DOI: 10.1007/s10535-013-0374-5
BIOLOGIA PLANTARUM 58 (1): 9-17, 2014
REVIEW
Brassinosteroids and their role in response of plants to abiotic stresses
Q. FARIDUDDIN1*, M. YUSUF1,2, I. AHMAD2, and A. AHMAD1
Plant Physiology and Biochemistry Section, Department of Botany1, and Department of Agricultural Microbiology2,
Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh-202002, Uttar Pradesh, India
Abstract
Brassinosteroids (BRs) are polyhydroxylated steroidal plant hormones that play pivotal role in the regulation of various
plant growth and development processes. BR biosynthetic or signaling mutants clearly indicate that these plant steroids
are essential for regulating a variety of physiological processes including cellular expansion and proliferation, vascular
differentiation, male fertility, timing senescence, and leaf development. Moreover, BRs regulate the expression of
hundreds of genes, affect the activity of numerous metabolic pathways, and help to control overall developmental
programs leading to morphogenesis. On the other hand, the potential application of BRs in agriculture to improve
growth and yield under various stress conditions including drought, salinity, extreme temperatures, and heavy metal
(Cd, Cu, Al, and Ni) toxicity, is of immense significance as these stresses severely hamper the normal metabolism of
plants. Keeping in mind the multifaceted role of BRs, an attempt has been made to cover the various aspects mediated
by BRs particularly under stress conditions and a possible mechanism of action of BRs has also been suggested.
Additional key words: antioxidant system, drought, heavy metals, high temperature, low temperature, oxidative stress,
photosynthesis.
Introduction
Plants constantly regulate their developmental and
physiological processes in response to various internal
and external stimuli. Studies have indicated that
biological processes are integrated by multiple hormonal
signals, and stresses induce the activities of different
hormonal signaling pathways in plants (Teale et al.
2008). Out of the recognized categories of plant
hormones, much attention has been focused on auxins,
cytokinins, gibberellins, abscisic acid, and ethylene.
Furthermore, brassinosteroids (BRs) are a group of
steroidal hormones that play pivotal roles in wide range
of developmental phenomena including cell division and
cell elongation in stems and roots, photo-morphogenesis,
reproductive development, leaf senescence, and also in
stress responses (Choudhary et al. 2012).
The identification of plant endogenous steroidal
hormones is the result of nearly 30 years of efforts to
identify novel growth-promoting substances present in
pollen grains of different plant species (Steffens 1991).
Mitchell et al. (1970) showed that the growth stimulating
activity was found in the organic solvent extract of pollen
from Brassica napus and the unidentified active
compound was named as brassin. The specific growth
promoting effects of the brassin have been reflected in
many bioassays including the bean second-internode
bioassay (Mandava 1988). Based on their ability to cause
marked changes in growth and differentiation at low
concentrations, Mitchell et al. (1970) proposed that
brassins constituted a new family of plant hormones
known as brassinosteroids (BRs). Further work
demonstrated that brassinosteroids not only induce stem
elongation, they also increase total biomass and yield.
Although brassinosteroids were known to be
endogenous regulators that induce dramatic growth
⎯⎯⎯⎯
Submitted 10 October 2012, last revision 24 June 2013, accepted 29 July 2013.
Abbreviations: 28norCS - 28-norcasterone; 6deoxoCS - 6-deoxocasterone; 6-deoxoTY - 6-deoxotyphasterol; BL - brassinolide;
BRI1 - brassinosteroids insensitive I; BRs - brassinosteroids; CAT - catalase; CS - castasterone; EBL - 24-epibrassinolide; HBL 28-homobrassinolide; LRR - leucine rich repeat; MT-sHSP - mitochondrial small heat shock protein; NPR1 - non-expressor of
pathogenesis related genes 1; P5C - pyrroline-5-carboxylase; POX - peroxidase; PR-1 - pathogenesis related 1; PS II - photosystem II;
ROS - reactive oxygen species; S/T kinase - serine/threonine kinase; SOD - superoxide dismutase; TE - teasterone; TY - typhasterol.
Acknowledgements: M. Yusuf gratefully acknowledges the financial assistance rendered by the University Grant Commission, New
Delhi, India in a form of the Dr. D.S. Kothari Postdoctoral Fellowship [F.4-2/2006(BSR) 13-608/2012/BSR].
* Corresponding author; fax: (+91) 571 2702016, e-mail: [email protected]
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Q. FARIDUDDIN et al.
effects in the bean second-internode bioassay, they were
not immediately accepted as plant hormones, as their role
in normal plant growth and development remained
elusive for many years. Young growing tissues contain a
higher content of BRs than mature tissues. Pollen and
immature seeds are the richest sources of BR with a range
of 1 - 100 μg kg-1(fresh mass), whereas shoots and leaves
usually possess lower amounts of 0.01 - 0.1 μg kg-1(f.m.).
Clouse and Sasse (1998) and Sasse (2003) disclosed that
BRs are required for normal growth and development
including shoot and root growth (Nemhauser et al. 2004),
vascular differentiation (Caño-Delgado et al. 2004),
fertility and seed germination (Taiz and Zeiger 2004).
Such responses may be involved in cell elongation
(Catterou et al. 2001), vascular differentiation (Ashraf
et al. 2010), xylem formation in epicotyls (Zurek et al.
1994), and also in the regulation of expression of several
genes involved in xylem development. However, a great
diversity exists in effects of BRs on pigments and
photosynthesis. Their influence on chlorophyll content
depends to some extent on the mode of application of
BRs and the relationship between exogenously applied
BRs and the basal chlorophyll content in various crop
species (Gomes 2011). In addition to this, BRs have the
ability to confer resistance to plants against various biotic
and abiotic stresses, such as salinity (Hayat et al. 2010),
water stress (Fariduddin et al. 2009a), temperature
extremes (Fariduddin et al. 2011, Gomes 2011), and
heavy metals (Bajguz and Hayat 2009, Fariduddin et al.
2009b, Yusuf et al. 2011, 2012).
In the following sections, the relationship between
BRs with oxidative stress, antioxidant system, and further
details of the role of BRs in relation to various abiotic
stresses are discussed. Apart from this, we tried to
suggest a possible mode of action of BRs established till
date.
Relationship of brassinosteroids with oxidative stress and antioxidant system
Like all aerobic organisms, plants have also welldeveloped metabolic pathways to utilize its energetic
potential in the presence of oxygen (Navrot et al. 2007).
One potentially damaging effect of this fact is the
deleterious production of reactive oxygen species (ROS)
during normal respiration, photosynthesis, and nitrogen
fixation (Mittler et al. 2011). Inhibition of the antioxidant
systems leads to oxidative stress causing degradative
changes of lipids, proteins, and nucleic acids (Prasad
2004) and to disruption of the redox homeostasis (Gille
and Sigler 1995). Moreover, when plants are subjected to
stresses, a variety of ROS are generated, such as superoxide radical, hydroxyl radical, and hydrogen peroxide.
ROS can undergo a series of oxidation/reduction
reactions known as the Halliwell-Asada pathway (Gratao
et al. 2006). To defend themselves, plants contain
antioxidant enzymes, such as superoxide dismutase
(SOD), catalase (CAT), guaicol peroxidase (POX),
ascorbate peroxidase (APX), monodehydroascorbate
reductase (MDHAR), glutathione reductase (GR), and
glutathione peroxidase (GPX) (Ruley et al. 2004,
Simonovicova et al. 2004), and non-enzymatic antioxidants, namely ascorbate, gluthathione, α-tocopherol,
and carotenoids (Vardhini and Rao 2003, Ozdemir et al.
2004, Sharma and Dubey 2005).
However, little is known about the role of BRs in the
plant response to oxidative stress. It was shown that
application of BRs modifies antioxidant enzymes as well
as non-enzymatic antioxidants. When maize seedlings
treated with brassinolide (BL) are subjected to water
stress, the activities of SOD, CAT, APX, as well as
ascorbic acid and carotenoid content increase (Li et al.
1998). On the other hand, BRs enhance the activity of
CAT and reduce the activities of POX and ascorbic acid
oxidase under osmotic stress in sorghum (Vardhini and
Rao 2003) and also regulate secondary metabolism in
tomato which may enhance tolerance to phenanthrene
10
(Ahammed et al. 2013).
Rice seedlings exposed to salinity stress and treated
with BRs show a significant increase in the activities of
CAT, SOD, and GR and a slight increase in the APX
activity (Nunez et al. 2003). Epibrassinolide (EBL)
treatment, at least in part, improves the tolerance of saltsensitive rice seedlings to short-term salt stress. The
differences in activities of antioxidant enzymes in saltsensitive rice cultivar suggest that the increased salt stress
tolerance in sensitive seedlings induced by EBL could be
due to an increased APX activity (Ozdemir et al. 2004).
Treatment of Chlorella vulgaris with brassinolide
increases activities of CAT, GR, and APX and a content
of ascorbic acid, carotenoids and glutathione (Bajguz and
Hayat 2009). A treatment of tomato leaf discs exposed to
high temperature by EBL leads to high activities of CAT,
POX, and SOD (Mazorra 2002).
It has been shown that the Arabidopsis mutant det-2,
which is blocked in the biosynthetic pathway of BRs, has
significantly thicker leaves, thicker cuticle and cell walls
in epidermis and mesophyll, increased stomatal density,
and more compact leaves due to smaller intercellular
spaces than the wild-type when grown under normal
conditions (Choe 2006). However, an addition of BL to
the growth medium results in leaves that are more similar
in morphology to those of the wild type. It has also been
demonstrated that ATPA-2 and ATP-24, genes encoding
peroxidases, are constitutively up-regulated in the det-2
Arabidopsis mutant (Goda et al. 2002). Furthermore,
oxidative stress-related genes encoding MDHAR and
thioredoxin, cold and drought stress response genes
COR-47 and COR-78, and heat stress-related genes
hsp83, hsp70, hsf3, hsc70-3, and hsc70-G7 have been
identified by a microarray analysis of either BR-deficient
or BR-treated plants (Mussig et al. 2002). The enhanced
oxidative stress resistance in det-2 plants correlates with a
constitutive increase in the SOD activity and increased
BRASSINOSTEROIDS UNDER ABIOTIC STRESSES
transcription of the CAT gene. Therefore, a possible
explanation for the fact that the det-2 mutant exhibits an
enhanced oxidative stress resistance is that the long-term
BR deficiency in the det-2 mutant results in a constant
physiological stress that, in turn, activates the constitutive
expression of some defense genes and, consequently, the
activities of related antioxidant enzymes. It may be
suggested that endogenous BRs in wild-type plants
somehow act to repress the transcription or post-
transcription activities of the defense genes to ensure the
normal growth and development of plants. However, it is
still unclear whether BRs directly or indirectly modulate
the responses of plants to oxidative stress (Cao et al.
2005). Moreover, BRs induce stress tolerance by
triggering the accumulation of apoplast H2O2 which
subsequently up regulates the antioxidant system (Jiang
et al. 2012).
Water stress
Water stress is characterized by a reduction of water
content and leaf water potential, closure of stomata, and
decreased growth. Severe water stress may result in the
arrest of photosynthesis, disturbance of metabolism and
finally the death of plant (Jaleel et al. 2008). However,
application of EBL or HBL prior to water stress results in
increased root nodulation, zeatin content, and nitrogenase
activity in unstressed Phaseolus vulgaris plants and also
ameliorates stress-induced decline in the same parameters. Moreover, EBL was relatively more effective
than HBL (Upreti and Murti, 2004). Arabidopsis thaliana
and Brassica napus seedlings grown in nutrient solution
containing 1 µM EBL and then transplanted to sand were
subjected to a drought stress by withholding water for
96 h (Arabidopsis thaliana) or 60 h (Brassica napus). In
this case, an EBL treatment enhances seedling tolerance
to drought stresses in both species (Kagale et al. 2007).
The ability of EBL to confer tolerance of plants to a
variety of stresses was confirmed by the analysis of
expression of drought stress marker genes (Kagale et al.
2007). In addition, Li et al. (2012) reported that EBL
induces changes in antioxidative enzyme activities and
content of antioxidant and so improve plant growth under
drought stress. Leaf wilting, reduction in growth, and
complete drying of some seedlings are frequently
observed in untreated, but are considerably reduced in
EBL-treated seedlings. In leaves of soybean drought
stressed plants, a BRs treatment increases the maximum
quantum yield of photosystem II (PS II), the activity of
ribulose-1,5-bisphosphate carboxylase/oxygenase, the
water potential, the content of soluble sugars and proline,
and the activities of POX and SOD in comparison with a
drought stress alone. BRs also decrease the malondialdehyde content and electrical conductivity of leaves
under drought stress, and increase biomass accumulation
and a seed yield in both control and drought stressed
soybean plants (Zhang et al. 2008). Moreover, Fariduddin
et al. (2009a) reported elevated activities of CAT, POX,
SOD, and an elevated proline content in mustard plants
treated with HBL and/or exposed to drought stress. This
study shows that BR can be used to minimize the loss of
yield in mustard caused by water deficits. However, further
investigation is necessary for an explanation of the
mechanism by which BRs confer tolerance to water stress.
Salinity
Salinity is a major abiotic stress affecting growth,
development and productivity of plants. It causes an
osmotic stress, ionic toxicity, and also disturbs the uptake
and translocation of mineral nutrients (Turkan and
Demiral 2009). Proline accumulates in plants exposed to
salinity and serves as osmolyte (Ashraf and Foolad 2007)
and a stress signal influencing adaptive responses (Lin
and Kao 2007). Under salinity and drought, a proline
accumulation is dependent on the activity of
Δ1-pyrroline-5-carboxylate synthetase (P5CS), a rate
limiting enzyme in the proline biosynthesis, and the
activity of proline dehydrogenase (PDH) which catalyzes
proline degradation. Özdemir et al. (2004) reported that a
treatment of seeds of salt-sensitive rice cv. IR-28 with
EBL improves seedling growth, alleviates lipid damage,
and decrease proline accumulation compared to the
seedlings treated with NaCl alone. However, except for
APX, EBL does not increase the activities of POX,
CAT, and GR under salinity. Moreover, Kagale et al.
(2007) demonstrated that EBL has an ability to
ameliorate NaCl-induced inhibition in seed germination
of Arabidopsis thaliana and Brassica napus. The
application of BRs increases the accumulation of proline
and enhances activities of antioxidant enzymes in salt
stressed Cicer arietinum (Ali et al. 2007) and Vigna
radiata (Hayat et al. 2010). In addition, an EBL
application counteracts the salt stress-induced deterioration of growth in eggplant (Ding et al. 2012) and grain
yield inhibition in wheat (Ali et al. 2008b). Divi et al.
(2010) reported that the redox-sensitive protein NPR1
(non-expressor of pathogenesis-related genes1) is likely a
critical component of an EBL-mediated increase in salt
tolerance, but it is not required for the EBL-mediated
induction of PR-1 (pathogenesis-related 1) gene
expression.
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Q. FARIDUDDIN et al.
High-temperature stress
High temperature stress is a serious threat to crop
production worldwide (Hopkins 1995). High temperature
severely damages the mesophyll cells and increases the
permeability of plasma membrane, e.g., in grapes (Zhang
et al. 2005), and also reduces water availability (Simoes
Aranjao et al. 2003), thus affecting leaf water potential
and photosynthesis that are considered as the most
important temperature sensitive processes (Bery and
Björkman 1980). However, tomato plants treated with
EBL were found more tolerant to high temperature than
untreated plants (Singh and Shono 2005) and this could
be due to a higher accumulation of mitochondrial small
heat shock proteins (MT-sHSP) in EBR treated tomato
under temperature stress, and also improved photosynthetic efficiency. In tomato cv. Amalia treated with
EBL and a polyhydroxylated spirostanic analog MH-5, a
SOD activity increased at both 25 and 40 °C (Mazorra
et al. 2002), and MH-5 was more prominent in its effect.
Moreover, Ogweno et al. (2008) showed that application
of EBL to tomato plants before exposure to high
temperature protects Rubisco and other enzymes involved
in the Calvin cycle and RuBP regeneration under a heat
stress. Furthermore, Arabidopsis thaliana seedlings were
exposed to 43 °C in the presence or absence of EBL for
1, 2, 3, or 4 h and then recovered at 22 °C for 7 d.
Seedlings exposed to the 2-, 3-, or 4-h heat stress exhibit
increasing bleaching, whereas EBL-treated seedlings
show bleaching only after 4 h of the heat stress (Kagale
et al. 2007).
Low-temperature stress
Low temperature (chilling and frost stress) is a major
limiting factor for the productivity of plant indigenous to
tropical and subtropical climates (Saltveit 2001). Chilling
stress has a direct impact on the photosynthetic apparatus,
essentially by disrupting the thylakoid electron transport,
the carbon reduction cycle, and the stomatal control of
CO2 supply, together with an increased accumulation of
sugars, peroxidation of lipids, and disturbance of water
balance (Allen and Ort 2001). A treatment with EBL
partially recovers the growth of mung bean subjected to a
chilling stress and 17 proteins (involved in methionine
assimilation, ATP synthesis, cell wall construction, etc.)
down-regulated by chilling are up-regulated (Huang et al.
2006). EBL injected into cotyledons or primary leaves of
rape seedlings diminishes a cold-induced increase in
membrane permeability (Janeckzo et al. 2007). Furthermore, the seedlings exposed to 2 °C and treated with EBL
have a significantly higher pigment content in leaves as
compared to a control, but at 20 °C, there is no difference
in the pigment content between leaves injected with EBL
or water. Brassica napus and Arabidopsis thaliana grown
on a nutrient solution containing EBL were exposed to a
cold stress by transferring seedlings to a growth chamber
set at 2 °C for 3 d. The transcription analysis indicates
that cold-related genes accumulate to higher levels in the
plants treated with EBL (Kagale et al. 2007). Furthermore, a study conducted by Xia et al. (2009) indicates the
involvement of EBL in enhancing activation of Rubisco
and expression of photosynthetic genes in cucumber
seedlings subjected to a chilling stress.
Heavy metal stress
Brassinosteroids have ability to regulate the uptake of
ions into plant cells and can be used to reduce the
accumulation of heavy metals and radioactive elements in
plants. Moreover, BRs also minimizes the toxic effects
and symptoms generated by excess of heavy metals
(Bajguz and Hayat 2009)
Cadmium is extremely toxic to plants even in traces.
It retards the biosynthesis of chlorophyll, alters water
balance, decreases activities of various enzymes, favors
stomatal closure, induces oxidative stress, and slows
down the rate of photosynthesis. Cd inhibits both the
“light” and “dark” reactions of photosynthesis, but the
Calvin cycle is most sensitive. The inhibition of
photochemical processes by Cd may mainly result from
the limitation in the use of ATP and NADPH in the
Calvin cycle (Vassilev and Yordanov 1997). Seedlings of
winter rape were cultured in vitro on media containing
EBL and Cd (Janeckzo et al. 2005). After 14 d of growth,
the kinetics of chlorophyll a fluorescence and the content
12
of photosynthetic pigments and Cd in cotyledons were
measured. Cd was strongly accumulated but its content in
cotyledons was 14.7 % lower in the presence of EBL.
Neither Cd nor EBR influenced the content of Chl a,
Chl b, and carotenoids. The number of active reaction
centres of photosystem II decreased by about 21.0 % and
the electron transport by about 17.1 %. Simultaneously,
under the influence of Cd, the activity of O2 evolving
centers diminished by about 19.5 % and energy
dissipation increased by about 14.6 % (Janeczko et al.
2005). The change in growth and photosynthesis of plants
subjected to a Cd stress and the role of HBL was also
verified by Hayat et al. (2007) in Brassica juncea. They
observed that plants fed with Cd alone exhibited a decline
in growth, the activity of carbonic anhydrase, the content
of chlorophyll, net photosynthetic rate, nitrate content,
the activity of nitrate reductase, and sugar content. These
effects are overcome if stressed plants are sprayed with
HBL. The activities of CAT, POX, and SOD and the
BRASSINOSTEROIDS UNDER ABIOTIC STRESSES
content of proline increases in Cd-treated plants and
especially in mustard plants also supplemented with HBL
(Bajguz and Hayat 2009). The effects of EBL and HBL
on seed germination and seedling growth of radish under
Cd stress were studied by Anuradha and Rao (2007a).
Both the BRs (EBL or HBL) cause a considerable
increase in seedling growth under the stress and restore
their growth to the level of unstressed control seedlings.
Beside this, BR enhanced proline accumulation and CAT,
APX, GPX, and SOD activities, whereas reduced POX
and ascorbic acid oxidase activities. Moreover, lipid
peroxidation induced by Cd was reduced with the
supplementation of BRs (Anuradha and Rao 2007).
Hasan et al. (2008) revealed that the negative effects of
Cd were overcome by foliar application of HBL through
increased accumulation of proline and activities of CAT,
POX, and SOD).
Among the pollutants of agricultural soils, copper has
become increasingly hazardous due to its involvement in
fertilizers, fungicides, and pesticides. The high content of
Cu may be phytotoxic and may cause an inhibition of
plant growth or even death. When Brassica juncea seeds
are treated with EBL before germination and then
submitted to a Cu stress, there is an improvement in shoot
emergence and plant biomass production, but reduced Cu
uptake and accumulation (Sharma and Bhardwaj 2007).
In addition, Fariduddin et al. (2009a) reported that the
activities of SOD, CAT, and POX, and proline content
increase in response to a Cu stress and more after a HBL
treatment. Therefore, it may be suggested that the
elevated activity of the antioxidant system by HBL may
be at least in part responsible for conferring resistance
against Cu stress in Brassica juncea reflected in the
improvement of plant growth and photosynthesis in the
presence of Cu.
The aluminum toxicity is the major growth-limiting
factor for crop cultivation on acidic soils. Seedlings of
mung bean were subjected to an Al stress and sprayed
with EBL or HBL (Ali et al. 2008a). The activities of
SOD, CAT, and POX, and proline content increased in
response to the Al stress and more in the HBL or EBL
treated plants. The increase in the Al resistance conferred
by BRs was reflected in the improvement of plant
growth, photosynthesis, and related processes in the
presence of Al. It was also noticed that EBL is more
effective than HBL. Other study verified that BLs
promote growth of mung bean seedlings under an Al
stress (Abdullahi 2003). EBL significantly increases the
fresh masses of shoots and roots, and chlorophyll content
in mung bean under an Al stress (Ali et al. 2008a).
Although nickel is an essential element, its high
concentration is toxic and inhibits photosynthesis,
respiration, the activities of enzymes, and protein content.
The plants of Brassica juncea supplied with 50 or
100 µM Ni were subsequently sprayed with HBL (Alam
et al. 2007). The plants treated with Ni alone exhibited
reduced growth, net photosynthetic rate, the content of
chlorophyll, and the activities of nitrate reductase and
carbonic anhydrase, whereas the activities of POX and
CAT and proline content increased. Spraying with HBL
partially neutralizes the toxic effect of Ni on most of the
parameters. Also, seeds of Brassica juncea soaked in
solutions with different concentrations of HBL were
subjected to a Ni stress (Sharma et al. 2008). The growth
of seedlings was inhibited by Ni and this reduction was
restored by the HBL treatment. The protein content and
activities of CAT, GR, APX, SOD, and GPX were also
increased by the HBL treatment. Seed germination and
seedling growth is significantly reduced by the Ni
treatment but the HBL treatment enhanced germination
percentage as well as shoot and root lengths in Ni
stressed as well as unstressed seedlings (Yusuf et al.
2011), and EBL also increases the nitrogen metabolism of
Vigna radiata plants under different concentrations of Ni
(Yusuf et al. 2012).
Possible mode of brassinosteroids action
The mechanism of action of BRs has been an attractive
target for many researchers but it is still far from final
solution. Considering the high variability of the
physiological effects of BRs, it is believed that more than
one molecular mechanism of their action exists. Two
main aspects of the primary mechanism have to be
considered: 1) the effects of BRs on the biosynthesis of
different enzymes via their effects on gene expressions
and 2) the effects of BRs on membrane properties. It is
well documented that steroids function as signaling
molecules both in animals and plants, and BRs in plants
are perceived by a cell surface receptor kinase,
brassinosteroid-insensitive 1 (BRI1).
EBL and HBL, the most active BRs in bioassays, bind
to the extracellular domain of the BRI1 receptor. BRI1 is
the plasma membrane localized leucine-rich repeat (LRR)
receptor of a serine/threonine (S/T) kinase (Friedrichsen
et al. 2000). The LRR receptor kinases constitute the
largest receptor class predicted in the Arabidopsis
genome, with over 230 family members. This family has
a conserved domain structure composed of a N-terminal
extracellular domain with multiple tandem (adjacent)
LRR motifs, a single trans-membrane domain, and a
cytoplasmic kinase domain with specificity towards
serine and threonine residues. In case of BRI1, the
number of LRRs is 25. BRI1 has also a unique feature
that is required for BR binding, a stretch of amino acids
called an island domain that interrupts the LRRs between
LRRs 21 and 22 (Kinoshita et al. 2005). This domain
plus the flanking LRR22 compose the minimum binding
site for BRs. BL binding to BRI1 triggers the interaction
between BRI1 and BRI1 associated receptor kinase 1
(BAK1). BRI1 is phosphorylated at multiple sites along
with its intracellular domain, some of them have been
13
Q. FARIDUDDIN et al.
shown to regulate receptor activity (Choudhary et al.
2012). The BR signal is then transmitted to the cytoplasm
by an unknown mechanism where it inhibits
brassinosteroid-insensitive 2 (BIN2) which is a negative
regulator of the BR biosynthetic pathway. BIN2 is a
protein kinase that interacts with and phosphorylates two
nearly identical transcription factors, BRI 1-EMS
supressor 1 (BES1) and brassinazole resistant 1 (BZR1),
negatively regulating their activities. BRI 1 supressor 1
(BSU1) dephosphorylates BES1 and BZR1 to counteract
the effect of BIN2. BRs regulate the expression of
hundreds of genes. A significant portion of the
unregulated genes is predicted to play a role in growth
processes. The BES1 binding activity and expression of
its target genes are enhanced synergistically by BES1interacting MYC-like1 (BIM1). B1M1 is another
transcription factor that dimerizes with BES1 and
increases its activity. Genes that are down-regulated by
BRs include several BR biosynthetic genes. BZR1 binds
to specific elements in their promoters to repress their
activity. The gene repression by BZR1 represents a
negative feedback loop for the regulation of growth by
BR (Fig. 1) (Wang et al. 2006, Kim and Wang 2010).
Fig. 1. BR binding to BRI-1 leads to decrease in an active BIN2 level; inactivated BIN2 favors the BR induced genes by transcription
factor BES1 which binds E-box elements to activate the expression of BR induced genes leading to physiological or morphological
changes. Alternatively, binding active BZR1 to CGTG(T/C)G sequences (mostly occurring at the promoter of BR biosynthetic genes)
represses the BR biosynthetic pathway (dotted). Abbreviations: BR - brassinosteroids, LRRRK - leucine rich repeat receptor like
kinase, BRI1 - BR receptor insensitive 1, BAK1 - BRI1-associated receptor kinase 1, BIN2 - brassinosteroid insensitive 2,
BES1 - bril1 EMS-suppressor 1, BZR1 - brassinazole resistant 1, BSU1 - BRI1 suppressor 1, BIM2 - BES1-interacting-Myc-like 2.
Adapted from Yuzuf (2011).
Concluding remarks and future perspectives
The end of the 20th and particularly the beginning of the
21st centuries brought unquestionable evidence that BRs
have the ability to improve yield quantity and quality of
various crop species, and also to protect plants against
various kinds of stresses. However, although several
14
attempts to resolve the actual relationship between these
phytohormones and functioning various parts of the
photosynthetic apparatus have been made, our knowledge on the mode of BR actions in the regulation of
photosynthetic processes is still far from being complete.
BRASSINOSTEROIDS UNDER ABIOTIC STRESSES
So far, it seems that the main site of BR impacts on
photosynthesis is probably the photosynthetic carbon
reduction cycle and that BRs can perhaps somehow
affect the activation state of Rubisco. We can also
speculate about the possible effect of BRs on the activity
of carbonic anhydrase.
The challenges that we are expected to face in order
to elucidate the relationship between BRs and
photosynthesis are: 1) the detailed examination of
participation of these phytohormones in the development
of photosynthetically active chloroplasts; 2) the analysis
of the role of BRs in photosynthetic electron transfer;
3) the determination of BR influences on all enzymes
participating in photosynthetic CO2 fixation (not only in
plants with the C3 pathway but also with the C4 and
CAM pathways) to clarify whether this part of
photosynthesis really serves as the main target for the
action of BRs; 4) more comprehensive BR structure
analyses which provide reasons why some photosynthetic characteristics seem to be affected only by a
specific BR type; 5) to answer a question why the effect
of BRs on photosynthesis is more pronounced in plants
subjected to unfavourable environmental factors;
6) more frequent utilization of modern methods of
molecular and cell biology including various “omics”
technologies to enhance our knowledge on BR roles in
the regulation of photosynthesis at the cellular level.
New information on the interconnection between BRs,
photosynthesis, and radiation is also necessary to
improve our understanding the complex network of
regulating pathways involving these phytohormones.
Moreover, the knowledge of the physical and chemical
properties of these steroids allures us to consider them as
a highly promising and environment friendly promoter
of agricultural productivity and a potent stress alleviator.
One of the major constraints to employ brassinosteroids
at larger scale in the fields is their high cost. However,
recent progress in the chemical synthesis of brassinosteroids and their analogs has led us to economically
feasible approaches that has brought large scale
applications very near to the reach of farmers for
improving yields.
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