Abiotic Stress & Secondary Metabolites in Medicinal Plants

Journal of Applied Research on Medicinal and Aromatic Plants 18 (2020) 100255
Contents lists available at ScienceDirect
Journal of Applied Research on Medicinal and Aromatic
Plants
journal homepage: www.elsevier.com/locate/jarmap
Understanding the consequence of environmental stress for accumulation of
secondary metabolites in medicinal and aromatic plants
T
Mitali Mahajana,b, Raju Kuirya, Probir K. Pala,b,*
a
Division of Agrotechnology of Medicinal, Aromatic and Commercially Important Plants, Council of Scientific and Industrial Research-Institute of Himalayan Bioresource
Technology (CSIR-IHBT), Post Box No. 6, Palampur, 176 061, HP, India
b
Academy of Scientific and Innovative Research (AcSIR), CSIR-IHBT, Post Box No. 6, Palampur, 176 061, HP, India
A R T I C LE I N FO
A B S T R A C T
Keywords:
Abiotic stress
Adaptation mechanism
Gene expression
Secondary metabolite
Terpenoids
Medicinal and aromatic plants
Abiotic stresses are the most critical hurdle for the growth and development of the plants. The abiotic stresses are
salinity, heat, drought, flood, heavy metals and plant nutrients. Plants develop different tolerance mechanisms
such as adjustment of membrane system, maintenance of cell wall architecture, production of secondary metabolites and antioxidants, phytohormones, and accumulation of osmolytes in response to abiotic stresses. The
secondary metabolites, developed through various physiological and biochemical process, play vital role to cope
up with different stresses. The presence of these compounds in the plant acts as an interface with its adverse
environment. Primary metabolites are the precursors for the secondary metabolites production in plants, but its
concentration and transport are influenced with the changes in climatic conditions. Stress conditions also enhance the expression level of corresponding genes involved in the natural product biosynthesis. The secondary
metabolites produced as a result of abiotic stresses are involved in plant defence system for survival. Secondary
metabolites never participate in building block processes rather they function to deal with many external agents.
They also protect plant from various biotic stresses and facilitate in pollination and fruit dispersal mechanism by
attracting the pollinating and dispersing agent through their beautiful colour and fragrance. In this review, we
tried to figure out how abiotic stresses affect the production of secondary metabolites in medicinal and aromatic
plants.
1. Introduction
The changes in climatic conditions leads to increase biotic and
abiotic stresses for the living organism. The productivity of medicinal
and aromatic plants (MAPs) was affected globally due to these stresses.
Abiotic stresses cause changes in agro-ecological conditions and affect
the growth and development of the plants. The MAPs are mainly grown
for various plant parts (root, stem, leaves, flowers, fruits and seeds),
which are rich source of natural metabolites. According to world health
organization (WHO), 80% population of developing countries and 60%
population of the world still depend upon medicinal herbs. Aromatic
plants are potent source of essential oil which is extensively used in
perfumes, soaps or cosmetics in beauty industry and as flavours in food
industry (Efferth and Greten, 2012). The demand of MAPs has been
radically increased in the last years, and because of low side effects its
uses accelerated in local, national and international interest (Lipp,
1996; Hyden, 2006). The natural stocks of MAPs are declining due to
increase in its demand globally for healthcare system, traditional
⁎
ethano-pharmacy as well as for cosmetics. The growth and productivity
of MAPs are strongly interrelated with the change in external climatic
factors. Plants are generally exposed to various kinds of abiotic stresses
like drought, higher concentration of salts, temperature, ozone, UVradiations and heavy metals which restrict their growth and productivity worldwide (Boyer, 1982; Araus et al., 2002). An abiotic stress
reduces the uptake and diffusion of CO2 and alters different biochemical reactions, which further inhibits photosynthesis (Flexas et al.,
2004). These stresses are the prime causes of crop failure and decreasing the yield by more than 50% (Bray et al., 2000) and pressurize
the sustainability of agriculture sector. Plants develop various adaptation mechanisms in response to environmental stresses. The enhanced
accumulation of secondary metabolites has been observed in many
MAPs in response to different abiotic stresses. Secondary metabolites
are a group of bioactive compounds, mainly produced from primary
metabolites and have no direct role in plant growth and development
but are well known for their role in plant defense and having aromatic
and medicinal properties of the plant. Also, these are potent source of
Corresponding author.
E-mail address: [email protected] (P.K. Pal).
https://doi.org/10.1016/j.jarmap.2020.100255
Received 4 December 2019; Received in revised form 14 April 2020; Accepted 17 April 2020
Available online 28 April 2020
2214-7861/ © 2020 Elsevier GmbH. All rights reserved.
Journal of Applied Research on Medicinal and Aromatic Plants 18 (2020) 100255
M. Mahajan, et al.
secondary metabolites under abiotic stresses is very limited as compared to other commercial crops. It is the high time that these plants
should be brought under priority area as they are important and potential sources for active biomolecules for nutraceuticals, cosmetics,
and pharmaceuticals.
cosmetics, food and pharmaceuticals. There are some examples of
secondary metabolites, which has pharmaceutical significance such as
glucosinolates from Tropaeolum majus is used for chemo-protection
against cancer (Bloem et al., 2014), vincamine is one of the major alkaloids present in Vinca minor leaves has pronounced cerebrovasodilatory and neuroprotective activities and also acts as CNS
stimulants (Abouzeid et al., 2017). Artemisinin derived from Artemisia
annua is well known for the treatment of malaria.
In plant system, the production of secondary metabolites directly
depends upon physiological and developmental conditions. Group of
scientists reported that during various biotic and abiotic stresses, certain group of gene expression increased, which are directly involved in
the biochemical pathway of secondary metabolites (Tuteja, 2007). In
this review we have tried to figure out the exact effects of various
stresses on secondary metabolite production, and attempts are made to
brief the exact mechanism related with each stress.
4. Biosynthesis and classification of secondary metabolites in
plants
Plants produce different types of secondary metabolites which are
classified into three major groups based on their origin: terpenoids,
phenolics, and nitrogen containing compounds. The aromatic properties of the plant arise due to the presence of qualitative compounds
known as “Terpenoids”. All terpenoids are derived from the isoprene
(C5) units combined in head and tail fashion. These are synthesized via
two routes in plants: mevalonate (MVA) pathway and 2-methylerythritol 4-phosphate (MEP) pathway (Lichtenthaler, 1999; Mahmoud
and Croteau, 2002; Degenhardt and Lincoln, 2006). Mevalonate
pathway occurs in cytoplasm where three molecules of Acetyl-CoA are
joined together in a stepwise manner to produce six carbon containing
mevalonic acid, which is the primary precursor of isopentenyl pyrophosphate (IPP). Isopentenyl diphosphate is the activated five carbon
building block of terpenes. However, production of dimethylallyl pyrophosphate from MEP pathway occurs in chloroplast and other plastids.
Isoprene units are assembled together to make monoterpenes (C10),
sesquiterpenes (C15), diterpenes (C20), triterpenes (C30) and tetraterpenes (C40). Monoterpenes, diterpenes and tetraterpenes are synthesized in plastids whereas sesquiterpenes and triterpenes are synthesized in cytosol (Fig. 2). Monoterpenes and sesquiterpenes are the
principal components of aromatic plants. Monoterpenes includes menthol, citral, geraniol, linalool, camphor, α-pinene, β-pinene, and many
others having antimicrobial and antioxidant activities. The emission of
these compounds depends upon different environmental factors. Volatile terpenoids provide protection to plants against thermal and oxidative stresses.
Phenolics are another important category of secondary metabolites
produced in response to abiotic stresses. These aromatic compounds
consist of more than one hydroxyl groups that are methylated or glycosylated. Phenols may be divided into five subgroups: phenolic acids,
flavonoids, coumarins, lignins and tannins (Gumul et al., 2007). The
shikimic acid and malonic acid pathways are responsible for the biosynthesis of the precursors of all phenolic compounds (Fig. 2). Most of
the plant phenolics are produced from shikimic acid pathway, but in
case of fungi and bacteria malonic acid pathway is more significant in
the biosynthesis of phenolic compounds. The shikimic acid pathway
converts erythrose-4-phosphate and phosphoenol pyruvate to the aromatic amino acid. Phenols have the ability to slow down the formation
of free radicals (Foti, 2007). Also, these compounds chelate heavy metal
ions (iron, manganese and copper) due to the presence of hydroxyl and
carboxyl functional groups.
Nitrogen is a common element of large group of plant secondary
metabolites. Nitrogen containing secondary metabolites are mainly
categorised into two types i.e. alkaloids and glycosides. Alkaloids are
third largest group of secondary metabolites, which contain heterocyclic nitrogen atoms. Alkaloids are further categorized into three
classes: true alkaloids, protoalkaloids and pseudoalkaloids. The true
alkaloids are basic and containing heterocyclic nitrogen. These are
derived from amino acids such as ornithine, lysine, phenylalanine,
tryptophan, tyrosine, histidine, and aspartic acid. The examples of this
group include nicotine, morphine and atropine. The precursor for
protoalkaloids is also amino acids. It is basic but does not contain nitrogen in a heterocycle. It includes alkaloid such as ‘mescaline’ derived
from phenylethylamine. The pseudoalkaloids are basic but are not
originated from amino acids, e.g. theobromine, caffeine and solanidine
(Irchhaiya et al., 2014). These alkaloids acquire their nitrogen atom
through transamination. Alkaloids production is increased during
2. Methodology
Wide ranges of scientific database were searched to collect relevant
information and citations to know the effect of various abiotic stresses
on secondary metabolites accumulation in MAPs. A scientific literature
was searched by web search engine Google Scholar, Web of Science,
Science Direct, Taylor and Francis, Mendeley, Springer link and Wiley
online library. In this review, an attempt has been made to compile all
the literature on individual effect of drought, salt, light, temperature,
heavy metals and soil nutrients on secondary metabolites production in
MAPs. The total 152 references have been assembled in this review
including research articles, review articles, and book references dating
from 1970 to 2018. In the present review article, two tables and three
figures have also been incorporated based on the synthesis of collected
references to present the various adaptation mechanisms of plants in
response to different abiotic stresses, classification and biosynthesis
pathway of the secondary metabolites and chemical structures of some
of the important secondary metabolites present in MAPs. The chemical
structures have been redrawn by using software “Chembiodraw ultra
14.0″.
3. Secondary metabolites act as a key player in plant defense
system
At molecular, anatomical and morphological levels varieties of tolerance or adaptation mechanisms have been developed by plants in
response to various climatic changes (Fig. 1). These efficient mechanisms include adjustment of membrane system and the cell wall architecture, changes in the cell cycle as well as rate of cell division, activation of specific ion channels and kinase cascades (Fraire-Velazquez
et al., 2011; Atkinson and Urwin, 2012). An abiotic stress also leads the
activation and repression of many genes at molecular level (Shinozaki
and Yamaguchi-Shinozaki, 2007; Delano-Frier et al., 2011; Grativol
et al., 2012). Plant also accumulates different reactive oxygen scavenging enzymes (Laloi et al., 2004), secondary metabolites and phytohormones (Spoel and Dong, 2008) for minimizing the biological loss
caused by these stresses. Among these, secondary metabolites are the
compounds that play an important function in adaptation and providing protection to plants against herbivores, pathogens and various
environmental stresses (Bennett and Wallsgrove, 1994; Akula and
Ravishankar, 2011). Primary metabolites i.e. carbohydrates, amino
acids, lipids and nucleotides are the precursors for the synthesis of
secondary metabolites. The biosynthesis, concentration and transport of
these compounds strongly depend upon the cultivation conditions such
as habitat, time of harvesting, climate (light, temperature) and nutrition
status of soil (Falk et al., 2007; Ballhorn et al., 2011). The interaction of
plants with diverse climatic conditions acts as a driving force for the
biosynthesis of plant secondary metabolites.
The research on MAPs with respect to the accumulation of
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M. Mahajan, et al.
Fig. 1. All the abiotic stresses such as drought, salt, temperature, light, heavy metals and soil nutrients affecting plant growth and development. Various adaptation
mechanisms adopted by the plants in response to severe abiotic stresses. A common mechanism includes stomatal closure, accumulation of osmolytes, production of
secondary metabolites, antioxidants, phytohormones, activation of specific ion channels and kinase cascades.
Fig. 2. Schematic overview of biosynthesis and
classification of secondary metabolites:
Secondary metabolites are classified based on
their chemical nature. The above scheme explains the interrelationship of secondary metabolite with primary metabolism. Secondary
metabolites are categorised into three major
types i.e. terpenoids, phenolic compounds, and
nitrogen containing compounds. Intermediates
of primary metabolism act as precursor for the
biosynthesis of all kinds of secondary metabolites. PAL: Phenylalanine ammonia lyase.
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M. Mahajan, et al.
et al., 2018).
Stress conditions also enhance the expression level of corresponding
genes involved in the natural product biosynthesis. The up-regulations
of squalene synthase (SQS) and β-amyrin synthase (BAS), key genes
involved in the production of saponins, have been reported under
drought stress (Nasrollahi et al., 2014). The upregulation of these genes
directly increases the concentration of glycyrrhizin in Glycyrrhiza
glabra. The biosynthesis and expression of three monoterpene synthases
in Salvia officinalis under drought stress have also been elucidated by
Radwan et al. (2017). They concluded that the concentration of three
most predominant cyclic monoterpenes cineole, camphor, and α/β
thujone was enhanced not only because of up regulation of three important enzymes i.e., cineole synthase, bornyl diphosphate synthase
and sabinene synthase but also due to passive shift. The maximum
concentration (% on dry weight of the leaves) of artemisinin in leaves of
Artemisia annua has been observed under salt, cold and water-logging
stresses due to an enhancement of gene expression in its biosynthesis
pathway (Vashisth et al., 2018). The up -regulation of all the major
pathway genes including 3-hydroxy-3- methyl-glutaryl coenzyme A
reductase (HMGR), farnesyl diphosphate synthase (FPPS), 1-deoxy-dxylulose-5-phosphate synthase (DXS), and 1-deoxy-dxylulose-5-phosphate reductoisomerase (DXR) have also been reported in Artemisia
annua under chilled conditions by Yang et al. (2010). Zhou et al. (2018)
noted the highest concentration of menthone in Schizonepeta tenuifolia
due to the changes in pulegone reductase activity under mild and
moderate salinity. These are some examples which show that the stimulation of secondary metabolites increases in stressed plants as
compared with normal plants. The presence of these compounds in a
plant acts as an interface with its adverse environment. The individual
effects of drought, salt, light, temperature, heavy metals and soil nutrients on secondary metabolites production are illustrated in detail
below.
abiotic stresses. Other than alkaloids, two important groups of N-containing secondary metabolites are also found; these are cyanogenic
glycosides and glucosinolates (Fig. 2). In general, cyanogenic glycosides
and glucosinolates are not toxic in themselves, but when the plant is
crushed, they release volatile poisons. The N-containing secondary
metabolites consist very specific as well as assorted pharmacological
properties.
5. Regulation of various secondary metabolites biogenesis
through abiotic stresses in MAPs
The MAPs growing under different agro-climatic conditions illustrate significant differences in the production and accumulation of
secondary metabolites. The chemical constituents of MAPs are directly
influenced by the environmental conditions (Moinuddin et al., 2012).
Abiotic stresses are the strong elicitors and exert impact on the metabolic pathway of secondary metabolites production (Karuppusamy,
2009). Nonetheless, the changes in the concentration of secondary
metabolites in plant under stress may be due to various mechanisms.
The two well-established mechanisms are “passive shift”, which caused
by over-reduced status generated in the cell (Selmar and Kleinwächter,
2013; Kleinwächter and Selmar, 2015), and “active” up-regulation of
the enzymes involved (Radwan et al., 2017; Yahyazadeh et al., 2018). A
specific group of secondary metabolites is accumulated under different
abiotic stress. The chemical structures of some common secondary
metabolites produced in the MAPs are presented in Fig. 3.
During drought stress, plants close their stomata to prevent water
loss. As a result of stomata closure rate of transpiration and uptake of
CO2 are markedly reduced but enhances the supply of reducing
equivalents (NADPH and H+), and consequently increase the ratio of
NADPH to NADP+ (Selmar and Kleinwächter, 2013; Kleinwächter and
Selmar, 2015). A massive oversupply of NADPH + H+ increases all
metabolic processes, which consume reduction equivalents, toward the
synthesis of highly reduced natural compounds, such as phenols, terpenoids, alkaloids, cyanogenic glycosides and glucosinolates (Selmar
and Kleinwächter, 2013; Kleinwächter and Selmar, 2015; Yahyazadeh
5.1. Drought stress
Drought stress is one of the foremost abiotic stresses, which shows
Fig. 3. Chemical diversity of important secondary metabolites presents in medicinal and aromatic plants.
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Table 1
Positive effect of drought and salinity on secondary metabolites of some medicinal and aromatic plants.
Abiotic stress
Medicinal and aromatic
plant
Secondary metabolites
Class of secondary
metabolite
References
Drought
Papaver somniferum
Morphine (Alkaloids)
Wang et al., 2010
Melissa officinalis
Hypericum Brasiliense
Helianthus annuum
Salvia officinalis
Essential oil
Total phenols, Rutin/ quercetin, Xanthones
Chlorogenic acid
Essential oil, Monoterpenes
Nitrogen containing
compounds
Terpenoids
Phenolics
Phenolics
Terpenoids
Artemisia annua
Catharanthus roseus
Artemisinin
Indole alkaloids
Cymbopogon pendulus
Brassica napus
Geraniol & citral
Glucosinolates
Melissa officinalis
Picea abies
Ocimum basilicum
Camellia sinensis
Cichorium intybus
Achnatherum inebrians
Rosemarinic acid
Tricyclene, α- 2 pinene, Camphene
Anthocyanin
Epicatechins
Kaempferol
Ergonovine and ergine (Alkaloids)
Stevia rebaudiana
Datura innoxia
Steviol glycosides
Tropane alkaloid
Mentha × piperita
Salvia officinalis
Matricaria chamomilla
Andrographis paniculate
Nigella sativa
Thymus vulgaris
Mentha pulegium
Digitalis purpurea
Pilocarpus jaborandi
Menthone (Monoterpenes)
V thujone and 1,8 cineol (Monoterpenes)
Protocatechuic, chlorogenic and caffeic acids
Aandrographolide, Neoandrographolide, and 14-deoxy-11,12didehydroandrographolide
Apigenin, quercetin, and trans-cinnamic acid
Thymol (Monoterpenes)
Total polyphenol
Cardenolides
Pilocarpine (Alkaloids)
Salvia officinalis
Coriandrum sativum
Achillea fragratissima
Solanum nigrum
1,8-cineole, Manool
(E)-2-dodecenal, Decanal, (E)-2-decenal
Phenols, Tannins
Solasodine (Alkaloids)
Rauvolfia tetraphylla
Reservine (Alkaloids)
Artemisia annua
Artemisinin
Salinity
Terpenoids
Nitrogen containing
compounds
Terpenoids
Nitrogen containing
compounds
Phenolics
Terpenoids
Phenolics
Phenolics
Phenolics
Nitrogen containing
compounds
Terpenoids
Nitrogen containing
compounds
Terpenoids
Terpenoids
Phenolics
Terpenoids
Phenolics
Terpenoids
Phenolics
Terpenoids
Nitrogen containing
compounds
Terpenoids
Terpenoids
Phenolics
Nitrogen containing
compounds
Nitrogen containing
compounds
Terpenoids
Abbaszadeh et al., 2009
de Abreu and Mazzafera, 2005
del Moral, 1972
Bettaieb et al., 2009; Nowak
et al., 2010
Marchese et al., 2010
Jaleel et al., 2007
Singh-Sangwan et al., 1994
Bouchereau et al., 1996
Toth et al., 2003
Kainulainen et al., 1992
Alishah et al., 2006
Hernandez et al., 2006
Taheri et al., 2008
Zhang et al., 2011
Shahverdi et al., 2017
Brachet and Cosson, 1986;
Selmar, 2008
Aziz et al., 2008
Hendawy and Khalid, 2005
Kovacik et al., 2009
Rajpar et al., 2011
Bourgou et al., 2010
Ezz El-Din et al., 2009
Queslati et al., 2010
Morales et al., 1993
de Abreu et al., 2005
Ben et al., 2010
Neffati and Marzouk, 2009
Abd El-Azim and Ahmed, 2009
Bhat et al., 2008
Misra and Gupta, 2006
Vashisht et al., 2018
anthraquinones in the leaves of Myrica lubra when exposed to medium
intensity water stress. Liu et al. (2011) also reported that yield of salvianolic acid B was increased in roots of Salvia miltiorrhiza, but the
amount of another important bioactive compound tanshinone IIA was
decreased. Thus, it is clear that enhancement of secondary metabolites
is condition specific. In case of Prunella vulgaris the production of urosolic, rosmarinic and oleanolic acid is increased during moderate
drought stress (Chen et al., 2011). The negative effect of water stress on
the growth of Prunella vulgaris is alleviated through production of these
compounds. The enhancement of alkaloids, phenolics and terpenoids
synthesis during water stress prevents too much generation of reactive
oxygen species and photoinhibition damage of chloroplast in MAPs
(Dixon and Paiva, 1995; Radasci et al., 2010). Under drought stress,
total content of terpenoids was found less in Melissa officinalis and Nepeta cataria (Manukyan, 2011). Saeidnejad et al. (2013) reported that
overall growth of Bunium persicum was reduced with increasing level of
drought stress, but the concentration of essential oil and antioxidant
activity were increased.
From a wide array of experiments, it has been established that
drought stress increases the percentage of essential oil in aromatic
plants. The effects of water stress on essential oil have been studied in
many aromatic plants such as Cymbopogon martinii, Cymbopogon winterianus, Melissa officinalis, Ocimum basilicum (Fatima et al., 2006;
Khalid, 2006; Aliabadi et al., 2009). Singh-Sangwan et al. (1994) also
dramatical changes in plant growth and yield. The condition of drought
arrives when the available water in the soil declines. It also occurs
because of insufficient rainfall and water loss continuously through the
process of transpiration and evaporation (Jaleel et al., 2007). The extent of stress tolerance is varying from one plant species to another.
Water stress is an important factor which limits the growth of plant at
initial stages. It adversely affects plant morphology of MAPs. Drought
stress reduces plant height, leaf length, leaf weight, leaf area, fresh and
dry weight in lemongrass species (Singh-Sangwan et al., 1994). Asadi
et al. (2012) have studied the effect of water deficiency on the morphology of Salvia sclarea populations and reported reduction in yield
and yield components under stress conditions. This shows the negative
impact of drought stress on plant biomass. The biomass yield of the
drought-exposed plant affects the total content of the secondary metabolites. The concentration and total content of naturally occurring
substances may be increased or decreased during stress conditions
(Eiasu et al., 2008; Khalil et al., 2010). It has been reported that total
content of secondary metabolites is not always enhanced under stress
conditions but also remain unchanged and decreased, although the
concentration is strongly elevated (Selmar and Kleinwächter, 2013).
During drought stress, drastic increase in concentration of various
phenolic compounds and betulinic acid was observed in Hypericum
brasiliense (de Abreu and Mazzafera, 2005). Yang and Li (2011) have
observed higher concentration of chlorogenic acids, flavonoids and
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M. Mahajan, et al.
Mentha pulegium (Queslati et al., 2010) also showed increase in the
phenol concentration with different saline treatments. Nigella sativa
grown under salt stress enhances the biosynthesis of apigenin, quercetin, and trans-cinnamic acid (Bourgou et al., 2010). Phenolic compounds such as phenolic acids, flavonoids, and tannins have antioxidant
property to eliminate reactive oxygen species generated during stress
conditions (Lee et al., 2004; Ksouri et al., 2007). Shahverdi et al. (2017)
studied the effects of different saline levels on Stevia rebaudiana and
showed that the low level of salt stress (30 mM) increased the percentage of stevioside and rebaudioside-A.
There is contradictory information available in the literature regarding the accumulation of essential oil and its constituents under salt
stress. Salinity affects the partitioning of assimilates during growth and
differentiation processes, which indirectly affects the production of
essential oil (Abdelmajeed et al., 2013). High salinization of soil and
water shows negative effect on essential oil yield of many MAPs e.g.
Mentha × piperita (Tabatabaie and Nazari, 2007), Mentha pulegium and
Mentha suaveolens (Aziz et al., 2008), Thymus maroccanus (Belaqziz
et al., 2009), Ocimum basilicum (Said-Al Ahl and Mahmoud, 2010),
Melissa officinalis(Ozturk et al., 2004), Majorana hortensis (Shalan et al.,
2006), Matricaria chamomilla (Razmjoo et al., 2008) and Salvia officinalis (Ben Taarit et al., 2010). In Origanum vulgare, the amount of carvacrol, p-cymene and γ-terpinene are found to be higher in control as
compared to stress condition (Said-Al Ahl and Hussein, 2010). In contrast, several reports are found on accumulation of higher essential oil
percentage under low level of salt concentration. An increase in essential oil content have been reported on Satureja hortensis (Baher et al.,
2002), Salvia officinalis (Hendawy and Khalid, 2005) and Thymus vulgaris (Ezz El-Din et al., 2009). Also, Baghalian et al. (2008) reported
higher concentration of essential oil constituents such as α-bisabololoxide B, α-bisabolol oxide A, α-bisabolol, trans-β-farnesene in Matricaria chamomilla under saline conditions. The production of all these
secondary metabolites in response to stress conditions provides defense
mechanisms to plant metabolism.
studied the influence of 45 and 90 days duration of water stress on
essential oil metabolism of two species of lemongrass (Cymbopogon
nardus and Cymbopogon pendulus). Results of that experiment indicated
that the concentration of major oil constituents such as geraniol and
citral was increased under drought conditions. Similarly, higher concentration of camphor, 1, 8 cineole and β- thujone under moderate
water deficit was reported in Salvia officinalis (Bettaieb et al., 2009).
Nowak et al. (2010) registered about 33% higher concentration of
monoterpenes in Salvia officinalis grown under moderate drought stress
as compared with under well-watered conditions. The concentration of
essential oil components does not always increase but depends upon the
plant species and intensity of applied stress conditions. The increase in
glucosinolates concentration in Tropaeolum majus due to drought stress
has been reported by Bloem et al. (2014). Kleinwächter et al. (2014) has
also observed that after 3 and 6 weeks of drought exposure of Thymus
vulgaris plants the concentration of terpene in the leaves is increased up
to 40% compared with the plants grown with well-watered condition;
however, overall content of terpenes is decreased due to the stress-related growth reductions. In another study it has been clearly mentioned
that the concentrations of terpenes (mg g−1 d.w) are enhanced in
Thymus vulgaris under drought stressed compared to the well-watered;
however, the total amount of terpenes per plant is markedly reduced
due to stress-related reduction of biomass (Paulsen and Selmar, 2016).
Mostly it has been seen from all previous studies that the accumulation
(per unit weight of biomass) of naturally occurring plant products are
significantly increased under drought stress conditions (Table 1). Thus,
plantation of MAPs in drought affected areas is the alternative way for
attaining higher production of secondary metabolites as well as proper
utilization of drought affected land.
5.2. Salt stress
Salt stress is a major obstacle for increasing growth and production
of plants throughout the world (Jamil et al., 2006). The problem of
salinity arises because of excess inorganic salts and poor quality of irrigation water. The shortage of leaching water and higher evapotranspiration rates lead to higher inorganic salts in soil. When the
electric conductivity of the soil solution reaches to 4 dS m−1 the soil is
considered to be saline, as consequence of that the osmotic pressure is
increased by about 0.2 MPa (Munns and Tester, 2008). The texture of
soil is altered with high concentration of salts resulting in decreased soil
porosity, soil aeration and water conductance (Mahajan and Tuteja,
2005). Plant growth in saline soil is restricted due to higher concentration of soluble salts and cytosolic osmotic pressure. Due to salt
stress, the basic requirements (water and nutrients) of plants are not
fulfilled, which further induce physiological and metabolic disturbances in plants. In general, salinization of soil or water adversely
affects the photosynthesis, respiration, morphological and biochemical
characteristics of the plants. However, plants grown under salt stress
accumulates various compatible osmoprotectants such as proline, glycine betaine and sugars to cope with the adverse effects of the salt stress
(Said-Al Ahl and Omer, 2011; Mahajan et al., 2020).
Exposure to salinity stimulates the production of secondary plant
products (Table 1). The total content of tropane alkaloid has been found
to be increased in Datura innoxia under saline stress (Brachet and
Cosson, 1986). In studies of Ricinus communis, it was found that the
level of ricinine (alkaloids) was significantly higher in shoots as compared to roots under salt stress (Ali et al., 2008). The accumulations of
solasodine, vincristine and reserpine, was obtained maximum in Solanum nigrum, Catharanthus roseus, and Rauvolfia tetraphylla respectively
(Anitha and Kumari, 2006; Misra and Gupta, 2006; Bhat et al., 2008)
when exposed to different level of salt stress. Cik et al. (2009) noted
significant increase in phenolic acids such as protocatechuic, chlorogenic and caffeic acids in Matricaria chamomilla. The studies published
on Nigella sativa (Bourgou et al., 2010), Achillea fragratissima (Abd ElAzim and Ahmed, 2009), Stevia rebaudiana (Rathore et al., 2014) and
5.3. Influence of light quality, quantity and duration on secondary
metabolites accumulation
An important and critical physical factor, involved in metabolic
production of plants, is light. The three parameters of light i.e. light
quality (color, wavelength), quantity (fluence rate), and photoperiod
(duration of illumination) strongly influence growth habits, plant
structure, flowering, and plant productivity (Chen et al., 2004; Casal
and Yanovsky, 2005). Ultraviolet (UV) radiation is a natural elicitor,
which stimulates the production of secondary metabolites, but the
higher dose of UV-B causes severe damage to the photosynthetic machinery, biochemical parameters such as nucleic acids and proteins, and
cell death (Pell et al., 1997). The effect of light irradiation on artemisinin biosynthesis in cultures of Artemisia annua was reported by Liu
et al. (2002). Li et al. (1996) observed higher ginsenoside content (g per
100 g of dry weight) in the roots of Panax quinquefolium plants when
exposed to longer periods of sunlight. The highest digitoxin accumulation was reported in Digitalis purpurea due to effect of light and hormones (Hagimori et al., 1982). The content of barbaloin, homonataloin,
and nataloin are found to be highest in leaves of Aloe mutabilis grown
under shade conditions as compared to direct sun light (ChauserVolfson and Gutterman, 1998). The low intensity of light significantly
changes the Ocimum basilicum oil content and its chemical composition.
The major aromatic compounds of basil i.e. linalool and eugenol content are significantly reduced under shading conditions. But the relative
concentration (%) of methyl eugenol is enhanced under lower daily
light integrals (75% shading) (Chang et al., 2008). The combination of
16 h day−1 light period with 200 μmol m-2 s-1 photosynthetic photon
flux produced highest concentration of 1-menthone and L-menthol in
Mentha arvensis var. piperascens (Malayeri et al., 2010). Bernard et al.
(2009) investigated the effect of UV-B light on Catharanthus roseus and
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M. Mahajan, et al.
cadmium, and oxalate have been influenced the secondary metabolite
production in various plants (Zhao et al., 2001). Accumulation of secondary metabolites in response to different heavy metal stress in some
MAPs are presented in Table 2. Silver nitrate (AgNO3) or cadmium
chloride (CdCl2) stimulates the production of scopolamine, and hyoscyamine (tropane alkaloids) in Brugmansia candida (Pitta-Alvarez et al.,
2000). Rai et al. (2004) exposed Ocimum tenuiflorum to different concentration of chromium (10, 20, 50 and 100 μM Cr), and reported
highest eugenol percentage with moderate chromium stress. Cadium
and cobalt increase diosgenin levels in Trigonella foenum-graecum (De
and De, 2011). The accumulation of sesquiterpenoids i.e. lubimin and
3-hydroxylubimin has been found to be higher in Datura stramonium
when treated with cadmium salts (Furze et al., 1991). However, Murch
et al. (2003) demonstrates that the presence of nickel decreases the
concentration of hyperforin, pseudohypericin and hypericin content in
Hypericum perforatum. The maximum content of total phenolics and
flavonoids had been observed in Cadium (cadmium 2 mg L−1) treated
Gynura procumbens, but the inverse results were obtained with combination of Ca and Cd (Ibrahim et al., 2017).
noted significant increase in the production of vinblastine and vincristine (indole alkaloids). Also, the exposure of UV-B light has been shown
to enhance the concentration of essential oil and phenols in Acorus
calamus (Kumari et al., 2009). UV irradiation induces flavonoids, sinapate esters, isoflavonoids and psoralens production (Hahlbrock,
1981; Lois, 1994). These compounds absorb UV-A and UV-B light and
provide a protection against its harmful effect. In callus culture of
Zingiber officinale, the gingerol and zingiberene production were raised
under the influence of light (Anasori and Asghari, 2008).
5.4. Temperature: heat stress and cold stress
Temperature is one of the important physical factors, which
strongly affects the ontology and developmental rate of plants. Elevated
temperature (heat stress) and low temperature (cold stress) cause
changes in various physiological, biochemical and molecular processes.
Temperature stress induces leaf senescence, membrane damage, degradation of chlorophyll, and denaturation of protein (Pradhan et al.,
2017). Due to these changes the production of secondary metabolites is
also affected. There are several reports available on the effect of temperature on composition or content of phenolics and terpenoids. In
flowering heads of Arnica montana the increase in ratio of quercetin:
kaempferol (flavonoids) has been reported with decreased temperature.
The ginsenoside concentration is enhanced with elevated temperature
in roots of Panax quinquefolius (Jochum et al., 2007) and Panax ginseng
(Yu et al., 2005). The effects of air temperature and thermo periodicity
were studied by Saleh (1970) on Matricaria chamomilla oil. He observed
highest chamazulene percentage at 15 °C night temperature. Loreto and
Schnitzler (2010) have noted that the increase in temperature strongly
enhances the emission of various terpenes. Terpenes stabilize the thylakoid membrane of chloroplast and have strong antioxidant activity. In
other studies, the highest concentration of α-bisabolol was obtained in
response to combination of 21−3 h photoperiod and 25−18 °C thermoperiod in Chamomilla recutita(Fahlen et al., 1997). Chan et al. (2010)
reported higher accumulation of anthocynanin under low temperature
(20 ± 2 °C) as compared to those incubated at 26 ± 2 °C and 29 ± 2 °C
in cell cultures of Melastoma malabathricum. Also, results of Soufi et al.
(2015) indicated that chlorophyll and carotenoid content were increased in pre-treated plants of Stevia rebaudiana as compared to control
under low temperature. Yin et al. (2008) and Vashisth et al. (2018)
observed that cold stress enhanced the accumulation of artemisinin in
Artemisia annua due to upregulation of genes involved in its biosynthesis pathway.
5.6. Disturbance in partioning and transport of soil nutrients: Soil nutrient
stress
The growth and development of plants strongly depend upon the
adequate quantities of nutrients present in the soil. Nutrients play important role in metabolic regulation, production and development of
new tissues and structural components of plants. The develpoment of
plant roots depends upon the soil texture and structure as well as on
available nutrients (Adelusi and Aileme, 2006). The nutrient stress
arises due to combination of other stresses such as water and saline
stress. These stresses disturb availability, partioning and transport of
nutrients. Nutrient deficiencies also occur due to the competition of
Na+ and Cl− with other nutrients such as Ca2+, K+, and NO3- with
increase in saline stress (Said-Al Ahl and Omer, 2011). The abundance
and limitation of nutrients in the soil have direct effects on biosynthesis
and concentration of secondary metabolites. It has been reported that
the deficiency in nitrogen enhances the accumulation and synthesis of
phenolic compounds, flavonoids, and phenyl propanoids. Plants allocate the extra carbon, which is not used in Calvin cycle, to the production of carbon based secondary metabolites due to low nitrogen
available in the soil (Bryant et al., 1983; Ibrahim et al., 2011). The
activity of phenyl alanine lyase, key enzyme of the phenylpropanoid
pathway, has been found to be higher in nitrogen deficient plants e.g.
Labisia pumila (Ibrahim et al., 2011) and Matricaria chamomilla (Kovacik
and Backor, 2007). On the other hand, higher nitrogen supply stimulates terpenoid production in Eucalyptus globules and Eucalyptus nitens
under nursery condition (Close et al., 2004). The negative impacts of
higher level of potassium nitrate and calcium nitrate were observed in
monoterpenoid and sesquiterpenoid content of Heterotheca subaxillaris
(Mihaliak and Lincoln, 1985). Isopentenyl diphosphate and dimethylallyl pyrophosphate, which are the precursors of terpenoids, consist of
high energy phosphate bonds. So, the terpenoids biosynthesis production is also influenced by phosphorus availability. The deprivation of
the phosphorus degrades cell membranes but compensates with greater
emission of isoprene (Ormeno and Fernandez, 2012). Sampedro et al.
(2011) have observed that the limited phosphorus does not affect the
concentration of monoterpenes and sesquiterpenes in Pinus pinaster.
Also, the presence of insufficient iron in soil raises the release and
content of phenolic acids, carboxylates and flavins (Abadia et al.,
2002). Naeem and Khan (2006) noted the maximum content of total
anthraquinone glycosides in seeds and sennoside in pods of Cassia tora
with the application of calcium.
5.5. Heavy metal stress
Heavy metals are rare naturally occuring elements found in the
soils, originating from weathering of parent rocks, pedogenesis and
anthropogenic activities. Heavy metals such as zinc, copper, molybdenum, manganese, and nickel are essential trace elements, plays
important role in various biological processes. The increases in anthropogenic activities such as atmospheric deposition, intensive agriculture, heavy traffic, metal industries, mining, and refuse dumping
enhance the concentration of several toxic heavy metals such as arsenic,
mercury, lead, cadmium etc. beyond optimal levels in soil, water and
air. As a result of this events detrimental effects are observed on crop
productivity (Sarma et al., 2012; Lydakis-Simantiris et al., 2016). It has
also been reported that the activities of total SOD, MnSOD and Cu/
ZnSOD in narrow-leafed lupins (Lupinus angustifolius) are declined
under Cu and Zn deficit conditions (Yu and Rengel, 1999)
Heavy metal stress causes contamination in soil which further induces several undesirable changes in metabolic activity of plants. The
uptake of heavy metals by plants can affect the photosynthetic pigments, sugars, proteins, and nonprotein production and leading to plant
death.
Metal ions including nickel, lanthanum, europium, silver and
6. Conclusions
Medicinal and aromatic plants are the biogenic pool of different
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Journal of Applied Research on Medicinal and Aromatic Plants 18 (2020) 100255
M. Mahajan, et al.
Table 2
Accumulation of secondary metabolites in response to different heavy metal stress.
Heavy metals ions
Plant species
Secondary metabolites accumulation
Status
References
Nickel
Iron
Cadmium
Hypericum perforatum
Trigonella foenum-graecum
Bacopa monnieri
Datura stramonium
Decrease
Decrease
Increase
Increase
Murch et al., 2003
De and De, 2011
Sinha and Saxena, 2006
Furze et al., 1991
Cobalt
Chromium
Zinc
Copper
Phyllanthus amarus Schum. and Thonn
Trigonella foenum-graecum
Ocimum tenuiflorum
Lepidium sativum
Amaranthus caudatus
Hyperforin, pseudohypericin and hypericin
Diosgenin
Bacoside-A
Lubimin, 3-hydroxylubimin
Alkaloids
Phyllanthin and hypophyllanthin
Diosgenin
Eugenol
Lepidine
Betacyanins
Decrease
Increase
Increase
Increase
Increase
Rai et al., 2005
De and De, 2011
Rai et al., 2004
Saba et al., 2000
Obrenovic, 1990
types of secondary metabolites, which enhance its exploitation. The
quality and quantity of natural metabolites depend upon the duration
and frequency of different biotic and abiotic stresses such as drought,
light, salt and temperature etc. During stress, the carbon fixed is predominantly allocated to secondary metabolites synthesis instead of
enhancing the plant growth. The production of secondary metabolites is
one of the important adaptative mechanism adopted by plants during
stress conditions. This consideration suggests that secondary metabolites may help the plant to prevent damages caused by various abiotic
stresses. These secondary metabolites are used as raw material in nutraceuticals, fragrances dyes, insecticides, cosmetics and pharmaceuticals etc. Although the climate change is disastrous for entire living
kingdom but it would be an opportunity for country like India, to shift
the cropping system from traditional crops to medicinal and aromatic
crops. It is evident that abiotic stress increases the secondary metabolite
production in the plants, which elevates the phytomedicine production,
and increases the quality of essential oil in aromatic plants. The practicing of MAPs crop cultivation can protect the natural sources, which
are under pressure due to excessive exploitation, and simultaneously it
can contribute for the advancement of Phytopharmaceutical and
Aromatic Industries.
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Declaration of Competing Interest
This is to certify that we do not have any competing financial interests or personal relationships that could have appeared to influence
the work reported in this paper. The authors do not have any conflict of
interest also.
Acknowledgement
Authors are thankful to Director, IHBT, Palampur for his constant
encouragement for the work. Authors acknowledge the Council of
Scientific and Industrial Research for financial support.
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