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150 A. K. Srivastava et al.
9.6 Conclusions and Future Perspectives
The miRNAs play significant role in regulating of seedling development, synthesis,
and modification of secondary metabolites in plants and stress adaptation. The
secondary metabolites of plants are used as therapeutic agents for curing severe
diseases including cancer. During stress condition, activity of miRNAs depend on
the identification of target genes involving several biogenesis pathways. Thus, the
upregulation and downregulation of miRNAs alter the synthesis of secondary
metabolites pathways in medicinal plants under different stress condition. Several
studies are accomplished in Arabidopsis plants to explore the miRNAs families
under different stress condition. The miRNAs are major components of in gene
regulatory networks for production of medicinal important compounds in plants,
however, a complete understanding of role of miRNAs would highly enhance
understanding of plant tolerance and production of medi cinal important chemicals
under distinct stress condition.
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155
Secondary Metabolites Biosynthesis
and Related Gene Expression Under
Ultraviolet-B Radiation
10
Avantika Pandey, Deepanshi Jaiswal, Madhoolika Agrawal,
and Shashi Bhushan Agrawal
Abstract
Plants have a diverse array of secondary metabolites as part of their defense
mechanism against various stress conditions. These secondary metabolites are
broadly classified into phenolics, alkaloids, and terpenes. Ultraviolet-B (UV-B)
radiation is one such environmental factor that acts both as a stressor and
regulator for plants. UV-B mediated responses of plants including regulation of
secondary metabolites biosynthesis involve two pathways, i.e., UVR8
(UV resistance locus 8) mediated UV-B specific and non-specific pathways. By
involving these two pathways UV-B regulate the biosynthesis of secondary
metabolites at the transcriptional level. UV-B radiation affects the expression of
numerous genes of the enzymes invol ved in the production of secondary
metabolites that may ultimately affect the accretion of secondary metabolites in
plants. However, these responses to UV-B vary depending on species, cultivars,
UV-B dose, developmental stage of plants, experimental conditions, and existing
environmental factors. Therefore, a thorough investigation of the effects of UV-B
on gene expression and biosynthesis of secondary metabolites in plants is covered
in the present review.
Keywords
UV-B radiation · Gene expression · Secondary metabolites · Biosynthesis
A. Pandey · M. Agrawal · S. B. Agrawal (✉)
Laboratory of Air Pollution and Global Climate Change, Department of Botany, Institute of
Science, Banaras Hindu University, Varanasi, India
D. Jaiswal
Department of Botany, Mahatma Gandhi Balika Vidyalaya (P.G.) College, Firozabad, 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_10
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156 A. Pandey et al.
10.1 Introduction
Ultraviolet-B (UV-B) radiation is a very well-known environmental factor that acts
both as a stressor and activator of secondary metabolites in plants. Plant’s secondary
metabolites are one of the key factors involved in defense related mechanisms under
stress conditions (Takshak and Agrawal
2019). Plants have evolved several ways to
alter metabolic proces ses and reconfigure the metabolic network in response to
UV-B radiation (Zhang et al.
2018). Secondary metabolites are a large group of
structurally diverse compounds originating from the secondary metabolic pathway
linked with several intermediates of the primary metabolic pathway (Pang et al.
2021). UV-B is believed to have at least two different impacts, one with respect to
provoked damage and the other with respect to the perception of UV-B by UVR8
(UV resistance locus 8) photoreceptor, which results in UV-B induced
photomorphogenic responses and thus acclimation. In general, UV-B causes the
activation of a wide range of different signaling responses leading to the alteration in
the expression of genes (Singh et al.
2015). Studies with UV-B and plants showed
that low doses of UV-B serve as a stimulator (eustress) of important secondary
metabolites, but high doses serve as distress (Csepregi et al.
2017). Generally,
several factors affect the harmony between the eustress and the distress responses
of UV-B, including dosages, duration, spectral quality, developmental stages,
genotypes, other environmental factors, and the acclimatization strategies operating
in plants. The major classes of secondary metabolites found in plants are categorized
into terpenes, phenolics, and nitrogen-containing compounds, such as alkaloids.
Alkaloids are a diverse class of secondary metabolites and it was found that there
is no generalized pathway for the biosynthesis of alkaloids however, depending on
their origin they are categorized as true alkaloids, pseudoalkaloids, and
protoalkaloids (Takshak and Agrawal
2019). Increased expression of different
classes of alkaloids and their related genes are reported in several plant species,
such as indole alkaloid in Psychotria brachyceras, tropane alkaloid in Anisodus
luridus, terpenoid indole alkaloid in Catharanthus roseus and indole alkaloid in
Clematis terniflora under exposure of UV -B radiation (Do Nascimento et al.
2013;
Qin et al.
2014; Binder et al. 2009; Gao et al. 2016). The terpenes biosynthetic
pathway, whi ch leads to the formation of different classes of terpenes, such as
monoterpenes, diterpenes, sesquiterpenes, triterpenes and tetraterpenes also showed
increased expression under UV-B radiation. The terpene content and its related gene
expression have been found to be enhanced in Prunus perscia, Mentha piperita,
Vitiis vinifera, Picea abies, and Camelia sinensis (Liu et al.
2017; Dolzhenko et al.
2010; Gil et al. 2012; Ohlsson et al. 2013; Shamala et al. 2020). Similarly, phenolic
compounds also enhanced under UV-B exposure. Several phenolic compounds
showed enhanced expression under UV-B, such as Vaccinium corymbosum, Capsi-
cum annuum, and Salvia verticillata (Inostroza-Blancheteau et al. 2016; Rodríguez-
Calzada et al. 2019; Rizi et al. 2021). According to the studies, UV-B altered the
expression of the genes of different classes of secondary metabolites and resulted in
different accumulation patterns of these secondary metabolites in plants. So, it is
important to decipher the detailed analysis of the genes involved in the activation of
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different classes of secondary metabolites’ biosynthetic pathways. This chapter spe-
cifically lightens the genes and their related metabolites altered under specific
exposure to UV-B radiation.
10 Secondary Metabolites Biosynthesis and Related Gene Expression... 157
10.2 Regulation of Secondary Metabolites Biosynthesis
Through UV-B Mediated Signaling
UV-B radiation is one among the numerous environmental variables that can
potentially influence the biosynthesis of numerous secondary metabolites by activa-
tion or inactivation of the relevant genes of the biosynthesis pathway (Apoorva et al.
2021). UV-B mediated responses of the plant including regulation of the gene
expression involve two pathways, i.e., UVR8 (UV resistance locus 8) mediated
UV-B specific pathway and non-specific pathway (Jenkins 2017) (Fig. 10.1).
UVR8-mediated responses involve the perception of the UV-B radiation by
UVR8 photoreceptors and following the perception of UV-B, inactive UVR8
homodimers (in the cytosol) are converted into active monomers. Further, the
UVR8 monomer interacts with the CONSTITUTIVELY PHOTOMORPHOGENIC
1 (COP1) and makes a UVR8-COP1 complex, which is further transported to the
Fig. 10.1 Diagrammatic representation of UV-B specific and non-specific pathways, (Adapted
from (Apoorva et al. 2021; Matsuura et al. 2013))
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nucleus. Moreover, the WD40-repeat proteins RUP1 and RUP2 (REPRESSOR OF
UV-B PHOTOMORPHOGENESIS 1 and 2) deactivate this process by interfering
with the UVR8-COP1 complex and then re-dimerize monomers of UVR8 via a
negative feedback cycle to replenish UVR8 homodimer. In the nucleus, the UVR8-
COP1 complex interacts with the ELONGATED HYPOCOTYL 5 (HY5) transcrip-
tion factor, which is a central mediator of UV-B responses. HY5 then regulates the
activity of numerous ot
her transcription factors (Pandey et al.
2023)
.
I
t was observed
that transcription factor binds to appropriate cis-elements found in the promoter area
of the genes they are aimed to stimulate or suppress or they may associate with other
transcription factors to establish a regulatory complex (Apoorva et al. 2021). The
MYB, bHLH, WRKY, ORCA3, and WDR families of transcription factors are well
known to control the diverse secondary metabolites biosynthesis pathways in
numerous plant species. Song et al. (
2022) revealed that VcMYBPA1,
MYBPA2.1, MYBA2, MYB114, and MYBF transcription factors stimulate the
expression of genes of flavonoids biosynthesis pathway and activate the UV-B
mediated flavonoids biosynthesis in Vaccinium corymbosum. In addition, the tran-
scription factor bHLH either interacts with MYB or directly controls the expression
of structural genes of secondary metabolites biosynthesis. Further, Song et al. (2022
)
s
ugges
t
ed that under UV-B irradiation, transcription factors bHLHL74 and bHLH25
may negatively control the biosynthesis of flavonoids in V. corymbosum by
suppressing the expression of genes that participated in the biosynthesis pathway
of flavonoids or by interacting with MYB. Under UV-B radiation, UVR8
(VviUVR1) and HY5 orthologs (VviHY5 and VviHYH) played a role in flavonol
accumulation in Vitis vinifera. UV-B promotes the accretion of flavonols by the
activation o
f VviHY5 and VviHYH in V. vinifera at various growth stages (Loyola
et al.
2016).
158 A. Pandey et al.
Furthermore, the non-sp
ecific UV-B responses involve the alteration in gene
expression due to enhanced production of reactive oxygen species (ROS), oxidative
stress, DNA damage, activation of MAP kinase, nitric oxide, and phytohormones
signaling (Jenkins
2017) (Fig. 10.1 ). Ruan et al. (2014) revealed that UV-B-induced
production of camptothecin in Camptotheca acuminata cells involves the nitrate
reductase-mediated signaling of nitric oxide. In response to variations in UV-B
levels, UVR8 non-specific pathways are anticipated to mediate gene expression in
plants. Jenkins (2017) reported that UVR8 non-specific signaling pathway may be
activated when plants acclimated to a certain level of UV-B are exposed to a much
greater level of UV-B that may lead to changes in gene expression.
10.3 Effects of UV-B on Gene Expression in Relation
to Phenolics
There are numerous studies related to UV-B-mediated regulation of the gene expres-
sion of enzymes that participated in the biosynthesis of different classes of phenolics
(Table 10.1).
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6Wm
-2
with 16 h irradiation
(6 W16 h) and 4 W m
-2
with
The expression level of PAL,
TAT and RAS increased while
(continued)
10 Secondary Metabolites Biosynthesis and Related Gene Expression... 159
Table 10.1 Effect of UV-B on secondary metabolites accumulation and related gene expression in plants
Class of
secondary
metabolites Plants UV-B dose/duration Gene expression Response References
Phenolics Vitis vinifera L. 0.76 MJ m
-2
Enhanced expression of VvFLS4
and VvCHS1 while expression of
HY5 and bHLH transcription
factors not significantly varied.
Flavonol contents (particularly
quercetins and kaempferols)
increased
Del-
Castillo-
Alonso et al.
(2021)
Taxus cuspidata
Sieb. Et Zucc
3Wm
-2
PAL1, PAL2, PAL3, C4H,
CHS1, CHS2, CHS3, FLS1, and
F3′5′H2 were upregulated
Content of bilobetin,
isoquercitrin, ciadopitysin and
ginkgetin enhanced while
isoginkgetin showed
non-significant variation
Jiao et al.
(2022)
Astragalus
mongholicus
Bunge
804 J m
-2
for 40 min d
-1
CHI, IFS, IOMT, I3’H and
UCGT upregulated in root while
downregulated in above ground
parts
Calycosin-7-O- d-glucoside,
daidzein, ononin and
formononetin enhanced in root
while decreased in aboveground
parts
Liu et al.
(2020)
Astragalus
membranaceus
Bunge
5.4–172.8 kJ m
-2
d
-1
for
0.5–16 h
Enhanced expression level of
PAL, C4H, CHI, CHS, IFS and
I3′H genes
Total isoflavonoids content
increased by 2.29-fold at optimal
elicitation dose (86.4 kJ m
-2
d
-
1
)
Jiao et al.
(
2015)
Cuminum
cyminum L.
54 kJ m
-2
h
-1
for 3–12 h Expression of PAL enhanced Enhanced accumulation of
flavonoids and anthocyanins
Ghasemi
et al. (
2019)
Glycyrrhiza
uralensis
(Fisch.)
0.024 W m
-2
for 12, 24, 48 and
96 h
Enhanced expression of PAL
and C4H
Flavonoids content increased Zhang et al.
(
2018)
Salvia
verticillata L.
10.97 kJ m
-2
d
-1
for 10 day Enhanced expression of PAL,
TAT and RAS
Total phenols and flavonoids
content increased
Rizi et al.
(
2021)
Perilla
frutescens L.
Yoshida
et al. (
2022)
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Table 10.1 (continued)
Class of
secondary
metabolites Plants UV-B dose/duration Gene expression Response References
continuous irradiation
(4 W 24 h)
that of CHS, F3H, ANS and DFR
decreased
Content of rosmarinic acid
increase whereas anthocyanins
decreased
Alkaloids Taxus cuspidata
Sieb. Et Zucc
3Wm
-2
TASY, BAPT1, BAPT2, T5αH,
and ERF15 genes upregulated
10-deacetyl baccatin III,
baccatine III, 7-xylosyl-10
deacetyltaxol, 10-
desacetyltaxol, cephalomannine,
paclitaxel, and 7-epitaxol
enhanced significantly
Jiao et al.
(2022)
Mahonia bealei
fortune
104.4 kJ m
-2
d
-1
for 6 h,
followed by 54 h dark period
Enhanced expression of tbo Protoberberine alkaloids, such as
berberine, increased
Zhu et al.
(2021)
Catharanthus
roseus L.
1345 μWcm
-2
for 1–3h
followed by 72 h darkness
The mRNA expression levels of
dat, t16h, d4h, ORCA3, str, g10h
and 10-hgo were upregulated
The contents of strictosidine,
ajmalicine, vindoline and
catharanthine in leaves after 1 h
of UV-B irradiation and 72 h of
dark incubation increased
Zhu et al.
(2015)
Psychotria
brachyceras
Mull. Arg.
68.89 kJ m
-2
d
-1
TDC, ACO, UDP-glu, Ser/Thre
and lip
Brachycerine concentration
significantly increased.
Do
Nascimento
et al. (
2013)
Anisodus luridus
link ex Spreng.
9000 UW cm
-2
PMT, TRI, CYP80F1 and H6H
upregulated
More accumulation of
scopolamine and lower
accumulation of hyoscyamine
Qin et al.
(
2014)
Terpenes Mentha
piperita L.
7.1 kJ m
-2
d
-1
DXS, Ippi, Mds and GPPS were
upregulated
Essential oil content increased Dolzhenko
et al. (
2010)
Prunus
persica L.
150 μWcm
-2
Transcript level of PpTPS1
decreased while PpTPS2
transcript level increased
Linalool decreased
while (E,
E)-α-farnesene increased
Liu et al.
(
2017)
160 A. Pandey et al.
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