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Cuminum
Lcyminum
1-
d
2-
mkJ4.75 wereDXSandHMGRGPPs,
upregulated
increasedTerpenes
2019)
Ghasemi
(al.et
Chrysanthemum
indicum var.
aromaticum.
400 μWcm
-2
Expression levels of FPS,
HMGR, DXR, TPS, GPS and
DXS were upregulated
Calamenene, cadinene,
α-thujone, thujone, β- thujone
and cajuputole increased
He et al.
(2019)
Achyranthes
bidentata Blume
0.738,1.476, 2.214 and
2.952 kJ m
-2
Enhanced expression of HMGS,
HMGR, PMK, FPS, SS, SE, β-AS
and CAS
Oleanolic acid and ecdysterone
content increased
Li et al.
(2019)
Withania
coagulans L.
2.8 W m
-2
DXR, DXS and HMGR were
upregulated
Enhancement in withanolides Tripathi
et al. (2021)
Conyza blini H.
lev
20, 40 and 80 μWcm
-2
DXS and DXR upregulated Blinin content increased Zhan et al.
(2021)
10 Secondary Metabolites Biosynthesis and Related Gene Expression... 161
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162 A. Pandey et al.
Zhang et al. (2018) observed that UV-B radiation upregulates the PAL and C4H
gene expression and hence leads to the conversion of phenylalanine (which is a key
precursor of all phenolics) to flavonoids by stimulating the activity of PAL and C4H
enzyme in Glycyrrhiza uralensis. It was also found that UV-B radiation differen-
tially regulates the expression of genes at different growth stages of plants. Del-
Castillo-Alonso et al. (
2021) revealed that VvFLS4 and VvCH4 showed enhanced
expression at the post-harvest stage of Vitis vinifera exposed to UV-B radiation in
field conditions. Del-Castillo-Alonso et al. (
2021) observed linear regression
between quercetins and kaempferols (flavonols) content and the expression of the
VvCHS1 and VvFLS4 genes of V. vinifera. The findings of Maher et al. (
2021)
showed that UV-B radiation had an impact on unigenes involved in the production
of flavonoids. Therefore, the differences in the unigenes transcript level involved in
the flavonoids biosynthesis pathway were responsible for the variations in flavonoids
contents under UV-B exposure in Phoenix dactylifera (Maher et al.
2021). Indeed,
ROS are crucial signal molecules that can stimulate the production of antioxidant
phytochemicals. Jiao et al. (
2022) reported that enhanced ROS production under
UV-B radiation might be responsible for the upregulation of genes related to
flavonoids biosynthesis, such as FLS1 , F3′5′H2, C4H, PAL1, PAL2, PAL3, CHS1
and CHS2 in Taxus cuspidata. Upregulation of these genes under UV-B radiation
was found to be correlated with enhanced accumulation of flavonoids (bilobetin,
isoquercitrin, ciadopitysin, and ginkgetin) in plantlets of T. cuspidata. UV-B is also
known to cause tissue-specific accumulation of different classes of secondary
metabolites. In Astragalus mongholicus content of flavonols and flavanones
enhanced in leaves while the content of isoflavonoids increased in the roots under
UV-B radiation. In addition, exposure of UV-B to A. mongholicus causes
upregul
ation of different isoflavonoids genes (IFS, CHI, I3’H, IOMT, and UCGT)
and consequently leads to enhanced accumulation of isoflavonoids (Calycosin-7-O-
d-glucoside, ononin, daidzein, and formononetin) in roots. However, the
downregulation of these genes in above-ground parts causes a reduction in the
content of isoflavonoids in aboveground parts under UV-B radiation (Liu et al.
2020). An experiment was conducted by Jiao et al. (
2015) to observe the effect of
different doses of UV-B radiation (5.4–172.8 kJ m
-2
d
-1
) on gene expression and
subsequent isoflavonoids accum ulation in Astragalus membranaceus. Jiao et al.
(2015
) observed that optimal dose of UV-B for accumulation of isoflavonoids was
86.4 kJ m
-2
d
-1
. Further, they found a correlation between the expression level of
PAL, CHI, C4H, and I3′H genes and isoflavonoi ds accumulation, which showed that
enhanced accumulation of isoflavonoids under UV-B radiation in A. membranaceus
might occur due to upregulation of these genes of isoflavonoids biosynthesis path-
way. Exposure of UV-B (10.97 kJ m
-2
d
-1
) to Salvia verticillata stimulates the
expression of PAL, RAS, and TAT genes and results in increased contents of
phenolics, and hence the antioxidant property of S. verticillata under UV-B radiation
(Rizi et al.
2021). Treatment of UV-B to Perilla frutescens grown in plant factories
leads to upregulation of PAL, RAS, and TAT genes taking part in the biosynthesis of
rosmarinic acid consistent with increased accumulation of rosmarinic acid. How-
ever, CHS, F3H, ANS, and DFR genes related to the enzymes of anthocyanins
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biosynthesis showed downregulated expression under UV-B and might be responsi-
ble for the reduction in anthocyanins in P. frutescens (Yoshida et al. 2022).
10 Secondary Metabolites Biosynthesis and Related Gene Expression... 163
10.4 Effects of UV-B on Gene Expression in Relation to Terpenes
The terpene’s defensive antioxidant pathway and emission of isoprene in plants
perform a prominent ecological and physiological role in defense against environ-
mental challenges (Loreto and Schnitzler
2010). Biosynthesis of terpenoid occurs
via two pathways including the mevalonic acid (MVA) pathway, which operates in
the cytosol, and the methylerythritol phosphate (MEP) pathway operated in plastids,
which lead to the formation of C5 compounds isopentenyl pyrophosphate (IPP) and
dimethylallyl pyrophosphate (DMAPP) (Yang et al.
2013). The genes involved in
both the pathways, such as GPPS and DXS in the MEP pathway and FPPS and
HMGR in the MVA pathway, were found to be stimulated under UV-B radiation
(Dolzhenko et al.
2010; Wang et al. 2016).
Previous studies revealed UV-B-induced upregulation in the expression of
numerous terpene biosynthetic genes, such as GPPS, DXS, FPPS, and TPS (Fan
et al.
2018). Increased terpenoid synthase activity was also observed in response to
UV-B radiation in Vitis vinifera (Gil et al.
2012). Contrary to this, Liu et al. (2017)
reported both the reduced and increased expression of transcripts PpTPS1 (a TPS-g
subfamily member) and PpTPS2 (a TPS-b subfamily member), respectively in
Prunus persica. A study by Dolzhenko et al. (2010) on Mentha piperita showed
activation of the expression of terpenoids biosynthetic genes: MDS, DXS, GPPS,
IPPI, LS, PR, MR, MFS, L3oh, FPPS, and a putative S-TPS under UV-B exposure.
Ghasemi et al. (
2019
) reported the increased expression of genes DXS, HMGR
and GPP after UV-B treatment indicating that both MVA and MEP pathway
functions independently and ultima tely increasing the terpenes content in Cuminum
cyminum. Increased expression of HMGR, DXR, TPS, GPS, FPS, and DXS was
found after UV-B exposure in Chrysanthemum indicum. In the MVA pathway, FPS
gene expression leads to an increase in the contents of calamenene and cadinene,
while HMGR gene expression is involved in inducing the 1-caryophyllene content.
Furthermore, in the MEP pathway, expressions of DXR, TPS, and GPS lead
to an
increase α-thujone, thujone,
and β-thujone. Moreover, DXS gene expression is
involved in inducing cajuputole content in Chrysanthemum indicum under UV-B
exposure (He et al. 2019
). A short-term exposure of UV-B to Achyranthes bidentata
showed upregulation of HMGR, HMGS, PMK, SS, FPS, β-AS, SE, and CAS genes
related to oleanolic acid and ecdysterone biosynthesis (Li et al. 2019). A study by
Tripathi et al. (2021) denoted a 1.78-fold higher upregulation of the HMGR gene.
Further, DXR and DXS genes exhibited over-expression under different exposures of
UV-B in Withania coagulans. A study by Dabiri et al. (
2020) indicated that
increased expression of DXS from the MEP pathway was found in Chrysanthemum
cinerariaefolium under different abiotic stress exposures including UV rays. More-
over, an incre ased content of blinin, a diterpene in Conyza blinii was observed as a
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result of the upregulation of 14 genes including DXS and DXR genes (Zhan et al.
2021).
164 A. Pandey et al.
10.5 Effects of UV-B on Gene Expression in Relation to Alkaloids
UV-B also regulates the expression of genes related to alkaloids biosynthesis in
plants (Table 10.1). However, studies related to the effects of UV-B on the gene
expression of alkaloids are not much explored. Psychot ria brachyceras contain a
monoterpene indole alkaloid namely, brachycerine and depict antimutagenic and
antioxidant properties. Do Nascimento et al. (
2013
) reported that under UV-B
radiation accumulation of brachycerine appears at least to some extent controlled
at the transcriptional level as observed by enhanced expression of TDC, ACO,
UDP-glu, Ser/Thre, and Lip genes related to brachycerine biosynthesis. In
Catharanthus roseus terpenoid indole alkaloids are synthesized by a key precursor
namely, strictosidine, which is then synthesized from tryptophan (shikimate path-
way) and geraniol (MEP pathway). Enhanced expression of genes involved in the
biosynthesis of strictosidine, such as g10h, tdc, sls, 10-hgo, and str leads to enhanced
content of strictosidine under stress condition (1345 μ W cm
-2
for 1–3 h followed by
72 h darkness). In addition, it was found that the transcription factor ORCA3 played
a significant role in the regulation of several genes of indole alkaloid biosynthesis in
C. roseus. Zhu et al. (2015) reveal ed that over-expression of ORCA3 enhanced the
expression of genes of indole alkaloid biosynthesis that subsequently leads to the
accretion of indole alkaloids in C. roseus under stress. Moreover, Zhong et al. (
2021
)
documented that UV-B stress causes dynamic alteration in mitochondria and induces
ATP production, controls the metabolite flow of MEP pathway for monoterpenes
(main skeleton of terpenoid indole alkaloids) biosynthesis, and results in the accu-
mulation of terpenoid indole alkaloids in C. roseus. Another medicinally imp ortant
plant Mahonia bealei widely used in traditional Chinese medicine for the cure of
jaundice and tuberculosis and have protoberberine alkaloids, such as berberine,
columbamine, and palmatine as its major active metabolites. Zhu et al. (2021)
found that treatment of UV-B (104.4 kJ m
-2
d
-1
) for 6 h followed by 54 h darkness
significantly enhanced the content of these protoberberine alkaloids. Further, an
increase in the content of these alkaloids was associated with enhanced expression of
the tetrahydroberberine oxidase (tbo) gene, which encodes the key enzymes
involved in the final step of berberine, columbamine, and palmatine alkaloids
biosynthesis. Moreover, Zhu et al. (2021) proposed that crosstalk of calcium signal-
ing with enhanced ROS production may also be responsibl e for enhanced biosyn-
thesis of protoberberine alkaloids in the leaves of M. bealei. Another study made by
Liu et al. (
2022) using the same dose of UV-B on M. bealei reported that exposure of
UV-B causes oxidative stress and activates the MAPK signaling pathway, which
might be responsible for the enhanced accumulation of alkaloids in M. bealei. It is
interesting to note that the jasmonic acid-responsive transcription factor, ethylene
response factor 15 (ERF15) can bind to the GCC-box of the taxadiene synthase
(TASY) gene to regulate the production of taxanes. In accordance with this Jiao et al.
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(2022) observed enhanced expression of genes taking part in jasmonate signaling
and taxoid biosynthesis under a mild dose of UV-B (3 W m
-2
). Jiao et al. (2022)
suggested that the UV-B-mediate d jasmonate signaling pathway might be responsi-
ble for the enhanced accumulation of taxoids in Taxus cuspidata.
10 Secondary Metabolites Biosynthesis and Related Gene Expression... 165
10.6 Conclusions
UV-B radiation can potentially regulate gene expression of enzymes taking part in
the biosynthesis of diverse secondary metabolites (belonging to phenolics,
terpenoids, and alkaloids class) in plants at the transcriptional level. UV-B-mediated
gene expression alteration subsequently changes biosynthesis and hence the accu-
mulation of secondary metabolites. Further, these responses of UV-B in plants are
mediated by UV-B-specific and non-speci fic pathways. Studies related to UV-B-
specific pathways on the gene expression of phenolics are explored largely. How-
ever, studies related to the effects of UV-B by involving UV-B specific and
non-specific pathways on the gene expression of alkaloids and terpenes has not
been extensively studies. So, there is a need for comprehensive studies involving
different doses of UV-B in relation to gene expression of diverse secondary
metabolites in plants under varied environments.
Acknowledgements The authors are grateful to the Head, Department of Botany, Banaras Hindu
University, for providing all the necessary laboratory facilities. Coordinator, Centre of Advanced
Study (CAS), Department of Botany, Interdisciplinary School of Life Sciences (ISLS) are acknowl-
edged for all research facilities. University Grants Commission (UGC) India is greatly acknowl-
edged for providing the financial support in the form of Senior Research Fellowship to Avantika
Pandey. Prof. Madhoolika Agrawal is thankful to SERB, New Delhi for providing J.C. Bose
Fellowship and Institute of Eminence (IoE), BHU for financial support. Prof. S.B. Agrawal is
also grateful to Council of Scientific and Industrial Research (CSIR), New Delhi, India for Emeritus
Scientist Project.
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169
Signaling Molecules in Medicinal Plants
Response to Cold Stress
11
Guru Kumar Dugganaboyana, Sahana Shivaramakrishna,
Jajur Ramanna Kumar, Gopalakrishnan Velliyur Kanniappan,
Chethan Kumar Mukunda, and Rathi Muthaiyan Ahalliya
Abstract
Plants undergo numerous morphological, physiological, biochemical, molecular,
and cellular alterations on exposure to various abiotic stresses. Cold stress
hampering seed germination, photosynthesis, osmotic balance, reproductive
development, antioxidant system, and so forth, is one of the prominent ecological
stresses in tropical and subtropical regions across the globe. Poor germination,
stunted growth, chlorosis, oxidative stress, necrosis, and so forth, are some of the
repercussions of non-freezing low temperatures resulting in a cold stress injury.
Plants develop complex multigenic signaling processes favored by an engineered
and integrated genetic makeup to activate molecular and cellular mechanisms
needed to overcome the damage and develop cold tolerance. Cold acclimation is
primarily achieved by the upregulation of cold-responsive genes and transcription
factors (CBF) that translate into several cold-regulated proteins (COR). Among
them are complex signaling hormones, anti-oxidant enzymes, melatonin,
miRNA-mediated regulatory molecules, and so forth. In addition, increased
G. K. Dugganaboyana (✉) · S. Shivaramakrishna · J. R. Kumar
Division of Biochemistry, School of Life Sciences, Mysuru, JSS Academy of Higher Education and
Research (Deemed to be University), Mysuru, Karnataka, India
e-mail: gurukumard@jssuni.edu.in
G. Velliyur Kanniappan
School of Medicine, Bule Hora University Institute of Health, Bule Hora University, Bule Hora,
Ethiopia
C. K. Mukunda
Department of Biochemistry, JSS College of Arts, Commerce and Science, Mysore, Karnataka,
India
R. M. Ahalliya
Department of Biochemistry, Karpagam Academy of Higher Education, Coimbatore, Tamil Nadu,
India
#
The Author(s), under exclusive license to Springer Nature Singapore Pte
Ltd. 2023
D. Singh et al. (eds.), Stress-responsive Factors and Molecular Farming
in Medicinal Plants,
https://doi.org/10.1007/978-981-99-4480-4_11
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expression of enzyme-coding genes leads to the synthesis of secondary
metabolites that are markedly important in cold tolerance. Medicinal herbs are
plants with high economic value, potential therapeutic properties, and increasing
pharmacological benefits. Thereby, the prime focus of this chapter is to address
the underlying mechanisms and signaling molecules involved in various medici-
nal plants to overcome the repercussions of cold stress injury.
170 G. K. Dugganaboyana et al.
Keywords
Cold stress · Medicinal plants · Signaling molecules · Cold acclimation
11.1 Introduction
World’s arable land is approximately 5 billion hectares or 38% of the global land
area as reported by FAO (dated 7 May 2020). Also, a comparative study of 60 years
(1961–2020) showed a significant decrease in the arable land from 0.45 hectares per
capita to 0.21 hectares per capita. Besides, World population predictions by the
United Nations, Department of Economic and Social Affairs for 2022 projected that
the global population marked to 8 billion as of November 15, 2022. This indefinite
increase in the global population and decrease in the arable land in a beeli ne leads to
food scarcity. Experts suggest that, global climate change is crucial in reverberating
this problem by escalating soil erosion and desertification (Ghassemi et al. 2021;
Yadav 2010). Amongst the various abiotic stresses, freezing (<0 °C), chilling
(0–15 °C), and sub-optimum temperatures collectively insult the crop yield by
approximately 70% and curtail crop productivity and plant growth (Hussain
2011).
The surge in the ambient temperature galvanizes diverse physiological, biochemical,
molecular, phenological, and metabolic alterations within sub-tropical and temperate
plants leading to their injury or death under extremities (Yadav
2010; Isah 2019).
Freezing injuries in plants are initiated when freezing air mass displaces the
warmer ambient air, culminating in lower ground temperature that triggers the
formation of ice crystals within plant cells. Whereas, frost injury, on the other
hand, the result of inversion of temperature within the plant tissues where they
radiate more heat into the atmosphere compared to what they receive. Both these
conditions vandalize plant development and overall yield. The severity of damage
varies amongst different plant species, developmental stages, ambient temperat ure
modification, the time-scale of exposure (Rajashekar et al. 1983; Steffen et al.
1989),
water availability, irradiance, and accessibility of micronutrients (Ercoli et al.
2004),
and a few others. Photosynthesis in plants is characterized by chlorophyll fluores-
cence (F
v
/F
m
) which is acutely reduced under cold stress. This reduction in F
v
/F
m
contracts the performance index (PI
ABS
) by 50–73%, Net photosynthetic rate (P
N
) by
81–84%, transpiration rate (E ), substomatal CO
2
concentration, Photosynthetic
pigments (Chl a, Chl b, carotenoids), etc., demolishing the functions of both PSI
and PSII (Hajihashemi et al.
2018).
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