguinea (Ceramiales, Rhodophyta). Hydrobiologia
326(327):511–514
Naidu BP, Jones GP, Paleg LG, Poljakoff-Mayber A (1987) Proline
analogues in Melaleuca species: response of Melaleuca lanceo-
lata and M. uncinata to water stress and salinity. Aust J Plant
Physiol 14:669–677
Nelson TE, Lewis BA (1973) Separation and characterization of the
soluble and insoluble components of insoluble laminaran.
Carbohydrate Res 33:63–74
Nelson WR, van Staden J (1984) The effect of seaweed concentrate
on wheat culms. J Plant Physiol 115:433–437
Nelson WR, van Staden J (1986) Effect of seaweed concentrate on the
growth of wheat. S Afr J Sci 82:199–200
Nitsch JP (1970) Hormonal factors in growth and development. In:
Hulme AC (ed) The biochemistry of fruits and their products, vol
1. Academic Press, London, pp 427–472
Nooden LD, Leopold AC (1978) Phytohormones and the endogenous
regulation of senescence and abscission. In: Letham DS,
Goodwin PB, Higgins TJ (eds) Phytohormones and Related
Compounds: A Comprehensive Treatise. Elsevier/Holland,
Amsterdam, pp 329–369
Norrie J, Keathley JP (2006) Benefits of Ascophyllum nodosum
marine-plant extract applications to ‘Thompson seedless’ grape
production. (Proceedings of the Xth International Symposium on
Plant Bioregulators in Fruit Production, 2005). Acta Hortic
727:243–247
Ordog V, Stirk WA, van Staden J, Novak O, Strnad M (2004)
Endogenous cytokinins in the three genera of microalgae from
the Chlorophyta. J Phycol 40:88–95
Painter TJ (1983) Algal polysaccharides. In: Aspinall GO (ed) The
polysaccharides. Academic Press, New York, pp 195–285
Ragan MA, Chapman DJ (1978) A biochemical phylogeny of the
protists. Academic Press, New York 317 pp
Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U,
Christophersen C, Steinberg P, Kjelleberg S, Givskov M (2000)
How Delisea pulchra furanones affect quorum sensing and
swarming motility in Serratia liquefaciens MG1. Microbiology
146:3237–3244
Rayorath P, Narayanan JM, Farid A, Khan W, Palanisamy R, Hankins
S, Critchley AT, Prithiviraj B (2008) Rapid bioassays to evaluate
the plant growth promoting activity of Ascophyllum nodosum
(L.) Le Jol. using a model plant, Arabidopsis thaliana (L.)
Heynh. J Appl Phycol 20:423–429
Reitz SR, Trumble JT (1996) Effects of cytokinin-containing seaweed
extract on Phaseolus lunatus L.: influence of nutrient availability
and apex removal. Bot Mar 39:33–38
Rioux LE, Turgeon SL, Beaulieu M (2007) Characterization of
polysaccharides extracted from brown seaweeds. Carbohydrate
Polym 69:530–537
Schmidt RE, Ervin EH, Zhang X (2003) Questions and answers about
biostimulants. Golf Course Manage 71:91–94
Siegel BZ, Siegel SM (1973) The chemical composition of algal cell
walls. In: Laskin AI, Lechevalier H (eds) Critical reviews in
microbiology. CRC Press, Cleveland, OK, pp 1–26
Skjak-Braek G, Grasdalen H, Draget KI, Smidsrod O (1989)
Inhomogeneous calcium alginate beads. In: Crescenzi V, Dea
ICM, Paoletti S, Stivala SS, Sutherland IW (eds) Biomedical and
biotechnological advances in industrial polysacharides. Gordon
and Breach, New York, pp 345–363
Sla
`vik M (2005) Production of Norway spruce (Picea abies) seedlings
on substrate mixes using growth stimulants. J For Sci 51:15–23
Stephenson WM (1966) The effect of hydrolyzed seaweed on certain
plant pests and diseases. Proc Int Seaweed Symp 5:405–415
Stevens GA, Westwood MN (1984) Fruit set and cytokinin-like
activity in the xylem sap of sweet cherry (Prunus avium)as
affected by rootstock. Physiol Plant 61:464–468
Stirk WA, van Staden J (1997) Isolation and identification of
cytokinins in a new commercial seaweed product made from
Fucus serratus L. J Appl Phycol 9:327–330
Stirk WA, Novak MS, van Staden J (2003) Cytokinins in macroalgae.
Plant Growth Regul 41:13–24
Stirk WA, Arthur GD, Lourens AF, Novak O, Strnad M, van Staden J
(2004) Changes in cytokinin and auxin concentrations in
seaweed concentrateswhen stored at an elevated temperature. J
Appl Phycol 16:31–39
Tay SA, Macleod JK, Palni LM, Letham DS (1985) Detection of
cytokinins in a seaweed extract. Phytochemistry 24:2611–2614
Temple WD, Bomke AA (1988) Effects of kelp (Macrocystis
integrifolia) on soil chemical properties and crop responses.
Plant Soil 105:213–222
Terriere LC, Rajadhyaksha N (1964) Reduced fecundity of the two-
spotted spider mite on metal-chelate treated leaves. J Econ
Entomol 57:95–99
Thompson B (2004) Five years of Irish trials on biostimulants: the
conversion of a skeptic. USDA For Serv Proc 33:72–79
Tietz A, Ruttkowski U, Kohler R, Kasprik W (1989) Further
investigations on the occurrence and the effects of abscisic acid
in algae. Biochem Physiol Pflanzen 184:259–266
Ugarte RA, Sharp G, Moore B (2006) Changes in the brown seaweed
Ascophyllum nodosum (L.) Le Jol. Plant morphology and
biomass produced by cutter rake harvests in southern New
Brunswick, Canada. J Appl Phycol 18:351–359
van Loon LC, van Strien EA (1999) The families of pathogenesis-
related proteins, their activities, and comparative analysis of PR-
1 type proteins. Physiol Mol Plant Pathol 55:85–97
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of the
inducible defense-related proteins in infected plants. Annu Rev
Phytopathol 44:7.1–7.28
van Staden J, Upfold J, Dewes FE (1994) Effect of seaweed
concentrate on growth and development of the marigold Tagetes
patula. J Appl Phycol 6:427–428
Varga A, Bruinsma J (1974) The growth and ripening of tomato fruits
at different levels of endogenous cytokinins. J Hortic Sci
49:135–142
Vernieri P, Borghesi E, Ferrante A, Magnani G (2005) Application of
biostimulants in floating system for improving rocket quality. J
Food Agric Environ 3:86–88
Vollner L (1990) Agrochemical formulations for improved efficacy
and reduced environmental impacts: slow release formulations
398 J Plant Growth Regul (2009) 28:386–399
123
with natural polymers. In: Mansour M (ed) Study and prediction
of pesticides behaviour in soils, plants and aquatic aystems. GSF,
Neuherberg, Germany, pp 136–145
Wachira F, Ogada J (1995) In vitro regeneration of Camellia sinensis
(L.) O. Kuntze by somatic embryogenesis. Plant Cell Rep
14:463–466
Wang Z, Pote J, Huang B (2003) Responses of cytokinins, antioxidant
enzymes, and lipid peroxidation in shoots of creeping bentgrass
to high root-zone temperatures. J Am Soc Hortic Sci 128:648–
655
Whapham CA, Blunden G, Jenkins T, Hankins SD (1993) Signifi-
cance of betaines in the increased chlorophyll content of plants
treated with seaweed extract. J Appl Phycol 5:231–234
Williams DC, Brain KR, Blunden G, Wildgoose PB, Jewers K (1981)
Plant growth regulatory substances in commercial seaweed
extracts. Proc Int Seaweed Symp 8:760–763
Wilson S (2001) Frost management in cool climate vineyards. In:
University of Tasmania Research Report UT 99/1, Grape and
Wine Research & Development Corporation
Winzer K, Williams P (2001) Quorum sensing and the regulation of
virulence gene expression in pathogenic bacteria. Int J Med
Microbiol 291:131–143
Wong TW, Chan LW, Kho SB, Heng PWS (2002) Design of
controlled-release solid dosage forms of alginate and chitosan
using microwave. J Control Release 84:99–114
Wu Y, Jenkins T, Blunden G, von Mende N, Hankins SD (1997)
Suppression of fecundity of the rootknot nematode, Meloidogyne
javanica. in monoxenic cultures of Arabidopsis thaliana treated
with an alkaline extract of Ascophyllum nodosum. J Appl Phycol
10:91–94
Zhang X (1997) Influence of plant growth regulators on turfgrass
growth, antioxidant status, and drought tolerance. Ph.D. disser-
tation, Virginia Polytechnic Institute and State University,
Blacksburg, VA
Zhang X, Ervin EH (2004) Cytokinin-containing seaweed and humic
acid extracts associated with creeping bentgrass leaf cytokinins
and drought resistance. Crop Sci 44:1737–1745
Zhang X, Ervin EH (2008) Impact of seaweed extract-based
cytokinins and zeatin riboside on creeping bentgrass heat
tolerance. Crop Sci 48:364–370
Zhang X, Schmidt RE (1997) The impact of growth regulators on the
a-tocopherol status in water-stressed Poa pratensis L. Int
Turfgrass Res J 8:1364–1373
Zhang W, Yamane H, Chapman DJ (1993) The phyto-hormone
profile of the red alga Porphyra perforata. Bot Mar 36:257–266
Zhang Q, Zhang J, Shen J, Silva A, Dennis DA, Barrow CJ (2006) A
simple 96-well microplate method for estimation of total
polyphenol content in seaweeds. J Appl Phycol 18:445–450
Zvyagintseva TN, Shevchenko NM, Popivnich IB, Isakov VV,
Scobun AS, Sundukova EV (1999) A new procedure for
separation of water-soluble polysaccharides from brown sea-
weeds. Carbohydrate Res 322:32–39
J Plant Growth Regul (2009) 28:386–399 399
123
