Content uploaded by Sanjoy Kumar Das
Author content
All content in this area was uploaded by Sanjoy Kumar Das on Dec 08, 2015
Content may be subject to copyright.
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Int J Pharm Sci Tech (© 2011)
Vol-6, Issue-1, January-June-2011
ISSN: 0975-0525 (Print) REVIEW ARTICLE
ROLES OF FLAVONOIDS IN PLANTS
Amalesh Samanta1*, Gouranga Das1,2, Sanjoy Kumar Das2
1Department of Pharmaceutical Technology, Jadavpur University, Kolkata (Calcutta) 700032, India.
2Institute of Pharmacy, Jalpaiguri, West Bengal, India.
Received:16/02/2011; Accepted: 25/05/2011; Published: 30/06/2011
Address for Correspondence:
Amalesh Samanta*
Department of Pharmaceutical Technology,
Jadavpur University, Kolkata (Calcutta)
700032, India
Tel.:+9133-24146666 (Extn. 2617); Fax:
+9133-24146677
E-mail address: asamanta61@yahoo.co.in
ABSTRACT:
Flavonoids are the low molecular weight polyphenolic secondary metabolic compounds, universally
distributed in green plant kingdom, located in cell vacuoles. Flavonoids play a variety of biological activities
in plants, animals, and bacteria. In plants, flavonoids have long been known to be synthesized in particular
sites and are responsible for color, aroma of flowers, fruit to attract pollinators consequently fruit dispersion;
help in seed, spore germination, growth and development of seedling. Flavonoids protect plants from
different biotic and abiotic stresses and act as unique UV-filter, function as signal molecules, allelopathic
compounds, phytoalexins, detoxifying agents, antimicrobial defensive compounds. Flavonoids have roles
against frost hardiness, drought resistance and may play a functional role in plant heat acclimation and
freezing tolerance. In the present review, our endeavor is to cover wide range of functions of flavonoids in
plant growth, development, propagation and protection against various adverse situations with biosynthetic
path way.
Keywords: Flavonoids, Plant, Polyphenolic compounds, Biosynthetic pathway, Stress.
INTRODUCTION:
Flavonoids are a large subgroup of secondary
metabolites categorized as phenolic compounds,
widely disbursed throughout plants and prokaryotes
(1, 2). More than 6,500 flavonoids have been
identified (3). Flavonoids protect plants against
various biotic and abiotic stresses and exhibit a
diverse spectrum of biological functions and play an
important role in the interaction between the plant
and their environment (4). Flavonoids absorbed the
harmful UV radiation induced cellular damage (5).
Flavonoids are not essential for plant survival;
nevertheless they are bioactive and influence the
transport of the plant hormone, auxin (6). Flavonoids
are responsible for flower colors, protecting the plants
from microbes and insects (7, 8, 9). Dr. Albert Szent-
Gyorgyi in 1936, announced the discovery of a
capillary permeability factor, “vitamin P” isolated by
him and his associates from red pepper and lemon.
At first he believed that “vitamin P” was a single
chemical substance and latter on he realized that
“vitamin P” was a compound of several flavonoids.
During 1946-47, the therapeutic value of “vitamin
P”was questioned. Sokoloff et al. worked on citrus
page-12
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
wastes with the original concept of Dr. Albert Szent-
Gyorgyi and confirmed the vitamin P as a flavonoid
complex (10). Flavonoids have only limited skeletal
varieties (Figure 1) and the diversity is due to the
substitution pattern (3). Flavonoids are synthesized
from phenylalanine and malonyl-coenzyme A (11).
The flavonoids are all structurally derived from the
parent substance flavones which are commonly
found in cell sap of young tissues of higher plants
(12, 13).
The majority of flavonoids exist naturally as
glycosides and the presence of sugars and hydroxyl
groups make them water soluble whereas methyl
groups and isopentyl units make flavonoids lipophilic
(14). This review paper will address the historical
background of flavonoid discovery, classification of
flavonoids, biosynthetic pathway and the role of
flavonoids in plants.
Classification of flavonoids:
The broad collection of natural products is referred
by the term flavonoid that includes a C6-C3-C6
carbon frame work. Depending on the position of
the linkage of the aromatic ring to the benzopyrano
(chromano) moiety, this group of natural product
may be divided into three classes: Flavonoids (2-
phenylbenzopyrans), Isoflavonoids (3-benzopyrans)
and Neoflavonoids (4-benzopyrans) (shown in
Figure 2). Depending upon the degree of oxidation
and saturation in the heterocyclic ring flavonoids may
be further sub-divided into the following groups
(Figure 3): Flavan, Flavanone, Dihydroflavonol,
Flavonol, Flavone, Flavone-3-ol and Flavone-3,4-
diol. Isoflavonoids are further divided into the
following subgroups (Figure 4): Isoflavan,
Isoflavone, Isoflavanone, Isoflavan-3-ene,
Isoflavanol, Rotenoid, Coumestane, 3-
arylcoumarin, Coumaronochromene,
Coumaronochromone and Pterocarpan.
Neoflavonoids are also divided into three categories
(Figure 5): 4-arylcoumaril, 3,4-dihydro-4-
arylcoumarin, Neoflavene. There are some minor
flavonoids (Figure 6) present in plants such as 2´-
OH-chalcone, 2´-OH-dihydrochalcone, 2´-OH-
retro-chalcone, Aurone and Auronols (15).
Biosynthetic pathway of flavonoids:
Flavonoids are produced in the cytosol of cell. It is
assumed that the enzymes of flavonoids biosynthesis
form a super-molecular complex through protein-
protein interaction and are hold in the endoplasmic
reticulum membrane. These biosynthetic enzymes are
categorized in various enzyme families, such as 2-
oxoglutarate-dependent dioxygenases (OGD),
cytochromes P450 (P450) and glycosyl transferases
(GT) (16). The biosynthetic enzymes associate as
loose aggregate and interaction among the constituent
enzymes allow the direct transfer of substrates from
one enzyme to another enzyme and the channeling of
intermediates. As a result the final products are
collected into the various places like hydrophilic
derivatives are accumulated in the vacuole and
lipophilic compounds in epidermal cells or exuded
from roots (17). The key precursors for the synthesis
of flavonoids are phenylalanine and malonyl-CoA
produced from shikimate pathway and the TCA cycle,
respectively (18). Phenylalanine is converted into
cinnamic acid by phenylalanine- ammonia lyase (PAL)
a generally tetrameric, ubiquitous enzyme in the plant
kingdom. Cinnamic acid undergoes hydroxylation
reaction to form p-coumaric acid mediated by
cinnamic acid 4-hydroxylase (CA4H) which requires
molecular oxygen, NADPH and mercaptoethanol
(17). The p-coumaric acid may be converted to 4-
coumaroyl-CoA by p-coumarate CoA ligase (4CL)
(18). In the phenylpropanoid pathway, p-coumaroyl
CoA is located at the junction of the metabolic routes
resulting to flavonoids or to phenylpropanoid
compounds. The p-coumaroyl CoA is a substrate of
chalcone synthase which catalyzes the production of
the flavonoid skeleton by condensation of p-
coumaroyl CoA with three malonyl CoA, under
release of three carbon dioxide molecules (19). A
linear phenyl propanoid tetraketide 4, 2´, 4´, 6´-
tetrahydroxy chalcone is formed via intramolecular
cyclization and aromatization. The formation of
flavanones from chalcones then occurs through an
page-13
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
isomarization performed by the enzyme chalcone
isomerase (CHI).Various biosynthetic enzymes
further down this pathway are accountable for
catalyzing the conversion of flavanones into the
different flavonoid molecules by hydroxylation,
oxidation, reduction, glycosylation, methylation, and
acylation (20). All flavonoids are synthesized from a
common precursor, (2S)-naringenin (flavanones),
through modifications by various tailoring enzymes
e.g. flavone synthase 1 (FLS 1) synthesizes apigenin
from (2S)-naringenin and flavanone 3 â-hydroxylase
(F3H) and flavonol synthase (FLS) sequentially
convert (2S)-naringenin into dihydrokaempferol and
kaempferol. FLS 1, F3H, and FLS belong to the 2-
oxoglutarate dependent oxygenases that are
nonheme iron dioxygenases utilizing 2-oxoglutarate
as a cofactor (21). Figure 7 shows the flavonoid
biosynthetic pathway.
Functions of flavonoids in plants:
Flavonoids play a variety of significant roles in plants.
Flavonoids act as signal molecules (23), phytoalexins
(24, 25), detoxifying agents, (26, 27, 28), stimulants
for germination of spores (29, 30), play significant
activities in seeds germination (31, 32), act as UV-
filters (33, 34), flavonoids in temperature acclimation
(35) and in drought resistance (36) pollinator
attractants (37) and allelochemical agents (38, 39).
Flavonoids as signal molecules
Flavonoids play a significant role as signal molecules
in plant-microorganism symbiosis (40). Plants
synthesize a wide variety of flavonoids in both root
and shoot tissues during normal growth and
development. Flavonoids are currently considered
to play an important role inside the root during nodule
meristem formation (41). Rhizobia, the soil bacteria
include Rhizobium, Bradyrhizobium,
Sinorhizobium, Mesorhizobium and Azorhizobium
can infect plant roots. Through this infection a
symbiotic relationship is established between the
plant and bacteria and thereby root nodules formation
takes place. In side the nodules bacteria present in
the form of bacteroid and reduces the atmospheric
nitrogen to ammonia and thus fix nitrogen (42).
Nitrogen fixation is initiated by chemical signals that
are recognized by soil bacteria (43). Legume (Pisum
sativum L.) forms a symbiotic association with
rhizobium leguminosarum and produce nitrogen
fixing root nodules on the plants of P. sativum.
Legume-rhizobial nodulation starts with signal
exchange between the symbiotic partners and this
process is initiated by host-specific signal molecules
flavonoid and isoflavonoid compounds liberated
through the plant roots (44). Legume plants produce
characteristic flavonoids and used as signals for
various microbes, including symbionts as well as
pathogens. Garden pea (Pisum sativum) is a legume
plant and Nectria haematococca MPVI is a soil-
born pathogen. In this system, garden pea serves as
a useful model in studying host-flavonoid recognition.
Nectria haematococca MPVI reveals flavonoid
induction of specific pathogenicity genes and
stimulation of development required for pathogenesis
(45). It is investigated that the ability of
Azorhizobium caulinodans ORS571 tagged with
reporter genes, to internally colonize roots of non-
legume dicot plant like Arabidopsis thaliana which
is used as a model plant to study the interactions
between diazotrophic bacteria and non-legume dicot
plant. The reporter genes will help to identify and
visualize the bacteria found association with plant
roots. They have shown reproducible, high
frequency, internal colonization at the points of lateral
root emergence of A. thaliana by ORS571. The
ORS571 colonization was found to be stimulated
significantly by specific flavonoids at low
concentrations independently of nod genes (46).
Flavonoid acts as chemoattractants for rhizobia and
as specific inducers of rhizobial nodulation genes
(nod-genes) (47). Nod-genes are involved in the
synthesis of lipochitooligosaccharide signals, called
Nod factors, which induce the accumulation of
flavonoids resulting in the secretion of more
flavonoids by the root. Due to the accumulation of
more flavonoids further induction of Nod factors
takes place (48). Figure 8 shows a schematic model
of flavonoid secretion from soybean roots and the
interrecognition between legume and rhizobium.
page-14
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Nod-factors perceived by receptors in the host plant
induce various signaling events such as ‘calcium
spiking’ response ultimately in the production of
nodules (49). Flavonoids and nitrogenous
metabolites are major components of plant seeds.
In combination they are soluble in water and easily
released as chemical signal following imbibitions.
After releasing the combination including flavonoids
in to the soil act as eco-sensing signals for suitable
rhizobia and other fungal partners in order to
accomplish symbiotic mutualisms (50). The
symbiotic relationship for nitrogen fixation in nature
is affected by micro-ecology of the plant rhizosphere
i.e. soil temperature, pH, texture, moisture, salinity
and deficiency in essential elements preventing all
stages of symbiotic establishment evaluated to date
(42). Parasitization by Orobanche is a complex
process, which is mediated by host-derived chemical
signals, ultimately control parasite seed germination
and haustorium initiation and help in the union of two
plant species. It is reveled that host flavonoid
production is not essential for Orobanche
parasitization (51). Parasitic plants under the family
scrophulariaceae produce infective root structure
known as haustoria in response to chemical signal
secreted from host-plant roots. Several phenolic
compounds such as flavonoids induce hausteria in
Triphysaria versicolor root tips within hours after
treatment and are also important signaling molecules
for mediating parasitic plant-host plant interaction in
the rhizosphere. Hausteria perform a number of
functions for the parasite such as they attach the
parasite and host roots, they invade the host tissues
through a combination of enzymatic and physical
process and the haustoria serve as physical channels
through which the parasite steals water and nutritional
substances from the host plant (52).
Flavonoids as phytoalexins
Many plant species produces certain chemical
substances when they are infected by
microorganisms. These chemical substances, known
as phytoalexins, ward off the disease organisms from
the plants. These chemical substances are simple
phenolics, stilbenoids, alkaloids, terpenoids,
coumarins, polyacetylenes, and so on, were reported
as phytoalexins (37). Isoflavonoids are characterized
by a migration of phenyl ring and occur principally in
legumes and are involved in the defense response of
plants against pathogens. In lotus species, the main
phytoalexin synthesized is vestitol, which belong to
the class of isoflavans (33). Fawe et al. worked on
Silicon-mediated accumulation of flavonoid
phytoalexins in cucumber and they found that silicon
is involved in the increased resistance of cucumber
to powdery mildew by enhancing the antifungal
activity of infected leaves. Flavonol aglycone
rhamnetin (3,5,3',4'-tetrahydroxy-7-O-
methoxyflavone) was first reported as a phytoalexin
in the plant kingdom and of a flavonol phytoalexin in
cucumber, a chemical defense long been believed to
be nonexistent in the family Cucurbitaceae (24).
Mcnally et al. worked on the synthesis of C-glycosyl
flavonoid phytoalexins as a site-specific response to
fungal penetration in cucumber. Phytochemical
analyses and fluorescence microscopy observations
revealed the production of autofluorescent C-glycosyl
flavonoid phytoalexins within the epidermal tissues
of disease-resistant plants undergoing fungal entry.
Phytoalexin production was triggered by the
combination of an eliciting/inoculation treatment, and
tissue autofluorescence. After a second eliciting
treatment, disease-resistant plants produced
phytoalexins more rapidly (25). The attack of weed
plants by mycoherbicidal organisms (Alternaria
cassiae) can be inhibited by the antifungal flavonoid
phytoalexins accumulated upon infection and the
measurement of phytoalexin levels is problematic due
to interference by pigments and other plant
metabolites (53). Jeandet et al. worked on Vitaceae
and reported that it would produce stilbene
phytoalexin which act against phytopathogenic
microorganisms (54). Phytoalexins accumulated in
woody plants in response to the microbial attack or
stress are reviewed and listed with respect to their
chemical structure and probable biogenetic origin by
Gottstein and Gross. Woody plants contain an
extremely high number of organic compounds with
enormous chemical diversity. Many of these
secondary plant products possess antimicrobial
activities and are considered to be part of the cellular
page-15
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
defense system of the plant against microbial
phytopathogen attack (55). Low molecular weight
phytoalexin antimicrobial compounds synthesized at
the site of infection in response to microbial attack
or elicitation have long been proposed to be a vital
factor against plant pathogens (56). Isoflavonoids
function as regulatory substances and phytoalexins,
but only a few data available concerning the
significance of phytoalexins in the interaction between
rhizobia and their legume host (57).
Flavonoids as detoxifying agent
The photosynthetic electron transport system in plant
is the major source of active oxygen species.
Chloroplasts have evolved a highly developed
ascorbate-glutathione cycle i.e. detoxification system
to avoid oxygen-mediated toxicity. Flavonoids may
scavenge photo produced active oxygen species in
the chloroplast. Super oxide anion radical can not
readily diffuse into vacuoles where flavonoids are
localized from chloroplast but H2O2 can diffuse
across membranes (26). Efficient scavenging of ROS
by phenolic compounds has been found to reduce
ultraviolet radiation stress (27). Flavonoid-
Peroxidase reaction may act as a mechanism for
H2O2 scavenging and thus flavonoids acts as
detoxifying agent (26). Flavonoids accumulated
under the elicitation of toxic metals not only able to
detoxify the ROS but also the toxic metals by
chelating depending on the diversity of molecular
structures. In the fungus Alternaria alternata the
application of quercetin and morin showed substantial
protection against the inhibition of fungal growth by
copper while naringenin and rutin were less effective.
For cell cultures of Ginkgo biloba, it was reported
that flavonoids accumulated in response to heavy
metal stress upto 12 fold when treated with copper
sulphate as compared to that of untreated cells.
Similarly in callus cultures of legume plant Ononis
arvensis, flavonoid levels increased after elicitation
with copper sulphate, but also with cadmium chloride
(58). Phenolic compounds may inactivate iron ions
by chelating and additionally suppressing the super
oxide-driven Fenton reaction. The chelating action
of these compounds may be due to high nucleophilic
character of the aromatic rings. The antioxidant ability
of flavonoids depends on the molecular structure and
position of hydroxyl groups. It is reported that
flavonoids may alter peroxidation kinetics by chelating
the lipid packing order and thus stabilize the
membranes, prevent the diffusion of free radicals and
stop peroxidation. Flavonoids not only bind with
protein but can interact with membrane phospholipids
by hydrogen bond. In vitro study revels that
flavonoids can directly scavenge Oÿ2
", H2O2, ·OH,
singlet oxygen or peroxyl radical. Their antioxidant
capacity due to donation of electrons or hydrogen
atom and structural features such as 3´4´”dihydroxy
structure in the B-ring such as quercetin, the 2, 3-
double bond in C-ring (which allows electron
delocalization) and presence of 3-OH (most
significant electron donating ability) and 5-OH group
in C-ring and A-ring respectivelym (28).
There are two electron transport path ways in plant
cell mitochondria i.e. the cytochrome path way and
the alternative path way. Alternative oxidase (AOX)
acts as terminal oxidase in alternative path way found
only in plants, green algae, fungus and protozoa. It is
shown that flavonoids (myricetin, quercetin and
kaempferol) exhibit antioxidant property by inhibiting
the AOX activity (59). Agate et al. reported that
orthodihydroxy B-ring substituted flavonoids like
quercetin and luteolin are accumulated in the
mesophyll and epidermal tissue of leaves of
Ligustrum vulgare in response to high intensity of
sunlight and protect the tissue from the oxidative
damage induced by sunlight (60). Light induces the
biosynthesis of ascorbic acid and peroxidase in
grapevine leaves and induced peroxidase catalyze
the oxidation of flavonoids (quercetin, kaempferol)
but not ascorbic acid. Ascorbate peroxidase
isoenzymes detoxify H2O2 in most plants but are not
detected in grapevine leaves extract. Flavonoid-redox
cycle was considered as an alternative system to
detoxify H2O2 in grapevine leaves (61). Yamasaki et
al. examined the stress protectant property of
flavonoids (quercetin, kaempferol) in plant cells by
scavenging H2O2. The glycosides and aglycones of
isolated flavonols were oxidized by H2O2 in the
page-16
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
presence of peroxidase. The rates of oxidation were
in the order quercetin > kaempferol > quercetin
glycoside >> kaempferol glycoside (26). Flavonoids
having antioxidant abilities protect plants from various
biotic and abiotic stresses and lead to the formation
of brown pigments in plant tissues, plant-derived
foods and beverages and flavonoid oxidation is mainly
catalyzed by polyphenol oxidases (catechol oxidases
and laccases) and peroxidases during seed and plant
development at the level of transcription to post-
translational mechanisms, sub cellular
compartmentalization of enzymes and substrates (4).
Experimental evidence shows that antioxidant
function of flavonoids in plants limited to a few
individual flavonoids under very specific experimental
and developmental conditions. So, the widely
accepted antioxidant function of flavonoids in plants
is still a matter of debate (62). The antioxidant and
scavenging properties of kolaviron, a flavonoid
extract of Garcinia kola seeds was evaluated and
reported marked reducing power and antioxidant
activity by inhibiting the peroxidation of linoleic acid.
Kolaviron exhibited scavenging effect on superoxide,
hydrogen peroxide, effective activities as a hydrogen
donor, reaction with hydroxyl radical (·OH) by
inhibiting deoxyribose oxidation induced by a Fenton-
type reaction system (63). Different adverse
conditions lead to increased production of free
radicals and other oxidative species in plants which
are counteracted by the development of classical
antioxidant system (superoxide dismutase, ascorbate
peroxidase, catalase, monodehydroascorbate
reductase, glutathione reductase and the low
molecular weight antioxidants ascorbate and
glutathione). The role of secondary metabolic
pathways in plant response to oxidative stress which
is responsible for the synthesis of phenolic metabolites
such as flavonoids, tannins, hydroxycinnamate esters
and the structural polymer lignin (64).
Flavonoids as stimulants for germination of
spores
Flavonoids exudate from legume roots stimulates
spore germination of a number of soilborne fungi
which interact with these plants (29). Morandi et al.
tested the effect of two isoflavonoids (glyceollin I,
and coumestrol) and 1 flavonoid (quercetin) on in
vitro spore germination of Gigaspora margarita
and concluded insignificant germination rate by any
of these compounds (30). Scervino et al. studied
the effect of flavonoids (chrysin, isorhamnetin,
kaempferol, luteolin, morin and rutin) on pre-
symbiotic growth, such as spore germination, hyphal
length, hyphal branching and the formation of
auxiliary cells and secondary spores, of the
arbuscular mycorrhizal fungi (Gigaspora rosea, G.
margarita, Glomus mosseae and G. intraradices)
and reported the tested flavonoids could be classified
according to genus and/or species specific or
specific, for a certain developmental stage of pre-
symbiotic growth (65). Flavonoid-induced
stimulation study on N. haematococca germination
showed the involvement of cAMP pathway
controlling the germination response. Germination
was induced in cAMP treated spores while prevented
with the treatment of H-89, an inhibitor of cAMP-
dependent protein kinase A (PKA) (45). Flavonoid
treatment transiently induced the cAMP levels in
macroconidia. Hypothesis of Bagga et al. was that
flavonoids modulated cAMP levels through direct
inhibition of N. haematococca cAMP
phosphodiesterase. The result of their work suggests
that the ability of specific flavones and flavanones to
inhibit cAMP phosphodiesterase is a potential
mechanism through which they can induce cAMP
levels and so promote germination (29). In a previous
study, Kensuke et al. showed that spores of the
ectomycorrhizal fungus Suillus bovinus germinated
through the combination of activated charcoal
treatment of media and co-culture with seedlings of
Pinus densiflora, which suggested that some
substances contained in root exudates induced the
germination. Among these substance flavonoids have
been elucidated to play various and substantial roles
in plant-microbe interactions and they investigated
the effects of flavonoids on basidiospore germination
of S. bovinus. Hesperidin, morin, rutin, quercitrin,
naringenin, genistein, and chrysin, had greater effects
than controls, whereas flavone, biochanin A, luteolin,
page-17
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
and quercetin showed no positive effects (66). Root
exudates contain different types of compound, such
as flavonoids, plant hormone, organic acids etc. many
researchers have reported that flavonoids stimulate
the spore germination. Leguminous plant Root
exudates affect the spore germination, hyphal growth,
and colonization of arbuscular mycorrhizal fungi.
Many researchers have reported that flavonoids
which is present among with other compounds such
as amino acids, reducing sugars, organic acids and
plant hormones in root exudates, stimulate the spore
germination including hyphal growth, and colonization
of arbuscular mycorrhizal fungi (67). Spores of
Nectria haematococca mating population VI which
cause root rot disease, germinate within 24 h in a 7-
mm radius of a germinating seed. Specific flavonoids
and isoflavonoids present in root exudates have
induced spores germination. Root exudates-induced
spore germination was found to occur by two
separate mechanisms, the flavonoid responsive
pathway that is inhibited by H89, a cAMP-dependent
inhibitor of protein kinase A and a nutrient-responsive
pathway that is impervious to H89 (68). Various
external factors influence the rate of spore germination
and the length and duration of hyphal growth e.g.
soil extract, soil microorganisms, certain soil
phosphorus concentrations, suspension cell cultures
and exudates, plant root volatiles, plant root exudates,
isolated flavonoids and other isolated phenolics. The
stimulation of Arbuscular mycorrhiza-hyphal
growth by root exudates and flavonoids is increased
synergistically by the addition of carbon dioxide. The
optimal growth enhancement of Gigaspora
margarita by flavonoids is obtained in the presence
of 1.0 %-2.5 % carbon dioxide but 5.0 % and above
reduces hyphal growth of G. margarita (69). In an
attempt to develop ecofriendly compounds for
controlling plant diseases caused by Fusarium
oxysporum ,different extracts of three weed plants,
namely Capparis deciduas, Lantana camara and
Tridax procumbens were tested for the antifungal
activity. They reported that the free flavonoids and
sterols of Tridax procumbens and bound flavonoids
of Capparis deciduas totally inhibited spore
germination of the fungi (70).
Flavonoids in seed germination
In the plants, flavonoids act as internal physiological
messengers and for this function flavonoids are
required relatively small amount. Flavonoids are
stored in the tapetosomes. Tapetosomes are
organelles present in the tapetum cells, which
correspond to the inner most anther coat layer.
During pollen development, the flavonoids are
released from the tapetosomes and react with the
pollen coat, allowing pollen tube growth germination.
Pollen-specific gene products induced by the
kaempferol have been characterized in petunia plant
(71).The flavonoids as secondary metabolites
present at high level in most plant seeds and protect
the seeds against pathogen and predators and take
part in seeds maturation and dormancy (31). The
transient accumulation of purple flavonoid in the rims
of the cotyledons and in the hypocotyls epidermal
layers in Arabidopsis seedlings is observed but their
role in seedlings is unknown. The wide distribution
of flavonoids in plants suggests their fundamental
importance and prophylactically protection of the
seedlings against pathogens or UV light (72).
Germination and growth inhibitory effects of some
secondary metabolites are some times associated
to allelopathy. These metabolites such as quercetin,
isoquercitrin, rutin, and quercetrin among many
others have shown effects on plant growth (73). The
exogenous application of flavonoids reports plant
growth regulation. Plant growth regulators especially
gibberellins (GAs) are known to promote plant
growth, germinate seed and response toward
environmental stresses. GAs has also been reported
to promote synthesis of flavonoids, by GA3
promoted levels of flavonoid-specific mRNAs (74).
Accumulation of dihydroflavonoids in the seed coat
inhibits embryo growth, either directly or indirectly.
Proanthocyanidine assists in the reinforcement of
plant tissues, to the maintenance of seed dormancy
as well as seed longevity in storage. Testa
pigmentation by proanthocyanidine help in the
resistance to solute leakage, imbibitions, damage and
page-18
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
attract by soil-born fungi, as a result improve seed
vigor and germination in legumes. High concentrations
of phenolics especially flavonoids in emerging
seedling also associated with protection against UV-
B damage at the critical stage of development (32).
Flavan-3-ol polymers may form a barrier for
important processes to continue the dormancy of
seed, the main effects produced by the seed coat,
are interference with water uptake; mechanical
resistance to radicle protrusion; interference with gas
exchange, particularly oxygen and carbon dioxide;
prevention of inhibitor leakage from the embryo and
light filtration. Many studies have reported that
flavonoids possess the inhibitory effect in seed
germination (71, 75). The oxidative products of
flavonoids, semiquinones, quinones are highly reactive
and can react with phenolic compounds, proteins,
or scavenge free radicals and may protect plants from
oxidative stresses as a result strengthen the testa
structure by cross linking with protein and
carbohydrates of cell wall. Further, flavonoids may
also decrease oxygen supply for embryo to develop,
by fixing it through enzymic reactions catalyzed by
phenol oxydoreductases (71). Effect of isovitexin,
leucocyanidin, gallic acid, and protocatechuic acid
on seed germination and subsequent seedling growth
of a crucifer Brassica campestris, and two legumes
Lens esculenta and R. minima, as well as effects of
isovitexin on rooting of onion bulbs are illustrated.
Nandakumar and Rangaswamy have reported that
neither of the flavonoids affects seed germination in
any of the three systems (76). Some seeds must have
excellent capacity to cope with potential infecting
organisms because they lie dormant for long period
before germination. Many allelochemicals are
identified as seed components such as tricin in seed
of Orobanche, quercetin and myricetin in seeds of
Trifolium, rutin in seeds of Brassica and apigenin
glycosides in celery seeds (8).
Flavonoids as UV-filters
In plants, the flavonoid path way has been well
characterized and involves numerous branches
leading to the accumulation of wide range of end
products with various functions: colourful
anthocyanins, antimicrobial isoflavonoids, UV
protecting flavonoids, deterrent condensed tannins
(33). Another important role of flavonoids is their
action as a screen against severe sunlight illumination.
The spectrum of UV radiation reaching the earth’s
surface has been divided into lower energy UV-A
(320-400 nm), higher energy UV-B (280-320 nm)
and UV-C (254-280 nm) regions. The most severe
damage caused by ultraviolet (UV) light particularly
UV-B band. UV-B radiation may affect
photosynthesis and transpiration, pollination and
DNA and cellular damage, competitive balance in a
community, susceptibility to diseases, environmental
stress and pollution it also induces changes in plant
foliar chemistry, including decreases in
carbohydrates concentrations (77, 78). Flavonoids
generally absorb UV-B band and thus act as UV-
filters and protect the tissue from damage (34).
Pigments, generally localized in the epidermal cells,
reduce epidermal penetration of UV-B radiation
selectively protecting internal tissues without
interfering photosynthesis (79). UV-B stimulated the
biosynthesis of UV-B absorbing compounds and
carotenoids, which both perform a photoprotective
function (80). UV-B radiation disables the processes
of cell division and alters the pattern of plant growth
and development such as dormancy and flowering.
UV-B radiation weakened the defense mechanisms
of the plants and enhances the pathogenicity of the
organisms such as fungus (81). Phenylpropanoids
phenolics could also serve as UV-filters and probably
as the original ones, their absorption coefficients are
lower than flavonoids on a molar or weight basis. A
mixture of flavanones (including their three hydroxy
forms or dihydroflavonols), flavones and flavonolos
in the central vacuole of epidermal cells of leaves
serves as a filter lessening UV-B and UV-A
irradiation (82). The responses of plants to more
intense UV-B radiation resulting in a reduction in
radiation absorption on the leaf surface as radiation
occur mostly at the physiological and biochemical
level (83, 84). In higher plants specific
photoreceptors (e.g. cryptochromes) play vital role
in the defense against UV-B radiation.
page-19
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Photoreceptors regulate the biosynthesis of
flavonoids and are thus indirectly involved in the
formation of the anthocyanins responsible for
absorption (85). Radiation causes severe damage
to plants having lines that have reduced level of
flavonoids (Anthocyanins) than in those with normal
pigment complements (8).
Flavonoids in stress condition
Flavonoids play a significant role in temperature
acclimation. It is established that temperature
acclimation results from a complex process involving
a number of physiological and biochemical changes,
including changes in membrane structure and
function, tissue water content, global gene
expression, protein, lipid, and primary and secondary
metabolite composition (35). There is an adjustment
in plant growth and cellular metabolism in case of
chilling-resistance biennial plants e.g. Brassica napus
L. var. oleifera L. in cold (>0ÚC) to overcome low
temperature stress and results in higher resistance
of cells to extracellular freezing. Exposure of plants
in very low temperature affects the properties of
plasma membranes and induces specific signaling
path ways. Stefanowska et al. have reported that
cold acclimation of plants leads to remarkable
increase in phenylalanine ammonia-lyase (PAL)
activity resulting in the accumulation of phenolics
depending upon the range of low temperature to
which the plants are subjected (86). Flavonoids may
perform functional role in plant cold acclimation and
freezing tolerance. During cold acclimation and
freezing, flavonoids especially quercetin may
scavenge reactive oxygen species and act as potent
antioxidants. Under freezing conditions, large amount
of water is removed from the cell into intercellular
ice crystal, in this circumstances flavonoids are
expected to partition even more strongly into lipid
phase of cell membranes and thus stabilize them (87).
Hernandez et al. evaluated drought-induced changes
in flavonoids in the leaves of Cistus clusii Dunal
and reported that the flavonoids epigallocatechin
gallate, epicatechin and epicatechin gallate
concentrations increased progressively during
drought and attain maximum values after 30 days of
stress. These flavonoids are responsible for the leaf
morphological changes and are efficient chain-
breaking antioxidants and transition metals chelators,
thus they may help to inhibit lipid peroxidation and
prevent oxidative damage during drought-stressed
condition (36). Chutipaijit et al. evaluated the proline
level and flavonoids levels with respect to the relative
water content (RWC) of four varieties of indica rice
seedling against salinity. In less salt sensitive varieties,
the RWC were decreased less than those of more
salt sensitive seedlings and the former case showed
that the lesser extent of membrane damage due to
enhanced the proline level and flavonoids level than
those of the more sensitive varieties (88).
Flavonoids as pollinator attractants
Anthocyanins contribute a number of roles in the plant
cell. Perhaps the most obvious is as an attractants
for pollinators via flower color and for seeds dispersal
agent via brightly color food (89). The presence of
anthocyanins as pollinator attractants is well known
as a function of flavonoids in plants. Pollination was
identified as the trigger for rapid anthocyanin synthesis
(90). A variety of functions have been attributed to
the different classes of flavonoids, e.g. red and blue
anthocyanin pigments in combination with UV-
absorbing flavonol copigments acts as insect pollinator
attractants (91). Flavones and flavonols also act as
pollinator attractants in addition to visible
anthocyanins (35). According to the classic view of
pollination biology flower visitors have relatively fixed
color preferences (Table 2). This idea is applied for
specific color association for each type of flower
visitor (8). Different parts of a flower may have
different pigments and colors to attract more than
one type of pollinators. Generally younger flowers
are bee pollinated, the older are visited by birds, and
the plant switches to birds visitation by increasing the
sugar concentration in the nectar as the flower ages.
Color production in flower is a dynamic process and
color may change after pollination and lose their
attractiveness to the insects (92). Major classes are
the monomeric red to purple anthocyanins in flowers
and fruits. In angiosperms, flavonoids are concerned
with sexual reproduction via pollination, seed
page-20
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
dispersal, germination, and longevity. In Arabidopsis
thaliana, anthocyanins are found in sporophytic
tissue cell vacuum (93).
In angiosperms, color play important role in order
to attract pollinators such as bees, butterfly, birds,
insects, etc., although the color is frequently one of
a number of factors like fragrance, floral shape,
nectar and even petal epidermal cell shape, which
combine to determine pollinator choice (94). The
color variations in flowers and fruit depend on the
presence of flavonoids belonging to different pigment
groups (Table 1).
In flowering plants, color including fragrance, floral
shape, epidermal cell shape, and nectar reward in
combination determine the pollinator’s choice.
Generally beetle pollinated flowers are cream, white,
or green whereas bees pollinated flowers are UV-
absorbing pigmented with chalcone and flavonol type
flavonoids which may show UV-visible patterning in
flower petals and often combine with UV-reflective
carotinoid pigments. Bees also choice the presence
of nectar in the flowers indicated by the appearance
of distinctive spots or pigment lines on different floral
parts. Elegant plant-animal co-evolution is found to
occur in orchid genus, ophrys apply scent, shape
and color to mimic female bees causing the male
bee to attempt copulation and thereby pollination
takes place (94). The color change during the later
stages of flower development or in response to
pollination has been recognized for long time. In
Lantana flowers, the color change from yellow to
purple over an ageing period of three days takes
place and the pollinator’s choice the younger yellow
flowers which are fertile, offer nectar and pollen that
older flowers do not and are preferred by butterfly
pollinator (95). A number of flowering plant species
have depend strictly on mobile organisms for their
pollination and acquire the capacity to produce
different compounds that appeal to the visual,
olfactory and taste senses of insects or animals to
visit the flowers and pass the pollen to another plant
of the same species rather than spread pollen around
at random (96). Many of these colors are dependent
on possible complexes with Fe+++ and Al+++ as
well as pH. Quercitrin, chlorogenic acid and methyl
gallate have no remarkable effect on the color,
spectra, or stability of cyanidin 3-glucoside in aqueous
solution at pH 3-6.5. In acetate buffer solutions (pH
5.45) containing aluminium salts, quercitrin and
chlorogenic acid produce highly colored co-
ordination complexes with anthocyanin. The
production of these co-pigment-aluminium-
anthocyanin complexes depends not only on pH but
also on the type of organic acids which constitute
the buffering system (97). The entire color of Tulipa
gesneriana is purple, except the bottom, which is
blue. To observe the mechanism of different color
development in the same petal, they prepared
protoplasts from the purple and blue epidermal
regions and determined the flavonoid composition,
the vacuolar pH and element content and revealed
that the anthocyanin and flavonol compositions in both
purple and blue color protoplasts were the same.
There was no significance difference in vacuolar pH
(pH 5.5 and 5.6 respectively) but the ferric ion
content in blue protoplast was ~9.5 mM which is 25
times higher than in the purple protoplast. Shoji et al.
confirmed that the Fe+++ is essential for blue color
development in the tulip (98).
Flavonoids as allelochemicals
Alleopathy is defined by most scientists as the adverse
effect of one plant species on neighboring plants
through the release of phytotoxins (allelochemicals)
into the environment. Allelopathy is a component of
one plant or plant interference the other being
competition for resources such as nutrients, light and
water (39, 99). 5,7,42 -trihydroxy-32 ,52 -
dihydroxyflavone was isolated and identified from
an allelopathic rice accession PI 312777 along with
3-isoprppyl-5-acetoxycyclohexene-2-one-1 and
momilatone B. Kong et al. observed the release of
these compounds at different ages of seedlings and
indicated that PI 312777 seedlings could release
sufficient quantities of these substances including
flavone into the environment to act as allelochemicals
preventing the growth of associated weeds (100).
They have grown four legume species under
greenhouse conditions to observe the effects of 7,
page-21
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
8-benzoflavone (from Russian knapweed) and (±)-
catechin (from Spotted knapweed) on rhizosphere
interactions among legume roots and associated
rhizobia. Pure cultures of four rhizobia strains showed
different responses when grown with 7,8-
benzoflavone or (±)-catechin. Plants that were
inoculated and nodulated generally reveled no
response to 7,8-bebzoflavone and ±catechin but
when were not inoculated exhibited stronger
responses to 7,8-benzoflavone or (±)-catechin.
Therefore, inoculation and nodulation may confer
resistance to allelochemicals (101). The plant
flavonoids flavone, chrysin, apigenin, kaempferol,
morin, quercetin, myricetin and phloretin were found
to prevent in a dose-dependent manner the
cytochrome P-450 dependent ecdysone 20-
monooxygenase activity concerned with adult female
Aedes aegypti. The concentrations of these
flavonoids required to elicit a 50% inhibition of the
steroid hydroxylase activity in all the insects ranged
from ca 1 × 10"5 to 1 × 10"3 M (102).
Allelochemicals are the secondary metabolites
obtained through branching of the main metabolic
pathways of carbohydrates, fats, and amino acids.
From the structural diversity of the allelochemicals it
is obvious that allelopathy must involve more than
one action mechanism, different synergism patterns
and diverse targets of interaction (103).
Allelochemicals when present in low enough
concentrations, they may stimulate rather than inhibit
growth. Allelochemicals are present (usually in
conjugated form) in virtually all plants and in many
tissues, including leaves, flowers, fruits, buds, seeds,
stems, and roots. Under certain conditions, these
chemicals may be released into the environment
(atmosphere or successional plant (104). Almost all
allelochemicals substances are secondary
metabolites, synthesized by plants and
microorganisms through Shikimic acid and Acetated
pathways. These substances are released into the
surrounding by environmental factors such as i)
release of essential oils into atmosphere, ii) above
ground factors like insects, fungi, etc.; light; moisture;
plant density; temperature; and other allelochemicals,
iii) below ground factors like insects, fungi, etc.;
nutrient stress; water status; other allelochemicals
influencing root exudation, extracting and leaching,
iv) plant residues decay and action of microorganisms.
In soil, allelopathic substances remain in inactive
forms bound to clay or organic matters and are lost
from soil by leaching, drainage, microbial
breakdown, chemical processes (38). The chemicals
secreted into the soil by roots are broadly referred
to as root exudates. Through the exudation of a wide
variety of compounds, roots may regulate the soil
microbial community in their immediate vicinity, cope
with herbivores, encourage beneficial symbiosis,
change the chemical and physical properties of the
soil, and inhibit the growth of competing plant species
(105).
Conclusions
Plants have several popular regulatory metabolites
to control the flower color, flavoring factors,
pollination, pollen tube germination, seed maturation
and seed coat browning, seeds and spore
germination, plant growth and development and
establish themselves against biotic and abiotic stress
conditions. Flavonoids are a large group of low
molecular weight, ubiquitously distributed,
polyphenolic secondary metabolites. These
compounds play a significant role in various stages
of plant growth and their existence in the
environmental stresses. Flavonoids are remarkable
reactive oxygen species scavengers and fight
continuously against polluted atmosphere. These
metabolites are effective in temperature stress,
drought situation, freezing injuries of cell membranes
and unusual salinity. Flavonoids act as signal
molecules to take preventive measures in order to
save them from pathogenic microbial attack.
Flavonoids are responsible for unique colors of
flowers and fruit which are necessary for pollination
and subsequently fruit dispersion in different places
and thus help in reproduction. The significance of
flavonoids in plant physiology is unparallel and more
and more efforts may require for their biosynthetic
aspects in order to explore better production,
mechanism of actions and ensure safety.
page-22
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
page-23
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
page-24
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
page-25
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
page-26
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Figure 7. Anthocyanin 3-O-glucoside biosynthetic pathway in plants (22)
Abbreviations: CHS: chalcone synthase; CHI: chalcone isomerase; FNR: flavanone reductase; FLS:
flavonol synthase; F3´H: flavonoid-3´-hydroxylase; CoA: coenzyme A; ANS: anthocyanidin synthase; 3-
GT: UDPG-flavonoid 3-O-glucosyl transferase; DFR: dihydroflavonol 4- reductase; FHT: flavanone 3â-
hydroxylase.
page-27
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Figure 8. A schematic model of flavonoid secretion from soybean roots and the interrecognition between
legume and rhizobium (49)
REFERENCES
1. Middleton EJ. Effect of plant flavonoids on
immune and inflammatory cell function. Adv.
Exp. Med. Biol. 1998; 439:175–182.
2. Woo HH, Kuleck G, Hirsch AM, Hawes MC.
Flavonoids: signal molecules in plant
development. In Bela SB, Michael EB. (eds.),
Flavonoids in cell function, New York,
USA, Kluwer Academic/ Plenum Publishers,
2002, pp. 51-60.
3. Boumendjel A, Pietro AD, Dumontet C, Barron
D. Recent Advances in the Discovery of
Flavonoids and Analogs with High-Affinity
Binding to P-Glycoprotein Responsible for
Cancer Cell Multidrug Resistance. Med.
Res. Rev. 2002: 22: 512-529.
4. Pourcel L, Routaboul JM, Cheynier V. et al.
Flavonoid oxidation in plants: from
biochemical properties to physiological
functions. Trends Plant Sci. 2007; 12(1):
29-36.
5. Takahashi A, Ohnishi T. The significance of the
study about the biological effects of solar
ultraviolet radiation using the exposed facility
on the internal space station. Biol. Sci. Space
2004; 18(4): 255-260.
6. Buer CS, Imin N, Djordjevic MA. Flavonoids:
New roles for old molecules. J. Integrative
Plant Biol. 2010; 52 (1):98-111.
7. Griesbach RJ. Biochemistry and genetics of
flower color. Plant Breed. Rev. 2005;
25:89-114.
page-28
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
8. Bohm BA. Introduction to flavonoids.
Amsterdam, The Netherlands, Hardwood
academic publishers, 1998, pp. 365-394.
9. Yao LH, Jiang YM, Shi J. et al. Flavonoids in
Food and Their Health Benefits. Plant Foods
Hum. Nutr. (Formerly Qualitas
Plantarum). 2004; 59: 113-122.
10. Sokoloff B, Chamelin I, Biskind M. et al. Citrus
vitamin P. Florida state horticultural
society. 1956, pp.128-131.
11. Winkel-shirley B. Flavonoid biosynthesis. A
colourful Model for Genetics, Biochemistry,
Cell Biology, and Biotechnology. Plant
Physiol. 2001; 126: 485-493.
12. Kurian A, Sankar MA. Medicinal plants.
Peter KV. (ed.), New Delhi, India, New India
Publishing Agency, 2007, pp. 26.
13. Yoshida K, Mori M, Kondo T. Blue flower
color development by anthocyanins: from
chemical structure to cell physiology. Nat.
Prod. Rep. 2009:26: 884-915.
14. Crozier A, Jaganath IB, Clifford MN. Phenols,
Polyphenols and Tannins: An overview. In
Crozier A, and Clifford MN. (eds.), Plant
secondary Metabolites: occurrence,
structure and role in the human diet.
Singapore, Blackwell Publishers Limited,
2006, pp.1-24.
15. Stobiecki M, Kachlicki P. Isolation and
Identification of Flavonoids. In Grotewold E.
(ed.), The Science of Flavonoids. Published
by Springer Science + Business Media I.I.C.
New York, USA, 2008, pp.47-70.
16. Tanaka Y, Sasaki N, Ohmiya A. Biosynthesis
of plant pigments: anthocyanins, betalains and
carotenoids. Plant J. 2008; 54(4):733-749.
17. Dinelli G, Bonetti A, Elementi S, D´Antuono
LF, Catizone P. Biosynthesis of Polyphenol
Phytoestrogens in Plants. In Yildiz F. (ed.),
Phytoestrogens in Functional Foods.
Published by CRC Press Taylor & Francis
Group, Boca Raton FL, 2006, pp. 19-80.
18. Davies KM. Modifying Anthocyanin
Production in Flowers. In Gould K, Davies
KM, Winefield C. (eds.), Anyhocyanins
Biosynthesis, Functions and Applications.
2009, pp. 49-84.
19. Besseau S, Hoffmann L, Geoffroy P, Lapierre
C. et al. Flavonoid Accumulation in
Arabidopsis Repressed in Lignin Synthesis
Affects Auxin Transport and Plant Growth.
The Plant Cell. 2007; 19: 148-162.
20. Fowler ZL, Koffas M. Microbial Biosynthesis
of Fine chemicals: An Emerging Technology.
In Smolke CD. (ed.), The metabolic
pathway engineering handbook: tools and
applications. Published by CRC Press Taylor
& Francis Group, Boca Raton FL, 2010, pp.
22-1.
21. Katsuyama Y, Funa N, Miyahisa I, Horinouchi
S. Synthesis of unnatural flavonoids and
stilbenes by exploiting the plant biosynthetic
pathway in Escherichia coli. Chem. Biol.
2007; 14(6):613-621.
22. Yan Y, Chemler J, Huang L, Martens S. et al.
Metabolic engineering of anthrocyanin
biosynthesis in Escherichia coli. Appl.
Environ. Microbiol. 2005; 71(7): 3617-
3623.
23. Peer WA, Murphy AS. Flavonoids as signal
molecules: Targets of flavonoid action. In Peer
page-29
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
WA, and Murphy AS. (eds.), The Science
of Flavonoids. Springer, New York, 2006,
pp. 239-268.
24. Fawe A, Abou-Zaid M, Menzies JG, Belanger
RR. Silicon-mediated accumulation of
flavonoid phytoalexins in cucumber.
Phytopathology. 1998; 88(5):396-401.
25. McNally DJ, Wurms KV, Labbe C, Belanger
RR. Synthesis of C-glycosyl flavonoid
phytoalexins as a site-specific response to
fungal penetration in cucumber. Physiol. Mol.
plant path.2003; 63(6):293-303.
26. Yamasaki H, Sakihama Y, lkehara N.
Flavonoid-Peroxidase Reaction as a
Detoxification Mechanism of Plant Cells
against H202. Plant Physiol. 1997;
115:1405-1412.
27. Jansen MAK, Van den Noort RE, Tan MY.
et al. Phenol-oxidizing peroxidases contribute
to the protection of plants from ultraviolet
radiation stress. Plant Physiol. 2001;
126:1012-1023.
28. Michalak A. Phenolic compounds and their
antioxidant activity in plants growing under
heavy metal stress. Polish J. of Environ.
Stud. 2006; 15(4): 523-530.
29. Bagga S, Straney D. Modulation of cAMP
and phosphodiesterase activity by flavonoids
which induce spore germination of Nectria
haematococca MP VI (Fusarium solani).
Physiol. Mol. Plant Path. 2000; 56(2):51-
61.
30. Morandi D, Branzanti B, Gianinazzi-Pearson
V. Effect of some plant flavonoids on in vitro
behaviour of an arbuscular mycorrhizal fungus.
Agronomie. 1992; 12(10): 811-816.
31. Shirley BW, Flavonoids in seeds and grains:
physiological function, agronomic importance
and the genetics of biosynthesis. Seed Sci.
Res. 1998; 8: 415-422.
32. Gould KS, Lister C. Flavonoid Functions in
plants. In Andersen ØM, Markham KR. (eds.),
Flavonoids. CRC Press, Boca Raton, 2006,
pp. 397-442.
33. Lanot A, Morris P. Elicitation of isoflavan
phytoalexins. In Marquez AJ (ed.), Lotus
japonicus handbook. Springer, The
Netherlands, 2005, pp. 355-361.
34. Vergas FD, Lopez OP. Natural colourants
for food and nutraceutical uses. CRC press,
USA, 2003, pp. 93-109.
35. Kaplan E, Kopka J, Haskell DW. et al.
Exploring the Temperature-Stress Metabolome
of Arabidopsis. Plant Physiol. 2004; 136:
4159-4168.
36. Hernandez I, Alegre L, Munne-Bosch S.
Drought-induced changes in flavonoids and
other low molecular weight antioxidants in
Cistus clusii grown under Mediterranean field
conditions.Tree Physiol. 2004; 24:1303-
1311.
37. Iwashina T. Flavonoid function and activity to
plants and other organisms. Biol. Sci. Space.
2003:17(1): 24-44.
38. Mamolos AP, Kalburtji KL. Significance of
Allelopathy in crop rotation. In Kohli RK,
Singh HP, Batish DR. (eds.), Allelopathy in
Agroecosystems. Published by Food
Products Press. Binghamton, USA, 2001, pp.
197-218.
page-30
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
39. Duke SO. The emergence of grass root
chemical ecology. Proc. Natl. Acad. Sci.
2007; 104(43): 16729-16730.
40. Dixon RA, Steele CL. Flavonoids and
isoflavonoids a gold mine for metabolic
engineering. Trends Plant Sci. 1999; 4(10):
394-400.
41. Sundaravarathan S, Kannaiyan S. Role of plant
flavonoids as signal Molecules to Rhizobium.
In Kannaiyan S. (ed.), Biotechnology of
Biofertilizers. Co published by Kluwer
Academic Publisher, The Netherlands, 2002,
pp. 144-164.
42. Begum AA, Leibovitch S, Migner P, Zhang F.
Specific flavonoids induced nodes of
Rhizobium leguminosarum increased pea
(Pisum sativum L.) and lentil (Lens culinaris
L.) nodulation in controlled growth chamber
environment. J. Exp. Bot. 2001; 52(360):
1537-1543.
43. Fox JE, Starcevic M, Kow KY, Burow ME.
et al. Nitrogen fixation: Endocrine disrupters
and flavonoid signalling. Nature.
2001:413(6852): 128-129.
44. Subramanian S, Stacey G, Yu O. Distinct,
crucial roles of flavonoids during legume
nodulation. Trends Plant Sci. 2007:
12(7):282-285.
45. Straney D, Khan R, Tan R, Bagga S. Host
recognition by pathogenic fungi through plant
flavonoids. In Buslig BS, Manthey JA (eds.),
Flavonoids in cell function: Advances in
experimental medicine and biology. Vol.
505, Kluwer Academic/Plenum publishers,
New York, USA, 2002, pp. 9-22.
46. Gough C, Galera C, Vasse J, Webster G. et
al. Specific Flavonoids Promote Intercellular
Root Colonization of Arabidopsis thaliana
by Azorhizobium caulinodans ORS571. Mol.
Plant Microbe Interact. 1997; 10(5); 560-
570.
47. Tsai SM, Phillips DA. Flavonoids released
naturally from alfalfa promote development of
symbiotic Glomus spores in vitro. Appl.
Environ. Microbiol. 1991; 57(5): 1485-1488.
48. Steinkellner S, Lendzemo V, Langer I, Schweiger
P. et al. Flavonoids and strigolactones in root
exudates as signals in symbiotic and pathogenic
plant-fungus interactions. Molecules. 2007;
12: 1290-1306.
49. Sugiyama A, Shitan N, Yazaki K. Signaling from
soybean roots to rhizobium An ATP-binding
cassette-type transporter mediates genistein
secretion. Plant Signal Behav. 2008; 3(1):38-
40.
50. Ndakidemi PA, Dakora FD. Legume seed
flavonoids and nitrogenous metabolites as signals
and protectants in early seedling development.
Funct. Plant Biol. 2003; 30(7):729-745.
51. Westwood JH. Characterization of the
Orobanche–Arabidopsis system for studying
parasite–host interactions. Weed Sci. 2000;
48:742-748.
52. Albrecht H, Yoder JI, Philips DA. Flavonoids
Promote Hausteria Formation in the Root
Parasite Triphysaria versicolor. Plant Physiol.
1999; 119, pp. 585- 591.
53. Sharon A, Gressel J. Elicitation of a flavonoid
phytoalexin accumulation in Cassia obtusifolia
by a mycoherbicide: Estimation by AlCl3-
spectrofluorimetry. Pest. Biochem.
Physiol.1991:41(2): 142-149.
54. Jeandet P, Douillet-Breuil AC, Bessis R. et al.
Phytoalexins from the Vitaceae: Biosynthesis,
page-31
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Phytoalexin Gene Expression in Transgenic
Plants, Antifungal Activity, and Metabolism. J.
Agric. Food Chem. 2002; 50(10):2731-
2741.
55. Gottstein D, Gross D. Phytoalexins of woody
plants. Trees. 1992; 6: 55-68.
56. Bajaj YPS. Biotechnology in Agriculture
and Forestry 37: Medicinal and natural
plants IX. Germany, Springer-Verlag Berlin
Heidelberg, 1996, pp. 104.
57. Parkniske M, Ahlborn B, Werner D.
Isoflavonoid-Inducible resistance to the
phytoalexin Glyceolin in soybean rhizobia. J.
Bacteriol. 1991; 173(11):3432-3439.
58. Keilig K, Muller JL. Effect of flavonoids on
heavy metal tolerance in Arabidopsis thabiana
seedlings. Bot. Studies. 2009; 50: 311-318.
59. Shimoji H, Yamasaki H. Inhibitory effects of
flavonoids on alternative respiration of plant
mitochondria. Biologia Plantarum. 2005;
49(1): 117-119.
60. Agate G, Stefano G, Biricolti S, Tattini M.
Mesophyll distribution of
‘antioxidant’flavonoid glycosides in Ligustrum
vulgare leaves under contrasting sunlight
irradiance. Ann. Bot. 2009; 104(5):853-861.
61. Perez FJ, Villegas D, Mejia N. Ascorbic
acid and flavonoid-peroxidase reaction as a
detoxifying system of H2O2 in grapevine
leaves. Phytochemistry. 2002; 60(6): 573-
580.
62. Hernández I, Alegre L, Breusegem FV, Munné-
Bosch S. How relevant are flavonoids as
antioxidants in plants? Trends Plant Sci. 2009;
14(3): 125-132.
63. Farombi EO, Akanni OO, Emerole GO.
Antioxidant and Scavenging Activities of
Flavonoid Extract (Kolaviron) of Garcinia kola
Seeds. Pharm. Biol. 2002; 40(2): 107-116.
64. Grace SC, Logan BA. Energy dissipation and
radical scavenging by the plant
phenylpropanoid pathway. Philos Trans R
Soc Lond B Biol Sci. 2000; 355(1402):
1499–1510.
65. Scervino JM, Ponce MA, Erra-Bassells R. et
al. Flavonoids exhibit fungal species and genus
specific effects on the presymbiotic growth of
Gigaspora and Glomus. Mycol. Res. 2005;
109(7):789-794.
66. Kensuke K, Norihisa M, Kazuo S, Taizo H.
Flavonoids induce germination of
basidiospores of the ectomycorrhizal fungus
Suillus bovinus. Mycorrhiza. 2007; 17 (7):
563-570.
67. Isobe K, Tateishi A, Nomura K. et al.
Flavonoids in the Extract and Exudate of the
Roots of Leguminous Crops. Plant Prod. Sci.
2001; 4 (4): 278-279.
68. Gunawardena U, Rodriguez M, Straney D. et
al. Tissue-Specific Localization of Pea Root
Infection by Nectria haematococca.
Mechanisms and Consequences. Plant
Physiol. 2005; 137: 1363-1374.
69. Mandelbaum CI, Piche Y. The role of root
exudates in Arbuscular mycorrhiza initiation.
In Mukerji KG. (ed.), Mycorrhizal Biology.
Kluwer Academic/Plenum Publishers, New
York, 2000, pp.153-172.
70. Sharma B, Kumar P. In vitro antifungal potency
of some plant extracts against Fusarium
oxysporum. Int. J. Green Pharm. 2009;
3(1): 63-65.
page-32
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
71. Poureel L, Grotewold E. Participation of
Phytochemicals in Plant Development and
Growth. In Osbourn AE, Lanzotti V. (eds.),
Plant-derived Natural Product. Springer,
Dordrecht, Heidelberg, London, New York,
2009, pp. 269-282.
72. Kubasek WL, Shirley BW, McKillop A. et
al. Regulation of Flavonoid Biosynthetic
Genes in Germinating Arabidopsis Seedlings.
The Plant Cell. 1992; 4: 1229-1236.
73. Fritz D, Bernardi AP, Haas JS. et al.
Germination and growth inhibitory effects of
Hypericum myrianthum and H.
polyanthemum extracts on Lactuca sativa L.
Braz. J. Pharmacognosy. 2007; 17(1): 44-
48.
74. Kim YH, Hamayun M, Khan AL. et al.
Exogenous application of plant growth
regulators increased the total flavonoid
content in Taraxacum officinale Wigg. Afr.
J. Biotechnol. 2009; 8 (21): 5727-5732.
75. Debeaujon I, Lepiniec L, Poureel L,
Routaboul JM. Seed coat development and
dormancy. In Bradford K, Nonogaki H.
(eds.), Seed Development, Dormancy
and Germination, Annual Plant Reviews.
Vol. 27, Blackwell Publishing Ltd, 2007, pp.
25-49.
76. Nandakumar L, Rangaswamy NS. Effect of
some Flavonoids and Phenolic acids on Seed
Germination and Rooting. J. Exp. Bot.
1985; 36(8): 1313-1319.
77. Tevini M, Teramura AH. UV-B effects on
terrestrial plants. J. Photochem. Photobiol.
1989; 50:479-487.
78. Richard LL, Rainer WH, Bruce DC. et al.
Population differences in Trifolium repens L.
response to ultraviolet-B radiation: foliar
chemistry and consequences for two
lepidopteran herbivores. Oecologia. 2000;
122: 20-28.
79. Caldwell MM, Robberecht R, Flint SD.
Internal filters: Prospects of UV-acclimation in
higher plants. Physiol. Plant.1983; 58(3):
445-450.
80. Campos JL, Figueras X, Pinol MT. et al.
Carotenoid and conjugated polyamine levels
as indicators of ultraviolet-C induced stress in
Arabidopsis thaliana. Photochem. Photobiol.
2008; 53(5): 689-693.
81. Sharma R. Impact of Solar UV-B on Tropical
Ecosystems and Agriculture. Case Study:
Effect of UV-B on Rice. Proc. SEAWPIT98
& SEAWPIT2000. 2001; 1: 92-101.
82. Stafford HA. Flavonoid Evolution: An enzymic
approach. Plant Physiol. 1991; 96: 680-685.
83. Hollósy F. Effects of ultraviolet radiation on
plant cells. Micron. 2002; 33:179–197.
84. Cen YP, Bornman JF. The effect of exposure
to enhanced UV-B radiation on the penetration
of monochromatic and polychromatic UV-B
radiation in leaves of Brassica napus. Physiol.
Plant. 1993; 87: 249-255.
85. Pinter J, Kosa E, Hadi G. et al. Effect of
increased UV-B radiation on the anthocyanin
content of maize (Zea mays L) leaves. Acta
Agronomica Hugarica. 2007; 55(1): 7-17.
86. Stefanowska M, Kuras M, Kacperska A. Low
Temperature-induced Modifications in cell
ultrastructure and Localization of Phenolics in
winter Oilseed Rape (Brassica napus L. var.
oleifera L.) Leaves. Ann. Bot. 2002; 90: 637-
645.
page-33
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
87. Korn M, Peterek S, Mock HP. et al. Heterosis
in the freezing tolerance, and sugar and
flavonoid contents of crosses between
Arabidopsis thaliana accessions of widely
varying freezing tolerance. Plant cell Environ.
2008; 31(6): 813-827.
88. Chutipaijit S, Cha-Um S, Sompornpailin K.
Differential accumulations of Proline and
Flavonoids in indica rice varieties against
Salinity. Pak. J. Bot. 2009; 41 (5): 2497-
2506.
89. Deroles S. Anthocyanin Biosynthesis in the
plant cell cultures: A potential source of
Natural colourants. In Gould K, Davies K,
Winefield C. (eds.), Anthocyanins:
Biosynthesis, Functions, and Applications.
Springer Science and Business media, New
York, USA, 2009, pp. 107-168.
90. Ram HYM, Mathur G. Flower Colour
Changes in Lantana camara. J. Exp. Bot.
1984; 35(11): 1656-1662.
91. Napoli CA, Fahy D, Wang HY, Taylor LP.
White anther: A petunia Mutant that abolishes
pollen Flavonol Accumulation, Induces male
sterility, and is complemented by a Chalcone
Synthase Transgene. Plant Physiol. 1999;
120: 615-622.
92. Harborne JB. The flavonoids: advances in
research since 1986. Chapman and Hall/
CRC, USA, 1994, pp. 591.
93. Marinova K, Pourcel L, Weder B. et al. The
Arabidopsis MATE Transporter TT12 Acts
as a Vacuolar Flavonoid/H1-Antiporter Active
in Proanthocyanidin-Accumulating Cells of the
Seed Coat. The Plant Cell. 2007; 19: 2023–
2038.
94. Davies KM. An introduction to plant pigments
in Biology and commerce. In Davies K. (ed.),
Plant Pigments and their Manipulation.
Annual plant Reviews, Vol.14, CRC Press
Blackwell Publishing Ltd, Oxford, UK. 2004,
pp. 1-22.
95. Davies K, Schwinn K. Developmental control
and Biotechnology of Floral Pigmentation. In
Jordan BR. (ed.), The Molecular Biology
and Biotechnology of Flowering. 2nd edition,
CABI publishing, Oxfordshire, UK, 2006:178-
236.
96. Cseke LJ, Lu CR, Kornfeld A. et al. How and
Why These Compounds Are Synthesized by
Plants. In Cseke LJ, Kirakosyan A, Kaufman
PB, Warber SL, Duke JA, Brielman HL. (eds.),
Natural Products from Plants. 2nd edition,
Published by CRC Press, Taylor and Francis
Group, Boca Raton, FL, 2006, pp. 51-100.
97. Jurd L, Asen S. The formation of metal and
Øco-pigmentØ complexes of cyanidin 3-
glucoside. Phytochemistry. 1966; 5(6): 1263-
1271.
98. Shoji K, Miki N, Nakajima N. et al. Perianth
Bottom-Specific Blue Colour Development in
Tulip cv.Murasakizuisho requires Ferric ions.
Plant Cell Physiol. 2007; 48 (2): 243-251.
99. Roth CM, Shroyer JP, Paulsen GM. Allelopathy
of sorghum on wheat under several tillage
systems. Agron. J. 2000; 92:855-860.
100. Kong C, Liang W, Xu X. et al. Release and
Activity of Allelochemicals from Allelopathic
Rice Seedlings. J. Agric. Food Chem. 2004;
52 (10):2861-2865.
101. Alford ER, Vivanco JM, Paschke MW. The
Effects of Flavonoid Allelochemicals from
page-34
Vol-6, Issue-1, 2011
Int J Pharm Sci Tech (© 2011)
Knapweeds on Legume- Rhizobia Candidates
for Restoration. Restoration Ecol. 2009;
17(4):
506-514.
102. Mitchell MJ, Keogh DP, Crooks JR, Smith
SL. Effects of plants flavonoids and other
allelochemicals on insect cytochrome P-450
dependent steroid hydroxylase activity. Insect
Biochem. Mol. Biol. 1993; 23(1): 65- 71.
103. Lotina-Hennsen B, King-Diaz B, Aguilar MI,
Terrones MGH. Plant secondary mechanisms
of allelopathy. In Reigosa MJ, Pedrol N,
Gonzalez L. (eds.), Allelopathy: A
physiological process with ecological
implications. Published by Springer, The
Netherlands, 2006, pp. 229-266.
104. Putnam AR. Allelochemicals from plants as
herbicides. Weed Tec h. 1988; 2(4):510-518.
105. Walker TS, Bais HP, Grotewold E, Vivanco
JM. Root exudation and rhizosphere biology.
Plant Physiol. 2003; 132:44-51.
page-35
