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Plant growth regulator mediated consequences of secondary metabolites in

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DOI: 10.1016/j.jarmap.2017.12.003

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Contents lists available at ScienceDirect

Journal of Applied Research on Medicinal and Aromatic

Plants
journal homepage: www.elsevier.com/locate/jarmap

Plant growth regulator mediated consequences of secondary metabolites in T

medicinal plants
⁎
Komal Jamwal, Sujata Bhattacharya , Sunil Puri
Shoolini University, Post Box No.9, Head Post Office, Solan, H.P, 173212, India

A R T I C L E I N F O A B S T R A C T

Keywords: Secondary metabolites not only play vital role in plant defense against herbivory and other interspecies defenses
Secondary metabolites but also used by humans as medicines, flavorings, pharmaceuticals, agrochemicals, fragrances, colours, bio-
Growth regulators pesticides, food additives and drugs. Many of the drugs retailed today are simple synthetic modifications of the
Medicinal plants naturally obtained substances. The developing commercial status of secondary metabolites in recent years has
resulted in a great interest in secondary metabolism. Different strategies have been extensively studied with the
objective of improving the production of secondary metabolites in plants. Based on this limelight, the focus of
the present review is to study the application of plant growth regulators for the production of some essential
plant secondary metabolites. This review covers brief introduction of secondary metabolites and plant growth
regulators and production of secondary metabolites by using different plant growth regulators according to their
classification.

1. Introduction
Plants face a number of opponents in natural systems and therefore
possess innumerable defense and have evolved multiple resistance
mechanisms through which they are capable to cope with various kinds
of biotic and abiotic stress (Ballhorn et al., 2009). Plants defend
themselves by producing some compounds of diverse chemical nature
called as secondary metabolites. Plant secondary metabolites are re-
cognized as compounds that are essential for the plant acclimatization
and defense but have no vital role in the continuation of life processes
in the plants. It is believed that most of the 100,000 known secondary
metabolites are to be involved in plant chemical defense systems, which
are made throughout millions of ages during which plants have co-ex-
isted with their invaders (Wink, 1999). Secondary metabolites are sig-
nificant source of pharmaceuticals as well as play a dynamic role in the
adaptation of plants to their environment (Rao and Ravishankar, 2002).
Secondary metabolites are responsible for the medicinal value of the
plants but they have very limited distribution than primary metabolites.
Research on plant secondary metabolites has increased during last 50
years due to value necessity of the daily lives including health care on
these plant products (Mulabagal and Tsay, 2004). Many of these mo-
lecules are found in ppm levels in nature thus requires immense har-
vesting to attain adequate amounts of the drug. Therefore it is required
to use eco-friendly system to achieve complex chemical structures
biosynthesized by rare or endangered plant species that oppose
domestication and the plants having slow growth rate (e.g., Taxus trees
reach a peak production of taxol only after 60 years of growth). Cul-
tivation of medicinal plants and in vitro production of plant secondary
metabolites are the only sustainable ways to achieve the market de-
mand. Accumulation of secondary metabolites normally occurs in
plants introduced to various signal molecules or elicitors.
Plant growth regulators (PGRs) have been used as proficient elici-
tors to stimulate production of plant secondary metabolites. Plant
growth regulators include hormonal substances of natural occurrence
(phytohormones) as well their synthetic analogues (Basra, 2000)
(Table 1). The concept of phytohormone was recommended at the end
of 19th Century by Julian von Sachs, who described them as mobile
endogenous compounds (Spartz and Gray, 2008). Plant growth reg-
ulators are simple molecules that have specific effects on plant growth
and are effective even in low concentrations (Nambara and Marion-
Poll, 2005; Teale et al., 2006). Traditionally, synthetic plant growth
regulators are used as precious research tools to elucidate physiological
responses of plants or to explore biochemical control mechanisms.
Since 1940, natural as well as synthetic growth regulators have been
used in agriculture to control developmental processes like germina-
tion, growth, vegetative reproduction, maturation, senescence and post-
harvest (Basra, 2000). PGRs not only control antioxidant potential,
fundamental growth and developmental processes but are also known
to regulate plant secondary metabolites production in plant tissue cul-
ture (Dörnenburg and Knorr, 1995). According to Zhao et al. (2005),

⁎
Corresponding author.
E-mail address: deanacademics@shooliniuniversity.com (S. Bhattacharya).

https://doi.org/10.1016/j.jarmap.2017.12.003
Received 23 June 2017; Received in revised form 15 December 2017; Accepted 17 December 2017
Available online 06 March 2018
2214-7861/ © 2017 Elsevier GmbH. All rights reserved.
K. Jamwal et al. Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38

Table 1 to Duangporn and Siripong (2009) naphthalene acetic acid (NAA) and
Major hormones and their types. benzyl adenine (BA) increased secondary product accumulation in
callus cultures of Phyllanthus acidus. It was observed that production of
Major hormones Natural hormones Synthetic hormones
secondary metabolite in tissue culture was improved with indole acetic
Auxin Indole-3-acetic acid Indole 3 butyric acid (IBA) acid (IAA) and naphthalene acetic acid in Coscinium fenestratum (Nair
(IAA) et al., 1992) or else by 2,4-dichlorophenoxyacetic acid (2, 4-D) in Ni-
Indole-3-acetonitrile Indole 3 propionic acid (IPA)
cotiana tabacum (Ikeda et al., 1976).
(IAN)
Indole-3-acetaldehyde Indazole 3 acetic acid When adventitious roots were treated with KIN (kinetin) and IBA
(IAc) (indole 3 butyric acid) in combination with thidiazuron (TDZ), fresh
Ethylindoleacetate Chlorophenoxypropionic acids weight (FW) and dry weight (DW) reduced but secondary metabolite
Indole-3- pyruvic acid Naphthalene acetic acid (NAA) content increased in Morinda citrifolia and the secondary metabolite
(IPyA)
content was (including 1, 1-diphenyl-2-picrylhydrazyl activity) higher
Phenoxy acetic acid (PAA)
2, 4-dichlorophenoxy acetic acid in TDZ (thidiazuron) treated than in kinetin-treated roots (Baque et al.,
(2, 4-D) 2010). Differences in cytokinin concentrations even in combination
2,4,5- trichlorophenoxy acetic acid with NAA (equimolar concentrations) considerably affected secondary
(2,4,5-T)
metabolite production in some cases in Aloe arborescens (Amoo et al.,
Naphthalene acetamide (NAAM)
2-napthoxyacetic acid (NOA) 2012). Sakakibara et al. (2006) observed that cytokinins significantly
2, 3,5-Triodobenzoic acid (TIBA) suppress some transporters of macronutrients such as nitrate, sulphate,
Thianaphthen-3-propionic acid ammonium and phosphate on one hand and nitrate on the other side
(IPA) normalizes the genes expression involved in secondary metabolite
Cytokinin Ribosylzeatin 6-Benzyl amino purine
pathways. Rawat et al. (2013) reported that 6-benzyl amino purine
Zeatin 6-Phenyl amino purine
Isopentinyladenine Kinetin (BAP) was found to be more efficient in improving shoot regeneration
Dihydrozeatin [(N-Benzyl-9-(2-etrahydropyranyl) and production of secondary metabolite in Aconitum violaceum com-
adenine] (PBA) pared to thidiazuron and differences in concentrations of cytokinins
Diphenylurea
significantly enhanced secondary metabolite production in some cases.
Thidiazuron
Benzimidazole
Cytokinins have enhancing effect on the secondary metabolites in
Adenine Hypericum sampsonii and Hypericum perforatum plantlets (Liu et al.,
6-(2-Thenylamino) purine 2007). Kalt et al. (2001) observed that ABA (abscisic acid) application
Gibberellins GA GA caused oxidative stress in Orthosiphon stimaneus and at the same time
GA4 GA3
stimulated the secondary metabolites production. Gibberellic acid
GA7
Ethylene Ethylene Ethephon (GA3) has also been shown to stimulate the growth of hairy roots in
Ethrel numerous species with a variable amount of secondary metabolite
Brassinosteroids Dolicholide Five 5-hydroxy-6-ketone production in Chicorium intybus (Bais et al., 2001). Although salicylic
28-homodolicholide
acid (SA), methyl jasmonate and jasmonate (JA) may trigger plant
Castasterone
Dolichosterone
secondary metabolite biosynthesis through distinct signaling pathways
28-homodolichosterone (Zhao et al., 2005), they are all act together with NO (nitric oxide) in
Typhasterol facilitating plant secondary metabolite production. NO has been re-
Jasmonates Jasmonic acid Methyl dihydrojasmonate ported to play significant roles in elicitor-induced secondary metabolite
Di hydrojasmonic acid
production in tissue and cell cultures of medicinal plants (Zhang et al.,
Methyl jasmonate
Strigolactones Strigol GR24 2012). The NO production in Taxus chinensis cells increased with the
orobanchol MeJA treatment, suggesting a dose-dependent stimulation by MeJA
(Wang and Wu, 2005). When MeJa was applied exogenously to plant
cell cultures of a variety of species it stimulated the operation of sec-
PGRs are active at low concentrations, have specific effects on growth ondary biosynthetic pathways and led to increased production of mis-
and development and are involved in plant secondary metabolism. cellaneous plant secondary metabolites, including terpenoids, alkaloids,
flavonoids and phenylpropanoids (Uppalapati et al., 2005; Rischer
2. Influence on secondary metabolites et al., 2006; Wasternack and Hause, 2013). CA (Caffeic Acid) and MeJA
applications considerably enhanced secondary metabolite production in
The plant reaction to plant growth regulators may differ with spe- Rubia tinctorum root cultures (Bicer et al., 2017).
cies, age of plant, varieties, environmental conditions, stage of devel- There are three foremost groups of secondary metabolites i.e., ter-
opment, physiological and nutritional status and endogenous hormonal penes, phenolics and nitrogen, sulphur comprising compounds (Fig. 1).
balance (Aftab et al., 2010; Idrees et al., 2010a, 2010b, 2011, 2012; Terpenes are composed of 5-C isopentanoid units. Phenolics synthe-
Naeem et al., 2009, 2010, 2011). A number of studies have been per- sized principally from products of the shikimic acid pathway. Members
formed and confirmed in vast plants to find out the effects of unlike of the third major group i.e., nitrogen, sulphur comprising compounds
plant growth regulators on secondary metabolite production (Weathers are synthesized largely from common amino acids (Van Etten et al.,
et al., 2005; Rojbayani, 2007; Khan et al., 2008; Shilpashree and Rai, 2001). They have a much delimited distribution than primary meta-
2009). bolites in the entire plant kingdom i.e., they are frequently found only
Azeez and Ibrahim (2014) revealed that presence of active com- in one plant species or a taxonomically related group of species.
pounds in cultured cells at higher levels through optimization of cul-
tural conditions may be due to PGRs, added to the medium for initiation 2.1. Terpenes
of callus of Hypericum triquetrifolium. Increase in production of sec-
ondary metabolites is due to cell multiplication and division caused by Terpenes signify one of the most largest and diverse classes of sec-
PGRs (Staba, 1980). Since PGRs have significant effects on the meta- ondary metabolites (Table 2) and are linked by their communal bio-
bolism of secondary metabolites, they are effective to stimulate sec- synthetic source from acetyl-coA or else glycolytic intermediates
ondary metabolite production in Saintpaulia ionantha (Al-Sane et al., (Grayson, 1998). Majority of the different terpenes structures produced
2010) and Hypericum mysorense (Shilpashree and Rai, 2009). According by plants as secondary metabolites are supposed to be intricate in

27
K. Jamwal et al.
Fig. 1. Types of plant secondary metabolites.
defense as toxins and feeding constraints to a vast number of insects and
mammals used plants as food (Gershenzon and Croteau, 1991). They
are required to tackle various stress situations. These compounds are
also very important in the human diet because they can protect against
many diseases, such as cancer (lycopene, squalene). Plant growth reg-
ulators stimulate terpenoid biosynthesis and growth in several aromatic
plants, which is beneficial for both quantity and quality of terpenoids
(Shukla et al., 1992). As PGRs have effects on enzymatic pathways of
terpenoid biosynthesis their application may affect essential oils
(Sangwan et al., 2001). Application of abscisic acid has been shown to
enhance the terpenoids production in Cannabis sativa (Mansouri et al.,
2009) thus, indicating the importance of abscisic acid in increasing the
production of secondary metabolites in plants. An increase in essential
oil content in Cymbopogon citratus treated with IAA + GA3; benzyla-
minopurine and N6-isopenteniladenine (Quiala et al., 2006). Increased
level of auxin, like 2, 4-D in medium induced callus formation and
secondary metabolites like ubiquinone-10 in Nicotiana tabacum (Ikeda
et al., 1976). Mahmoud (1995) reported the influence of IAA, KIN and
GA on essential oils yield and composition of Ocimum basilicum. The
same opinion was made by Fraternale et al. (2003) who found that
spraying Thymus mastichina plants by cytokinin caused rise in the
concentration of essential oils. Secondary metabolites like terpenoids
are elicited by JA (jasmonic acid) and its analogue MeJA (methyl jas-
monate) in Picea abies (Martin et al., 2002). Reda et al. (2005) reported
that GA application on plant Thymus vulgaris showed an increase in the
essential oils yield. Production of essential oil was also increased by
kinetin and diphenylurea in species of Lamiaceae (Mentha suaveolens,
Mentha × piperita, Salvia officinalis, Mentha spicata, Lavandula vera) (El-
Keltawi and Croteau, 1987). Higher essential oil content and increased
terpenoids were observed in Salvia officinalis when treated with gib-
berellic acid, 2, 4-D and BA (benzyl adenine) (Povh and Ono, 2006).
Phatak and Heble (2002) reported increased terpenoids in shoot culture
of Mentha arvensis when treated with BA + NAA (1‐naphthalene acetic
acid). Myristin production was observed in Myristica fragrans when
treated with NAA and TDZ (Iyer et al., 2009).
2.1.1. Monoterpenes (C10H16)
Monoterpenes are composed of two isoprene units (Table 2).
Monoterpenes are found in the essential oils of many plants like vege-
tables, fruits and herbs. They prevent the carcinogenesis process at both
initiation and promotion/progression stages (Gould, 1997). It was ob-
served that foliar application of cytokinin triggered essential oil accu-
mulation because of direct effect on metabolism of monoterpenoids in
Mentha × piperitaand Salvia officinalis (El-Keltawi and Croteau, 1987).
It was found that BAP (benzylaminopurine) acts like IAA with an
28
Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38
increase in essential oils yield and without any variation in methyl
chavicol content. This quantitative dissimilarity has been noticed in
several species Lavandula dentata (Oudin et al., 2007), Cymbopogon ci-
tratus (Craveiro et al., 1981), Thymus mastichina (Fraternale et al.,
2003), Mentha spicata, Mentha piperita, Mentha suaveolens, Salvia offici-
nalis, Lavandula vera (El-Keltawi and Croteau, 1987).
2.1.2. Sesquiterpenes (C15H24)
These consist of three isoprene units (Table 2). They are found
mainly in higher plants. Sesquiterpenes are the most diverse class of
isoprenoids; some of them are grabing attension because of their potent
anticancer, antitumor, antiviral, cytotoxic and antibiotic properties.
Plants of Artemisia annua produce artemisinin, a sesquiterpene lactone
widely used in malaria treatment. Artemisinin is an effective ingredient
for malaria treatment; however, its utilization has been limited due to
low yield in plants of Artemisia annua. Accumulation of artemisinin can
be induced by the phytohormone jasmonate (JA) (Yu et al., 2012).
According to Zia et al. (2007) BAP produced more artemisinin in
comparison to NAA and KIN. Addition of SA induced the growth of
sesquiterpenes (bilobalide and ginkgolide) in cell suspension cultures of
Ginkgo biloba (Kang et al., 2006). Stojakowska and Malarz (2006) re-
ported sesquiterpene lactones of eudesmane type in roots cultures of
Inula macrocephala and Inula royleana on addition of methyl jasmonate.
Induction in sesquiterpene content was also reported in hairy root
culture of Lactuca virosa treated with 2, 4‐D (Kisiel et al., 1995).
2.1.3. Diterpenes (C20H32)
These are composed of four isoprene units (Table 2). The diterpenes
arise from geranylgeranyl diphosphate and contain 20 carbon units in
their basic skeletal type. Diterpenes have attracted increasing attention
because of their remarkable biological as well as pharmacological ac-
tivities. Taxol (paclitaxel) and its derivatives are widely used in the
treatment of several types of cancer, including mammary, ovarian,
prostate and non-small-cell lung carcinoma, AIDS-associated Kaposi’s
sarcoma and other types of tumor (Onrubia et al., 2013). Yukimune
et al. (1996) by applying 100 μM MeJA on Taxus baccata, achieved
120–130-fold increased taxoid production, (48.3 mg/L of paclitaxel and
53.5 mg/L of baccatin III). Increase in paclitaxel production (40-fold)
was reported in Taxus canadienses cell suspension cultures by addition
of 200 μM MeJA (Ketchum et al., 1999). Enhanced yield of taxane in
Taxus baccata were achieved in cell suspension culture by using dif-
ferent concentrations of SA (Khosroushahi et al., 2006). Treatment with
MeJA is one of the most effectual strategies for boosting taxane pro-
duction in Taxus cell cultures (Onrubia et al., 2013). Treatment with 2,
4-D in suspension of Torreya nucifera caused increase in diterpenoids
K. Jamwal et al. Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38

Table 2
Plant growth regulator induced alterations in plant secondary metabolites of class terpenes.

Secondary metabolites Plant growth regulators Plants name References

Monoterpenes (C10H16)
1–8, Cineole Cytokinins Mentha spicata Stoeva and Iliev (1997)
Iridoids Eucomis autumnalis Masondo et al. (2014)
Menthone, Menthol Mentha × piperita Santoro et al. (2013)
1, 8-Cineole GA Salvia officinalis Schmiderer et al. (2010)
T-anethole Ocimum gratissimum Hazzoumi et al. (2014)
Menthol, Isomenthone, L-Methone, TRIA (Triacontanol) Mentha arvensis Naeem et al. (2011)
Menthyl acetate
Linalool, β-ocimene MeJA Gossypium hirsutum Rodriguez-Saona et al. (2001)
Methyl chavicol Ocimum basilicum Kim et al. (2006); Li et al. (2007)
Thymol derivatives Inula macrocephala, Inula royleana Stojakowska and Malarz (2009)
Valepotriates IAA + KIN Centranthes ruber Gränicher et al. (1995)
Limonin 2, 4-D + KIN Citrus species Barthe et al. (1987)

Sesquiterpenes (C15H24)
Artemisinin TRIA + GA Artemisia annua Aftab et al. (2010); Weathers et al. (2005); Ferreira et al. (2005); Zhang
et al. (2005)
MeJA or JA Artemisia annua Baldi and Dixit (2008a); Wang et al. (2010); Caretto et al. (2011); Maes
et al. (2011); Wu et al. (2011); Mehrjerdi et al. (2013)
IAA + KIN Artemisia annua Rao et al. (1998)
NAA + KIN Artemisia annua Baldi and Dixit (2008b)
Cytokinin Artemisia annua Sa et al. (2001); Weathers et al. (2005)
KIN Ambrosia tenuifolia Goleniowski and Tirppi (1999)

Diterpenes (C20H32)
Tanshinone GA + ABA Salvia miltiorrhiza Yuan et al. (2008); Yang et al. (2012a,b)
Paclitaxel MeJA Taxus cuspidata Patil et al. (2014); Ketchum et al. (2003)
ABA Taxus chinensis Luo et al. (2001)
SA Taxus chinensis Wang et al. (2007)
Corylus avellana Rezaei et al. (2011)
Taxol 2, 4-D + BA Taxus species Wu et al. (2001)
IBA Taxus wallichiana Datta et al. (2006)
Taxol baccatin III 2, 4-D + KIN + GA3 Taxus baccata Cusidó et al., (1999)
Carnosic acid, carnosol IAA + BAP Salvia officinalis Grzegorczyk and Wysokinska (2010)
Forskolin IAA + KIN Coleus forskohlii Sasaki et al. (1998)

Triterpenes (C30H48)
Cucurbitacin-E, Cucurbitacins 2, 4-D + KIN Citrullus colocynthis Hegazy et al. (2010)
Diosgenin 2, 4-D + BA + 2, 4-D Diocorea doryophora, Dioscorea Huang et al. (1993); Kaul and Staba (1968)
deltoidea
Gymnemic acid 2, 4-D Gymnema sylvestre Ali Ahmed et al. (2009)
2, 4-D + IAA Gopi and Vatsala (2006)
Asiaticoside 2, 4-D Centella asiatica Kim et al. (2007a,b)
Paek et al. (1996)
Azadirachtin Azadirachta indica Sujanya et al. (2008)
Asiaticoside 2, 4-D + KIN Centella asiatica Kiong et al. (2005)
BAP + IAA Kim et al. (2004a,b)
Cycloartane IAA + NAA Astragalus mongholicus Ionkova et al. (1997)
Gymnemic acid IAA + BA Gymnema sylvestre Devi et al. (2006)
Ginsenosides MeJa Panax ginseng Thanh et al. (2005); Kim et al. (2004a,b); Palazón et al. (2003a,b)
SA Tewari and Paek (2011); Ali et al. (2007)
Centellosides MeJa Centella asiatica Bonfill et al. (2010)

Tetraterpenes (C40H64)
Carotenoids BA + IBA Thymus vulgaris Karalija and Parić (2011)
SA Artemisia annua Aftab et al. (2010)
ABA Lactuca sativa Li et al. (2010)
Putrescine + SA Trachyspermum ammi Zeid et al.(2014)

(Orihara et al., 2002). 2.1.5. Tetraterpenes (C40H64)

2.1.4. Triterpenes (C30H48)
They consist of six isoprene units (Table 2). Triterpenes contain a
large class of compounds having a number of important biological ac-
tivities; they arise from squalene, a coupling of two farnesil diphosphate
units (Abe, 2007). Staniszewska et al. (2003) reported increased tri-
terpenoid content in suspension culture of Ammi majus when treated
with 2, 4-D and BA. Increase in triterpenes were observed in Eriobotrya
japonica callus culture containing NAA + BA (Taniguchi et al., 2002),
callus culture of Glycyrrhiza glabra on addition of IAA + KIN and 2, 4-D
(Ayabe et al., 1990) and in suspension culture of Hyssopus officinalis
containing 2, 4-D and IAA (Skrzypek and Wysokinsku, 2003).
These contain eight isoprene units (Table 2). Tetraterpenoids in-
clude important pigments (e.g., beta-carotene, lycopene) and are
available in colored plant parts. Fruits and vegetables are a rich source
of carotenoids. They are found in all plants, bacteria, and fungi. These
are also known as carotenoids. Fruits and vegetables are a rich source of
carotenoids. They provide health benefits by decreasing the risk of
various diseases, particularly certain cancers and eye diseases and an-
tioxidants activity. Total carotenoid content and size of xanthophyll
collection, increased considerably with an increase in SA concentration
in both Triticum aestivum and Vigna radiata seedlings (Moharekar et al.,
2003). Application of salicylic acid and vermicompost improved the
contents of chlorophyll a, total chlorophyll and carotenoid of Petunia
hybrida under drought conditions (Saberi et al., 2015).

29
K. Jamwal et al. Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38

Table 3
Plant growth regulator induced alterations in plant secondary metabolites of class phenolics.

Secondary metabolite Plant growth regulator Plant name Reference

Total phenolics
Resveratrol IAA + GA
Anthraquinone IAA + GA3 Cinchona succirubra Khouri et al. (1986)
Hypericin NAA + GA3 Hypericum perforatum Hohtola et al. (2005)
Rosmarinic acid IAA + BAP Salvia officinalis Grzegorczyk and Wysokinska
(2008)
Anthraquinone Cytokinin Rubia akane Jin et al. (1999)
TDZ + IAA Cassia obtusifolia Ko et al. (1995)
TDZ + NAA Frangula alnus Kovačević and Grubišić (2005)
Rosmarinic acid 2, 4-D Anchusa officinalis De-Eknamkul and Ellis (1985)
Anthraquinone Rubia tinctorum Sato et al. (1991)
Rosmarinic acid 2, 4-D + KIN Agastache rugose Lee et al. (2007)
Resveratrol Arachys hypogaea Kim et al. (2008)
Rosmarinic acid IAA + KIN Zataria multiflora Francoise et al. (2007)
Anthraquinone NAA + KIN Cruciata glabra Dörnenburg and Knorr (1996)
Anthraquinone Rubia akane Park and Lee (2009)
Chlorogenic acid KIN Nicotiana tabacum Bergmann (1965)
Anthraquinone Isoplexis isabelliana Arrebola et al. (1999)
Salvianic acid A, Salvianolic acid B ABA Salvia miltiorrhiza Hao et al. (2012)
Caftaric acid GA3 + Paclobutrazole + Uniconazole Echinacea purpurea Jones et al. (2009)
Hypericin BA + IAA Hypericum perforatum Kornfeld et al. (2007)
BA + TDZ Hypericum perforatum Santarem and Astarita (2003)
Coumarins
Umbelliferone BAP Ammi majus Królicka et al. (2006)
Scopoletin, Dehydrogeijerin Benzo (1,2,3)-thiadiazole-7-carbothionic acid S-methyl ester (a salicylic acid Staniszewska et al. (2003)
analogue)
Scopoletin KIN Nicotiana tabacum Bergmann (1965)

Flavonoids
Anthocyanin 2, 4-D + KIN Aralia cordata Sakamoto et al. (1994)
Kaempferol, Quercetin, Luteiolin BAP + NAA + KIN + 2, 4-D Momordica charantia Agarwal and Kamal (2007)
Anthocyanin KIN + NAA, IAA + KIN Crataegus sinaica Maharik et al. (2009)
Narayan et al. (2005)
Withanoloid A IAA + KIN Withania somnifera Murthy et al. (2008)
Anthocyanin 2, 4-D Daucus carota Narayan et al. (2005)
Oxalis reclinata Makunga et al. (1997)
Flavonol 2, 4-D + NAA Camellia chinensis Nikolaeva et al. (2009)
Anthocyanin 2, 4-D + BA Fragaria ananassa Mori and Sakurai (1994)
BA + 2, 4-D Nakamura et al. (1999)
Rutin NAA + 2, 4-D Fabiana imbricate Schmeda-Hirschmann et al.
(2004)
Withaferin A 2, 4-D + BA Withania somnifera Mirjalili et al. (2009)
Anthocyanin BA Oxalis linearis Meyer and Van Staden (1995)
BAP + NAA Vitis vinifera Qu et al. (2006)
ABA Lactuca sativa Li et al. (2010)
Vitis rotundifolia Sandhu et al. (2011)
GA3 Digitalis lanata Ohlsson and Bjork (1988)
Vitis rotundifolia Teszlák et al. (2005)
Petunia hybrid Weiss et al. (1990)
Flavonol IAA + GA3 Fagopyrum esculentum Trotin et al. (1993)
Flavones 2, 4-D + NAA Camellia chinensis Nikolaeva et al. (2009)
Anthocyanin Ethylene Fragaria ananassa McSteen and Zhao (2008)
MeJa Vaccinium pahalae Fang et al. (1999)
JA Solanum lycopersicum Li et al. (2004); Uppalapati et al.
(2005)
Silymarins MeJa Silybum marianum Gabr et al. (2016)
Quercetin NAA + BAP Pluchea lanceolata Arya et al. (2008)
Rutin NAA Fagopyrum esculentum Lee et al. (2007)
Catechin IBA + BA Rheum ribes Sepehr and Ghorbanli, (2005)

Isoflavonoids
Isoflavone KIN + 2, 4-D, TIBA (Triiodo benzoic acid) + KIN Genista tinctoria Luczkiewicz et al. (2014)
TDZ + BAP Psoralea cordifolia Shinde et al. (2009)

2.2. Phenolic compounds
Plants produce a vast variety of secondary products comprising of a
phenol group, a hydroxyl functional group on an aromatic ring
(Table 3). Plants defense system employ phenols against pests and
diseases including root parasitic nematodes (Wuyts et al., 2006). These
are one of largest group of secondary plants components produced by
vegetables, fruits, teas, cocoa and other plants that have certain health
profits. They possess anti-inflammatory, antioxidant, anti-carcinogenic
and other important biological properties and may protect from oxi-
dative stress and some diseases (Park et al., 2001). Phenolic content
was enhanced in callus culture of Scutellaria columnae after addition of
2, 4-D and kinetin (Stojakowska and Kisiel, 1999). When callus culture
of Eucalyptus tereticornis treated with 2, 4-D, sterols and phenolic
compounds increased (Venkateswara et al., 1986). Ethylene was ef-
fective to improve phenolic acids production in Fragaria × ananassa
(McSteen and Zhao, 2008) and Daucus carota (Heredia and Cisneros-
Zevallos, 2009). Induction of total phenolic compounds was recorded in

30
K. Jamwal et al.
plantlets after addition of plant growth regulators BA + IBA to the
medium of Thymus vulgaris (Karalija and Parić, 2011). As the con-
centration of ABA increased, total phenolic production of Orthosiphon
stamineus also increased (Ibrahim and Jaafar, 2013). ABA, GA and
ethylene were all effective to induce production of phenolic acids and
increase activities of TAT (tyrosine amino transferase) and PAL (phe-
nylalanine ammonia lyase) in hairy roots of Salvia miltiorrhiza (Liang
et al., 2013). Exogenously applied ABA was reported to increase the
phenolic compounds content in Vitis rotundifolia (Sandhu et al., 2011)
and Phragmites communis (Ding et al., 2010).
2.2.1. Coumarin
They are simple phenolic compounds, widespread in vascular plants
(Table 3). Phenols are derived from the shikimic acid pathway (Murray
et al., 1982). They comprised a highly active group of molecules with
an extensive range of anti-microbial activity against both fungi and
bacteria (Brooker et al., 2008). Exogenously applied gibberellic acid
enhanced growth, branching patterns and coumarin content in Ci-
chorium intybus (Bais et al., 2001).
2.2.2. Furano-coumarins
Furano-coumarins are a type of coumarin with special interest of
phyto-toxicity and profuse in members of the family Umbelliferae
(Table 3). Kaul and Staba (1967) reported increased furano-coumarin in
suspension culture of Ammi visnaga containing IAA + GA3. In another
study suspension culture of Glehnia littoralis had enhanced furano-
coumarin when treated with 2, 4-D + KIN (Kitamura et al., 1998).
2.2.3. Lignin
It is a highly branched polymer of phenyl-propanoid groups, made
from three dissimilar alcohols viz., coniferyl, coumaryl and sinapyl
which oxidized to free radicals (ROS) by a pervasive plant enzyme-
peroxidase, reacts instantaneously and randomly to form lignin (Mazid
et al., 2011). Bergmann (1965) reported that the concentration of lignin
in callus tissue of Nicotiana tabacum improved after the kinetin addi-
tion. Lignin synthesis was enhanced by a low concentration of GA3, but
a high concentration of GA3 had no significant effect in N. tabacum
tissue culture (Li et al., 1970). Both auxin and gibberellin regulate
lignin biosynthesis in Coleus blumei (Aloni et al., 1990). Enhancement in
podophyllotoxin and 6-methoxypodophyllotoxin growth in cell sus-
pension cultures of Linum album cell line 2–5aH after elicitation with
MeJA (Van Fürden et al., 2005). After addition of MeJA exogenously
hairy root cultures to Linum tauricum increased the 41-dimethyl-6-
methoxypodo-phylotoxin and 6-methoxypodophyllotoxin yield 1.2-fold
(Ionkova, 2009).
2.2.4. Flavonoids
Flavonoids belong to one of the largest classes of plant phenolics
(Table 3). Flavonoids are polyphenolic compounds that are abundant in
nature. Several occur in vegetables, fruits and beverages like tea, coffee
and fruit drinks (Pridham, 1960). According to Winkel-Shirley (2001)
application of different growth regulators induces production of sec-
ondary metabolites and increase in anthocyanin content which is useful
to protect plants from UV radiation damage. Flavonoid content has
been increased with PGR treatment in various plant tissue cultures: IAA
in Scutellaria baicalensis (Zhou et al., 1997), IAA + KIN in Glycyrrhiza
echinata (Ayabe et al., 1986), IAA in Glycyrrhiza glabra (Asada et al.,
1998) and BAP + NAA in Vaccinium myrtillus (Hohtola et al., 2005).
Different combinations and concentrations of cytokinins and auxins
strongly stimulated production of flavonoids in cell suspension cultures
of Digitalis lanata (Bota and Deliu, 2015). Total flavonoids production in
Orthosiphon stamineus were influenced by levels of ABA (Ibrahim and
Jaafar, 2013). It was also observed that BA enhanced the flavonoids
production in Thymus vulgaris (Karalija and Parić, 2011). GA speeds
growth and reduces CHS (chalcone synthase) activity in Ginkgo biloba so
that flavonoid biosynthesis exhibited (Carrier et al., 1990). SA (salicylic
31
Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38
acid), KIN and GA3 significantly induced secondary metabolites, which
show the significance of PGRs in the flavonoids biosynthesis (Klessig
and Malamy, 1994). The total flavonoid content was significantly in-
creased by GA3, SA and KIN, while it decreased with ethephon appli-
cation in Taraxacum officinale (Kim et al., 2009). JA and its analogue
MeJA elicited secondary metabolites like flavonoids in many plants like
Picea abies (Martin et al., 2002), Rubus sp. (Wang et al., 2008) and
Nicotiana tabacum (Zayed and Wink, 2009).
2.2.5. Isoflavonoids
They are large group of water-soluble flavones that are plant pig-
ments, have antioxidants properties and are found in a variety of foods,
especially soy products (Table 3). NAA greatly enhanced isoflavonoid
accumulation and ratio of the NAA (auxin) to BAP (cytokinin), was
reported to have significant effect on both callus growth and iso-
flavonoid accumulation in Glycine max (Downey et al., 2013). Fastest
growth and the highest isoflavone content in Genista tinctoria were
obtained on the medium supplemented with KIN and 2, 4‐D
(Luczkiewicz et al., 2014). Daidzein content was significantly higher in
callus tissues of Pueraria tuberosa containing BA and sucrose than in vivo
plant material (Vaishnav et al., 2006). Enhanced production of iso-
flavonoids was reported on addition of TDZ in calli induced from stem
explants of Pueraria candollei var. mirifica (Udomsuk et al., 2009).
2.3. Tannins
Tannins are the most plenteous secondary metabolites made by
plants, commonly ranging from 5% to 10% dry weight of tree leaves. It
was observed that applied PGRs increased the condensed tannins in the
in vitro regenerants of Eucomis autumnalis (Masondo et al., 2014).
Robbins et al. (1996) reported that BA had little effect at low con-
centrations but lead to rise in tannin levels in Lotus corniculatus. Tannin
content increased in Geranium thunbergii hairy root culture when
treated with 2, 4-D + BAP (Ishimaru and Shimomura, 1991).
2.4. Sulphur containing secondary metabolites
Due to the diversity in chemical structures and modes of action,
sulphur-containing natural products provide plants with a versatile
range of chemical defenses against an extensive range of potential
enemies. They are responsible for the spicy tang of numerous species of
the Brassicaceae, e.g., Brassica sp. and Raphanus sativus (Schnug, 1990,
1993).
2.4.1. Glucosinolates
Glucosinolates (GSL) present almost entirely in plants of the order
Brassicales. Glucosinolates consist of a sulphur-linked β-D-glucopyr-
anose moiety and an amino acid-derived side chain (Halkier and
Gershenzon, 2006). Jasmonic acid induces metabolites which are free
and conjugated forms of glucosinolates and antioxidants (Memelink
et al., 2001). Ullah et al. (2012) reported accumulation of glucosino-
lates in seed oil after treatment with SA and Put (Putrescine) under
unstressed conditions in Brassica napus. Cultivation with the plant
growth regulator KIN (0.5 mgL−1) enhanced GS accumulation in Bras-
sica rapa hairy roots (Kastell et al., 2013). Plant growth regulators
methyl jasmonate and jasmonic acid acted as effectual elicitors, en-
hancing the total glucosinolate contents of the sprouts mainly, glucor-
aphanin in MeJA-treated Brassica oleraceae, glucoraphenin in MeJA-
treated Raphanus sativus and glucobrassicin in MeJA-treated Brassica
rapa and Brassica napus sprouts (Baenas et al., 2014).
Root elicitation with MJ and SA augmented the concentrations of
Indole glucosinolates, especially 1-methoxy-3-indolylmethyl glucosi-
nolate as well as 3-indolylmethyl and 4-methoxy-3-indolylmethyl glu-
cosinolates and 2-phenylethyl glucosinolate in the Brassica rapa ssp.
rapa exudates (Schreiner et al., 2011). Treatment of broccoli (Brassica
oleracea var. Green Magic) with MeJA resulted higher levels of indole
K. Jamwal et al. Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38

Table 4
Plant growth regulator induced alterations in nitrogen containing plant secondary metabolites.

Secondary metabolite Plant growth regulator Plant name Reference

Alkaloids
Vincristine Vinblastine 2, 4-D + KIN + IAA Catharanthus roseus Ataei-Azimi et al. (2008)
Aconites 2, 4-D + KIN Aconitum heterophyllum Giri et al. (1997)
Capsaicin Capsicum annum Umamaheswai and Lalitha (2007); Johnson et al. (1990)
Caffeine Coffea arabica Waller et al. (1983)
Cryptosin Cryptolepis buchanani Venkateswara et al. (1987)
Withanoloid IAA + KIN Withania somnifera Murthy et al. (2008)
Securinine Allosecurinine Securine gasuffruticosa Raj et al. (2015)
Quinine KIN Cinchona ledgeriana Kueh et al. (1985)
Scopolin Nicotiana tabacum Bergmann (1965)
Nicotine NAA + KIN Nicotiana tabacum Mantell et al. (1983)
Codeine BA + NAA Papaver somniferum Williams and Ellis (1992)
Quinine 2, 4-D + KIN Cinchona ledgeriana Wijnsma et al. (1985)
Quinine 2, 4-D Cinchona ledgeriana Hamill et al. (1989); Schripsema et al. (1999)
Catharathine Catharanthus roseus Ramani and Jayabaskaran (2008)
Cuscohygrine 2, 4-D + BA Calystegia sepium Jung and Tepfer (1987)
Piperine Piper solmsianum Balbuena et al. (2009)
Capsaicin 2, 4-D + GA3 Capsicum annum Varindra et al. (2000)
Vincristine Catharanthus roseus Lee-Parsons and Royce (2006)
Corydaline 2, 4-D + BAP Corydylis terminalis Taha et al. (2008)
Berberin Coscinium fenustratum Khan et al. (2008)
Berberin IAA + BAP Coscinium fenustratum Nair et al. (1992)
Vincamine BAP Vinca major Tanaka et al. (2004)
Thebaine IAA Papaver somniferum Furuya et al. (1972)
Reserpine Rauvolfia serpentina Nurchgani et al. (2008)
Corydaline IAA Corydalis ambigua Hiraoka et al. (2004)
IAA + GA3 Corydalis cava Rueffer et al. (1994)
Vincristine GA3 Catharanthus roseus Alam et al. (2012)
Withanolides SA Withania somnifera Sivanandhan et al. (2013)
Serpentine, Thiabersonine, Vindoline Catharanthus roseus El-Sayed and Verpoorte (2004)
Serpentine BAP + IAA Rauvolfia serpentina Salma et al. (2008)
Hyocyamine MS + IAA Datura stramonium Hilton and Rhodes (1993)
Camptothecin BA + KIN Ophiorrhiza rugosa var. decumbens Vineesh et al. (2007)
Reserpine MJ Rauwolfia serpentina Harisaranraj et al. (2009)

Cyanogenic glucosides
Saponin IBA Panax ginseng Bupleurum falcatum Kim et al. (2007a,b)
Saikosaponins Kusakari et al. (2000)
Saponin SA Panax ginseng Ali et al. (2006)
Glycyrrhiza glabra Shabani et al. (2009)
KIN Agave amanuensis Andrijany et al. (1999)
IAA + TDZ Saponaria officinalis Fulcheri et al. (1998)
MeJA Gypsophila paniculata Medicago truncatula Fulcheri et al. (1998)
Suzuki et al. (2002)
Centella asiatica Kim et al. (2007a,b)
Azadirachta indica Satdive et al. (2007)
Panax ginseng Palazón et al. (2003a,b)
Panax ginseng Hu and Zhong (2008)
Centella asiatica Mangas et al. (2006)
2, 4-D + BAP Gynostemma pentaphyllum Fei et al. (1993)
Saikosaponins 2, 4-D Bupleurum falcatum Wang and Huang (1982)
Saponin 2, 4-D + KIN Solanum chrysotrichum Villarreal et al. (1997)

glucosinolates and moderate levels of aromatic glucosinolates (Liu
et al., 2014). The highest augment of indole glucosinolate levels with
significant enhancement of the 1-methoxy-indol-3-ylmethyl glucosino-
late content, was achieved with treatments of sprouts and mature leaves
with methyl jasmonate and jasmonic acid (Wiesner et al., 2013).
2.4.2. Phytoalexins
One of the most important defensive systems in plants against pa-
thogen attack is the production of antimicrobial compounds called
phytoalexins (Kodama et al., 1992). Auxins arouse phytoalexin pro-
duction as well as synthesis of enzymes related to phytoalexin biosyn-
thetic routes in Phaseolus vulgaris (Hughes and Dickerson, 1990).
Belhadj et al. (2006) and Larronde et al. (2003) observed that the
exogenous application of MeJA on Vitis vinifera plants enhance che-
mical defense responses like accumulation of phytoalexins. Further
Zeneli et al. (2006) and Krokene et al. (2008) also reported that MeJA
treatment increase phytoalexins production in Picea abies. MeJA
defense responses are based on ability to produce secondary metabo-
lites such as terpenoids, stilbenoids, flavonoids and phenol acids which
are considered as phytoalexins (Faurie et al., 2009; Zhao et al., 2004).
Tamogami et al. (1997) also reported that exogenously applied JA in
rice leaves (Oryza sativa) stimulated phytoalexin production.
Kuroyanagi et al. (1998) observed enhanced phytoalexins in hairy root
culture of Hyoscyamus albus after addition of NAA + GA3. Phytoalexins
like phaseollin and kievitone were increased in Phaseolus vulgaris when
given treatment of ABA and BAP (Goosens and Vendrig, 1982). Appli-
cation of cytokinin enhanced scopoletin and capsidiol in Nicotiana ta-
bacum (Großkinsky et al., 2011).
2.5. Nitrogen containing secondary metabolites
A variety of plant secondary metabolites contain nitrogen as part of
their structure such as alkaloids, cyanogenic glucosides and non-protein
amino acids. They are of great interest because of their medicinal

32
K. Jamwal et al.
properties.
2.5.1. Alkaloids
Alkaloids have various and significant physiological effects on hu-
mans and other animals (Table 4). Khater and Elashtokhy (2015) re-
ported high concentrations of total alkaloids in callus tissues with 2 mg/
L of both NAA and IAA. An increase of biomass and alkaloid yield was
noted in the presence of NAA and BAP in the medium of Tabernae-
montana divaricata (Sierra et al., 1992). Many studies have reported
increased alkaloids in Catharanthus roseus when treated with cytokinin
(Oudin et al., 2007) and with GA (Srivastava and Srivastava, 2007).
Subroto and Doran (1994) reported that GA3 had positive influence on
enhancement of steroidal alkaloids accumulation in the Solanum avi-
culare plants. JA is known to generate secondary metabolites like qui-
nones, alkaloids and antioxidants (Memelink et al., 2001; Howe, 2005).
Alkaloid content has been increased in various plant tissue cultures
with treatment of PGRs: IAA in root culture of Cephaelis ipecacuanha
(Teshima et al., 1988), IAA in Fumaria capreolata (Tanahashi and Zenk,
1985), NAA + BA in Duboisia leichhardtii (Yamada and Endo, 1984), 2,
4-D + KIN in Ailanthus altissima (Anderson et al., 1987), 2, 4-D + KIN
in Brucea javanica (Liu et al., 1990), 2, 4-D + KIN in Corydalis ophio-
carpa (Iwasa and Takao, 1982), 2, 4‐D + KIN in Nandina domestica
(Ikuta and Itokaw, 1988), 2, 4-D + KIN in Nicotiana rustica (Tabata and
Hiraoka, 1976), KIN in Papaver somniferum (Furuya et al., 1972), 2, 4-D
in Peganum harmala (Sasse et al., 1982), and 2, 4‐D + KIN in Fritillaria
unibracteata (Gao et al., 2004). The highest enhancement of total al-
kaloid content was found in media containing 2, 4-D and BA of Cath-
aranthus roseus (Verma et al., 2012).
The presence of 2, 4-D, IAA and NAA enriched the production of
indole alkaloids in cell cultures of Cinchona ledgeriana (Harkes et al.,
1985). Various scientist reported increased indole alkaloids in different
plant tissue cultures after addition of IAA in Catharanthus roseus
(Moreno et al., 1993), IAA + GA3 in Catharanthus trichophyllus
(Davioud et al., 1989), 2, 4‐D + GA3 + vanadium in Catharanthus ro-
seus (Tallevi and Dicosmo, 1998) and NAA + KIN in Catharanthus roseus
(Zhao et al., 2001). Various PGR treatments given to different plants
tissue culture enhanced tropane alkaloids 2, 4‐D + BA in hairy root
culture of Anisodus luridus (Jovanović et al., 1991), 2, 4‐D + BA in
Hyocyamus niger (Yamada and Hashimoto, 1982), BA + NAA in Brug-
mansia candida (Giulietti et al., 1993), 2, 4-D + IAA in Brugmansia
candida (Marconi et al., 2008) and IAA + KIN in Hyocyamus niger
(Jaziri et al., 1988).
2.5.2. Cyanogenic glucosides and non-protein amino acids (Table 4)
Increased glucosides content was obtained when suspension culture
of Aloe saponaria treated with 2, 4-D + KIN (Yagi et al., 1983); Gentiana
macrophylla treated with IAA + Kin (Tiwari et al., 2007) and Gentiana
sp. treated with kinetin (Skrzypczak et al., 1993).
3. Conclusions
It is evident from the above compilation that plant growth reg-
ulators influence secondary metabolite production in significant
amount. They are effective when used in combinations as well as solely.
Both in‐vitro and in‐vivo conditions have been used by researchers to
enhance various secondary metabolites in different plants, however cell
cultures provide control of environment, production, quality and are
cost effective. They are proficient of producing specific medicinal
compounds at a rate comparable or even greater to that of intact plants.
An intensive research is needed for the production of high yields ap-
propriate for commercial utilization and the various human health
promoting plant secondary metabolites in the coming future.
Acknowledgements
The authors are thankful to the Vice-Chancellor, Shoolini
33
Journal of Applied Research on Medicinal and Aromatic Plants 9 (2018) 26–38
University, Solan for encouragement and cooperation.
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