review

Plant Signaling & Behavior 6:11, 1720-1731; November 2011; ©2011 Landes Bioscience

Influence of abiotic stress signals

on secondary metabolites in plants
Akula Ramakrishna and Gokare Aswathanarayana Ravishankar*
Plant Cell Biotechnology Department; Central Food Technological Research Institute (Constituent Laboratory of Council of Scientific and Industrial Research); Mysore, India

Key words: abiotic stress, anthocyanin, climate change, cold stress, jasmonates, plant cell and tissue culture, polyamines, secondary
metabolites

Abbreviations: ABA, abscisic acid; JA, jasmonic acid, MeJ, methyl jasmonate; Put, putrescine; Spd, spermidine; Spm, spermine;
BRs, brassinosteroids

metabolites also contribute to the specific odors, tastes and col-

Plant secondary metabolites are unique sources for
ors in plants.2 Plant secondary metabolites are unique sources for
pharmaceuticals, food additives, flavors, and industrially
important biochemicals. Accumulation of such metabolites
food additives, flavors, pharmaceuticals and industrially impor-
often occurs in plants subjected to stresses including various tant pharmaceuticals.3,4 Chemicals include calcium, abscisic acid
elicitors or signal molecules. Secondary metabolites play a (ABA), salicylic acid (SA), polyamines and Jasmonates (JA), nitric
major role in the adaptation of plants to the environment oxide are involved in stress responses in plants.5 Accumulation of
and in overcoming stress conditions. Environmental factors metabolites often occurs in plants subjected to stresses includ-

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viz. temperature, humidity, light intensity, the supply of ing various elicitors or signal molecules. Secondary metabolites
water, minerals and CO2 influence the growth of a plant and have significant practical applications in medicinal, nutritive and
secondary metabolite production. Drought, high salinity cosmetic purposes, besides, importance in plant stress physiol-
and freezing temperatures are environmental conditions ogy for adaptation.1 The production of these compounds is
that cause adverse effects on the growth of plants and the often low (less than 1% dry weight) and depends greatly on the

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productivity of crops. Plant cell culture technologies have
physiological and developmental stage of the plant.6 Some of
been effective tools for both studying and producing plant
secondary metabolites under in vitro conditions and for plant
the plant derived natural products include drugs such as mor-
improvement. This brief review summarizes the influence phine, codeine, cocaine, quinine etc. Catharanthus alkaloids,
of different abiotic factors include salt, drought, light, heavy belladonna alkaloids, colchicines, phytostigminine, pilocarpine,
metals, frost etc. on secondary metabolites in plants. The reserpine and steroids like diosgenin, digoxin and digitoxin, fla-
focus of the present review is the influence of abiotic factors vonoids, phenolics etc. In this communication we have reviewed
on secondary metabolite production and some of important the literature on the environmental influence on plant secondary
plant pharmaceuticals. Also, we describe the results of in metabolite production in in vitro and in vivo conditions, except
vitro cultures and production of some important secondary where our studies are quoted, the information is largely based on
metabolites obtained in our laboratory. others work from published literature.

Abiotic Factors Influencing Secondary Metabolites

Introduction A wide range of environmental stresses (high and low temperature,

drought, alkalinity, salinity, UV stress and pathogen infection)
Plant secondary metabolites are often referred to as compounds are potentially harmful to the plants.1 Elicitation has been widely
that have no fundamental role in the maintenance of life pro- used to increase the production or to induce de novo synthesis of
cesses in the plants, but they are important for the plant to inter- secondary metabolites in in vitro plant cell cultures.7 A number
act with its environment for adaptation and defense. However we of researchers have applied various elicitors for enhancement of
are beginning to understand the crucial role played by them in secondary metabolite production in cultures of plant cell, tissue
plant growth and development. In higher plants a wide variety of and organ.8,9 Environmental stresses, such as pathogen attack,
secondary metabolites are synthesized from primary metabolites UV-irradiation, high light, wounding, nutrient deficiencies, tem-
(e.g., carbohydrates, lipids and amino acids). They are needed perature and herbicide treatment often increase the accumula-
in plant defense against herbivores and pathogens. Often they tion of phenylpropanoids.10 Nutrient stress also has a marked
may confer protection against environmental stresses.1 Secondary effect on phenolic levels in plant tissues.11 The concentrations of
various secondary plant products are strongly dependent on the
*Correspondence to: Gokare A. Ravishankar; Email: [email protected] growing conditions and have impact on the metabolic pathways
Submitted: 07/17/11; Accepted: 08/03/11 responsible for the accumulation of the related natural products.
DOI: 10.4161/psb.6.11.17613
Exposure to drought or salt stress causes many common reactions

1720 Plant Signaling & Behavior Volume 6 Issue 11

 REVIEW

Figure 1. Various abiotic stress signals creating stress in plants (adapted from Mahajan and Tuteja 2005).13

Table 1. Influence of various abiotic signals on secondary metabolites salinity. Expression levels of certain genes have been shown to
in plants increase in response to reactive oxygen species, cold temperature,
Abiotic signals Reference high temperature and osmotic stress.12 Salt stress in soil or water

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Methyl jasmonate 97
is one of the major stresses especially in arid and semi-arid regions
and can severely limit plant growth and productivity.13 Bryant
Jasmonic acid 94
et al. (1983)14 have hypothesized that when plants are stressed,
Salicylic acid 45 an exchange occurs between carbon to biomass production or
Calcium 110 formation of defensive secondary compounds. A stress response

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Polyamines
Nitric oxide
Melatonin
Serotonin
90
5
130
134
is induced when plants recognizes stress at the cellular level.
Secondary metabolites are involved in protective functions in
response to both biotic and abiotic stress conditions. Formation
of phenyl amides and dramatic accumulation of polyamines in
bean and tobacco under the influence of abiotic stresses were
Brassino steroids 135
reported, suggesting antioxidant role of these secondary metabo-
Abscisic acid 5
lites.15 Similarly anthocyanin accumulation is stimulated by vari-
Metal ions 41 ous environmental stresses, such as UV, blue light, high intensity
Plant growth regulators 9 light, wounding, pathogen attack, drought, sugar and nutrient
Light 71 deficiency.16
Nutrient stress 11
Climate change 116
Salt Stress
Temperature 61
Salt environment lead to cellular dehydration, which causes
Cold 50
osmotic stress and removal of water from the cytoplasm resulting
Drought 25 in a reduction of the cytosolic and vacuolar volumes. Salt stress
Salt 12 often creates both ionic as well as osmotic stress in plants, result-
Chemical stress 13 ing in accumulation or decrease of specific secondary metabolites
in plants.13 Anthocyanins are reported to increase in response to
in plants. Both stresses lead to cellular dehydration, which causes salt stress.17 In contrast to this, salt stress decreased anthocyanin
osmotic stress and removal of water from the cytoplasm to vacu- level in the salt-sensitive species.18 Petrusa and Winicov (1997)19
les. Different abiotic stress factors creating stress is depicted in demonstrated that salt tolerant alfalfa plants rapidly doubled
Figure 1 and Table 1. their proline content in roots, whereas in salt sensitive plants
Deficiencies in nitrogen and phosphate directly influence the the increase was slow. However, Aziz et al. (1998)20 reported a
accumulation of phenylpropanoids.10 Potassium, sulfur and mag- correlation between proline accumulation and salt tolerance in
nesium deficiency are also reported to increase phenolic concen- Lycopersicon esculentum and Aegiceras corniculatum respectively.
trations. Low iron level can cause increased release of phenolic In tomato cultivars under salt stress endogenous JA was found to
acids from roots.11 Calcium levels have been implicated in plant accumulate.21 Polyphenol synthesis and accumulation is generally
response to many abiotic stresses including cold, drought and stimulated in response to biotic or abiotic stresses.10,22 Increase in

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polyphenol content in different tissues under increasing salinity Table 2. Salt stress increases various secondary metabolites in plants
has also been reported in a number of plants.17 Navarro et al. Secondary
Plant species Reference
(2006)23 showed increased total phenolics content with mod- metabolite
erately saline level in red peppers. Plant polyamines have been Sorbitol Lycopersicon esculentum 140
shown to be involved in plant response to salinity. Salinity- GABA Sesamum indicum L. 141
induced changes of free and bound polyamine levels in sunflower
Flavonoids Hordeum vulgare 142
(Helianthus annuus L.) roots was reported.24 The influence of salt
stress on secondary metabolites in plants are shown in Table 2. Jasmonic acid Lycopersicon esculentum 21
Polyphenol Cakile maritima 143
Drought Stress Tropane alkaloids Datura innoxia 144
Anthocyanins Grevillea spec. 17
Drought stress is one of the most significant abiotic stress that Trigonelline Glycine max 145
affect plant growth and development.25 Drought stress occurs Glycinebetaine Trifolium repens 146
when the available water in the soil is reduced to such critical
Polyamines Oryza sativa 147
levels and atmospheric conditions adds to continuous loss of
Glycine betaine Triticum aestivum 148
water. Drought stress tolerance is seen in all plants but its extent
varies from species to species. The drought stress arises due to Sucrose and Starch Cenchrus pennisetiformis 149
the water deficit, usually accompanied by high temperatures and Adapted from Parvaiz and Satyavati 2008.150
solar radiation.25 Water deficit and salt stress are global issues to
ensure survival of agricultural crops and sustainable food produc- Table 3. Influence of drought stress on various plant secondary
tion.26 Drought often causes oxidative stress and was reported to metabolites
show increase in the amounts of flavonoids and phenolic acids in Secondary metabolite Plant species Reference

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willow leaves.27 Drought stress influenced changes in the ratio of Glycosides Scrophularia ningpoensis 151
chlorophyll “a” and “b” and carotenoids.28 A reduction in chloro-
Morphine alkaloids Papaver somniferum 152
phyll content was reported in cotton under drought stress29 and
Trigonelline Glycine max 153
Catharanthus roseus.30 Drought conditions decreased the content
of saponins in Chenopodium quinoa from 0.46% dry weight (dw) Glucosinolates Brassica napus 154

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in plants growing under low water deficit conditions to 0.38% in Chinolizidin alkaloids Lupinus angustifolius 155
high water deficit plants.30 Anthocyanins are reported to accumu- Epicatechins Camellia sinensis 156
late under drought stress and at cold temperatures. Plant tissues Betulinic acid Hypericum brasiliense 157
containing anthocyanins are usually rather resistant to drought.31 Rutine Hypericum brasiliense 157
For example, a purple cultivar of chilli resists water stress better
Flavonoids Prisms sativum 27
than a green cultivar.32 Flavonoids have protective functions dur-
Anthocyanins Pisum sativum 158
ing drought stress. Flavonoids are implicated to provide protec-
tion to plants growing in soils that are rich in toxic metals such as Chlorogenic acid Helianthus annuum 159
aluminum.16 The influence of drought stress on various second- Rosmarinic acid Salvia miltiorrhiza 160
ary metabolites are given in Table 3. Adapted from Bartels and Sunkar 2005.161

Influence of Heavy Metal Stress on Secondary on the production of secondary metabolites.40 In an attempt to
Metabolites enhance betalaines production, the hairy roots were exposed
to metal ions.41 Obrenovic (1990)42 has demonstrated stimula-
Metal ions (lanthanum, europium, silver and cadmium), and oxa- tory effects of Cu 2+ on the accumulation of betacyanins in cal-
late are also influenced secondary metabolite production.33 The lus cultures of Amaranthus caudatus. Addition of Zn2+ (900 μM)
trace metal nickel (Ni) is essential component of urease enzyme, enhanced the yield of lepidine in cultures of Lepidium sativum.42
is needed for plant development.33 However, elevated Ni concen- However, Cu proved more effective than Zn in enhancing the
trations reduce plant growth.34 The significant decrease in antho- yield.43 AgNO3 or CdCl2 elicited overproduction of two tropane
cyanin levels due to Ni stress has been reported by Hawrylak et al. alkaloids, scopolamine and hyoscyamine, in hairy root cultures
(2007).35 Moreover, Ni has been shown to inhibit accumulation of Brugmansia candida.44 Rare-earth metal (lanthanum) had
of anthocyanins.36 Trace metals obviously limit anthocyanin bio- influence on production of taxol in cell culture of Taxus sp.45
synthesis by inhibiting activity of l-phenylalanine ammonia-lyase Oat and bean plants treated with cadmium and copper signifi-
(PAL).36 Effective accumulation of metals (Cr, Fe, Zn and Mn) cantly increased putrescine (Put) content.46 However, a decrease
also produced an increase of oil content up to 35% in Brassica in Put level in Cd 2+ or Cu 2+ treated sunflower leaf disks has been
juncea.37 Cu2+ and Cd 2+ have been shown to induce higher yields reported. Sunflower leaf disks showed a significant decreased in
of secondary metabolites such as shikonin38 and also on the pro- spermidine (Spd) content and no variation in spermine (Spm)
duction of digitalin.39 Cu2+ also stimulated the production of bet- level when they were treated with Cd 2+ or Cu 2+ respectively.47
alains in Beta vulgaris.40 Co2+ and Cu 2+ exhibit stimulatory effect However, Jacobsen et al. (1992)48 reported no changes in Spd

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or Spm content in chromium-exposed leaves of barley and rape Elevated temperatures increase leaf senescence and root second-
plants, but Put accumulated with increasing chromium concen- ary metabolite concentrations in the herb Panax quinquefolius.62
trations or exposure time. Lin and Kao (1999)49 reported that Elevated temperatures by 5°C would reduce photosynthesis and
copper treatment increased Put, but a decrease in Spm concentra- biomass production of P. quinquefolius, on the contrary storage
tion in rice leaves. ginsenoside is reported to be enhanced.63
Several studies have examined the effects of increased temper-
Influence of Cold Stress on Secondary Metabolites atures on secondary metabolite production of plants.61 Lower soil
temperatures caused an increase in levels of steroidal furostanol
Low temperature is one of the most harmful abiotic stresses and spirostanol saponins.64 Temperature variations has multiple
affecting temperate plants. These species have adapted to varia- effects on the metabolic regulation, permeability, rate of intracel-
tions in temperature by adjusting their metabolism during lular reactions in plant cell cultures.61 Changing the culture tem-
autumn, increasing their content of a range of cryo-protective perature may change the physiology and metabolism of cultured
compounds to maximize their cold tolerance.50 In the cryopreser- cells and subsequently affect growth and secondary metabolite
vation process, environmental changes including osmotic injury, production.61 Temperature range of 17–25°C is normally used for
desiccation and low temperature can impose a series of stresses the induction of callus tissues and growth of cultured cells.6 Yu
on plants.50 During over wintering, temperate plant metabolism et al. (2005) 65 reported the influence of temperature and light
is redirected toward synthesis of cryoprotectant molecules such as quality on production of ginsenoside in hairy root culture of
sugar alcohols (sorbitol, ribitol, inositol) soluble sugars (saccha- panax ginseng. Chan et al. (2010) 66 reported that Melastoma mal-
rose, raffinose, stachyose, trehalose), and low-molecular weight abathricum cell cultures incubated at a lower temperature range
nitrogenous compounds (proline, glycine betaine).50 Cold stress (20 ± 2°C) grew better and had higher anthocyanin production
increases phenolic production and their subsequent incorpora- than those grown at 26 ± 2°C and 29 ± 2°C. Optimum tempera-
tion into the cell wall either as suberin or lignin.51 In addition, ture (25°C) maximizes the anthocyanin yield as demonstrated

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apple tree adaptation to cold climate was found to be associated in cell cultures of Perilla frutescens67 and strawberry.68 Lower
with a high level of chlorogenic acid.52 Lignification and suberin temperature favors anthocyanin accumulation, but reduces cell
deposition are also shown to increase resistance to cold tempera- growth. For strawberry cell culture, maximum anthocyanin con-
tures. A mechanism by which suberin and lignin may protect tent was obtained at 15°C and it was about 13-fold higher than
plants from freeze damage.51 Christie et al. (1994)53 reported the that obtained at 35°C.68 For suspension cultures of Perilla fru-

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accumulation of anthocyanins during cold stress. Pedranzani et
al. (2007)54 reported that cold and water stresses produce changes
in endogenous jasmonates in Pinus pinaster. Lei et al. (2004)55
reported that melatonin protect against cold-induced apoptosis
tescens, anthocyanin production was remarkably reduced at the
relatively high temperature of 28°C, whereas 25°C was optimal
for the productivity of the pigment.67 Similar observations on
optimal productivity of anthocyanin in cell suspension cultures
in carrot suspension cells by upregulation of polyamines (putres- of Daucus carota was reported.69 Pigment release from hairy root
cine and spermine). Moreover, Melatonin applied to cucumber cultures of Beta vulgaris under the influence of different tempera-
(Cucumis sativus L.) seeds improves germination during chilling tures was reported.70
stress.56 Recently, Zhao et al. (2011)57 reported that melatonin
improves the survival of cryopreserved callus of Rhodiola crenu- Influence of Light on Secondary Metabolite
lata. The survival rate of the cryopreserved callus increased when Production
the callus was pretreated with 0.1 μM melatonin.
Recently, the effect of cold stress on polyamime accumulation It is well known that light is a physical factor which can affect the
was reported.58 When leaves of wheat (Triticum aestivum L.) are metabolite production. Light can stimulate such secondary metab-
exposed to a cold temperature, accumulation of putrescine (6–9 olites include gingerol and zingiberene production in Z. officinale
times), spermidine accumulates to a lesser extent and, spermine callus culture.71 A positive correlation between increasing light
decreases slightly. Moreover, alfalfa (Medicago sativa L.) also intensity and levels of phenolics has been reported.11 Larsson et al.
accumulates putrescine under low temperature stress.59 Hummel (1986)72 reported decreases in foliar tannin and phenolic glyco-
et al. (2004) 60 reported that cold tolerance was associated with sides in shaded willow foliage. Arakawa (1993) studied the effect
increased levels of polyamines (agmatine and putrescine) and of UV light on anthocyanin accumulation in light colored sweet
their levels could be a significant marker of chilling tolerance in cherry. In apples, UV light from 280–320 nm synergistically
seedlings of P. antiscorbutica. stimulate anthocyanin synthesis when it was combined with red
light.74 Effect of light irradiation on anthocyanin production in
Temperature Variations Influence Plant Growth cell suspension cultures of Perilla frutescens was reported.75 Chan
and Secondary Metabolite Production et al. (2010) 66 investigated the effects of different environmental
factors, such as light intensity, irradiance (continuous irradiance
Temperature strongly influences metabolic activity and plant or continuous darkness), on cell biomass yield and anthocyanin
ontology, and high temperatures can induce premature leaf production in cultures of Melastoma malabathricum. Moderate
senescence.61 Carotenoids in Brassicaceae, including β-carotene, light intensity (301–600 lx) induced higher accumulation of
were found to be slightly decreased after thermal treatments.61 anthocyanins, the cultures exposed to 10-d continuous darkness

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showed the lowest pigment content, while the cultures exposed to broad effectiveness can be explained by the fact that these mol-
10-d continuous irradiance showed the highest pigment content. ecule acts as elicitors in a wide spectrum of signaling pathways.
Light irradiation exhibited significant influence on the accumu- MeJ and JA have been proved to be able to elicit the production of
lation of anthocyanins by cell cultures of strawberry,76 Daucus several compounds (alkaloids, terpenoid and phenolic phytoalex-
carota69 and Centaurea cyanus.77 ins, coumarins and taxanes) in many plant species.94 Exogenous
UV-B have been seen to increase in flavonoids in barley,78 and jasmonates applied to plants have been shown to exhibit morpho-
in polyamines in cucumber.79 Hagimori et al. (1982) 80 reported logical and physiological effects.94 Jasmonates have been associ-
the effect of light and plant growth regulators on digitoxin forma- ated with the accumulation of secondary metabolites, which are
tion in Digitalis purpurea L. Moreover, effect of light irradiation also part of the defense response.94 MeJA increased the content of
influenced artemisinin biosynthesis in hairy roots of Artemisia shikonin and its derivatives (red naphthoquinonone) in Onosma
annua.81 Fett-Neto et al. (1995) 82 reported the effect of white light paniculatum cultured cells. MeJA can also promote the biosyn-
on taxol and baccatin III accumulation in cell cultures of Taxus thesis of endogenous IAA in plants.95 Exogenous application of
cuspidate. UV-B irradiation enhanced the concentration of flavo- jasmonates greatly stimulated the biosynthesis of a wide range of
nols in Norway spruce (Picea abies).83 Catharanthus roseus plants, secondary metabolites in cell suspension cultures, and in intact
exposed to UV-B light show significant increases in the produc- plants.94 MeJA induced anthocynin accumulation was reported
tion of vinblastine and vincristine, which have proven effective in Arabidopsis thaliana,96 strawberry fruits,97 Vaccinium pahalae,98
in the treatment of leukemia and lymphoma.84 UV-B radiation Vitis vinifera99 and tulip leaves.100 Moreover, MeJA and salicylic
could increase flavonoid content and phenylalanine ammonia- acid induce anthocyanin production in in vitro callus cultures of
lyase (PAL) activity, associated with a decrease in chlorophyll D. carota.101
content.85 UV (300–400 nm) increased flavonoids in the roots MeJA inhibited the cell growth and promoted the sec-
of pea plants.86 UV-B was also shown to induce the production ondary metabolite production in root cultures of Bupleurum
of flavonols in silver birch and grape leaves.87 Moreover, under falcatum L.,102 Taxus spp.103 and rice.104 The effects of exog-

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six different daily doses of UV-radiation (UV-A and UV-B), enously applied MeJ on the content of biogenic amines include
photosynthetic pigments, condensed tannins were accumulated putrescine, spermidine, tyramine, cadaverine and 2-phenyl-
whereas its precursor, (+)-catechin, decreased significantly.88 Our ethylamine in seedlings of common buckwheat (Fagopyrum
recent report suggests that photoperiod regimes influence endog- esculentum) were investigated.105 Influence of different abiotic
enous indoleamines (serotonin and melatonin) in cultured green factors on secondary metabolites in various plant species were

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algae Dunaliella bardawil.89

Influence of Polyamines on Secondary Metabolites

shown in Table 4.

Influence of Plant Growth Regulators

on Secondary Metabolites
Polyamines, putrescine, spermine and spermidine are found in a
wide range of organisms-bacteria, plants and animals. In plants, The production of useful secondary metabolites via plant tissue
polyamines are involved in various physiological events such as and organ culture has been reported by many researchers. Many
development, senescence and stress responses.90 High cellular lev- efforts have been made to improve the productivity of the plant
els of polyamines correlate with plant tolerance to a wide array tissue cultures, such as studies on hormone-dependency, media
of environmental stresses. Moreover, as compared with suscep- composition and light exposure.5,9 Many researchers have tried to
tible plants, stress-tolerant ones generally have a large capacity enhance anthocyanin accumulation through the manipulation of
to enhance polyamine biosynthesis in response to abiotic stress.90 phytohormones in cell suspensions of strawberry (Fragaria anan-
Conversely, treatments with polyamine biosynthesis inhibitors assa),106 Daucus carota,69 Ipomoea batatas107 and Oxalis reclinata.108
reduce stress tolerance, but this effect is reversed by concomitant Plant cell cultures are an excellent source for anthocyanin pro-
application of exogenous polyamines.91 The influence of poly- duction in view of the higher productivity ranging from 10 to
amines on in vitro morphogenetic response and caffeine biosyn- 20% on dry weight basis.109 The influence of different growth
thesis were reported in Coffea canephora.91 Apart from primary regulators on biomass accumulation and anthocyanin content in
metabolic functions, external feeding of certain polyamines are solid-state and liquid state batch cultures of Daucus carota was
known to act as elicitors.91 Spermidine and putrescine, each at studied.69 While growth regulators such as 2,4-D, IAA and NAA
0.75 mM significantly enhanced betalaine production in hairy supplemented at different levels, supported growth as well as
root cultures of red beet.92 Moreover, putrescine at 0.6 mM treat- anthocyanin synthesis. Among the cytokinins, kinetin (0.1 and
ment stimulated polysaccharide synthesis in suspension cultures 0.2 mg l-1) supported highest productivity. The combinations of
of Dendrobium huoshanense.93 IAA at 2.5 mg l-1 and kinetin at 0.2 mg l-1 was superior to other
combinations.69 Lower 2,4-D concentration in the medium lim-
Influence of Methyl Jasmonate and Jasmonic Acid ited cell growth and enhanced both anthocyanin production and
on Secondary Metabolites anthocyanin methylation.69,107 The most significant enhancement
in anthocyanin synthesis was obtained when treated with MeJ.98
It is well known that jasmonic acid (JA) and methyl jasmonate Calcium is an ubiquitous molecule involved in various sig-
(MeJ) are signal molecules in biotic and abiotic stresses.94 Their nal transduction pathways in plants. Calcium have been found

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 Table 4. Effect of different abiotic elicitors on the production of various secondary metabolites in plants
Plant species Abiotic factor Secondary metabolite Reference
Ocimum basilicum Methyl Jasmonate Rosmarinic acid, Caffeic acid 162
Beta vulgaris Calcium, magnesium, manganese, zinc, copper, iron and cobalt Betalain 163
Dioscorea bulbifera CuSO4 Diosgenin 164
Beta vulgaris Metal ions Betalaines 41
Beta vulgaris Polyamines and Mej Betalaine 165
Taxus chinensis Lanthanum Taxol 166
Beta vulgaris and Tagetes patula Micro algal extracts Betalaine 167
Vitis vinifera suspension cultures Jasmonic acid and light irradiation Anthocyanin 99
Beta vulgaris Spermidine, Putrescine and Cu2+ Betalaine 91
Beta vulgaris polyamines Betalaine 91
Brugsmansia candida Salicylic acid Scopolamine Hyposcyamine 45
Lepidium sativum Zn2+ Lepidine 43
Cichorium intybus Polyamines Coumarins 168
Capsicum Nitrate and phosphate Capsaicinoids 169
Capsicum Cinnamic acid, coumaric acid, caffeic acid and ferulic acid Capsaicin production 170
Vanilla planifolia Blue light Vanillin 171
Amaranthus caudatus Cu 2+
Betacyanins 42
Vitis vinifera Sucrose Osmotic stress Anthocyanin 110

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to increase in response to stress such as light, salinity, cold and
drought.110 The influence of calcium on anthocyanin accumula-
tion was studied by Sudha and Ravishankar (2003).8 The treat-
agents was found to regulate anthocyanin production in Vitis
vinifera cultures.110

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ment of Daucus carota cell cultures with low levels of calcium
resulted in the enhancement of both growth and anthocyanin
production. The accumulation of anthocyanin in cell cultures
of Daucus carota and the enzymes involved in their biosynthe-
Influence of Climate Change
on Secondary Metabolites

Climate change is the major threat to biodiversity and one of

sis were investigated. Our recent report suggest that exogenously the main factors affecting human health and well-being over the
administered calcium enhance somatic embryogenesis in in vitro coming decades.116 Cold weather crops like rye, oats, wheat and
cultures of C. canephora.111 Exogenously applied melatonin stim- apples are expected to decline their productivity by about 15% in
ulates root growth and raises endogenous indole-3-acetic acid the next 50 y and strawberries will drop as much as 32% simply
(IAA) in roots of etiolated seedlings of Brassica juncea.112 The because of projected climate changes.116 Plants are extremely sen-
influence of different growth regulators on secondary metabolites sitive to such changes, and do not generally adapt quickly. Ozone
were given in Table 5. exposure has been shown to increase conifer phenolic concentra-
tions,117 but low ozone exposure had no effect on monoterpene
Influence of Nutrient Stress and resin acid concentrations.118 Changes in crop quality due to
on Secondary Metabolites ozone exposure have been studied in a limited number of crops.
For example, in wheat, ozone reduced yield but increased grain
When plants are stressed, secondary metabolite production may protein concentration.119 Moreover, ozone was found to have
increase because growth is often inhibited more than photosyn- positive effects on the quality of potato tubers by reducing sug-
thesis, and the carbon fixed is predominantly allocated to second- ars and increasing the vitamin C content.120 In contrast, O3 has
ary metabolites.1 The Daucus carota callus subjected to phosphate been found to reduce the oil, protein and carbohydrate contents
stress produced 7.2% dry wt anthocyanin against 5.4% dry weight in rape seeds.121 Moreover, in leaves of Ginkgo biloba ozone fumi-
(DW) in the control.113 Nutrient stress also has a marked effect gation increased the concentrations of terpenes, decreased the
on phenolic levels in plant tissues.11 Deficiencies in nitrogen and concentrations of phenolics.122
phosphate lead to the accumulation of phenyl propanoids and Plants grown at high CO2 levels exhibit significant changes
lignification.10 In tomato, the 3-fold increase in anthocyanidins of their chemical composition.123 A prominent example of a CO2
level and the simultaneous doubling of quercetin-3-O-glucoside effect is the decrease of the nitrogen (N) concentration in veg-
occurs under nutrient stress stress.114 Zeid (2009)115 reported that etative plant parts as well as in seeds and grains resulting in the
the increased urea concentration in the nutrient solution mark- decrease of the protein levels.123 Previous studies have shown that
edly increased putrescine contents in Phaseolus vulgaris cell sus- elevated CO2 increases phenolics and condensed tannins in the
pensions. Osmotic stress created by sucrose and other osmatic leaves. In conifers, elevated CO2 influenced a decrease/increase

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 Table 5. Increased secondary metabolite production from in vitro plant tissue and organ culture
Plant species Plant growth regulator Secondary metabolite Reference
Psoralea cordifolia MS + TDZ + BA Isoflavones 172
Vitis vinifera MS + IAA + GA3 + UV Resveratrol 173
Azadirachta indica MS + 2,4-D Azadirachtin 174
Catharanthus roseus MS + 2,4-D + UV-B Catharathine 175
Rauvolfia serpentina MS + BAP + IAA Serpentine 176
Rauvolfia serpentina MS + IAA + Cu2+ Reserpine 177
Stevia rebaudiana MS + BA + NAA Stevioside 178
Capsicum annum MS + 2,4-D + Kin Capsiacin 179
Zataria multiflora MS + IAA + Kinetin Rosmarininc acid 180
Vitis vinifera MS + BAP + NAA Anthocyanin 181
Gymnema sylvestre MS + 2,4-D + IAA Gymnemic acid 182
Gymnema sylvestre MS + IAA + BA Gymnemic acid 183
Catharanthus roseus MS + 2, 4-D + GA3 Vincristine 184
Hydrocotyle bonariensis 2,4-D + Kinetin Flavonoids 185
Daucus carota IAA +Kn Anthocyanin 69
Fabiana imbricate MS + NAA + 2,4-D Rutin 186
Cichorium intybus NAA + Kn Esculin, Esculetin 187
Capsicum annum MS + 2,4-D + GA3 Capsaicin 188

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Cassia acutifolia
Phytolacca americana
Taxus spp
MS + 2,4-D + Kinetin
MS + 2,4-D
B5 + 2,4-D + BA
Anthraquinones
Betacyanin
Taxol
189
190
191

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Catharanthus roseus MS + IAA Indole alkaloids 192
Gynostemma pentaphyllum MS + 2,4-D + BA Saponin 193
Coscinium fenustratum LS + NAA + 2,4-D + BA Berberin 194
Beeta vulgaris MS + IAA Betalain 195
Anisodus luridus MS + 2,4-D + BA Tropane alkaloids 196
Capsicum annuum MS + 2,4-D + Kn Capsaicin 197
Catharanthus trichophyllus MS + IAA + GA3 Indole alkaloids 198
Catharanthus roseus MS + 2,4-D + GA3 + Vanadium Indole alkaloid 199
Mucuna pruriens MS + IAA L-Dopa 200
Adapted from Karuppusamy, 20098; Vijaya Sree et al. 2010. 201

in concentrations of some individual monoterpenes124 and an secondary metabolites.61 The synthesis of secondary metabo-
increase in total phenolics have been reported.123 Increased con- lites, including saponins, response to environmental factors and
centrations of the monoterpene a-pinene was noticed in elevated part of an adaptative strategy leading to tolerance of abiotic
CO2 composition.123 In contrast to this, Williams et al. (1994)124 stresses. Saponins occur in roots, leaves, stems, bulbs, flowers
found decreased concentrations of b-pinene in needles under and fruit of Panax ginseng, and their content influence by envi-
elevated CO2. Several studies have been reported the effect of ronmental abiotic factors.64 The accumulation of saponins in
temperature on secondary metabolite production in plants. plant reproductive organs, play a role in chemical protection
Secondary metabolites increase in response to elevated tempera- and the plant response to environmental factors.126 American
tures.60,62,63 In contrast to this Snow et al. (2003)125 reported that ginseng plants exposed to longer sunlight were found to have
high temperature decreases monoterpene levels in Douglas fir higher root ginsenoside contents than those exposed to shorter
(Pseudotsuga menziesii). periods of direct sunlight.127 He et al. (2009)128 reported the
effect of CO2 or ozone on endogenous hormones in the leaves of
Influence of Environmental Factors Ginkgo biloba. Huang et al. (2010)129 reported that elevated O3
on Secondary Metabolites reduce the concentrations of the isorhamnetin aglycon (7%),
but increase the concentration of quercetin aglycon (6%).
The local geoclimate, seasonal changes, external conditions Elevated CO2 reduce the concentrations of keampferol aglycon
such as light, temperature, humidity affect composition of (10%), isorhamnetin aglycon (15%).

1726 Plant Signaling & Behavior Volume 6 Issue 11

 Melatonin, a neurohormone produced by the pineal gland, was associated with enhancement of ABA, ethylene levels, pheno-
has recently been reported in the plant kingdom.130,131 Melatonin lics and terpenoids. BR-induced disease resistance was also noted
is an environmentally friendly-molecule with broad spectrum in barley and cucumber plants. In cucumber plants increased
antioxidant capacity. High levels of melatonin exist in an aquatic activities of peroxidase and polyphenoloxidase enzymes, which
plant, the water hyacinth, which is highly tolerant of environmen- are involved in the metabolism of polyphenols, was suggested as
tal pollutants.132 Elevated levels of melatonin probably help plants a factor contributing to BR-induced disease resistance.137
to protect against environmental stress caused by water and soil
pollutants. Recently, the potential relationships between melato- Conclusion
nin supplementation and environmental tolerance in plants was
reported.132 In pea plants treated with high levels of copper in the Thus it is evident that abiotic stress factors influence growth and
soil. Copper contamination kills pea plant, however, melatonin secondary metabolite production in higher plants. The influences
added to the soil significantly enhanced their tolerance therefore, are well marked. In fact, productivities depend on the changed
increased their survival.132 Serotonin is an indoleamine neurohar- ecosystem also. For example, influence of climate change on
mone in vertebrates. Recently, serotonin has also been reported bees, butterflies, soil microflora, etc. also effect plant antogeny,
in wide range of plant species.133 Serotonin involved in various adaptation and productivities. Such holistic studies are lacking.
physiological functions in plants viz. protect from environmen- Most importantly, climate change drastically influence water
tal stress, protective against pathogenic infection. Serotonin is availability, salinity and several adverse soil conditions which will
believed to play a protective role against reactive oxygen species have direct bearing on original yields. The major advantage of
(ROS) leading to a delay in the process of senescence.133 In D. the cell cultures include synthesis of bioactive secondary metabo-
metel serotonin acts as an antioxidant in protecting the young lites, independently of environmental and soil conditions. The
reproductive tissues from environmental stress. The exposure of use of in vitro plant cell culture for the production of chemicals
Datura flower to a cold stress significantly increased the concen- and pharmaceuticals has made great strides. The use of genetic

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trations of serotonin.134 tools and regulation of pathways for secondary metabolism will
provide the basis for the commercial production of seconadary
Influence of Brassino Steroids on Secondary metabolites. The increased level of natural products for medic-
Metabolites inal purposes coupled with the low product yields and supply
concerns of plant harvest has renewed interest in large-scale plant

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Brassinosteroids (BRs) are a group of naturally occurring plant
steroidal compounds with wideranging biological activity.135
Several reports suggest that treatment with BRs enhances plant
resistance to a variety of environmental stresses.136 And also
cell culture technology. Biotic and abiotic factors which influence
secondary metabolite production have a bearing on enhancing
the potential to over produce useful phytochemicals for var-
ied applications. Moreover, molecular understanding of stress
confer resistance to plants against various abiotic and biotic response will be useful in plant improvement with enhanced
stresses.137 The chlorophyll content was maintained in BR-treated adaptation and efficacy.
seedlings during the cold treatment, increasing even further dur-
ing recovery from cold.138 The possible role of BRs to enhance Acknowledgments
plant resistance against fungal pathogen infection has been inves- Mr. Ramakrishna gratefully acknowledges CSIR, New Delhi,
tigated.139 The increase in resistance in BR-treated potato tubers India, for awarding Senior Research Fellowship.
9. Karuppusamy S. A review on trends in production of 16. Winkel-Shirley B. Flavonoid biosynthesis, A color-
References
secondary metabolites from higher plants by in vitro ful model for genetics, biochemistry, cell biology
1. Seigler DS. Plant Secondary Metabolism. Boston MA: tissue, organ and cell cultures. J Med Plants Res 2009; and biotechnology. Plant Physiol 2001; 26:485-93;
Chapman and Hall (Kluwer Academic Publishers) 3:1222-39. PMID:11402179; DOI: 10.1104/pp.126.2.485.
1998:711. 10. Dixon RA, Paiva N. Stressed induced phenyl pro- 17. Parida AK, Das AB. Salt tolerance and salinity effects
2. Bennett RN, Wallsgrove RM. Secondary metabolites panoid metabolism. Plant Cell 1995; 7:1085-97; on plants: a review. Ecotoxicol Environ Saf 2005;
in plant defence mechanisms. New Phytol 1994; PMID:12242399; DOI: 10.1105/tpc.7.7.1085. 60:324-49; PMID:15590011; DOI:10.1016/j.
127:617-33. 11. Chalker-Scott L, Fnchigami LH. The role of phenolic ecoenv.2004.06.010.
3. Ravishankar GA, Venkataraman LV. Food applications compounds in plant stress responses. In: Paul HL, 18. Daneshmand F, Arvin MJ, Kalantari KM. Physiological
of plant cell cultures. Curr Sci 1990; 57:381-3. Ed. Low temperature stress physiology in crops. Boca responses to NaCl stress in three wild species of potato
4. Ravishankar GA, Rao SR. Biotechnological production Raton, Florida: CRC Press Inc. 1989:40. in vitro. Acta Physiol Plant 2010; 32:91-101.
of phytopharmaceuticals. J Biochem Mol Biol Biophys 12. Tuteja N. Mechanisms of high salinity tolerance 19. Petrusa LM, Winicov I. Proline status in salt tolerant
2000; 4:73-102. in plants. Methods Enzymol 2007; 428:419-38; and salt sensitive alfalfa cell lines and plants in response
5. Tuteja N, Sopory SK. Chemical signaling under abiotic PMID:17875432. to NaCl. Plant Physiol Biochem 1997; 35:303-10.
stress environment in plants. Plant Signal Behav 2008; 13. Mahajan S, Tuteja N. Cold, salinity and drought 20. Aziz A, Martin-Tanguy J, Larher F. Stress-induced
3:525-36; PMID:19513246. stresses: An overview. Arch Biochem Biophys 2005; changes in polyamine and tyramine levels can regulate
6. Rao SR, Ravishankar GA. Plant cell cultures: chemical 444:139-58; PMID:16309626; DOI:10.1016/j. proline accumulation in tomato leaf discs treated with
factories of secondary metabolites. Biotechnol Adv abb.2005.10.018. sodium chloride. Physiol Plant 1998; 104:195-202.
2002; 20:101-53; PMID:14538059; DOI:10.1016/ 14. Bryant JP, Chapin FSI, Klein DR. Carbon/nutrient bal- 21. Pedrazani H, Racagni G, Alemano S, Miersch O,
S0734-9750(02)00007-1 ance of boreal plants in relation to vertebrate herbivory. Ramirez I, Pena-Cortes H, et al. Salt tolerant tomato
7. Dicosmo F, Misawa M. Eliciting secondary metabolism Oikos 1983; 40:357-68. plants show increased levels of jasmonic acid. Plant
in plant cell cultures. Trends Biotechnol 1985; 3:318-22. 15. Edreva AM, Velikova V, Tsonev T. Phenylamides in Growth Regul 2003; 412:149-58.
8. Sudha G, Ravishankar GA. Elicitation of anthocy- plants. Russ J Plant Physiol 2000; 54:287-301. 22. Muthukumarasamy M, Gupta SD, Pannerselvam R.
anin production in callus cultures of Daucus carota and Enhancement of peroxidase, polyphenol oxidase and
involvement of calcium channel modulators. Curr Sci superoxide dismutase activities by tridimefon in NaCl
2003; 84:775-9. stressed Raphanus sativus L. Biol Plant 2000; 43:317-20.

www.landesbioscience.com Plant Signaling & Behavior 1727

23. Navarro JM, Flores P, Garrido C, Martinez V. Changes 42. Obrenovic S. Effect of Cu (11) D-penicillanine on 60. Hummel I, EI-Amrani A, Gouesbet G, Hennion F,
in the contents of antioxidant compounds in pepper phytochrome mediated betacyanin formation in Couee I. Involvement of polyamines in the interact-
fruits at ripening stages, as affected by salinity. Food Amaranthus caudatus seedlings. Plant Physiol Biochem ing effects of low temperature and mineral supply on
Chem 2006; 96:66-73. 1990; 28:639-46. Pringlea antiscorbutica (Kerguelen cabbage) seedlings. J
24. Mutlu F, Bozcuk S. Salinity-induced changes of free 43. Saba PD, Iqbal M, Srivastava PS. Effect of ZnSO4 Exp Bot 2004; 399:1125-34.
and bound polyamine levels in sunflower (Helianthus and CuSO4 on regeneration and lepidine content in 61. Morison JIL, Lawlor DW. Interactions between
annuus L.) roots differing in salt tolerance. Pak J Bot Lepidium sativum. Biol Plant 2000; 43:253-6. increasing CO2 concentration and temperature on
2007; 39:1097-102. 44. Angelova Z, Georgiev S, Roos W. Elicitation of plants. plant growth. Plant Cell Environ 1999; 22:659-82.
25. Xu Z, Zhou G, Shimizu H. Plant responses to drought Biotechnol, Biotechnol Equip 2006; 20:72-83. 62. Jochum GM, Mudge KW, Thomas RB. Elevated tem-
and rewatering. Plant Signal Behav 2010; 5:649-54; 45. Pitta-Alvarez SI, Spollansky TC, Giullietti AM. The peratures increase leaf senescence and root secondary
PMID:20404516. influence of different biotic and abiotic elicitors on the metabolite concentration in the understory herb Panax
26. Gosal SS, Wani SH, Kang MS. Water and agricul- production and profile of tropane alkaloids in hairy quinquefolius (Araliaceae). Am J Bot 2007; 94:819-26;
tural sustainability strategies. Kang MS, Ed. CRC Press root cultures of Brugmansia candida. Enzyme Microb PMID:21636451.
2010:259. Technol 2000; 26:252-8; PMID:10689085. 63. Gera M. Jochum, kenneth W, Mudge, Richard B,
27. Larson RA. The antioxidants of higher plants. 46. Weinstein LH, Kaur-Sawhney R, Venkat Rajam M, Thomas, Elevated temperatures increase leaf senescence
Phytochemistry 1988; 27:969-78. Wettlaufer SH, Galston AW. Cadmium-induced accu- and Root secondary metabolite concentrations in the
28. Anjum F, Yaseen M, Rasul E, Wahid A, Anjum S. mulation of putrescine in oat and bean leaves. Plant understory herb Panax quinquefolius (araliaceae). Am J
Water stress in barley (Hordeum vulgare L.). II. Effect Physiol 1986; 82:641-5; PMID:11539091; DOI: Bot 2007; 94:819-26; PMID:21636451.
on chemical composition and chlorophyll contents. Pak 10.1104/pp.82.3.641. 64. Szakiel A, Paczkowski C, Henry M. Influence of envi-
J Agric Sci 2003; 40:45-9. 47. Groppa MD, Tomaro ML, Benavides MP. Polyamines ronmental abiotic factors on the content of saponins in
29. Massacci ASM, Nabiev L, Pietrosanti SK, Nematov as protectors against cadmium or copper-induced oxi- plants. Phytochem Rev 2010; In press; DOI10.1007/
TN, Chernikova K. Thor, Leipner J. Response of the dative damage in sunflower leaf discs. Plant Sci 2001; s11101-010-9177-x.
photosynthetic apparatus of cotton (Gossypium hirsu- 161:481-8. 65. Yu K, Niranjana Murthy H, Hahn E, Paek K.
tum) to the onset of drought stress under field condi- 48. Jacobsen S, Hauschild M, Rasmussen U. Induction by Ginsenoside production by hairy root cultures of Panax
tions studied by gas-exchange analysis and chlorophyll chromium ion of chitinases and polyamines in barley ginseng: influence of temperature and light quality.
fluorescence imaging. Plant Physiol Biochem 2008; (Hordeum vulgare L.) and rape (Brassica napus L. ssp Biochem Eng J 2005; 23:53-6.
46:189-95; PMID:18053735. oleifera). Plant Sci 1992; 84:119-28. 66. Chan LK, Koay SS, Boey PL, Bhatt A. Effects of abiotic
30. Soliz-Guerrero JB, de Rodriguez DJ, Rodriguez- 49. Lin CC, Kao CH. Excess copper induces an accumula- stress on biomass and anthocyanin production in cell
Garcia R, Angulo-Sanchez JL, Mendez-Padilla G. tion of putrescine in rice leaves. Bot Bull Acad Sin cultures of Melastoma malabathricum. Biol Res 2010;
Quinoasaponins: concentration and composition 1999; 40:213-8. 43:127-35; PMID:21157639.
analysis. In: Janick J, Whipkey A, Eds. Trends in 50. Janska A, Marsik P, Zelenkova S, Ovesna J. Cold 67. Zhong JJ, Yoshida T. Effects of temperature on cell

©2011L
andesBiosc
ienc
e.
New Crops and New Uses. Alexandria: ASHS Press stress and acclimation—what is important for meta- growth and anthocyanin production in suspension
2002:110. bolic adjustment? Plant Biol 2010; 12:395-405; cultures of Perilla frutescen. J Ferment Bioeng 1993;
31. Chalker-Scott L. Environmental significance of antho- PMID:20522175. 76:530-1.
cyanins in plant stress responses. Photochem Photobiol 51. Griffith M, Yaish MWF. Antifreeze proteins in overwin- 68. Zhang W, Seki M, Furusaki S. Effect of temperature
1999; 70:1-9. tering plants: a tale of two activities. Trends Plant Sci and its shift on growth and anthocyanin production in
32. Bahler BD, Steffen KL, Orzolek MD. Morphological 2004; 9:399-405; PMID:15358271; DOI:10.1016/j. suspension cultures of strawberry cells. Plant Sci 1997;

Donotdi
str
ibut
e.
and biochemical comparison of a purple-leafed and tplants.2004.06.007. 127:207-14.
a green-leafed pepper cultivar. HortScience 1991; 52. Perez-Ilzarbe J, Hernandez T, Estrella I, Vendrell M. 69. Narayan MS, Thimmaraju R, Bhagyalakshmi N.
26:736. Cold storage of apples (cv. Granny Smith) and changes Interplay of growth regulators during solid-state and
33. Marschner H. Mineral nutrition of higher plants, in phenolic compounds. Z Lebensm Unters Forsch liquid-state batch cultivation of anthocyanin produc-
Academic Press, London 1995; 889. 1997; 204:52-5. ing cell line of Daucus carota. Process Biochem 2005;
34. Hagemeyer J. Ecophysiology of plant growth under 53. Christie PJ, Alfenito MR, Walbot V. Impact of low- 40:351-8.
heavy metal stress. In: Prasad MNV, Hagemeyer J, temperature stress on general phenylpropanoid and 70. Thimmaraju R, Bhagyalakshmi N, Narayan MS,
Eds. Heavy Metal Stress in Plants, Berlin: Springer anthocyanin pathways: Enhancement of transcript Ravishankar GA. Kinetics of pigment release from
1999:222. abundance and anthocyanin pigmentation in maize hairy root cultures of Beta vulgaris under the influence
35. Hawrylak B, Matraszek R, Szymanska M. Response seedlings. Planta 1994; 194:541-9. of pH, sonication, temperature and oxygen stress.
of lettuce (Lactuca sativa L.) to selenium in nutrient 54. Pedranzani H, Sierra-de-Grado R, Vigliocco A, Miersch Process Biochem 2003; 38:1069-76.
solution contaminated with nickel. Veg Crop Res Bull O, Abdala G. Cold and water stresses produce changes 71. Anasori P, Asghari G. Effects of light and differentia-
2007; 67:63. in endogenous jasmonates in two populations of Pinus tion on gingerol and zingiberene production in callus
36. Krupa Z, Baranowska M, Orzol D. Can anthocyanins pinaster Ait. Plant Growth Regul 2003; 52:111-6. culture of Zingiber officinale Rosc. Res Pharm Sci 2008;
be considered as heavy metal stress indicator in higher 55. Lei XY, Zhu RY, Zhang GY, Dai YR. Attenuation of cold 3:59-63.
plants? Acta Physiol Plant 1996; 18:147-51. induced apoptosis by exogenous melatonin in carrot sus- 72. Larsson S, Wiren A, Ericsson T, Lundgren L. Effects
37. Singh S, Sinha S. Accumulation of metals and its effects pension cells: the possible involvement of polyamines. J of light and nutrient stress on defensive chemistry
in Brassica juncea (L.) Czern. (cv. Rohini) grown on vari- Pineal Res 2004; 36:126‑31; PMID:14962064; DOI: and susceptibility to Galerucella lineola (Coleoptera,
ous amendments of tannery waste. Ecotoxicol Environ 10.1046/j.1600-079X.2003.00106.x. Chrysomelidae) in two Salix species. Oikos 1986;
Saf 2005; 62:118-27; PMID:15978297. 56. Posmyk MM, Balabusta M, Wieczorek M, Sliwinska E, 47:205-10.
38. Mizukami H, Konoshima M, Tabata M. Effect of Janas KM. Melatonin applied to cucumber (Cucumis 73. Arakawa O. Effect of ultraviolet light on anthocyanin
nutritional factors on shikonin derivative formation in sativus L.) seeds improves germination during chilling synthesis in light-colored sweet cherry, cv.Sato Nishiki.
Lithospermum callus cultures. Phytochemistry 1977; stress. J Pineal Res 2009; 46:214-23; PMID:19141087; J Japan Soc Hort Sci 1993; 62:543-6.
16:1183-6. DOI: 10.1111/j.1600-079X.2008.00652.x. 74. Arakawa O, Hori Y, Ogata R. Relative effectiveness
39. Ohlsson AB, Berglund T. Effect of high MnSO4 levels 57. Zhao Y, Qi L, Wei-Ming Wang W, Saxena PK, and interaction of ultraviolet-B, red and blue light
on cardenolide accumulation by Digitalis lanata tissue Chun-Zhao Liu C. Melatonin improves the sur- in anthocyanin synthesis of apple fruit. Physiol Plant
cultures in light and darkness. J Plant Physiol 1989; vival of cryopreserved callus of Rhodiola crenulata. J 1985; 64:323-7.
135:505-7. Pineal Res 2011; 50:83-8; PMID:21073518; DOI: 75. Zhong JJT, Seki SI, Kinoshita, Yoshida T. Effect of light
40. Trejo-Tapia G, Jimenez-Aparicio A, Rodriguez-Monroy 10.1111/j.1600-079X.2010.00817.x. irradiation on anthocyanin production by suspended
M, De Jesus-Sanchez A, Gutierrez-Lopez G. Influence 58. Kovacs Z, Simon-Sarkadi L, Szucs A, Kocsy G. culture of Perilla frutescens. Biotechnol Bioeng 1993;
of cobalt and other microelements on the production of Differential effects of cold, osmotic stress and abscisic 38:653-8.
betalains and the growth of suspension cultures of Beta acid on polyamine accumulation in wheat. Amino 76. Sato K, Nakayama M, Shigeta J. Culturing conditions
vulgaris. Plant Cell Tissue Organ Cult 2001; 67:19-23. Acids 2011; 38:623-31; PMID:19960214; DOI: affecting the production of anthocyanin in suspended
41. Thimmaraju BN, Ravishankar GA. In situ and 10.1007/s00726-009-0423-8. cell cultures of strawberry. Plant Sci 1996; 113:91-8.
ex situ adsorption and recovery of betalains from 59. Nadeau P, Delaney S, Chouinard L. Effects of cold 77. Kakegawa K, Hattori E, Koike K, Takeda K. Induction
hairy root cultures of Beta vulgaris. Biotechnol Prog hardening on the regulation of polyamine levels in of anthocyanin synthesis and related enzyme activities
2004; 20:777‑85; PMID:15176882; DOI: 10.1021/ wheat (Triticum aestivum L.) and Alfalfa (Medicago sati- in cell cultures of Centaurea cyanus by UV-light irradia-
bp0300570. va L.). Plant Physiol 1987; 8:73-7; PMID:16665409; tion. Phytochemistry 1991; 30:2271-3.
DOI: 10.1104/pp.84.1.73.

1728 Plant Signaling & Behavior Volume 6 Issue 11

78. Liu L, Dennis C, Gitz III, Jerry W. McClure. Effects 96. Peng Z, Han C, Yuan L, Zhang K, Huang H, Ren C. 115. Zeid IM. Effect of arginine and urea on polyamines
of UV-B on flavonoids, ferulic acid, growth and photo- Brassinosteroid enhances jasmonate-induced anthocy- content and growth of bean under salinity stress. Act
synthesis in barley primary leaves. Physiol Plant 1995; anin accumulation in Arabidopsis seedlings. J Int Plant Physiol Plant 2009; 35:65-70.
93:734-8. Biol 2011; 53:632-40. 116. Pimm SL. Climate disruption and biodiversity. Curr
79. Kramer GF, Norman HA, Krizek DT, Mirecki RM. 97. Perez AG, Sanz C, Olias R, Olias JM. Effect of methyl Biol 2009; 19:595-601; PMID:19640498.
Influence of UV-B radiation on polyamines, lipid jasmonate on in vitro strawberry ripening. J Agric Food 117. Rosemann D, Heller W, Sandermann H. Biochemical
peroxidation and membrane lipids in cucumber. Chem 1997; 45:3733-7. plant responses to ozone. II. Induction of stilbene
Phytochemistry 1991; 30:2101-8. 98. Fang Y, Smith MAL, Pepin MF. Effects of exogenous biosynthesis in Scots pine (Pinus sylvestris L.) seedlings.
80. Hagimori M, Matsumoto T, Obi Y. Studies on the methyl jasmonate in elicited anthocyanin-producing Plant Physiol 1991; 97:1280-6; PMID:16668544.
production of Digitalis cardenolides by plant tissue cul- cell cultures of ohelo (Vaccinium pahalae). In Vitro Cell 118. Kainulainen P, Holopainen JK, Holopainen T. The
ture III. Effects of nutrients on digitoxin formation by Dev Biol Plant 1999; 35:106-13. infuence of elevated CO2 and O3 concentrations on
shoot-forming cultures of Digitalis purpurea L. grown 99. Zhang W, Curtin C, Kikuchi M, Franco C. Integration Scots pine needles: changes in starch and secondary
in liquid media. Plant Cell Physiol 1982; 23:1205-11. of jasmonic acid and light irradiation for enhancement metabolites over three exposure years. Oecologia 1998;
81. Liu C, Guo C, Wang Y, Ouyang F. Effect of light of anthocyanin biosynthesis in Vitis vinifera suspension 114:45560.
irradiation on hairy root growth and artemisinin bio- cultures. Plant Sci 2002; 162:459-68. 119. Pleijel H, Mortensen L, Fuhrer J, Ojanpera K,
synthesis of Artemisia annua L. Process Biochem 2002; 100. Saniewski M, Horbowicz M, Puchalski J, Ueda J. Danielsson H. Grain protein accumulation in relation
38:581-5. Methyl jasmonate stimulates the formation and the to grain yield of spring wheat (Triticum aestivum L.)
82. Fett-Neto AG, Pennington JJ, Di Cosmo F. Effect of accumulation of anthocyanin in Kalanchoe blossfeldi- grown in open-top chambers with different concentra-
white light on taxol and baccatin III accumulation ana. Acta phy plant 2003; 25:143-9. tions of ozone, carbon dioxide and water availability.
in cell cultures of Taxus cuspidata and Zucc. J Plant 101. Sudha G, Ravishankar GA. Influence of methyl jasmo- Agric Ecosyst Environ 1999; 72:265-70.
Physiol 1995; 146:584-90. nate and salicylic acid in the enhancement of capsaicin 120. Piikki K, Vome V, Ojanpera K, Pleijel H. Potato tuber
83. Fischbach RJ, Kossmann B, Panten H, Steinbrecher R, production in cell suspension cultures of Capsicum sugars, starch and organic acids in relation to ozone
Heller W, Seidlitz HK, et al. Seasonal accumulation of frutescens Mill. Curr Sci 2003; 85:1212-7. exposure. Potato Res 2003; 46:67-79.
ultraviolet-B screening pigments in needles of Norway 102. Aoyagi H, Kobayashi Y, Yamada K, Yokoyama M, 121. Ollerenshaw JH, Lyons T. Impacts of ozone on the
spruce (Picea abies (L.) Karst). Plant Cell Environ Kusakari K, Tanaka H. Efficient production of saiko- growth and yield of field grown winter wheat. Environ
1999; 22:27-37. saponins in Bupleurum falcatum root fragments Pollut 1999; 106:67-72; PMID:15093060.
84. Bernard YK, Binder, Christie AM, Peebles Jacqueline combined with signal transducers. Appl Microbiol 122. He X, Huang W, Chen W, Dong T, Liu C, Chen
V, Shanks, Ka-Yiu San. The effects of UV-B stress Biotechnol 2001; 57:482-8; PMID:11762592. Z, et al. Changes of main secondary metabolites in
on the production of terpenoid indole alkaloids in 103. Yukihito Y, Homare T, Yosuke H, Yasuhiro H. Methyl leaves of Ginkgo biloba in response to ozone fumi-
Catharanthus roseus hairy roots. Biotechnol Prog 2009; jasmonate-induced overproduction of paclitaxel and gation. J Environ Sci (China) 2009; 21:199-203;
25:8615. baccatin III in Taxus cell suspension cultures. Nat PMID:19402422.

©2011L
andesBiosc
ienc
e.
85. Liang B, Huang X, Zhang G, Zhang F, Zhou Q. Effect Biotechnol 1996; 14:1129-32; PMID:9631065. 123. Idso CD, Idso KE. Forecasting world food supplies:
of lanthanum on plants under supplementary ultravio- 104. Kim EH, Kim YS, Park S, Koo YJ, Choi Y, Chung Y, et The impact of rising atmospheric CO2 concentration.
let-B radiation: Effect of lanthanum on flavonoid con- al. Methyl Jasmonate reduces grain yield by mediating Technology 2000; 7:33-55.
tents in Soybean seedlings exposed to supplementary stress signals to alter spikelet development in rice. Plant 124. Williams RS, Lincoln DE, Thomas RB. Loblolly pine
ultraviolet-B radiation. J Rare Earths 2006; 24:613-6. Physiol 2009; 149:1751-60; PMID:19211695. grown under elevated CO2 affects early instar pine
86. Shiozaki N, Hattori I, Gojo R, Tezuka T. Activation of 105. Horbowicz M, Kosson R, Wiczkowski W, Koczkodaj sawfly performance. Oecologia 1994; 98:64-71.

Donotdi
str
ibut
e.
growth and nodulation in symbiotic system between D, Mitrus J. The effect of methyl jasmonate on accu- 125. Snow MD, Bard RR, Olszyk DM, Minster LM, Hager
pea plants and leguminous bacteria by near UV radia- mulation of 2-phenylethylamine and putrescine in AN, Tingey D. Monoterpene levels in needles of
tion. J Photochem Photoboi B. Biology 1999; 50:33-7. seedlings of common buckwheat (Fagopyrum esculen- Douglas fir exposed to elevated CO2 and temperature.
87. Tegelberg R, Julkunen-Tiitto R, Aphalo PJ. Red: far- tum). Acta Physiol Plant 2010; 33:897-903. Physiol Plant 2003; 117:352-8; PMID:12654035.
red light ratio and UV-B radiation: their effects on leaf 106. Nakamura M, Takeuchi Y, Miyanaga K, Seki M, 126. Lin JT, Chen SL, Liu SC, Yang DJ. Effect of harvest
phenolics and growth of silver birch seedlings. Plant Furusaki S. High anthocyanin accumulation in time on saponins in Yam (Dioscorea pseudojaponica
Cell Environ 2004; 27:1005-13. the dark by strawberry (Fragaria ananassa) callus. Yamamoto). J Food Drug Anal 2009; 17:116-22.
88. Lavola A, Aphalo PJ, Lahti M, Julkunen-Tiitto R. Biotechnol Lett 1999; 21:695-9. 127. Li TSC, Mazza G, Cottrell AC, Gao L. Ginsenosides
Nutrient availability and the effect of increasing UV-B 107. Nozue M, Kubo H, Nishimura M, Yasuda H. Detection in roots and leaves of American ginseng. J Agric Food
radiation on secondary plant compounds in Scots pine. and characterization of a vacuolar protein (VP24) in Chem 1996; 44:717-20.
Environ Exp Bot 2003; 49:49-60. anthocyanin-producing cells of sweet potato in suspen- 128. He X, Huang W, Chen W, Dong T, Liu C, Chen
89. Ramakrishna A, Dayananda C, Giridhar P, Rajasekaran sion culture. Plant Cell Physiol 1995; 36:883-9. Z, et al. Changes of main secondary metabolites in
T, Ravishankar GA. Photoperiod influences endog- 108. Makunga NP, van Staden J, Cress WA. The effect of leaves of Ginkgo Biloba in response to ozone fumi-
enous indoleamines in cultured green alga Dunaliella light and 2,4-D on anthocyanin production in Oxalis gation. J Environ Sci (China) 2009; 21:199-203;
bardawil. Indian J Exp Biol 2011; 49:234-40; reclinata callus. Plant Growth Regul 1997; 23:153-8. PMID:19402422.
PMID:21452604. 109. Ravishankar GA, Venkataraman LV. Role of plant 129. Huang W, He XY, Liu CB, Li DW. Effects of elevated
90. Gill SS, Tuteja N. Polyamines and abiotic stress toler- cell cultures in food biotechnology: commercial pro- carbon dioxide and ozone on foliar flavonoids of
ance in plants. Plant Signal Behav 2010; 5:26-33; spectus and problems. New Delhi: Oxford IBH Press Ginkgo biloba. Adv Mat Res 2010; 165:113-6.
PMID:20592804. 1993:255. 130. Arnao MB, Hernandez-Ruiz J. The physiological func-
91. Kumar V, Giridhar P, Chandrashekar A, Ravishankar 110. Tuteja N, Mahajan S. Calcium signaling network in tion of melatonin in plants. Plant Signal Behav 2006;
GA. Polyamines influence morphogenesis and caffeine plants: an overview. Plant Signal Behav 2007; 2:79-85; 3:89-95; PMID:19521488.
biosynthesis in in vitro cultures of Coffea canephora P PMID:19516972. 131. Ramakrishna A, Giridhar P, Ravishankar GA.
ex Fr. Acta Physiol Plant 2008; 30:217-23. 111. Ramakrishna A, Giridhar P, Ravishankar GA. Calcium Indoleamines and calcium channels influence morpho-
92. Bais HP, Madhusudhan R, Bhagyalakshmi N, and calcium ionophore A23187 induce high frequency genesis in in vitro cultures of Mimosa police L. Plant
Rajasekaran T, Ramesh BS, Ravishankar GA. Influence somatic embryogenesis in cultured tissues of Coffea Signal Behav 2009; 12:1136-41.
of polyamines on growth and formation of secondary canephora P ex Fr. In Vitro Cell Develop Biol-Plant 132. Tan DX, Manchester LC, Helton P, Reiter RJ.
metabolites in hairy root cultures of Beta vulgaris and 2011; DOI: 10.1007/s11627-011-9372-5. Phytoremediative capacity of plants enriched with
Tagetes patula. Acta Physiol Plant 2000; 22:151-8. 112. Chen Q, Qi W, Reiter RJ, Wei W, Wang B. Exogenously melatonin. Plant Signal Behav 2007; 2:514-6;
93. Wei M, Jiang S, Luo J. Enhancement of growth and applied melatonin stimulates root growth and raises PMID:19704544.
polysaccharide production in suspension cultures of endogenous indoleacetic acid in roots of etiolated seed- 133. Ramakrishna A, Giridhar P, Ravishankar GA.
protocorm-like bodies from Dendrobium huoshanense lings of Brassica juncea. J Plant Physiol 2009; 166:324- Phytoserotonin: A review. Plant Signal Behav 2011;
by the addition of putrescine. Biotechnol Lett 2007; 8; PMID:18706737. 6:800-9; PMID:21617371.
29:495-9; PMID:17136569. 113. Rajendra L, Ravishankar GA, Venkataraman LV, 134. Murch SJ, Alan AR, Cao J, Saxena PK. Melatonin and
94. van der Fits L, Memelink J. ORCA3, a jasmonate Prathiba KR. Anthocyanin production in callus cul- serotonin in flowers and fruits of Datura metel L. J
responsive transcriptional regulator of plant primary tures of Daucus carota as influenced by nutrient stress Pineal Res 2009; 47:277-83; PMID:19732299.
and secondary metabolism. Science 2000; 289:295-7; and osmoticum. Biotechnol Lett 1992; 14:707-12. 135. Clouse SD, Sasse JM. Brassinosteroids: essential
PMID:10894776. 114. Bongue-Bartelsman M, Phillips DA. Nitrogen stress regulators of plant growth and development. Annu
95. Grsic S, Kirchheim B, Piepe K, Fritsch M, Hilgenberg regulates gene expression of enzymes in the flavonoid Rev Plant Physiol Plant Mol Biol 1998; 49:427-51;
W, Ludwig-Mueller J. Induction of auxin biosynthetic biosynthetic pathway of tomato. Plant Physiol Biochem PMID:15012241.
enzymes by jasmonic acid and in clubroot diseased 1995; 33:539-46.
Chinese cabbage plants. Physiol Plant 1999; 105:521-31.

www.landesbioscience.com Plant Signaling & Behavior 1729

136. Ikekawa N, Zhao Y. Application of 24-EpiBR in 157. de Abreu IN, Mazzafera P. Effect of water and tem- 175. Ramani S, Jayabaskaran C. Enhanced catharathine
Agriculture. Brassinosteroids: Chemistry, Bioactivity perature stress on the content of active constituents of and vindoline production in suspension cultures of
and Application. ACS Symposium Series 474. Hypericum brasiliense Choisy. Plant Physiol Biochem Catharanthus roseus by ultraviolet-B light. J Mol Signal
1991; 280. 2005; 43:241-8; PMID:15854832. 2008; 3:9-14; PMID:18439256.
137. Fujioka S, Yokota T. Biosynthesis and metabolism of 158. Noguees S, Allen DJ, Morison JIL, Baker NR. 176. Salma U, Rahman MSM, Islam S, Haque N, Jubair
brassinosteroids. Annu Rev Plant Biol 2003; 54:137- Ultraviolet-B radiation effects on water relations, TA, Haque AKMF, et al. The influence of differ-
64; PMID:14502988. leaf development and photosynthesis in drough- ent hormone concentration and combination on cal-
138. Katsumi M. Physiological modes of brassinolide ted pea plants. Plant Physiol 1998; 117:173-81; lus induction and regeneration of Rauvolfia serpen-
action in cucumber hypocotyl growth. In: Cutler PMID:9576786. tina (L.) Benth. Pak J Biol Sci 2008; 11:1638-41;
HG, Yokota T, Adam G, Eds. Brassinosteroids: 159. Del Moral R. On the variability of chlorogenic acid PMID:18819656.
Chemistry, Bioactivity and Applications. ACS Symp concentration. Oecologia 1972; 9:289-300. 177. Nurchgani N, Solichatun S, Anggarwulan E. The reser-
Ser 474. Washington, DC: American Chemical Society 160. Liu H, Wang X, Wang D, Zou Z, Liang Z. Effect of pine production and callus growth of Indian snake root
1991:246. drought stress on growth and accumulation of active (Rauvolfia serpentina (L.) Benth. ex Kurz.) cultured by
139. Khripach V, Zhabinskii V, de Groot A. Brassinosteroids: constituents in Salvia miltiorrhiza Bunge. Ind Crops addition of Cu2+. Biodiversitas 2008; 9:177-9.
A new class of plant hormones. San Diego, CA: Prod 2011; 33:146-51. 178. Dheeranapattana S, Wangprapa M, Jatisatienr A. Effect
Academic Press 1999; 263. 161. Bartels D, Sunkar R. Drought and salt tolerance in of sodium acetate on stevioside production of Stevia
140. Tari I, Kiss G, Deer AK, Csiszar J, Erdei L, Galle A, plants. Crit Rev Plant Sci 2005; 24:23-58. rebaudiana [ISHS]. Acta Hortic 2008; 786:269-72.
et al. Salicylic acid increased aldose reductase activity 162. Kim HJ, Chen F, Wang X, Nihal C, Rajapakse NC. 179. Umamaheswai A, Lalitha V. In vitro effect of various
and sorbitol accumulation in tomato plants under salt Effect of Methyl Jasmonate on Secondary Metabolites growth hormones in Capsicum annum L. on the callus
stress. Biol Plant 2010; 54:677-83. of Sweet Basil (Ocimum basilicum L.). J Agric Food induction and production of Capsiacin. J Plant Sci
141. Bor M, Seckin B, Ozgur R, Yilmaz O, Ozdemir F, Chem 2006; 54:2327-32; PMID:16536615. 2007; 2:545-51.
Turkan I. Comparative effects of drought, salt, heavy 163. Savitha B, Thimmaraju R, Bhagyalakshmi N, 180. Francoise B, Hossein S, Halimeh H, Zahra NF. Growth
metal and heat stresses on gamma-aminobutryric acid Ravishankar GA. Different biotic and abiotic elicitors optimization of Zataria multiflora Boiss. Tissue cultures
levels of sesame (Sesamum indicum L.). Acta Physiol influence betalain production in hairy root cultures and rosmarininc acid production improvement. Pak J
Plant 2009; 31:655-9. of Beta vulgaris in shake-flask and bioreactor. Process Biol Sci 2007; 10:3395-9; PMID:19090157.
142. Ali RM, Abbas HM. Response of salt stressed barley Biochem 2006; 41:50-60. 181. Qu JG, Yu XJ, Zhang W, Jin MF. Significant improved
seedlings to phenylurea. Plant Soil Environ 2003; 164. Narula A. Sanjeev Kumar, Srivastava PS. Abiotic anthocyanins biosynthesis in suspension cultures of
49:158-62. metal stress enhances diosgenin yield in Dioscorea Vitis vinifera by process intensification. Sheng Wu Gong
143. Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, bulbifera L. cultures. Plant Cell Rep 2005; 24:250-4; Cheng Xae Bao 2006; 22:299-305; PMID:16607960.
Abdelly C. Salinity effects on polyphenol content and PMID:15809888. 182. Gopi C, Vatsala TM. In vitro studies on effects of plant
antioxidant activities in leaves of the halophyte Cakile 165. Suresh B, Thimmaraju R, Bhagyalakshmi N, growth regulators on callus and suspension culture

©2011L
andesBiosc
ienc
e.
maritima. Plant Physiol Biochem 2007; 45:244-9; Ravishankar GA. Polyamine and methyl-jasmonate biomass yield from Gymnema sylvestre. Afr J Biotechnol
PMID:17408958. influenced enhancement of betalain production in 2006; 5:1215-9.
144. Brachet J, Cosson L. Changes in the total alkaloid hairy root cultures of Beta vulgaris grown in a bubble 183. Devi CS, Murugesh S, Srinivasan VM. Gymnemic acid
content of Datura innoxia Mill. subjected to salt stress. column reactor and studies on efflux of pigments. production in suspension calli culture of Gymnema
J Exp Bot 1986; 37:650-6. Process Biochem 2004; 39:2091-6. sylvestre. J Appl Sci 2006; 6:2263-8.
145. Cho Y, Lightfoot DA, Wood AJ. Trigonelline concen- 166. Wu J, Wang C, Mei X. Stimulation of taxol production 184. Lee-Parsons CWT, Rogce AJ. Precursor limita-

Donotdi
str
ibut
e.
trations in salt stressed leaves of cultivated Glycine max. and excretion in Taxus spp cell cultures by rare earth tions in methyl jasmonate-induced Catharanthus
Phytochemistry 1999; 52:1235-8. chemical lanthanum. J Biotechnol 2010; 85:67-73; roseus cell cultures. Plant Cell Rep 2006; 25:607-12;
146. Varshney KA, Gangwar LP. Choline and betaine PMID:11164964. PMID:16432630.
accumulation in Trifolium alexandrinum L. during salt 167. Rao SR, Tripati U, Suresh B, Ravishankar GA. 185. Masoumian M, Arbakariya A, Syahida A, Maziah M.
stress. Egypt J Bot 1988; 31:81-6. Enhancement of secondary metabolite production Flavonoids production in Hydrocotyle bonariensis callus
147. Krishnamurthy R, Bhagwat KAM. Polyamines as in hairy root cultures of Beta vulgaris and Tagetes tissues. J Med Plant Res 2011; 5:1564-74.
modulators of salt tolerance in rice cultivars. Plant patula under the influence of microalgal elicitors. Food 186. Schmeda-Hirschmann G, Jordan M, Gertn A, Wilken
Physiol 1989; 91:500-4; PMID:16667061. Biotechnol 2001; 15:35-46. D, Hormazabal E, Tapia AA. Secondary metabolite
148. Krishnamurthy R, Bhagwat KAM. Accumulation of 168. Bais HP, George J, Ravishankar GA. Influence of content in Fabiana imbricate plants and in vitro cul-
choline and glycinebetaine in salt-stressed wheat seed- polyamines on growth and production of coumarins tures. Z Naturforsch 2004; 5:48-54.
lings. Curr Sci 1990; 59:111-2. in hairy root cultures of Cichorium intybus L cv. 187. Bais HP, Sudha G, George J, Ravishankar GA.
149. Ashraf M. Changes in soluble carbohydrates and Lucknow local. J Plant Growth Regul 1999; 18:33-7; Influence of exogenous hormones on growth and sec-
soluble proteins in three arid-zone grass species under PMID:10467017. ondary metabolite production in hairy root cultures of
salt stress. Trop Agric 1997; 74:234-7. 169. Ravishankar GA, Sarma KS, Venkataraman LV, Kadyan Cichorium intybus L. In Vitro Cell Dev Biol Plant 2001;
150. Parvaiz A, Satyavati S. Salt stress and phyto-biochem- AK. Effect of nutritional stress on capsaicin production 37:293-9.
ical responses of plants—a review. Plant Soil Environ in immobolised cell cultures of Capsicum annuum. 188. Varindra S, Saikia R, Sandhu S, Gosal SS. Effect of
2008; 54:89-99. Curr Sci 1988; 57:381-3. nutrient limitation on capsaicin production in callus
151. Wang DH, Du F, Liu HY, Liang ZS. Drought stress 170. Sudhakar Johnson T, Ravishankar GA, Venkataraman culture derived from pericarp and seedling explants of
increases iridoid glycosides biosynthesis in the roots LV. Biotransformation of ferulic acid and vanillyl amine Capsicum annum L. varieties. Plant Tissue Cult 2000;
of Scrophularia ningpoensis seedlings. J Med Plants Res to capsaicin and vanillin in immobilized cell cultures 10:9-16.
1020; 4:2691-9. of Capsicum frutescens. Plant Cell Tissue Organ Cult 189. Nazif NM, Rady MR, Seif MM. Stimulation of anthra-
152. Szabo B, Tyihak E, Szabo LG, Botz L. Mycotoxin and 1996; 44:117-21. quinone production in suspension cultures of Cassia
drought stress induced change of alkaloid content of 171. Havkin-Frenkel D, Podstolski A, Knorr D. Effect of acutifolia by salt stress. Fitoterapia 2000; 71:34-40;
Papaver somniferum plantlets. Acta Bot Hung 2003; light on vanillin precursors formation by in vitro cul- PMID:11449467.
45:409-17. tures of Vanilla planifolia. Plant Cell Tissue Organ Cult 190. Zang W. Furusaki. Production of anthocyanins by
153. Cho Y, Njitiv N, Chen X. Light food DA, Wood AJ. 1996; 45:133-6. plant cell cultures. Biotech Bioprocess Eng 1999;
Trigonelline concentration in field-grown soybean in 172. Shinde AN, Malpathak N, Fulzele DP. Induced high 4:231-52.
response to irrigation. Biol Plant 2003; 46:405-10. frequency shoot regeneration and enhanced isoflavones 191. Wickremesinhe ERM, Arteca RN. Taxus cell suspen-
154. Jensen CR, Mogensen VO, Mortensen G, Fieldsend production in Psoralea corylifolia. Rec Nat Prod 2009; sion cultures: optimizing growth and production of
JK, Milford GFJ, Andersen MN, et al. Seed gluco- 3:38-45. taxol. J Plant Physiol 1994; 144:183-8.
sinolate, oil and protein contents of field-grown rape 173. Kin N, Kunter B. The effect of callus age, VU radiation 192. Moreno PRH, Heijden RVD, Verpoorte R. Effect of
(Brassica napus L.) affected by soil drying and evapora- and incubation time on trans-resvertrol production in terpenoid precursor feeding and elicitation on forma-
tive demand. Field Crops Res 1996; 47:93-105. grapevine callus culture. Tarim Bilimleri Dergisi 2009; tion of indole alkaloids in cell suspension cultures of
155. Christiansen JL, Jornsgard B, Buskov S, Olsen CE. 15:9-13. Catharanthus roseus. Plant Cell Rep 1993; 12:702-5.
Effect of drought stress on content and composition of 174. Sujanya S, Poornasri DB, Sai I. In vitro produc- 193. Fei HM, Mei KF, Shen X, Ye YM, Lin ZP, Peng
seed alkaloids in narrow-leafed lupin, Lupinus angusti- tion of azadirachtin from cell suspension cultures LH. Transformation of Gynostemma pentaphyllum by
folius L. Eur J Agron 1997; 7:307-14. of Azadirachta indica. J Biosci 2008; 33:113-20; Agrobacterium rhizogenes saponin production in hairy
156. Hernaendez I, Alegre L, Munne-Bosch S. Enhanced PMID:18376076. root cultures. Acta Bot Sin 1993; 35:626-31.
oxidation of flavan-3-ols and proanthocyanidin accu-
mulation in water-stressed tea plants. Phytochemistry
2006; 67:1120-6; PMID:16712885.

1730 Plant Signaling & Behavior Volume 6 Issue 11

194. Nair AJ, Sudhakaran PR, Madhusudanan JR, 197. Johnson T, Ravishankar GA, Venkataraman LV. In 200. Brain KR. Accumulation of L-DOPA in cultures from
Ramakrishna SU. Berberine synthesis by callus and vitro capsaicin production by immobilized cells and Mucuna pruriens. Plant Sci Lett 1976; 7:157-61.
cells suspension cultures of Coscinium fenustratum. placental tissue of Capsicum annuum L. grown in liquid 201. Vijaya Sree N, Udayasri PVV, Aswani kumar Y, Ravi
Plant Cell Tissue Organ Cult 1992; 29:7-10. medium. Plant Sci 1992; 70:223-9. Babu B, Phani kumar Y, Vijay Varma M. Advancements
195. Taya M, Mine K, Kinoka M, Tone S, Ichi T. Production 198. Davioud E, Kan C, Hamon J, Tempe J, Husson HP. in the production of secondary metabolites. J Nat Prod
and release of pigments by cultures of transformed Production of indole alkaloids by in vitro root cultures 2010; 3:112-23.
hairy roots of red beet. J Ferment Bioeng 1992; 3:31-6. from Catharanthus trichophyllus. Phytochemistry 1989;
196. Jobanovic V, Grubisic D, Giba Z, Menkovid N, Ristic 28:2675-80.
M. Alkaloids from hairy root cultures of Anisodus 199. Tallevi SG, Dicosmo F. Stimulation of indole alka-
luridus (Scolopia lurids Dunal Solanaceae Tropane alka- loid content in vanadium treated Catharanthus roseus
loids). Planta Med 1991; 2:102. suspension cultures. Planta Med 1998; 54:149-52;
PMID:17265225.

©2011L
andesBiosc
ienc
e.
Donotdi
str
ibut
e.

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