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Plant Cell Reports
https://doi.org/10.1007/s00299-021-02736-y
REVIEW
miRNAs play critical roles inresponse toabiotic stress bymodulating
cross‑talk ofphytohormone signaling
PujaSingh1,2· PrasannaDutta1,2· DebasisChakrabarty1,2
Received: 5 April 2021 / Accepted: 10 June 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract
One of the most interesting signaling molecules that regulates a wide array of adaptive stress responses in plants are the
micro RNAs (miRNAs) that are a unique class of non-coding RNAs constituting novel mechanisms of post-transcriptional
gene regulation. Recent studies revealed the role of miRNAs in several biotic and abiotic stresses by regulating various
phytohormone signaling pathways as well as by targeting a number of transcription factors (TFs) and defense related genes.
Phytohormones are signal molecules modulating the plant growth and developmental processes by regulating gene expres-
sion. Studies concerning miRNAs in abiotic stress response also show their vital roles in abiotic stress signaling. Current
research indicates that miRNAs may act as possible candidates to create abiotic stress tolerant crop plants by genetic engi-
neering. Yet, the detailed mechanism governing the dynamic expression networks of miRNAs in response to stress tolerance
remains unclear. In this review, we provide recent updates on miRNA-mediated regulation of phytohormones combating
various stress and its role in adaptive stress response in crop plants.
Keywords Abiotic stress· Transcription regulation· Heavy metals· miRNA· Phytohormones
Introduction
The harsh outer world provides enormous amount of strain
for the sessile plants to live, yet most of them survive dur-
ing these adverse environmental conditions by developing
various mechanisms to overcome such stresses. The mode
of gene regulation to combat the unavoidable abiotic stress
mainly involves the up-regulation or down-regulation of
targeted genes (Fig.1). The suppression of gene expression
happens mainly due to the presence of innumerable tiny sol-
diers residing within the plant system, which protects them
from the extreme conditions. One of these defence system
comprises of the members of the ‘small RNA world’, the
micro-RNAs (miRNAs), discovered in the early 1990s which
are highly conserved group of non-coding RNA molecules
usually 20–24 nucleotides long, functioning via inhibiting
translation or cleaving transcripts of targeted genes (Lee
etal. 1993; Wightman etal. 1993). The mature miRNAs
are produced from primary miRNAs (pri-miRNAs) tran-
scribed from target DNA sequences via RNA polymerase II
that mostly down-regulates the mRNAs by binding to its 3’
UTR region or sometimes to the 5’ UTR region, promoter
and coding sequence. Dicer-Like1 (DCL1) recognises the
stem loop structured single-stranded RNAs and cuts the pri-
miRNAs forming precursor microRNAs (pre-miRNAs) and
subsequently converting it to the miRNAs. These miRNAs
are then loaded into the argonaute associated micro-RNA
induced silencing complexes (miRISCs) for future process-
ing. The miRNAs tend to be present in the nucleus, nucleo-
lus, mitochondria and endoplasmic reticulum membrane and
control the post-transcriptional gene silencing mechanism
by commuting through those different sub-cellular compo-
nents (Makarova etal. 2016). The miRNAs are involved
for providing abiotic stress tolerance, maintaining nutrient
homeostasis and transcriptional regulation of gene expres-
sion in plants. Due to a complicated network of action, very
few miRNAs have been characterized for their role in abiotic
Communicated by Neal Stewart.
Puja Singh and Prasanna Dutta contributed equally to this work.
* Debasis Chakrabarty
chakrabartyd@nbri.res.in
1 Molecular Biology andBiotechnology Division, CSIR-
National Botanical Research Institute, Lucknow, India
2 Academy ofScientific andInnovative Research (AcSIR),
Ghaziabad201002, India
Plant Cell Reports
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stress but this field is dynamically expanding nowadays with
more miRNAs being characterized.
Since, one of the major challenges for our world today is
“food security” and abiotic stress apparently adds to it by
reducing growth and productivity of plant. Thus, a detailed
study of the mode of action of miRNAs would be highly ben-
eficial in developing strategies for mitigation of a wide array
of abiotic stresses in plants. Various physical and chemical
factors such as high soil salinity, drought, flooding, extreme
temperatures, ultraviolet (UV) radiation, heavymetal (HM)
toxicityand nutrient scarcity collectively comprising the
abiotic stress affect plants worldwide (Wang etal. 2003;
Wani etal. 2016). In response to the abiotic stress, several
signaling pathways involving various phtohormones are
alsoactivated. Although miRNAs and phytohormones have
different metabolic and transduction pathways, recent studies
suggest interplay in miRNAs pathways and phytohormone
responses during a number of abiotic stresses. This interac-
tion results in overcoming various abiotic stresses either via
modulating miRNAs using phytohormones or by control-
ling phytohormonal level using miRNAs as intermediate.
So, the phytohormonal homeostasis and miRNA regulation
walk parallel during abiotic stress responses, suggesting an
interconnected network operating in regulating the genes
responsible for abiotic stress tolerance (Noman and Aqeel
2017). This review deals with the functional regulation of
phytohormones by miRNAs in response to various abiotic
stresses encountered by plants.
Linking miRNAs andphtohormones
inabiotic stress response
In nature, plants are generally exposed to multiple stresses
at the same time which triggers different responses depend-
ing on the type and intensity of stress. The responses can be
stress specific or it can also be a converged response as in
case of drought and freezing stress which results in dehydra-
tion in plants. Once a stress is perceived it is passed on to
regulators through secondary messengers which results in
production of protective effectors such as reactive oxygen
species (ROS), late embryogenesis abundant (LEA) proteins,
protease inhibitors, chaperones and phytohormones (Patel
etal. 2019). Phytohormones are vital signaling molecules
required for mostly all biological activities of the plants
such as plant physiology, architecture, and stress adaptation
(Peleg and Blumwald 2011). Till now, auxin (AUX), ethyl-
ene (ET), gibberellic acid (GA), cytokinin (CK), abscisic
acid (ABA), brassinosteroids (BR), jasmonic acid (JA), sali-
cylic acid (SA) and strigolactones have been identified as the
characteristic plant hormones, which control transcription
factor (TF)-mediated hormonal response. Amongst these
phytohormones, ABA and ET are most important in gov-
erning abiotic stress tolerance in plants.
During abiotic stress, a number of miRNAs are also
up-regulated or down-regulated, suggesting their involve-
ment in regulating stress by targeting various genes or TFs
(Sunkar and Zhu 2004; Wani etal. 2016). The up-regulation
or down-regulation of miRNAs varies in different plant spe-
cies during different stresses; therefore, targeting the same
Fig. 1 Overview of abiotic
stress-mediated gene regulation
in plants. This figure depicts
miRNA-mediated regulation of
gene expression during various
abiotic stresses. This positive
or negative regulation results
in providing stress tolerance
to plants by involving MAPK,
calcium signaling and phyto-
hormones
Drought Salt Heat FloodingFreezing Heavy
Metals
Stress Response by Down-regulation
of genes
Stress Response by Up-regulation
of genes
Regulation of gene expression
ABIOTIC STRESS
Calcium
Signaling
MAPK
Signaling
Hormone
Signaling
miRNA mediated
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miRNAs for improving stress tolerance in different plant
species will have different outputs (Djami-Tchatchou etal.
2017). Hormone and abiotic stress response elements such
as heat shock-responsive element (CCA AAT ), MYB bind-
ing elements, MYC binding elements, early response to
dehydration (ERD), copper-responsive elements (CuREs),
ethylene-responsive elements (ERE) and gibberellic acid-
responsive elements (GARE) are reported in the promoter
region of miRNAs which controls the expression of effector
genes (Zhou etal. 2013). In a recent study, freezing stress
as well as exogenous application of gibberellic acid (GA),
salicylic acid (SA) and methyl jasmonate (MeJA) modulated
the activity of miR475b, its promoter and its targetsin Popu-
lus suaveolens suggesting a cross talk with phytohormones
during abiotic stress (Niu etal. 2016).
The highly conserved miRNAs also controls several
developmental processes which is generally a characteristic
of phytohormones. The existence of functional connection
between miRNAs and phytohormones has been established
in a plant carrying hyl1 mutation which exhibited multiple
developmental defects, reduced accumulation of miRNAs
and sensitivity to phytohormones- AUX, CK and ABA
(Han etal. 2004). A number of miRNAs are also reported
to induce the production of trans-acting small interfering
RNAs (tasiRNAs), which acts as a mobile signaling mol-
ecule (Marin etal. 2010; Si-Ammour etal. 2011). The abil-
ity of miRNAs in trans-regulation and controlling various
developmental processes makes it a prominent applicant for
coordinating various phytohormonal signaling responses
during abiotic stress.
miRNA‑Phytohormone response todrought
stress
Drought is the condition where plant faces water deficiency
either due to reduced precipitation or less soil moisture con-
tent resulting in constant loss of water via evapo-transpira-
tion, stomatal opening, turgor pressure change and accu-
mulation of toxic chemicals inside cellular compartments.
Plants regulate this condition by monitoring the stomatal
activity, which involves presence of the key phytohormone
ABA. ABA acts by binding to its receptors andopening the
ion channels therebycausing decrease in turgor pressure
leading to stomatal closure, thus helping leaves to conserve
water inside. Aquaporins are also important factors main-
taining the transport of water and other solutes which are
regulated by the phytohormones ABA and GA. Drought
stress is a complicated combination of many other abiotic
stresses such as salinity, heat and freezing stress affecting
the overall growth and development of plant. Rapidly chang-
ing climate dynamics makes drought a serious threat to the
sustainability of food production systems throughout the
world (Kogan etal. 2020).
Small RNA sequencing studies identified the presence
of many drought-responsive miRNAs in Arabidopsis,
tomato, maize, common bean, barley and rice (Liu etal.
2008, 2017; Aravind etal. 2017; Wu etal. 2017; Ferdous
etal. 2017; Zhou etal. 2010). In response to drought
stress the relative expression of miR156, miR158,
miR159, miR165, miR167, miR168, miR169, miR171,
miR319, miR393, miR394 and miR396 was altered (Liu
etal. 2008). In Arabidopsis thaliana, the auxin signaling-
mediated miR390-TAS3-ARF2/ARF3/ARF4 pathway is
controlled by miR390 targeting the production of TAS3-
derived trans-acting small interfering RNA (tasi RNA)
which is responsible for regulating lateral root develop-
ment and polarity organisation via targeting the ARF2,
ARF3 and ARF4 transcription factors (Meng etal. 2010).
Drought stress also induces the expression of miR160
and lateral root development via miR390-mediated
changes in auxin levels (Bustos-Sanmamed etal. 2013;
Yoon etal. 2010). The adventitious and lateral root
development is increased by inducing ARF, GAMYB
and HD-ZIP transcription factors via down-regulation
of miR159 (Xue etal. 2017). Resistance towards drought
stress was observed in Arabidopsis over-expressing
ABA-responsive miR168, miR393 and miR394, confer-
ring the role of miRNA in ABA-mediated abiotic stress
adaptation (Baek etal. 2016) (Table1). Mutant studies of
the key genes involved in miRNA synthesis like DCL1,
HEN1, HYL1, HASTY and SE in Arabidopsis showed that
the hyl1, dcl1 and hen1 mutants were hypersensitive to
ABA, whereas se and hasty mutants were sensitive to
ABA, thus providing the link between miRNA and ABA
response (Lu and Fedoroff 2000; Cambiagno etal. 2021;
Zhang etal. 2008). In germinating seedlings of Arabi-
dopsis, ABA and water deficiency induces the formation
of miR159a which cleaves the transcripts for MTB33 and
MYB101. Thus, the modified cleavage-resistant MYB33
and MYB101 forms showed ABA hypersensitivity in
miR159a over-expressing lines compared to the cleav-
age-susceptible lines which were hyposensitive (Reyes
etal. Reyes and Chua 2007). Several reports suggest that
ABA induces the synthesis of miR393, miR397b and
miR402, while suppressing the expression of miR389a
in Arabidopsis (Sunkar and Zhu 2004; Reyes and Chua
2007; Liu etal. 2007; Jung and Kang 2007; Li et al.
2008; Jia etal. 2009). The miR399f over-expressing lines
in A. thaliana showed higher drought sensitivity due to
reduced ABA sensitivity (Baek etal. 2016). Also, the
ABA response is suppressed due to degradation of the
ABA INSENSITIVE 4 (ABI4) transcription factor and
the enzyme β-1,3- GLUCANASE1 (BG1) responsible
for ABA production by miR165 and miR166 (Yan etal.
Plant Cell Reports
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Table 1 List of miRNAs targeting various phytohormones and TFs during abiotic stress in plants
Abiotic stress/tolerance
type
miRNA Targeted genes Plant species and their
families
Functional response to
stress
References
Drought stress miR393 TIR1/AFB2 Arabidopsis thaliana
(Brassicaceae)
Up-regulation Sunkar and Zhu (2004);
Chen etal. (2012); Liu
etal. (2008)
miR397 Laccase Up-regulation
miR167 ARF Up-regulation
miR168 AGO Up-regulation
miR156 SPL Solanum lycopersicum
(Solanaceae)
Up-regulation Visentin etal. (2020)
miR393 OsTIR1,OsAFB2 Oryza sativa (Poaceae) Up-regulation Bian etal. (2012)
miR167 ARF Down-regulation
Salinity stress miR172c and miR166g-
3p
AP2-like ethylene
responsive factor SNZ
and SAM-dependent
methyltransferase gene
Raphanus sativus (Bras-
sicaceae)
Down-regulation Sun etal. (2015a, b)
miR160 ARFs Gossypium sp. (Malva-
ceae)
Up-regulation Yin etal. (2017)
miR167 ARF 6 Up-regulation
miR169g & NF-YA TF Oryza sativa (Poaceae) Up-regulation Zhao etal. (2009)
miR169n
miR1848 OsCYP51G3 Up-regulation
Cold stress miR169 NFY/MtHAP 2–1 Arabidopsis thaliana
(Brassicaceae)
Up-regulation Sunkar and Zhu (2004);
Liu etal. (2008)
miR172 AP2 Up-regulation
miR397 Laccase Up-regulation
miR812q CIPK10 Oryza sativa (Poaceae) Up-regulation Jeong and Green. (2013)
UV-B radiation miR160 ARF Arabidopsis thaliana
(Brassicaceae)
Up-regulation Zhou etal. (2007)
miR165/166 HD-ZIPIII Up-regulation
miR167 ARF Up-regulation
miR393 T1R1 Up-regulation
miR159 MYB Triticum aestivum
(Poaceae)
Up-regulation Wang etal. (2013)
Plant Cell Reports
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Table 1 (continued)
Abiotic stress/tolerance
type
miRNA Targeted genes Plant species and their
families
Functional response to
stress
References
Hypoxia miR159 GAMYB Zea mays (Poaceae) Down-regulation Liu etal. (2012)
miR166 HD-ZIPII Up-regulation
miR167 ARF Up-regulation
miR171 SCL Arabidopsis thaliana
(Brassicaceae)
Up-regulation Moldovan etal. (2010)
miR159a MYB Up-regulation
Heavy metal stress Cu stress miR408 Cu ion binding protein,
laccase, Plantacyanin
Arabidopsis thaliana
(Brassicaceae)
Up-regulation Song etal. (2018)
Cd stress miR1535b Glyma07g38620.1 Glycine max (Fabaceae) Up-regulation Fang etal. (2013)
miR393 E3 ubiquitin ligase or
TIR1 Brassica napus (Bras-
sicaceae)
Up-regulation Huang etal. (2010)
Al stress miR160 ARFs Oryza sativa (Poaceae) Down-regulation Lima etal. (2011); Zhou
etal. (2007)
miR166 HD-ZIP III
miR393 bHLH, transport inhibitor
response 1/auxin F-box
Up-regulation Lima etal. (2011)
miR528 F-box domain and LRR
containing protein,
F-box/LRR-repeat
MAX2, L-ascorbate
oxidase, OsDCL1, Cu
binding proteins (CBP)
Up-regulation
miR390 tasi-RNA-generating
locus
Glycine soja (Fabaceae) Down-regulation Zeng etal. (2012)
As stress miR319 TCP Brassica juncea (Bras-
sicaceae)
Up-regulation Srivastava etal. (2012)
miR167 ARFs Down-regulation
Cr stress miR156/157 SPL3, SPL6, SPL9,
SPL13 and SPL15 Raphanus sativus (Bras-
sicaceae)
Down-regulation Liu etal. (2015)
miR397 LAC17 Down-regulation
miR5293 Transcription factor
TCP15
Down-regulation
HSP90-like protein
GRP94 (SHD),
cytochrome P450 90A1
(CPD)
Transcription factor
TCP21,
Plant Cell Reports
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2016). Hence, the mutant lines of miR165 and miR166
show both drought and ABA hypersensitivity.
Recent study in tomato showed that strigolactones act as
a molecular bridge between drought and miR156 and this
miR156 acts as a mediator of ABA‐dependent activity of
strigolactones on drought-affected stomata (Visentin etal.
2020) (Table1). Amongst 30 miRNAs in rice, 16 were
down-regulated and 14 were up-regulated in response to
water scarcity (Zhou etal. 2010). Over-expressing miR393
in rice resulted in early maturity and increased tiller num-
ber along with drought and salinity tolerance by regulating
the auxin receptors OsTIR1 and OsAFB2, thereby indicat-
ing the role of auxin in stress response (Bian etal. 2012)
(Fig.2). During drought stress in Arabidopsis miR167 is
up-regulated while in rice and maize miR167 is down-
regulated upon ABA treatment (Liu etal. 2008; Zou etal.
2009) (Fig.2). Drought stress in maize resulted in sup-
pression of miR167 expression but higher transcript abun-
dance of phospholipase D (PLD), suggesting that PLD is
responsible for ABA-mediated stomatal movement and that
it act as the target of miR167 (Wei etal. 2009; Zhang etal.
2005) (Table1).
miRNA‑Phytohormone response tosalinity
stress
Salinity refers to the increased salt concentration in the
soil resulting in alteration of the osmotic potential gradi-
ent thereby hindering the normal physiology of the plants.
Elevated salt concentration reduces the soil water potential
making the process of water absorption harder for the roots
and increasing efflux of intra-cellular water causing plas-
molysis and subsequently cell death. In the past few dec-
ades a large number of salinity stress-induced miRNAs have
been reported from various species such as Zea mays, Oryza
sativa, Gossypium sp, Raphuanus sativus, Populus sp. and
Salicornia europaea (Fu etal. 2017; Macovei and Tuteja
2012; Mondal etal. 2018; Yin etal. 2017; Sun etal. 2015a,
b; Li etal. 2008; Chen etal. 2017; Feng etal. 2015).
In Raphanus sativus, the AP2-like ethylene-respon-
sive factor, SNZ and SAM-dependent methyltransferase
gene were induced by the suppression of miR172c and
miR166g-3p, under high salinity condition (Sun etal.
2015a, b) (Table1). Under high salinity stress in cotton,
expression of auxin-responsive factors ARF10, ARF 16
and ARF 17 mediated by miR160 and miR167 resulted
in enhanced salinity tolerance (Yin etal. 2017) (Table1;
Fig. 2). The osa-miR319a over-expressing Agrostis
stolonifera showed higher tolerance to drought and salin-
ity stress by regulating the TCP transcription factors (Zhou
etal. 2013). The miR169g and miR169n, regulating the
transcription factor Nuclear factor Y subunit A (NF-YA),
Table 1 (continued)
Abiotic stress/tolerance
type
miRNA Targeted genes Plant species and their
families
Functional response to
stress
References
Putative galacturono-
syltransferase-like 7
(GATL7)
Mitogen-activated protein
kinase kinase kinase 1
(MEKK1)
Transcription factor
TCP6, Ethylene-
responsive TF
rsa-miRn39 HSP81-2 Up-regulation
miR159 MYB101, SPL, MYB104 Oryza sativa (Poaceae) Down-regulation Dubey etal. (2020)
miR160 ARF16, ALMT9 Down-regulation
Plant Cell Reports
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were down-regulated in Triticum aestivum during drought
stress but were up-regulated in Populus trichocarpa dur-
ing salt stress (Zhao etal. 2009). This miR169n may be
regulated by the phytohormone ABA as it has a cis-acting
ABA-responsive element (ABRE) in the upstream. High
salinity induces the expression of miR169g and miR169n
in rice, which cleaves the transcription factor NF-YA by
binding to the CCAAT box region of the gene (Table1).
In rice, the miR1848 suppresses the cytochrome P enzyme
gene (OsCYP51G3) mediating BR biosynthesis, so over-
expressing miR1848 under salinity stress causes BR defi-
ciency (Xia etal. 2015) (Fig.2).
miRNA‑phytohormone response tocold
stress
The two extreme temperature conditions, elevated heat and
freezing condition, severely affect plant growth and devel-
opment and are of particularly greater concern nowadays
due to the prevailing global warming problem. Numerous
miRNAs are reported to be expressed during cold stress in
plants (Cao etal. 2014).
In Arabidopsis, cold stress induces expression of
miR165/166, miR393, miR396 and miR408, whereas
miR156/157, miR159/319, miR164, miR394 and miR398
are transiently or mildly expressed. During cold stress in
Arabidopsis, CBF (C-repeat binding F factors) transcription
factors bind to the dehydration-responsive element (DRE)
resulting in up-regulation of cold-responsive proteins. Vari-
ous miRNAs control ABA signaling which thereby provides
tolerance to cold stress in many plants. Further studies also
suggested that cold-tolerant varieties show higher ABA
levels during cold stress as compared to the cold-sensitive
varieties (Kumar 2014). Cold stress resulted in up-regulation
of miR169, miR172 and miR397 in Arabidopsis (Table1).
Cold stress in rice resulted in expression of 18 cold-respon-
sive miRNAs most of which are generally down-regulated
at 4°C (Lv et al. 2010). Contrary to this, expression of
miR812qis up-regulated during the initial reproductive
phase in rice upon cold stress treatment (Table1). This
miR812q further targets and down-regulates CIPK10 which
is the mediator in calcium-dependent CBL-CIPK signaling
pathway (Jeong and Green 2013).
miRNA‑phytohormone response tohypoxia
Flooding or water logging condition results in lowering of
available oxygen to the plants, referred to as hypoxia resulting
in variation in transcriptome due to the metabolic shift from
aerobic to anaerobic respiration (Bailey-Serres and Voesenek
2008). Studies show increased expression of miR156g,
miR157d, miR158a, miR159a, miR172a,b, miR391 and
miR775 but decreased expression of miR395 during hypoxia
in Arabidopsis (Moldovan etal. 2010). In Arabidopsis,
miR171 regulates plant growth, root hair differentiation, light
signaling, GA signaling and transition of vegetative to floral
phase by targeting the scarecrow-like (SCL) family of gib-
berellic acid-insensitive (GAI), repressor of GAI (RGA) and
scarecrow (SCR) GRAS domain containing transcription fac-
tors (Ma etal. 2004) (Table1). During flooding condition in
maize, miR166, miR167, miR171 and miR399 were induced
whereas miR159 was down-regulated (Liu etal. 2012). The
miR159 modifies GA, ET and ABA biosynthesis by targeting
Fig. 2 Overview of miRNA
target-mediated phytohormones
crosstalk in response to abiotic
stress. During abiotic stress
various miRNAs participate
in hormone biosymthesis and
signaling. Some miRNAs
responsive to one hormone can
in turn regulate other hormones
thereby forming new connec-
tion in hormonal network. Black
I-bars indicate mutual inhibition
or repression, red T-bars indi-
cate inhibition or repression and
green arrows indicate molecular
receptor binding or activation
(Color figure online)
ABA
GA
BR
AUX
JA
miR160
ARF10/16
ARF 6/8
miR167
AUX Receptor
miR393
miR1848
miR159
ABI4
HD-ZIPIII
miR166
ABI3
GAMYB
miR159
ET
miR319
TCP
Mutual inhibition
Inhibition
Activation
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GAMYB and ACC synthase resulting in enhanced response to
defense and variation in root architecture (Zhang etal. 2008).
The miR166 indirectly regulates ABA signaling by targeting
HOMEODOMAIN ZIP III (HD-ZIP III) transcription factor
which further up-regulates ABI4 and b-glucosidase (BG1)
(Table1). This ABI4 activates ABA signaling genes, whereas
BG1 converts inactive conjugates into active ABA (Yan etal.
2016). The miR167 targets auxin-responsive factors (ARF),
thus playing a role in auxin signaling by controlling free auxin
levels and lateral root development (Fig.2).
miRNA‑phytohormone response toUV‑B
radiation
Among all the different radiations faced by the sessile plants
UV-B (280–320nm) has been found to severely affect the
plant growth and development, mainly due to membrane
damage via generation of reactive oxygen species (Mcken-
zie et al. 2007). In Arabidopsis, UV-B stress induced
the expression of miR156, miR157, miR159, miR319,
miR160, miR165, miR166, miR167, miR169, miR170,
miR171, miR172, miR393, miR398 and miR401 (Zhou
etal. 2007) (Table1). Under UV stress, miR160,miR165,
miR166,miR167andmiR393regulate auxin signaling path-
way by targeting various ARFs thereby affecting growth and
development of plants (Fig.2). Also miR159 is induced to
provide protection against UV-B in wheat by regulating
ABA and GA signaling pathways. During seed develop-
ment miR159 is induced by ABA which negatively regulates
MYB33 and MYB101.
miRNA‑phytohormone response toheavy
metals (HMs) stress
Heavy metals occur naturally in the environment but man-
made activities have increased HM contamination in a num-
ber of areas under crop cultivation. Heavy metals such as
Copper (Cu), iron (Fe), zinc (Zn) and manganese (Mn) are
essential HMs that play important role in growth and devel-
opment of plants at low concentrations but become toxic
at higher concentration (Rascio and Navari-Izzo 2011). On
miR
160
miR
164
miR
167
miR
393
miR
397
miR
156
miR
159
miR
396
Al
Cd
Cr
Cd Al
As
Cd
Al
As
Cd
Al
Cu
As
Cd
Cr
Cd
Cr
Cd
miR
168b
As
Cd
Regulates
jasmonic acid
LOX1,
LOX2
Gibberellic
acid
Cytokinin
Strigalactone
Abscisic
acid
Salicylic acid
Brassinosteroids
ARF 10/16/17ARF 6/8 TIR1
Auxin
Up-regulaon
Down-regulaon
Cr
Fig. 3 Schematic representation showing interaction between miR-
NAs and phytohormones during various Heavy metal stresses. An
overview of miRNA and their targets involved in regulating phytohor-
mones- auxin, cytokinin, gibberellic acid, abscisic acid, salicylic acid,
brassinosteroids and strigolactones during copper (Cu), cadmium
(Cd), aluminium (Al), arsenic (As) and chromium (Cr) stress. The
upward red arrow and downward green arrow indicate up-regulation
and down-regulation, respectively. The T-bars represent inhibition
and arrow indicates activation (Color figure online)
Plant Cell Reports
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the contrary, cadmium (Cd), aluminium (Al), arsenic (As)
and mercury (Hg) are non-essential HMs and are toxic even
at low concentrations (Gielen etal. 2012). Although Chro-
mium (Cr) neither belongs to the category of essential or
non-essential HM, it has also been discussed in this section
because of its highly carcinogenic and toxic characteristic.
Heavy metal stress is a type of abiotic stress that affects the
growth and development of plants by hampering various
physiological and metabolic activities (Gupta etal. 2014).
Recent studies suggested the role of miRNAs under HM
stress by regulating gene expression at transcriptional and
post translational levels (Yang etal. 2013). Apart from miR-
NAs, HM stress also triggers various signaling pathways
involving hormones such as AUX, CK, ET; calcium and
MAPK signaling (Sun etal. 2010; Potters etal. 2007).
Copper (Cu) is essential for various physiological activi-
ties of plants at low concentrations but becomes hazard-
ous at higher concentrations by affecting photosynthetic
rate, membrane integrity and protein metabolism of plants
(Ding etal. 2009). Cu-deprived conditions results in reduced
expression of CSDs (copper–zinc superoxide dismutase),
PC and laccases due to up-regulation of various miRNAs
such as miR397, miR398, miR408 and miR857 (Paul etal.
2015) (Table1). The promoters of miR397 inArabidop-
sis comprises of ABRE, MYC, CBF, SA andJA elements
suggesting that miR397 might be involved in overcoming
abiotic stress (Patel etal. 2019). Also, the up-regulation of
miR408 directly or indirectly regulates GA biosynthesis,
thereby promoting cell expansion and increase in biomass
in Arabidopsis (Song etal. 2018) (Table1). A study in Chla-
mydomonas suggested the involvement of squamosa pro-
moter binding protein-like 7 (SPL7) during Cu deficiency
which activates gene by binding to GTAC motifs in the pro-
moter of miR398 (Kropat etal. 2005). Additionally, SPL7
also regulates expression of various other Cu-related miR-
NAs such as miR857(Yamasaki etal. 2009). HY5 and SPL7
regulate miR408by interacting with the promoter (Zhang
etal. 2014).
Cadmium (Cd) is amongst the most dangerous pollutants
which adversely affect plant productivity by causing chloro-
sis, wilting, reduced growth and even plant death. In Bras-
sica napus, Cd stress results in up-regulation of miR393,
miR156a, miR167a/c, miR164b, miR394a/b/c(Huang etal.
2010) and down-regulation of miR156, miR160, miR171
and miR396a (Zhou etal. 2012) (Table1). The miR393
is anticipated to target F-box genes that include E3 ubiq-
uitin ligase or transport inhibitor response 1 (TIR1) that
play important role in the process of ubiquitination. Auxin
signaling is regulated by TIR1 by aggravating AUX/IAA
proteins (Chinnusamy etal. 2007). So during Cd stress, up-
regulation of miR393results in increased mRNA levels of
TIR1 thereby down-regulating auxin signaling with reduced
activity of E3 ubiquitin ligase. Thus, suggesting a cross talk
between Cd stress and auxin signaling. In soybean, Cd-
responsive miRNA, miR1535b is responsible for cleavage
of Glyma07g38620.1, thereby catalyzing de novo cytokinin
production by isopentenyl transferase (iPT). So, during Cd
stress up-regulation of Glyma07g38620.1correlates posi-
tively with the production of Cytokinin (Fang etal. 2013)
(Table1).
Aluminium (Al) toxicity is a major problem in acidic
soils having a pH 5.5 or lower, affecting 30–40% of world’s
fertile land (Gupta etal. 2014). It binds with –COOH and
–PO4
2− groups in the cell wall of roots resulting in reduced
root length thereby interfering with the water and mineral
absorption, affecting callose deposition, imbalanced cyto-
plasmic Ca2+ levels and oxidative stress (Ma etal. 2004;
Silva 2012). Al-responsive miRNAs, miR160 and miR390
regulate root growth by means of auxin response factors
(ARFs) (Table1). During Al stress, ARF10 and ARF16 are
targeted by down-regulated miR160 thereby affecting the
development of root cap (Wang etal. 2005). The miR390
functions in tasiRNA biogenesis which targets ARF2, ARF3
and ARF4, thereby regulating lateral root emergence (Yoon
etal. 2010) (Fig.3). Al toxicity in rice results in down-regu-
lation of miR393b which functions in proteasome-mediated
protein processing. In the auxin signaling pathway, up-reg-
ulation of miR160e and targeting of ARFs are antagonistic
to miR393b. The up-regulation of miR528 upon Al stress in
rice also suggests its probable role in SCF-mediated protein
production for handling metal toxicity. Therefore, in order to
combat Al stress in rice, miR160e, miR166k and miR528 are
up-regulated whereas miR393b is down-regulated (Table1;
Fig.3).
Arsenic (As) is a widely distributed metalloid belonging
to Class I carcinogen thatpossesses severe threat to vari-
ous organisms on Earth (Srivastava etal. 2012). Arsenic
toxicity in plants affects photosynthesis rate, carbohydrate
metabolism and increases generation of reactive oxygen
species (ROS) and lipid peroxidation. Till date very little
information is available about the miRNA-mediated regu-
lation of plants during arsenic stress. Detailed study will
provide information about the regulatory factors involved in
response to As toxicity at post transcriptional level. Study
in rice under arsenic stress resulted in identification of 36
new miRNAs and their mode of regulation of lipid metabo-
lism and jasmonic acid (JA) signaling upon As stress (Yu
etal. 2012). The role of jasmonic acid in response to arsenic
stress has been established very well, but there are only few
miRNAs that regulate JA biosynthesis (Singh etal. 2017;
Gupta etal. 2014). In a study, miR319 has been found to be
expressed during arsenic stress, affecting JA biosynthesis by
targeting the TCP transcription factor under As, Cd, Al and
Hg stress (Liu etal. 2012) (Fig.3). This indicates the role
of miRNAs in regulating biosynthesis of JA, thereby play-
ing a role in plant response to metal stress. During arsenic
Plant Cell Reports
1 3
stress, miR838 has a putative target lipase which mediates
oxylipin biosynthesis and further activates JA biosynthesis.
Under arsenic stress, exogenous application of AUX and
JA altered the expression of miR167, miR319 and miR854,
thus positively influencing the plant growth and regulating
crosstalk between hormones and miRNAs in response to
arsenic stress (Table1; Fig.3). Therefore, miRNAs play an
important role in JA biosynthesis which further has an active
role in response to heavy metal stress (Gupta etal. 2014).
Chromium (Cr) is the second most toxic heavy metal
which is released into the environment via anthropogenic
activities. Cr affects the growth and development of plants
by hampering the uptake of water, nutrients as well as by
interfering in photosynthesis and respiration. Cr stress in
radish (Raphanus sativus L.) resulted in differential expres-
sion of 16 novel and 54 known miRNAs. Amongst them
miR156, miR159, miR160, miR168, miR169, miR319,
miR397, miR398, miR399 and miR408 were down-reg-
ulated, whereas miR161, miR172, miR390 and miR394
were up-regulated under Cr stress (Liu etal. 2015). Studies
reported that miR156/157, miR159 and miR5293 might play
an important role in regulating Cr homeostasis as they target
various SPLs—SPL3, SPL6, SPL9, SPL13 and SPL15 in rad-
ish. Also, the expression of various genes during Cr stress
might be mediated by miR159, miR319 and miR858 by tar-
geting MYB3, 13, 101, 104 and 305. So, Cr stress in radish
is reduced by miRNA-mediated regulation of Cr stress via
targeting various transcription factors (Liu etal. 2015).
Recent study also suggested that miRNAs can regulate
Cr uptake, transportation as well as gene expression during
Cr stress. The miR5293 targets TCP6, TCP15 and TCP21
which binds to the promoter of lipoxygenase (LOX),
thereby regulating the JA biosynthesis pathway (Liu etal.
2015). The miR397a and rsa-miRn35 target laccase genes
which are involved in heavy metal sequestration. Heat
shock protein 81-2 (HSP81-2) is targeted by rsa-miRn39
which plays an important role in repairing damage caused
by Cr stress. Cr stress in plants results in generation of
ROS and to reduce this oxidative damage, plants activate
HM-responsive signaling molecules and hormones such as
ET, JA, AUX signaling F-box protein, calcium-dependent
protein kinase (CDPK), mitogen-activated protein kinase
kinase (MEKK). So, a large number of miRNAs targeting
various hormones and signaling molecules results in alle-
viating Cr toxicity in plants. Thedown-regulated miR160
in riceresults in increased expression of AUX by targeting
auxin response factor (ARF)therebypreventing Cr toxic-
ity. Similar response of osa-miR160 has been reported in
Arabidopsis in regulating root cap formation (Wanget al.
2005). Although the relation between MAPK and AUX
signaling during HM stress is not very clearly known,
IAA,ARFandPIN have been reported to be negatively
regulated by MAPK signaling (Zhao etal. 2014). Another
miRNA in rice, osa-miR159, targets and suppresses MAPK
signaling cascade, thereby inducing AUX signaling and
acting as a regulator of auxin response during Cr stress
(Dubey etal. 2020).
Conclusion
miRNAs regulate the expression of genes post transcription-
ally and also play an important role in various growth and
developmental processes in plants. Although under adverse
environmental conditions, these miRNAsprovide stress tol-
erance by regulating various stress-responsive genes, pro-
teins, TFs and phytohormones. The growth and development
of plants under environmental stress also involves hormonal
regulation. This review deals with the involvement of miR-
NAs in hormonal crosstalk during various abiotic stresses.
Generally, miRNAs control hormonal responses by regulat-
ing early hormone-responsive genes, thus regulating only
a part of growth and development. The miRNA regulation
also involves hormonal pathways such as brassinosteroids,
salicylic acid, plant peptide hormones, polyamines, nitric
oxide and strigolactones in addition to auxin, cytokinin, gib-
berellins, abscisic acid, ethylene and jasmonic acid. This
review also deals with the interconnection between MAPK
and calcium signaling with phytohormones during various
abiotic stresses, especially HM stress suggesting the role
of MAPK in regulation of signaling molecules at both up-
stream and down-stream.
The identification and validation of abiotic stress-respon-
sive miRNAs and their corresponding targets will help to
improve tolerance of plants against various stresses. Mostly,
the targets of miRNAs are transcription factors, suggesting
that miRNAs act as an important contributor to the regu-
latory processes but it must be experimentally validated
in order to establish the relation of miRNA with different
hormones to provide abiotic tolerance. Since the targets of
miRNAs are not conserved so, there is a need to validate the
targets of miRNAs in different plants. Reverse genetics fol-
lowed by target validation will provide appropriate reasons
for approving or disapproving their role in various abiotic
stress. Additionally, the miRNA-mediated gene silencing
may be used in future for developing transgenic crop plants
with improved abiotic stress tolerance.
The crosstalk between miRNAs and phytohormones dur-
ing abiotic stress, including HMs, is not very clearly under-
stood. Thus, detailed identification of miRNAs, interconnec-
tion between miRNAs and various metabolic and signaling
pathways as well as identification of regulatory elements
up-stream of miRNAs is required to provide a better under-
standing of the miRNA-phytohormone crosstalk. Therefore,
a more detailed study in future will be helpful to develop
better approaches for mitigating various abiotic stresses.
Plant Cell Reports
1 3
Acknowledgements Authors acknowledge Director, CSIR-National
Botanical Research Institute for providing facilities and support during
the study.This manuscript bears CSIR-NBRI communication number
’CSIR-NBRI_MS/2021/06/01.
Author contribution statement DC conceived, PS, PD designed and
wrote the review. PS, PD has done the literature survey and provided
idea about conceptual things. DC supervision. Editing DC, PS. All the
authors have reviewed and proofread the article.
Funding This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Declarations
Conflict of interest The authors declare no conflict of interest.
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