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141
Role of miRNA in Medicinal Plants Under
Stress Condition
9
Akhileshwar Kumar Srivastava, Ishita Chatterjee, Shreshtha Mishra,
Vaishnavi Tripathi, Wafia Zehra, Khushboo Chakrwal,
and Vibha Agrawal
Abstract
Several plant genes are activated under different stresses like drought, salt, cold,
heat, light, and oxidative stress. Recently, it has been delineated that plant
miRNAs play a vital function in stress condition. The first explanation for these
functions’ garners from bioinformatics assessment of miRNAs and their target
genes, and cloning of miRNAs from stress-treated plants like Arabidopsis
thaliana, which exhibited new miRNAs that had not been found in plants
grown in unstressed circumstances earlier. Knowing small RNA-guided stress
regulatory webs could give innovative ideas for the genetic upgradation in plant-
stress tolerance. Currently, researchers have elucidated that modification of
miRNA-guided gene regulation could aid in the engineering of stress-resistant
plants. In this chapter, the known and unknown functions of miRNAs in medici-
nal plants responses to environmental stresses will be deciphered.
Keywords
miRNA · Arabidopsis · Biogenesis · Stress condition
A. K. Srivastava
Department of Plant Cell Biotechnology, Central Food Technological Research Institute, Mysore,
India
I. Chatterjee · S. Mishra · V. Tripathi · W. Zehra · K. Chakrwal · V. Agrawal (
✉)
Department of Biotechnology, Shri Agrasen Kanya P. G. College, Varanasi, 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_9
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142 A. K. Srivastava et al.
9.1 Introduction
Plants being immobile organisms, constantly face adverse environmental conditions,
known as abiotic stresses, such as drought, soil salinity, severe temperatures, and
heavy metals. Abiotic stresses have become a crucial challenge because of their
ubiquitous nature and the deteriorating effects on plant growth, productions, and the
quality of secondary metabolites, including medicinal important compounds,
although plants have generated complex mechanisms for sensing and countering
to environmental alterations (Shriram et al.
2016a).
To switch on preventive events, plants stimulate a web of genetic regulations like
changed expression of genes by transcriptional and/or translational activities
(Ku et al.
2015). Plants induce for expression of the protective genes whereas
suppress the negative factors. At present, various protein-coding genes have been
explored for regulating the plant responses to abiotic stresses; but, information on the
regulatory events participated in such response are very limited and needs transfor-
mative mechanism to adapt plants to adverse environments (Zhang
2015). Such
posttranscriptional mechanisms are essential for plants to recover and re-establish
their cellular homeostasis and recovery from stress events, respectively (Sunkar et al.
2012).
Presently, it has been explained that plants entrust miRNAs as crucial post-
transcriptional gene-expression regulators to decrease plant growth and progress in
stress conditions. The miRNAs are a broad class of small (20–24 nt) endogenous
RNAs (Zhang 2015) and control the gene expression through regulating mRNA
breakage, translational suppressio n, chromatin remodeling, and/or DNA methyla-
tion. Generally, stress-induced miRNAs inhibit their target mRNAs, while, their
inhibition causes for cumulation and activity of positive regulators (Shriram et al.
2016a). Various reports have explored that abiotic stress stimulate abnormal
expressions of miRNAs in plants. High throughput sequencing and computational
methods have been employed to identify enormous number of stress-linked
miRNAs. Such outcomes suggest that miRNAs may act as crucial targets for genetic
modifications to engineer abiotic stress resistance in plants.
Plants have developed complex events for adapting to different environmental
stresses (Khraiwesh et al. 2012). Recently, it has been reported that plant miRNAs
involve in biotic and abiotic stress responses (Shukla et al.
2008; Ruiz-Ferrer and
Voinnet 2009). The first evidence for these functions came from bioinformatics
assessment of miRNAs and their target genes, and cloning of miRNAs from stress-
induced Arabidopsis thaliana plants that exhibited new miRNAs that were not
cloned earlier from plants grown in normal conditions (Jones-Rhoades and Bartel
2004; Sunkar and Zhu 2004). Exploring the small RNA-guided stress regulatory
webs might give innovative ideas for the genetic upgrade of plant-stress tolerance.
Several reports have also exhibited intricate and overlap in plant responses to distinct
stresses, and unraveling this complexity and overlay would possibly direct to new
methods to increase medicinal plants tolerance to adverse environmental conditions.
It has been explicated that manipulation of miRNA-guided gene regulation will aid
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to engineer of stress-resistant plants (Sunkar et al. 2006; Katiyar-Agarwal et al.
2007).
9 Role of miRNA in Medicinal Plants Under Stress Condition 143
Plant miRN As are cruci
al regulatory factor for the gene expression or silencing
by integrating to complementary sequences with target messenger RNA (mRNA)
resulting to translational suppre ssion or transcript degradation (Zhang et al.
2022).
The miRNAs govern complex regulatory networks and have been participated in
different diversity of biological events in eukaryotic cells that effect on plant growth
and response to environmental stresses (Šečić et al.
2021). The plants could enhance
tolerance to environmental factors abiotic stress by regulating the expression of
miRNAs or forming new miRNAs, to cope with abiotic stress. Upregulating or
downregulating the expression of miRNAs is highl y associated with distinct stresses,
specific miRNAs are also stimulated by various stresses in plants like elevated
temperature, chilling, drought, high salinity, oxidization, and heavy metals (Jian
et al.
2010).
Medicinal plant miRNAs are an endogenous group of small RNA important to the
posttranscriptional regulation of gene expression. Biosynthetic study has explained
that the mature miRNAs in medicinal plants are synthesized from either the standard
mRNA splicing event or the pre-ribosomal RNA splicing method. The role of
medicinal plant miRNA has been comprised into two phases: (i) the cross-kingdom
level that is controlling of disease-related genes in animal cells, and (ii) the intra-
kingdom level that is the involvement of metabolism, development, and stress
adaptation in plants. Escalating research continues augmenting the biosynthesis
and role of medicinal plant miRNAs (Sun et al. 2022). In this chapter, role of
miRNAs in regulating gene functions in plants will be discussed.
9.2 miRNA Biogenesis in Plants
The miRNA genes in plants are transcribed through RNA polymerase II to synthe-
size primary miRNA (Pri-miRNA) and their length largely varies between them-
selves (Ma et al.
2015; Chang et al. 2012
). Unlike animal, plant miRNA processing
is done inside the nucleus due to absence of protein processor such as Drosha and
DGCR8. In plant, DICER-LIKE 1 (DCL1) process maximum pri-miRNAs by
degradation. Pri-miRNAs become stable with a kind of RNA binding protein,
DAWDLE (DDL) that interacts with DCL1 in nuclear foci, called dicing bodies
(D-bodies). The synergistic role of some proteins such as SERRATE (SE) and
HYPONASTIC LEAVES 1 (HYL1), followed by DCL1 and the nuclear
cap-binding complex, resulted to develop a short duplex miRNA that is constituted
of mature miRNA guide cleavage and passenger miRNA strand (miRNA)
(Baranauske et al.
2015; Ha and Kim
2014). Next processing of this duplex caused
to the 20-Omethylation at 30 through the methyltransferase HEN1 (Baranauske et al.
2015). A family of enzymes, known as SMALL RNA DEGRADING NUCLEASE
(SDN) genes, is causing for the cumulation of miRNAs. SDN1 have revealed 30–50
exoribonuclease action for short and single-stranded RNA substrate s (Baranauske
et al. 2015; Myers et al. 2016). The HASTY (HST) is homolog to EXPORTIN5
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(EXP5), involves in major activity of transporting pre-miRNAs or mature miRNAs
to cytoplasm (Myers et al. 2016; Shriram et al. 2016b).
144 A. K. Srivastava et al.
In the cytoplasm, RNA-induce
d silencing complex (RISC) is produced by com-
plexation of ARGONAUTE (AGO) proteins with miRNA (Eckardt
2015; Arribas-
Hernández et al.
2016). AGO1 in the RISC is crucial factor for the miRNA event
(Ha and Kim 2014). AGO protein is made of PAZ and PIWI domain (Miyoshi et al.
2016). Mainly, PIWI domain produces RNaseH-like fold that involve in function of
endonuclease. Such endonuclease activity involves to cleave RNA targets, which are
complementary to the miRNA strand loaded AGO (Arribas-Hernández et al.
2016;
Miyoshi et al. 2016). AGO proteins in Arabidopsis thaliana like AGO1, AGO2, and
AGO10 has also endonuclease activity that results to splicing the mRNA targets
(Maunoury and Vaucheret 2011; Ji et al. 2011). The recruitments of the sliced
mRNA targets by miRNA can be explored by sequencing of mRNA degradome
(Mutum et al.
2016; Yang et al. 2013). Earlier, it has been reported that plant
miRNAs attach to their targets with greater complementary that leads to the cleaving
of target mRNA (Arribas-Hernández et al.
2016). Despite of cleavage, there are
various instances where the miRNA target is controlled at extent of protein without
alteration in mRNA level. Such outcomes indicate that plant miRNAs can interfere
the translation event of mRNA (Li et al.
2013; Beauclair et al. 2010).
9.3 Role of miRNAs in Plant under Stress Condition
In plants, the specific miRNA is upregulated or downregulated to produce new
miRNAs to combat with environmental stress. It has been proposed a model to
relate miRNA and transcription factors with their target genes under stress condition
(Fig.
9.1) (Samad et al. 2017). Enormous stress-regulated miRNAs have been
explored in model plants under different biotic and abiotic stress conditions, e.g.,
nutrient deficiency (Fujii et al. 2005), drought (Zhou et al. 2010), cold (Zhou et al.
2008), salinity (Sunkar et al. 2008), bacterial infection (Navarro et al. 1979), UV-B
radiation (Zhou et al. 2007), and mechanical stress (Lu et al. 2005). However, stress
regulation might indicate a major role of the regulated miRNA in stress responses, it
is cleared that a miRNA is distinctly regulated under environmental stress does not
essentially indicate that the miRNA plays vital role to adapt with stress responses.
It has been reported that the extents of 117 miRNAs under salinity, drought, and
low-temperature conditions had been assessed employing miRNA chips for all
known miRNAs explored in Arabidopsis (Liu et al.
2008). Seventeen stress-
inducible miRNAs had been identified and outcomes were validated by determining
their expression patterns and assessing the cis-regulatory elements in their promoter
sequences (Liu et al. 2008). It had been explored novel Arabidopsis miRNAs for the
target genes like superoxide dismutases, laccases, and ATP sulfurylases (APS)
(Jones-Rhoades and Bartel
2004). The expression of one specific miRNA
(miR395) was enhanced after sulphate deficient, revealing that miRNAs could be
stimulated by environmental components rather developmental processes. The
miR395 targets the genes, which encode ATP sulfurylases APS1, APS3, and
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APS4, catalyzing the first phase of inorganic sulfate assimilation (Jones-Rhoades
and Bartel 2004; Lu et al. 2005). It was developed a library of small RNAs from
Arabidopsis seedlings against several abiotic stresses such as cold, dehydration, high
salt, and abscisic acid (ABA), and explored various new miRNAs in abiotic stress
response (Lu et al.
2005
). For instance, miR393 had been over-expressed by cold,
dehydration, salinity, and ABA treatments; miR397b and miR402 were upregulated
to some degree by common stress treatments whereas miR319c was triggered by
cold only; although miR389a was downregulated by most of the stress treat ments.
The outcome suggested that stress-stimulated miRNAs target negative regulators of
stress responses or positive regulators of events, which are impeded by stresses and
that new
ly explored miRNAs, reveal tissue- or developmental stage-specific expres-
sion patterns. In a study, genome-wide profiling and assessment of miRNAs was
accomplished in drought-challenged rice (Zhou et al.
2010). It had been explored
48 miRNA sequences from the Populus genome and observed that several such
Populus miRNAs target developmental and stress/defense-related genes (Lu et al.
2005). It has been also reported that plant miRNAs might be stimulated by mechani-
cal stress and may act in crucial defense systems for structural and mechanical fitness
(Lu et al. 2005).
9 Role of miRNA in Medicinal Plants Under Stress Condition 145
Fig. 9.1 Model for miRNAs interactions with transcription factors in plant under stress condition
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146 A. K. Srivastava et al.
9.4 Abiotic Stress
9.4.1 Role of miRNAs in ABA-Mediated Stress
The phytohormone ABA plays pivotal role in plant responses to environmental
stresses. The first sign that miRNAs might be participated in ABA-mediated
responses appeared from ABA hypersensitivity in an Arabidopsis mutant having a
“pleiotropic recessive Arabidopsis transposon insertion mutation,” hyl1 (Lu and
Fedoroff
2000). Two research groups separately observed that either ABA or
gibberellin (GA) treatment controlled miR159 expression (Achard et al. 2004) and
floral organ development (Achard et al. 2004). In germinating Arabidopsis seeds,
miR159 had been expressed in ABA-treated seedlings (Reyes and Chua
2007). It
had been elucidated that the expression of miR393, miR397b and miR402 had been
induced by ABA treatment whereas miR389a was suppressed by ABA (Sunkar et al.
2008). Moreover, Arabidopsis have also explained upregulation of miR160 (Liu
et al. 2007) and miR417 (Jung and Kang 2007) and downregulation of miR169
(Li et al. 2008) and miR398 after treatment of ABA. In rice, miR319 was
overexpressed while miR167 and miR169 were suppressed under ABA-mediated
responses (Liu et al.
2009). In Phaseolus vulgaris, miR159.2, miR393, and miR2118
had been stimulated under ABA treatments while miRS1, miR1514, and miR2119
were slightly expressed in response to ABA (Arenas-Huertero et al. 2009). The
subordination of DNA methylation on miRNA levels was also revealed for an
ABA-responsive PpbHLH-miR1026 regulon in Physcomitrella patens. ABA treat-
ment resulted an enhance of miR1026 and a decline of its PpbHLH target RNA
(Khraiwesh et al.
2010).
9.4.2 miRNAs Activity under Drought and Salt Stress
In a study, it has been reported that Arabidopsis have exhibi ted extensive function
for miRNAs in drought and salt stresses. Various stress-associated miRNAs had
been explored because of sequencing of a library of small RNAs derived from
Arabidopsis seedlings faced to different stresses (Lu et al. 2005). In a study,
miRNAs like miR168, miR171, and miR396 had been observed to be perceptive
to high salinity, drought, and cold stress in Arabidopsis, hence encouraging the
hypothesis of a function for miRNAs to adapt under abiotic stress (Liu et al. 2008).
The miRNA-expression profiling in response of drought stress has been accom-
plished in Arabidopsis, rice, and Populus trichocarpa. In Arabidopsis , miR396,
miR168, miR167, miR165, miR319, miR159, miR394, miR156, miR39 3, miR171,
miR158, and miR169 were exhibited to be drought responsive (Liu et al. 2008). The
overexpression of miR39 3, miR319, and miR397 due to dehydration in Arabidopsis
has been observed (Lu et al. 2005). In rice, miR169g was highly expressed by
drought whereas miR393 was moderately stimulated by drought (Zhao et al. 2007).
Genome-wide profiling and assessment of miRNAs had been performed in drought-
challenged rice over a broad area of developmental stages, from tillering to
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inflorescence production, employing a microarray technique (Zhou et al. 2010). The
outcomes suggested that 16 miRNAs (miR156, miR159, miR168, miR170, miR171,
miR172, miR319, miR396, miR397, miR408, miR529, miR896, miR1030,
miR1035, miR10 50, miR1088, and miR1126) had been highly downregulated in
drought condition. In contrast, 14 miRNAs (miR159, miR169, miR171, miR319,
miR395, miR474, miR845, miR851, miR854, miR896, miR901, miR903, miR1026,
and miR1125) were highly upregulated under drought conditions. Some miRNA
gene families like m
iR171, miR319, and miR896, had been explored in both down-
and upregulated groups, and nine miRNAs (miR156, miR168, miR170, miR171,
miR172, miR319, miR396, miR397, and miR408) exhibited reverse expression to
that detected in drought-stressed Arabidopsis (Zhou et al.
2010). In Populus,
miR171l-n, miR1445, miR1446a-e, and miR1447 were observed to be drought-
responsive (Lu et al. 2005). In Phaseolus vulgaris, miRS1, miR1514a, and miR2119
exhibited a transient but apparen tly rise in accumulation after drought treatment
whereas the accumulation was higher for miR159.2, miR393, and miR2118 after
same treatment (Arenas-Huertero et al.
2009). In Medicago truncatula, miR169 was
suppressed only in the roots, and miR398a, b and miR408 were highly
overexpressed in both shoots and roots in response to drought condition (Trindade
et al.
2010). The miRNA expression patterns of drought-resistant wild emmer wheat
(Triticum turgidum ssp. Dicoccoides) in drought condition had been examined by
employing a plant miRNA microarray technique (Kantar et al. 2011). Expression
levels had been determined for 205 miRNAs in control and 438 miRNAs in drought-
stressed leaf and root tissues. The 13 miRNAs were observed to be distinctively
regulated under drought stress: miR1867, miR896, miR398, miR528, miR474,
miR1450, miR396, miR1881, miR894, miR156, miR1432, miR166, and miR171
(Kantar et al.
2011). Likewise, miR474 that targets proline dehydrogenase (PDH),
was upregulated in maize while drought condition (Wei et al. 2009).
9 Role of miRNA in Medicinal Plants Under Stress Condition 147
About 6%
of the total land is impacted by higher salinity (Chen et al.
2021).
Several genes and mechanism s in plants are impacted by salt stress. Various
distinctively regulated miRNAs were explored in plants under salt stress. In
Arabidopsis, miR156, miR158, miR159, miR165, miR167, miR168, miR169,
miR171, miR319, miR393, miR394, miR396, and miR397 were highly
overexpressed under salt stress, whereas the level of miR398 was reduced (Liu
et al. 2008). In Phaseolus vulgaris, the miRS1 and miR159.2 were enhanced after
addition of NaCl (Arenas-Huertero et al.
2009). In Populus trichocarpa, the expres-
sion of miR530a, miR1445, miR1446a-e, miR1447, and miR171l-n were decreased,
while miR482.2 and miR1450 were overexpressed while salt stress (Lu et al.
2005).
Further, miR169g and other miR169 family, miR169n had been observed to be
stimulated due to high salinity (Zhou et al. 2009). It has been observed that a
cis-acting ABA-responsive element (ABRE) in the upstream site of miR169n
might be ABA-regulated. Both miR169g and miR169n targeted nuclear factor Y
subunit A (NF-YA), a component that was earlier revealed to be downregulated in
wheat leaves under drought conditions (Stephenson et al.
2007). The microarray
experiments had explored the miRNA profile in a salt-tolerant and a salt-sens itive
line of maize (Zea mays) (Ding et al.
2009); the outcomes suggested that members of
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the miR156, miR164, miR167, and miR396 families had been suppressed whereas
miR162, miR168, miR395, and miR474 families were overexpressed in salt-stressed
maize roots.
148 A. K. Srivastava et al.
9.4.3 Action of miRNAs in Cold and Heat Stress
The upregulation of miRNAs in cold stress has been investigated in Arabidopsis (Liu
et al. 2008), Populus (Lu et al. 2005), and Brachypodium (Zhang et al. 2009). The
miR397 and miR169 had been overexpressed in all three species, and miR172 was
expressed in Arabidopsis and Brachypodium. Despite of such miRNAs, various
miRNAs (miR165/166, miR393, miR396, and miR408) had been stimulated under
cold stress in Arabidopsis, whereas other miRNAs (miR156/157, miR159/319,
miR164, miR394, and miR398) exhibited either transient or moderate regulation
in cold stress (Liu et al. 2008). In Populus, miR168a, b and miR477a, b had been
overexpressed whereas miR156g-j, miR475a, b, and miR476a were suppressed in
cold stress (Lu et al.
2005). Wheat miRNAs exhibited distinctively expression under
heat stress; by employing Solexa high-throughput sequencing, cloned the small
RNAs from wheat leaves after treatment of heat stress (Xin et al.
2010). Of the
32 miRNA families identified in wheat, nine conserved miRNAs were highly
responsive to heat stress. For instance, miR172 was highly reduced, and miRNAs
such as miR156, miR159, miR160, miR166, miR168, miR169, miR393 and
miR827 were highly expressed under heat stress.
9.4.4 miRNAs in Response to UV-B Radiation
A computational method had been employed to explore Arabidopsis miRNAs
triggered by UV-B radiation (Zhou et al. 2007). The 21 miRNAs belonging to
11 miRNA families had been explored in that study, the remaining had been
envisaged to be upregulated in UV-B stress: miR156/157, miR159/319, miR160,
miR165/166, miR167, miR169, miR170/171, miR172, miR393, miR398, and
miR401 (Zhou et al. 2007). Some of the same miRNA families, which had been
determined to be induced by UV-B radiation in Arabidopsis (miR156, miR160,
miR165/166, miR167, miR398, and miR168) were observed to be upregulated by
UV-B radiation in Populus tremula (Jia et al. 2009). Intriguingly, three families
(miR159, miR169, and miR393), which had been detected to be upregulated in
Arabidopsis were downregulated in Populus tremula, indicated that certain
responses to UV-B radiation stress might be species specific (Jia et al. 2009).
Here, it is cleared that the status of miRNA families in different plants are
associated with environmental factors. Hence, miRNAs of medicinal plants are
also impacted by adverse condition. Above explanation suggested that some
miRNAs are also conserved in wide range of plants diversity, which might respond
to different stress conditions to regulate the metabolic pathways for synthesis of
medicinal compounds. However, some of important miRNAs are downregulated
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under environmental stress, whi ch may impact directly or indirectly in biogenesis of
medicinal plants.
9 Role of miRNA in Medicinal Plants Under Stress Condition 149
9.5 Biotic Stress
In mam mals, various instances of miRNA-mediated suppression or increasing of
viral infection have been explained (Lecellier et al. 1979). In plants, Arabidopsis
miR393 was the first miRNA identified to involve in plant antibacterial PTI (pattern
triggered immunity) through governing the auxin signaling pathway. The miR393
had been stimulated by a bacterial PAMP (pattern associated molecular pattern)
peptide flg22 post-treatment (Navarro et al. 1979). Employing small
RNA-expression profiling on Arabidopsis leaves had taken at 1 and 3 h post-
inoculation (hpi) with Pst DC3000 hrcC. It had been explored three miRNAs
(miR160, miR167, andmiR393), which were greatly stimulated and miR825 was
suppressed after infection (Fahlgren et al.
2007). The function of miRNAs in plant
basal defense had been again supported by the finding that Arabidopsis miRNA-
deficient mutants dcl1 and hen1 exhibited the increased growth of the bacterium Pst
DC3000 hrcC and various bacteria strains, which are non-pathogenic to Arabidopsis
such as Pseudomonas syringae pv. phaseolicola, P. fluorescens, and E. coli
(Thiébeauld et al.
2021). It had been revealed that the stimulation of flg22-
responsive pri-miR393 and pri-miR396 in Arabidopsis was inhibited by the virulent
strain Pst DC3000 but not by the TTSS mutant strain Pst DC3000 hrcC (Thiébeauld
et al.
2021). The miR398 in Arabidopsis was suppressed by infection of with Pst
(avrRpm1) and Pst (avrRpt2) but was not affected by Pst DC3000 attack
(Jagadeeswaran et al.
2009). Also in Arabidopsis, miR156 and miR164 had been
triggered by infection of virus TYMV p69 and were stimulated in transgenic
Arabidopsis plants expressing the viral silencing suppressor P1/HC-Pro (Kasschau
et al.
2003). In tobacco, miR156, miR160, and miR164 had been triggered by virus
infection (Thiébeauld et al.
2021). After virus infection, new miRNAs (miR158 and
miR1885) had been explored in Brassica; miR158 and miR1885 were particularly
stimulated by turnip mosaic virus but not by cucumber mosaic virus or tobacco
mosaic virus (He et al.
2008
). The medicinal plants strive to fight against pathogenic
organisms such as viruses, bacteria, and so forth. The several miRNAs in plants are
impacted with pathogenic in filtration, which may alter the biogenesis in medicinal
plants. Due to biotic stress, some new miRNAs are formed that involve in protection
of plants from pathogenic organisms. Thus, miRNAs might play vital role to
maintain sustainability in medicinal under biotic stress. However, the more study
is required to explore the role of miRNAs against biotic stress.
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