Received: 8 December 2017 Revised: 11 May 2018 Accepted: 30 May 2018

DOI: 10.1111/pce.13364

REVIEW

Strigolactones in plant adaptation to abiotic stresses: An

emerging avenue of plant research
Mohammad Golam Mostofa1‡ | Weiqiang Li2 | Kien Huu Nguyen2 | Masayuki Fujita3 |

Lam‐Son Phan Tran4

1
Department of Biochemistry and Molecular
Biology, Bangabandhu Sheikh Mujibur Abstract
Rahman Agricultural University, Gazipur, Phytohormones play central roles in boosting plant tolerance to environmental
Bangladesh
2
stresses, which negatively affect plant productivity and threaten future food security.
Stress Adaptation Research Unit, RIKEN
Center for Sustainable Resource Science, Strigolactones (SLs), a class of carotenoid‐derived phytohormones, were initially dis-
Yokohama, Japan
covered as an “ecological signal” for parasitic seed germination and establishment of
3
Laboratory of Plant Stress Responses,
Department of Applied Biological Science,
symbiotic relationship between plants and beneficial microbes. Subsequent character-
Faculty of Agriculture, Kagawa University, izations have described their functional roles in various developmental processes,
Miki, Japan
4
including root development, shoot branching, reproductive development, and leaf
Plant Stress Research Group & Faculty of
Applied Sciences, Ton Duc Thang University, senescence. SLs have recently drawn much attention due to their essential roles in
Ho Chi Minh City, Vietnam; Stress Adaptation the regulation of various physiological and molecular processes during the adaptation
Research Unit, RIKEN Center for Sustainable
Resource Science, Yokohama, Japan of plants to abiotic stresses. Reports suggest that the production of SLs in plants is
Correspondence strictly regulated and dependent on the type of stresses that plants confront at vari-
Lam‐Son Phan Tran, Plant Stress Research
ous stages of development. Recently, evidence for crosstalk between SLs and other
Group & Faculty of Applied Sciences, Ton Duc
Thang University, Ho Chi Minh City, Vietnam; phytohormones, such as abscisic acid, in responses to abiotic stresses suggests that
Stress Adaptation Research Unit, RIKEN
SLs actively participate within regulatory networks of plant stress adaptation that
Center for Sustainable Resource Science,
Yokohama, Japan. are governed by phytohormones. Moreover, the prospective roles of SLs in the man-
Email: sontran@tdt.edu.vn; son.tran@riken.jp
agement of plant growth and development under adverse environmental conditions
Present Address
‡
Stress Adaptation Research Unit, RIKEN have been suggested. In this review, we provide a comprehensive discussion
Center for Sustainable Resource Science, 1‐7‐ pertaining to SL‐mediated plant responses and adaptation to abiotic stresses.
22, Suehiro‐cho, Tsurumi, Yokohama 230‐
0045, Japan.
KEY W ORDS

abiotic stress adaptation, hormonal crosstalk, nutrient deficiency, osmotic stress, plant architecture,
Funding information
Japan Society for the Promotion of Science, strigolactones, symbiosis
Grant/Award Number: 17K07459; Institute of
Physical and Chemical Research, Japan

1 | I N T RO D U CT I O N and molecular changes (Abdelrahman, Jogaiah, Burritt, & Tran, 2018;

Plants encounter multiple environmental stresses during their entire
life cycles. These environmental constraints, both biotic and abiotic,
are the leading causes of crop loss and are threats to sustainable agri-
culture and ecological purposes worldwide (Abdelrahman, Burritt, &
Tran, 2017; AbuQamar, Moustafa, & Tran, 2017; Millar & Bennett,
2016; Pandey, Irulappan, Bagavathiannan, & Senthil‐Kumar, 2017;
Suzuki, Rivero, Shulaev, Blumwald, & Mittler, 2014; Zhu, 2016). As a
survival strategy, plants have evolved various responses to adverse
conditions by triggering a series of morpho‐physiological, biochemical,
W. Li et al., 2017; Mostofa et al., 2015; Mostofa et al., 2018; Suzuki
et al., 2014), all of which are perceived and controlled by signal trans-
duction and reprogramming of genetic and metabolic pathways. Phy-
tohormones are integral components for the coordination of such
changes to generate sophisticated responses in order to optimize
plant growth and development under stress conditions (Abdelrahman,
El‐Sayed, Jogaiah, Burritt, & Tran, 2017; Choudhary, Yu, Yamaguchi‐
Shinozaki, Shinozaki, & Tran, 2012; S. Ha, Vankova, Yamaguchi‐
Shinozaki, Shinozaki, & Tran, 2012; W. Li, Herrera‐Estrella, & Tran,
2016; Wani, Kumar, Shriram, & Sah, 2016). Many exciting findings,

Plant Cell Environ. 2018;41:2227–2243. wileyonlinelibrary.com/journal/pce © 2018 John Wiley & Sons Ltd 2227

2228
particularly the identification of receptors and downstream signalling
components involved in signal transduction and crosstalk of phytohor-
mones, resulted in major breakthroughs which have increased our
understanding regarding the molecular mechanisms of how plants
respond to their growth environment.
Strigolactones (SLs) were first discovered approximately 60 years
ago in the root exudates of cotton plants (Cook, Whichard, Turner,
Wall, & Egley, 1966) and were identified as potent communicators
between host plants and root parasitic weeds of the genera Striga,
Phelipanche, Alectra, and Orobanche (Yoneyama, Awad, Xie, Yoneyama,
& Takeuchi, 2010). Upon exudation from the roots of host plants, SLs
act as chemical signals to induce the germination of nondormant seeds
of parasitic plants, enabling them to infect hosts to obtain their nutri-
ents, water, and other assimilates. This parasitism‐stimulating behav-
iour of SLs is a significant agricultural threat in sub‐Saharan Africa,
Asia, Europe, and the Americas, resulting in devastating annual yields
to many important crops, such as sorghum (Sorghum bicolor), maize
(Zea mays), pearl millet (Pennisetum glaucum), and legumes (Parker,
2009; Yoneyama et al., 2010; Zwanenburg, Mwakaboko, & Kannan,
2016). Since then, intensive research has been carried out to under-
stand why host plants release SLs into the rhizosphere to benefit
these parasites. Just a decade ago, it was discovered that SLs can also
function as a host‐derived signal for stimulating hyphal branching to
establish a beneficial relationship between plants and arbuscular
mycorrhizal (AM) fungi (AMFs; Akiyama, Matsuzaki, & Hayashi,
2005). This symbiotic relationship allows approximately 80% of the
land plants to be benefitted by obtaining minerals and nutrients for
their optimal growth, especially under nutrient‐deprived environments
(Smith, Jakobsen, Grønlund, & Smith, 2011; Smith & Read, 2008).
As mutants of SL biosynthesis and signalling became available
over the last decade (e.g., mutants with mutation in MORE AXILLARY
GROWTH [MAX] genes in Arabidopsis thaliana, DWARF [D] genes in
rice [Oryza sativa], RAMOSUS [RMS] genes in pea [Pisum sativum],
and DECREASED APICAL DOMINANCE [DAD] genes in Petunia hybrida),
various loss‐of‐function studies have reported the involvement of SLs
in many aspects of plant development, particularly in the regulation of
root system architecture, branching, photo‐morphogenesis, early
seedling development, secondary growth, and leaf senescence
(Brewer, Koltai, & Beveridge, 2013; Kapulnik, Delaux, et al., 2011;
Toh et al., 2012; Ueda & Kusaba, 2015; Umehara et al., 2008;
Urquhart, Foo, & Reid, 2015). Genetic studies also provided evidence
that the biosynthesis of SLs is regulated by various abiotic stresses,
including nutrient deprivation, drought, and salinity (Du et al.,
2018; C. V. Ha et al., 2014; Lv et al., 2018; H. Sun et al., 2014;
Umehara, Hanada, Magome, Takeda‐Kamiya, & Yamaguchi, 2010;
Visentin et al., 2016; Zhuang, Wang, & Huang, 2017). These findings
collectively provided important clues regarding the potential of SLs
in regulating plant responses and adaptation to environmental
stresses. Thus, an increasing number of studies have recently
focused on the implications of SLs in the adaptation of plants to
environmental constraints and have reported many novel findings
(Bu et al., 2014; Cooper et al., 2018; C. V. Ha et al., 2014; Liu
et al., 2015; Lv et al., 2018; Ma et al., 2017; Ruiz‐Lozano et al.,
2016; Umehara et al., 2010; Visentin et al., 2016; Y. Zhang, Lv, &
Wang, 2018). Moreover, the connection of SLs in AM symbiosis‐
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MOSTOFA ET AL.
mediated improvement of physiological responses has also been
reported in plants under abiotic stresses, such as high salinity and
drought (Aroca et al., 2013; Ruiz‐Lozano et al., 2016). Collectively,
the results of these studies highlight the key insights into how SLs
can assist plants to confront adverse environmental stresses by act-
ing as both rhizospheric and endogenous signals (Andreo‐Jimenez,
Ruyter‐Spira, Bouwmeester, & Lopez‐Raez, 2015; Cardinale, Korwin
Krukowski, Schubert, & Visentin, 2018; Koltai & Kapulnik, 2011;
López‐Ráez, 2016; López‐Ráez, Shirasu, & Foo, 2017).
Because many previous reviews have described SL biosynthesis,
signalling, and perception in detail (Al‐Babili & Bouwmeester, 2015;
Lopez‐Obando, Ligerot, Bonhomme, Boyer, & Rameau, 2015; Lumba,
Holbrook‐Smith, & McCourt, 2017; Morffy, Faure, & Nelson, 2016;
Waters, Gutjahr, Bennett, & Nelson, 2017), in this review, we will only
briefly cover SL biosynthesis and signalling. Subsequently, exclusive
focus will be given to the putative mechanisms of SLs in regulating
plant adaptation to abiotic stresses, particularly nutrient deficiency,
drought, and salinity. In addition, we will also update readers with
the latest findings on SL interactions with environmental stimuli in
the presence or absence of symbiosis. Lastly, crosstalk between SLs
and other phytohormones, such as abscisic acid (ABA), auxin, ethylene
(ET), and cytokinin (CK), during plant responses to environmental
stresses will also be briefly discussed.
2 | SL BIOSYNTHESIS AND SIGNAL
T R A N S D U C T I O N I N P LA N T S
SLs are a group of apocarotenoid‐class compounds (Matusova et al.,
2005), which are sequentially derived from carotenoids by the
action of a series of enzymes localized in plastids and cytosol
(Figure 1a). The consecutive steps involving isomerization by plastidal
β‐carotene isomerase (D27 in rice and A. thaliana D27 [AtD27] in
Arabidopsis) and oxidative cleavages by CAROTENOID CLEAVAGE
DIOXYGENASE7 (CCD7) and CCD8 (D17 and D10 in rice and
MAX3 and MAX4 in Arabidopsis, respectively) convert all‐trans‐β‐
carotene to carlactone (CL), the key intermediate for the production
of various SLs (Alder et al., 2012; Seto et al., 2014). CL mainly serves
as a precursor of canonical (having tricyclic lactone [ABC‐ring] linked
to butenolide group [D‐ring]) or noncanonical (lacking ABC‐ring but
having enol‐ether D ring linked to a variety of structures) SLs in
the cytosol, possibly depending on plant species. In rice, CL is
oxidized to orobanchol, a canonical SL, by the sequential actions of
two homologues of the Arabidopsis cytochrome P450 enzyme
MAX1, namely, CL oxidase (Os01g0700900) and orobanchol synthase
(Os01g0701400; Figure 1a; Y. X. Zhang et al., 2014). On the other
hand, MAX1 functions as CL oxidase that converts CL to carlactonoic
acid (CLA) in Arabidopsis (Abe et al., 2014; Brewer et al., 2016). A yet‐
unknown methyl transferase then methylates CLA to produce methyl
CLA that is subsequently transformed into an unknown SL‐like
compound by LATERAL BRANCHING OXIDOREDUCTASE (Brewer
et al., 2016).
The core components of the SL signal transduction pathway
include both activators (D14 and D3 in rice, corresponding to AtD14
and MAX2 in Arabidopsis) and repressors (D53 and SUPPRESSOR
 13653040, 2018, 10, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/pce.13364 by Readcube (Labtiva Inc.), Wiley Online Library on [10/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MOSTOFA ET AL. 2229

(a) (b)
all-trans-

D27/AtD27 (Isomerase)
C
A B D14/
AtD14
9-cis
D

D17/MAX3 (CCD7)

SCF
9-cis
E2
D10/MAX4 (CCD8)
D3/MAX2

4/
D1 D14
Carlactone At D53/
(CL) SMXL6,7,8
Os01g0700900
MAX1 (P450)
(CL oxidase)

Expression
ent-2’-epi-5-
deoxystrigol
Carlactonoic
Os01g0701400 acid (CLA)
DNA
(Orbanchol oxidase)
Me-O Shoot branching and angling, leaf senescence,
stem thickening, shoot and root development,
Methyl carlactonoate environmental stress responses
(MeCLA)
Orobanchol
LBO

Unidentified SL-like
compound (MeCLA+16Da)

FIGURE 1 Strigolactone (SL) biosynthesis and signal transduction pathways in rice (Oryza sativa) and Arabidopsis thaliana. (a) Current model of SL
biosynthesis: in plastids, the common SL precursor carlactone (CL) is synthesized from all‐trans‐β‐carotene by the sequential actions of the
enzymes DWARF27 (D27), D17, and D10 in rice, corresponding to A. thaliana D27 (AtD27), MORE AXILLARY GROWTH3 (MAX3), and MAX4 in
Arabidopsis. In the cytosol, CL oxidase (Os01g0700900) and orobanchol synthase (Os01g0701400) then convert CL into SLs in the case of rice,
whereas in Arabidopsis, the consecutive actions of cytochrome P450 MAX1, an unknown enzyme and LATERAL BRANCHING
OXIDOREDUCTASE (LBO), transform CL into carlactonic acid (CLA), methyl carlactonic acid (MeCLA), and finally, an unidentified SL‐like
compound (MeCLA+16 Da). (b) Current concept on SL perception and signalling: SLs are perceived though their interactions with an α/β‐hydrolase
receptor (D14 and AtD14 in rice and Arabidopsis, respectively). This ligand–receptor interaction triggers a conformational change in D14/AtD14,
which is suitable for interaction with the D3/MAX2‐based Skp1–Cullin–F‐box (SCF) complex (D3 and MAX2 in rice and Arabidopsis, respectively).
The newly formed protein complex triggers the ubiquitination of D53/SUPPRESSOR OF MAX2 1‐LIKEs (SMXLs; D53 and SMXLs identified in rice
and Arabidopsis, respectively), followed by proteasome‐mediated degradation, thereby initiating the SL signalling pathway leading to the
expression of genes involved in various physiological functions. U: ubiquitin; CCD: carotenoid cleavage dioxygenase

OF MAX2 1‐LIKE6, 7, and 8 [SMXL6, 7, and 8] in rice and Arabidopsis,
respectively; Figure 1b; Jiang et al., 2013; Wang et al., 2015; Waters
et al., 2017; Zhou et al., 2013). The perception of SL signalling starts
with the binding of SLs to the “open state” pocket of D14/AtD14, an
α/β‐hydrolase receptor (Arite et al., 2009; Yao et al., 2016). Upon bind-
ing, D14/AtD14 catalyses the removal of the ABC‐ring, allowing the D‐
ring to remain closely and irreversibly bound to the catalytic cavity of
D14/AtD14 (Figure 1b). Meanwhile, a conformational change in D14/
AtD14 results in a “closed state,” which induces its interaction with
the D3/MAX2‐based Skp1–Cullin–F‐box complex (Yao et al., 2016).
The newly formed protein complex polyubiquitinates transcriptional
repressors D53/SMXL6/7/8, thereby triggering 26S proteasome‐
mediated degradation of D53/SMXL6/7/8 that allows the expression
of SL‐responsive genes for various physiological functions (Figure 1b;
Waters et al., 2017; Yao et al., 2016). For instance, it has recently been
reported in rice that IDEAL PLANT ARCHITECTURE1, a SQUAMOSA
PROMOTER BINDING PROTEIN‐LIKE transcription factor, acts as a
direct downstream target of D53 in regulating tiller development and
SL‐mediated gene expression (Song et al., 2017).
3 | S L P R O D U CT I O N I N P L A N T S U N D E R
A B I O T I C ST R E S S E S
SLs are produced and exuded at extremely low quantities, being active
at pico‐ to nanomolar concentrations, and have been reported in a
variety of plant species (Andreo‐Jimenez et al., 2015; Delaux et al.,
2012; Xie, 2016). A single plant species can produce various types of
SLs, and even different varieties of the same plant species appear to
synthesize a blend of SL molecules in different quantities (Ruyter‐
Spira, Al‐Babili, van der Krol, & Bouwmeester, 2013; Xie, Yoneyama,
& Yoneyama, 2010). A large body of evidence has demonstrated that
plants modulate SL concentrations differently, according to various
types of abiotic stress (Table 1).
 TABLE 1 Strigolactone (SL) production and expression of SL biosynthesis‐related genes in various plant species under different abiotic stress conditions in the presence or absence of symbiosis

2230
Expression of
Plant species Type of stress Site of SL detection Names of SL compounds SL‐biosynthetic genes SL effects studied on References

Sorghum LP and LN Root tissues and (↑)5‐deoxystrigol NA Germination activity Yoneyama, Xie, et al. (2007)
(Sorghum bicolor) root exudates
Red clover LP Root exudates (↑)Orobanchol NA Germination activity Yoneyama, Yoneyama,
(Trifolium pretense) et al. (2007)
Tomato LP Root exudates (↑)Orobanchol, solanacol, and NA Germination activity and López‐Ráez et al. (2008)
(Solanum lycopersicum) didehydroorobanchol isomers hyphal branching
Rice (Oryza sativa) LP Root tissues and (↑)2′‐epi‐5‐deoxystrigol (↑)D10, D17, D27, Inhibition of tiller Umehara et al. (2010)
root exudates Os01g0700900, and bud outgrowth
Os01g0221900
Arabidopsis thaliana LP Root exudates and (↑)Orobanchol NA Axillary shoot branching Kohlen et al. (2011)
xylem sap
Rice (O. sativa) LP and LN Root exudates (↑)Orobanchol, 2′‐epi‐5‐ NA Germination activity Jamil et al. (2011)
deoxystrigol
Tomato Light Root tissues (↑)Solanacol, orobanchol, and (↑)SlCCD7 Light responses Koltai et al. (2011)
(S. lycopersicum) didehydro‐orobanchol isomers
Pea (Pisum sativum) HP Root exudates (↓)Fabacyl acetate and NA Regulation of AMF symbiosis Balzergue et al. (2011)
orobanchyl acetate
Alfalfa (Medicago sativa) LP Root exudates (↑)Orobanchol and NA Plant growth Yoneyama et al. (2012)
orobanchyl acetate
Chinese milk vetch LP and LN Root exudates (↑)Sorgomol and 5‐deoxystrigol NA Plant growth Yoneyama et al. (2012)
(Astragalus sinicus)
Marigold LP and LN Root exudates (↑)Orobanchol and NA Plant growth Yoneyama et al. (2012)
(Tagetes patula) orobanchyl acetate
Wheat LP and LN Root exudates (↑)Orobanchol NA Plant growth Yoneyama et al. (2012)
(Triticum aestivum)
Lettuce LP and LN Root exudates (↑)Orobanchol and NA Plant growth Yoneyama et al. (2012)
(Lactuca sativa) orobanchyl acetate
Tomato LP Root exudates (↑)Orobanchol NA Plant growth Yoneyama et al. (2012)
(S. lycopersicum)
Lettuce (L. sativa) Salinity Root extracts Total SLs (by germination NA Salt responses Aroca et al. (2013)
activity)
Pea (P. sativum) LP and LN Root exudates (↑)Fabacyl acetate and NA Mycorrhizal development Foo et al. (2013)
orobanchyl acetate and nodulation
Rice (O. sativa) LP and LN Root exudates (↑)Orobanchol, orobanchyl (↑)D10, D17, and D27 Root development H. Sun et al. (2014)
acetate, and 2′‐epi‐
5‐deoxystrigol
Rice (O. sativa) LP Root extracts (↑)ent‐2′‐epi‐5‐deoxystrigol (↑)Os01g0700900 Parasitic seed germination Cardoso et al. (2014)
and shoot branching
A. thaliana Dehydration Leaf tissues ND (↑)MAX3 and MAX4 Osmotic stress responses C. V. Ha et al. (2014)
and salinity
MOSTOFA

(Continues)
ET AL.

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 MOSTOFA
ET AL.

TABLE 1 (Continued)

Expression of
Plant species Type of stress Site of SL detection Names of SL compounds SL‐biosynthetic genes SL effects studied on References
Lotus japonicus LP Root exudates and (↑)5‐deoxystrigol (↑)LjD27, LjCCD7, Osmotic stress responses Liu et al. (2015)
root tissues and LjCCD8
L. japonicus PEG Root exudates and (↓)5‐deoxystrigol (↓)LjD27, LjCCD7, Osmotic stress responses Liu et al. (2015)
root tissues and LjCCD8
A. thaliana Heat, UV, and Root tissues ND (↑)MAX 3 Abiotic stress responses Marzec and Muszynska (2015)
wounding
A. thaliana Salinity Root tissues ND (↓)AtD27 Salinity responses Marzec and Muszynska (2015)
Chrysanthemum LP Root exudates and Chrysanthemum SL analogues (↑)DgCCD7 Shoot branching under P Xi et al. (2015)
(Dendranthema whole plant starvation
grandiflorum)
Tomato Drought with AMF Root extracts (↑)Solanacol and didehydro‐ (↑)SlCCD7 Drought responses and Ruiz‐Lozano et al. (2016)
(S. lycopersicum) orobanchol isomers 1 and 2 AMF symbiosis
Tomato Drought Root extracts (↓)Solanacol and didehydrooro‐ (↓)SlCCD7 Drought responses Ruiz‐Lozano et al. (2016)
(S. lycopersicum) banchol isomers 1 and 2
Alfalfa (M. sativa) LP and HN with Root extracts (↑) Orobanchol and NA Rhizobium‐legume symbiosis Peláez‐Vico et al. (2016)
Rhizobium orobanchyl acetate under nutrient shortage
A. thaliana LN Root tissues ND (↑)MAX3 and MAX4 Leaf senescence and Ito et al. (2016)
plant growth
Tomato Drought Shoot tissues ND (↑)SlCCD7 and SlCCD8 Drought responses Visentin et al. (2016)
(S. lycopersicum)
Tomato Drought Root tissues (↓)Solanacol, orobanchol, and (↓)SlCCD7 and SlCCD8 Drought responses Visentin et al. (2016)
(S. lycopersicum) didehydroorobanchol isomer
A. thaliana Salinity and Leaf tissues Not detected (↑)MAX3 and MAX4 Osmotic stress on stomatal Lv et al. (2018)
mannitol closure
Tall fescue Drought Crowns (↑)Total SLs (by ELISA) (↑)FaD17 Drought responses and Zhuang et al. (2017)
(Festuca arundinacea) axillary bud development
Sesbania cannabina Salinity with AMF Root extracts (↑)Total SLs (by germination NA Crosstalk with H2O2 and Kong et al. (2017)
activity) salt tolerance
Soybean (Glycine max) Dark chilling Root tissues ND (↓)GmCCD8 Chilling tolerance Cooper et al. (2018)
Rice (O. sativa) Drought Stem base ND (↓)D10, D14, D17, and D27 Drought escape and tillering Du et al. (2018)

Note. AMF: arbuscular mycorrhizal fungus; LP: low phosphorus; LN: low nitrogen; HN: high nitrogen; PEG: polyethylene glycol; ND: not determined; NA: not analysed; (↑): increased; (↓): decreased; D: DWARF; MAX:
MORE AXILLARY GROWTH; CCD: CAROTENOID CLEAVAGE DIOXYGENASE; ELISA: enzyme‐linked immunosorbent assay.
2231

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2232
3.1 | SL biosynthesis and production in plants under
nutrient‐deficiency stress
Nitrogen (N) and phosphorus (P), the two most limiting macronutrients
for plant growth in natural environment, maintain an intricate relation-
ship with SL production and exudation which is dependent upon the
type of plant species and nutrient availability in soils. Under P‐
deficient conditions, the majority of plant species promote SL produc-
tion in roots. For instance, P deficiency enhances SL exudation from
the roots of a range of plant species, including red clover (Trifolium pre-
tense), lettuce (Lactuca sativa), tomato (Solanum lycopersicum), wheat
(Triticum aestivum), marigold (Calendula officinalis), alfalfa (Medicago
sativa), sorghum, rice, and Lotus japonicus (Table 1; Jamil et al., 2011;
Liu et al., 2015; López‐Ráez et al., 2008; H. Sun et al., 2014; Umehara
et al., 2010; Yoneyama et al., 2012; Yoneyama, Xie, et al., 2007;
Yoneyama, Yoneyama, Takeuchi, & Sekimoto, 2007). In the case of
N deficiency, elevated levels of SLs were identified in the roots of sev-
eral species, including Chinese milk vetch (Astragalus sinicus), rice, let-
tuce, sorghum, wheat, and pea (Foo, Yoneyama, Hugill, Quittenden, &
Reid, 2013; Jamil et al., 2011; Yoneyama et al., 2012; Yoneyama, Xie,
et al., 2007; Yoneyama, Yoneyama, et al., 2007). On the other hand,
the production of SLs was almost unaffected by N deficiency in red
clover, alfalfa, and tomato roots (Yoneyama et al., 2012; Yoneyama,
Yoneyama, et al., 2007), suggesting that these plant species might
use different strategies for regulating SL levels in the roots in response
to N and P deficiencies. It has also been observed that N‐deficiency
stress reduced P content in the shoots of Chinese milk vetch, which
in turn enhances SL production and exudation from the roots, implying
that P status in shoots regulates SL levels in roots under N‐starvation
conditions (Yoneyama et al., 2012). Interestingly, deficiency in either N
or P induced a slight decrease, rather than increase, in SL exudation
from roots of white lupin (Lupinus albus; Yoneyama et al., 2008), sug-
gesting that being a nonmycorrhizal plant, white lupin might have
different adaptive strategies independent of SLs to cope with N‐ or
P‐deficient conditions.
SLs are mainly produced by the roots, and that their production in
the roots is much higher than in the aerial tissues under normal growth
conditions (Brewer et al., 2013; Visentin et al., 2016; Xie, 2016; Xie
et al., 2010). In contrast to roots, little and no effects on SL contents
were observed in the shoots of L. japonicus and sorghum, respectively,
under P‐deficient (L. japonicus) or P‐deficient and N‐deficient
(sorghum) conditions (Liu et al., 2015; Yoneyama, Yoneyama, et al.,
2007). These data indicate that nutrient deficiency upregulates SL
levels primarily in roots rather than in aboveground organs, at least
in the case of L. japonicus and sorghum. In accordance to these find-
ings, a study in chrysanthemum (Dendranthema grandiflorum) also
showed that P deficiency led to an increased level of SLs in roots
followed by that in basal and upper stems of chrysanthemum (Xi
et al., 2015). It should be noted that SL contents in roots can also be
modified by shoot‐derived signals that are dependent on the status
of N and P levels in shoots (Yoneyama et al., 2015). Intriguingly, simul-
taneous starvation in both P and N has lower effects on SL exudation
from roots of sorghum when compared with N or P starvation alone
(Yoneyama, Yoneyama, et al., 2007). Depletion of both N and P caused
a lower secretion of SLs from roots of rice and alfalfa than P deficiency
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MOSTOFA ET AL.
alone (Table 1; Jamil et al., 2011; Peláez‐Vico, Bernabéu‐Roda, Kohlen,
Soto, & López‐Ráez, 2016). It is plausible that this discrepancy in SL
production under the combined N and P deficiency might be ascribed
to excessive stress burden, leading to reduced plant vigor for the pro-
duction of SLs in roots.
Consistent with the increase in SL content, the transcript levels of
SL‐biosynthetic genes D10, D17, and D27 in rice roots were enhanced
under either N or P starvation in comparison with sufficient conditions
(Table 1; H. Sun et al., 2014), indicating that nutrient deficiency affects
SL production by regulating the expression of SL biosynthesis‐related
genes. Interestingly, under the same conditions, the transcript levels of
signalling genes D3 and D14 were decreased in rice roots (H. Sun
et al., 2014). A recovery experiment also showed that in accordance
to the reduced levels of SLs in roots, the transcript abundance of
several SL‐biosynthetic genes, such as D10, D17, D27, and
Os01g0700900, sharply decreased within 24 hr of transfer of rice
plants from P‐deficient to P‐sufficient medium (Umehara et al.,
2010). However, upon changing the P level in the growth medium,
the transcript level of the SL‐signalling gene D14 increased, whereas
that of D3 remained almost unchanged in roots (Umehara et al.,
2010). Taken together, these results may indicate that P availability
in the growth medium has a strict control over SL biosynthesis rather
than SL signal transduction at the gene level to facilitate the switch of
P acquisition strategies of plants (Czarnecki, Yang, Weston, Tuskan, &
Chen, 2013). Additionally, N‐deficient conditions also upregulate the
transcript levels of MAX3 and MAX4 in Arabidopsis roots (Ito et al.,
2016), which might suggest that SLs accumulate in N‐deficient root
tissues of Arabidopsis. Enhanced expression of the SL transporter‐
encoding gene PLEIOTROPIC DRUG RESISTANCE1 (PDR1), which is
required for root‐to‐shoot translocation of SLs (Sasse et al., 2015),
was also observed in roots of petunia and L. japonicus under P‐
deficient conditions (Kretzschmar et al., 2012; Liu et al., 2015). These
data suggest that there might be a systemic transfer of root‐produced
SLs to shoots under nutrient stress. Collectively, these findings
support the supposition that the expression levels of genes involved
in SL‐biosynthesis and SL‐transportation positively correlate with
nutrient deficiency‐induced SL production in roots.
3.2 | SL biosynthesis and production under osmotic‐
related stresses
Unlike nutrient‐shortage stresses, osmotic‐related stresses, such as
salinity and drought, negatively regulate SL production in the roots
of dicot plants, including tomato, lettuce, and L. japonicus (Aroca et al.,
2013; Liu et al., 2015; Ruiz‐Lozano et al., 2016). Polyethylene glycol
(PEG)‐mediated osmotic stress reduced the levels of SLs in both root
tissues and exudates of L. japonicus, which was further confirmed by
quantifying the transcript levels of SL‐biosynthetic genes LjD27,
LjCCD7 and LjCCD8, and LjPDR1 in the roots (Table 1; Liu et al.,
2015). Furthermore, this PEG‐induced reduction in the SL levels was
observed in either the presence or absence of P (Liu et al., 2015),
indicating that PEG‐mediated osmotic stress responses override P‐
deficiency responses in terms of SL production in L. japonicus roots.
In tomato, the drought‐reduced levels of SLs in roots were also posi-
tively correlated with the downregulation of SL‐biosynthetic gene

MOSTOFA ET AL.
SlCCD7 in the same organ (Ruiz‐Lozano et al., 2016). Similarly, Visentin
et al. (2016) reported that the transcript abundance of SL‐biosynthetic
genes SlCCD7 and SlCCD8 and SL levels were decreased in tomato
roots under drought. In contrast, an increase in the levels of SLs was
observed in rice roots in response to a water withholding‐induced
drought (Haider et al., 2018). The discrepancy in SL production in
roots might be ascribed to the different methods of drought
treatment and the different levels of drought imposed. Moreover,
there might be a difference in SL production in monocots and dicots
under drought, which could be confirmed in future by comparing SL
levels in the monocots and dicots under the same experimental
setup. On the other hand, the transcript levels of the SL‐biosynthetic
genes D27 and MAX1‐homologues Os01g0701400, Os01g0700900,
Os02g0221900, and Os06g0565100 were upregulated in rice shoots,
as was observed for SlCCD7 and SlCCD8 in the case of tomato (Haider
et al., 2018; Visentin et al., 2016). These data were in agreement with
the detection of increased transcript levels of SL‐biosynthetic
genes MAX3 and MAX4 in the leaves of Arabidopsis upon dehydration
(C. V. Ha et al., 2014) and NaCl and mannitol treatments (Lv et al.,
2018), as well as with the upregulation of the SL‐biosynthetic FaD17
gene in the crowns of tall fescue (Festuca arundinacea) and the D10,
D17, and D27 genes in the base of rice stems under drought stress
(Table 1; Du et al., 2018; Zhuang et al., 2017). Collectively, these find-
ings suggest that the induction of SL synthesis in the aboveground
organs of plants is triggered in response to osmotic stress. Unfortu-
nately, at the present time, this cannot be thoroughly investigated
because it is not possible to accurately quantify SLs with existing tech-
nology due to their extremely low endogenous levels in shoots (Liu
et al., 2015; Umehara et al., 2010; Xie et al., 2015). Nevertheless, a
study under high‐light intensity conditions reported an increase in SL
accumulation, as observed under P deficiency, and upregulation of
SlCCD7 gene in tomato roots (Koltai et al., 2011). Taken together,
these data signify that the alteration in SL synthesis in roots is depen-
dent upon the various type of stresses that plants are exposed to.
Under osmotic stresses, such as drought and salinity, it is apparent
that SL levels are commonly reduced in roots of dicot plants and that
this drop in SL production may send a systemic signal to their above-
ground parts to trigger local synthesis of SLs (Cardinale et al., 2018;
Visentin et al., 2016). Additionally, the upregulation of SL‐biosynthetic
genes in aboveground organs of different plant species might suggest
that SLs play an active role in the acclimatization of aboveground
organs to osmotic‐related stresses, which functions to increase plant
survivability under such stress conditions.
4 | SLs AND SYMBIOSIS: CURRENT
UNDERSTANDING DURING PLANT
RESPONSES AND ADAPTATION TO ABIOTIC
S T R E S SE S
SLs have been well recognized as an important mediator of plant inter-
actions with several (micro) organisms, especially soil‐grown AMFs
during responses to stress exposure under adverse environmental
conditions (Akiyama et al., 2005; López‐Ráez et al., 2017; López‐Ráez,
Charnikhova, Fernández, Bouwmeester, & Pozo, 2011; López‐Ráez,
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2233
Pozo, & García‐Garrido, 2011; Marzec, Muszynska, & Gruszka,
2013). Under optimal growth conditions, both SL production and
AM colonization in plants are absent or found at very low concentra-
tions (Aroca et al., 2013; Umehara et al., 2010; Yoneyama, Yoneyama,
et al., 2007). Under nutrient limiting conditions (mainly P and N defi-
ciencies), several studies using mutants defective in SL biosynthesis
and SL exudation provided evidence that root colonization with AMFs
in the mutants was lower than what was observed in wild‐type (WT;
Balzergue, Puech‐Pagès, Bécard, & Rochange, 2011; Breuillin et al.,
2010; Foo et al., 2013; Gomez‐Roldan et al., 2008; Kohlen et al.,
2011; Kohlen et al., 2012; Kretzschmar et al., 2012; van Zeijl
et al., 2015; Yoshida et al., 2012). On the other hand, elevated levels
of SLs in pea roots under either low‐N or low‐P levels, and in roots
of petunia under low‐P levels, correlated with improvement of AM
colonization (Balzergue et al., 2011; Breuillin et al., 2010; Foo et al.,
2013). These findings demonstrate that SLs are implicated in AM col-
onization under nutrient‐deficiency stress as positive regulators. In
comparison with low‐P levels, petunia plants displayed a decreasing
trend in fungal colonization in relation to the reduction in the SL‐
biosynthetic gene DAD1 expression in roots under high‐P conditions
(Breuillin et al., 2010). These observations initially suggested that the
transcriptional repression of SL genes (e.g., DAD1) may serve as a
key regulatory process to reduce AM root colonization under high‐P
conditions. However, the suppression of AM colonization by high‐P
conditions in WT pea and SL‐deficient dad1 mutant was not rescued
by the application of rac‐GR24 (Balzergue et al., 2011; Breuillin
et al., 2010), which is a synthetic SL analogue whose enantiomers in
the racemic mixture can activate both KAI2 and D14 pathways (De
Cuyper et al., 2017). Furthermore, Foo et al. (2013) reported that
SL‐deficient ccd8 pea mutant is less colonized than WT but still retains
a pattern of lower colonization under high P than low P, just like the
WT, suggesting that SLs are not essential for plants to show enhanced
mycorrhizal colonization under low‐P conditions, at least in pea. These
results indicate that SLs may not be the sole mediators of nutrient
deficiency‐induced AM colonization to host plants.
In the presence of AM symbiosis, enhancement of SL production
was also observed in roots under other abiotic stresses, such as in
roots of lettuce under salt stress and in roots of both lettuce and
tomato under drought (Aroca et al., 2013; Ruiz‐Lozano et al., 2016).
The increase of SLs in the roots of AM‐colonized plants under nutrient
and osmotic‐related stresses might have several beneficial aspects,
including (a) effective development of symbiosis to help plants cover
larger areas to uptake minerals and water and (b) promotion of physi-
ological responses, such as photosynthesis, to overcome the adverse
effects on growth and development of plants (Figure 2; Ruiz‐Lozano
et al., 2016). Moreover, the similar trend of SL production under nutri-
ent and osmotic‐related stresses in the presence of AMFs also sug-
gests that plants employ SLs potentially for the enhancement of
symbiosis irrespective of the types of stress they experienced
(Figure 2).
SLs can assist symbiotic relationships between plants and micro-
bial communities by activating several processes related to coloniza-
tion, including mitochondrial activity, spore germination, hyphal
branching, hyphopodium formation and bacterial motility in microbial
partner, and nodulation and root hair (RH) elongation in host plants

2234
Limited resource utilization
Balanced biomass production
Seed size
Stomatal
closure
Stem thickening Leaf
senescence
Inhibit extra
branching
SLs
SLs
Salinity
Salinity
AM
symbiosis
Drought
Drought
Nutrient
Nutrient
deficiency
deficiency
Water uptake
Mineral uptake
Nutrient uptake
Rhizobial
symbiosis
FIGURE 2 Proposed model for strigolactones (SLs)‐mediated plant
adaptation to abiotic stresses in the presence of symbiosis. When
arbuscular mycorrhizal fungi or rhizobial bacteria are present, plants
increase SL production and exudation in roots when they confront
abiotic stresses, such as drought, salinity, and nutrient shortage.
Elevated levels of SLs can modify the root system architecture by
increasing primary root length, root hair formation, and seminal root
development. These belowground roles of SLs permit plants to
explore more soil areas for water and nutrients under unfavourable
stress conditions. Under abiotic stress, SL contents in shoots may also
be increased in the presence of symbiosis due to the enhancement of
local production of SLs. The modulation of SL levels in the
aboveground may allow plants to achieve optimal biomass production
by maximizing the use of limited available resources. All of the
belowground and aboveground adjustments by symbiosis‐induced SL
production result in optimized plant adaptation to stresses. Dotted
arrows indicate processes that are known to be affected by SLs under
normal conditions, which may also be affected by symbiosis‐induced
SLs under stress conditions. Solid lines indicate positive roles of SLs
under stress conditions
(Akiyama et al., 2005; Besserer et al., 2006; De Cuyper et al., 2015;
Kobae et al., 2018; Mori, Nishiuma, Sugiyama, Hayashi, & Akiyama,
2016; Peláez‐Vico et al., 2016; Ruyter‐Spira et al., 2011). However,
direct evidence for the endogenous signalling role of SLs in AM
colonization is still lacking. In relative comparison with WT rice plants,
SL‐specific d14 signalling mutants showed an increase in AM coloniza-
tion (Gutjahr et al., 2015; Yoshida et al., 2012), whereas a reduction in
AM colonization was observed in mutants defective in the down-
stream SL‐signalling D3 (MAX2 orthologue in rice) and RMS4 (MAX2
orthologue in pea) genes (Foo et al., 2013; Gutjahr et al., 2015;
Yoshida et al., 2012). These findings indicate that AM colonization
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MOSTOFA ET AL.
requires D3/RMS4/MAX2, which is a checkpoint of both SL‐ and
karrikin‐like (KL) compound‐mediated signalling pathways (Morffy
et al., 2016), independently of the SL‐specific D14. Furthermore,
severe disruption in AM colonization was observed in the rice d14‐like
(D14‐like being the KAI2 orthologue in rice) but not in d14 mutant
plants (Gutjahr et al., 2015). These data suggest that the KAI2‐
MAX2 signalling pathway, rather than the SL‐associated D14‐MAX2
pathway, is involved in AM colonization. A recent study demonstrated
that the levels of AM colonization in the SL‐biosynthetic d10 and d17
rice mutants were severely compromised due to attenuation in
hyphopodium formation, which is a process that is required for suc-
cessful entry of hyphae into the roots (Kobae et al., 2018). The authors
also reported that d10 and d17 mutants were not impaired in other
processes involved in AM colonization, including arbuscular develop-
ment, metabolic activities of infection units and epidermal penetration
(Kobae et al., 2018). Similarly, kai2 rice mutant are also blocked in AM
colonization due to lack of hyphopodia and intraradical penetration
(Gutjahr et al., 2015). It seems that both SLs and KL are necessary
for early stages of colonization processes in rice, such as tissue infec-
tion rather than epidermal penetration and colonization. These results
related to the roles of SL and KL signalling pathways in AM coloniza-
tion were observed in the monocot rice; however, the SL and KL
signalling pathways may have differential roles in dicots, which needs
to be clarified in future studies.
5 | SLs FINE‐TUNE PLANT ARCHITECTURES
U N D E R A B I O TI C S T R E S S E S
Numerous studies involving SL‐deficient and SL‐insensitive mutants
and the use of GR24 revealed that SLs can act as positive regulators
of RH elongation, primary root (PR) growth, and secondary shoot
growth. In addition, SLs are also capable of functioning as repressors
of lateral root (LR) formation, adventitious root development, and
auxiliary bud outgrowth (Agusti et al., 2011; Brewer et al., 2013;
Gomez‐Roldan et al., 2008; Kapulnik, Delaux, et al., 2011; Koltai,
2011; Rasmussen et al., 2012; Ruyter‐Spira et al., 2011; Umehara
et al., 2008). Under nutrient‐deprived states, such as starvation in N
and/or P or osmotic related stresses, such as drought, SLs can affect
a number of important aspects of below‐ and above‐ground plant
architectures as briefly discussed in the next two subsections.
5.1 | Effects of SLs on belowground structure of
plants under nutrient stresses
Several studies have reported a positive relationship between PR
length and SL production in rice, wheat, and tomato under P‐starved
conditions (Table 1; Jamil et al., 2011; Yoneyama et al., 2012). Simi-
larly, SLs were observed to be involved in elongation of crown roots
in rice under limited P resources (Arite, Kameoka, & Kyozuka, 2012).
Very recently, SLs were shown to be required for the nitric oxide
(NO)‐mediated signalling pathway for the elongation of rice seminal
roots under low‐P and low‐N conditions (H. Sun et al., 2016). In rice,
mutants defective in SL production (d10 and d27) or insensitive to
SLs (d3) exhibited decreased seminal root length under P‐limiting con-
ditions (Table 1; H. Sun et al., 2014), indicating that SLs act as positive

MOSTOFA ET AL.
regulators of seminal root development under this nutrient‐deficient
state. On the other hand, increased LR density was observed in all of
these SL‐related mutants in comparison with WT during P starvation,
suggesting that SLs negatively regulate LR development in rice under
low‐P stress (H. Sun et al., 2014). This negative effect on LR growth
was associated with SL‐mediated inhibition of polar auxin transport
from shoots to the roots (H. Sun et al., 2014). Interestingly, in
Arabidopsis, P deficiency resulted in an enhancement of LR density in
WT when compared with that of SL‐biosynthetic max1 and max4
mutants (Ruyter‐Spira et al., 2011), suggesting that endogenous SLs
in WT play key regulatory roles in triggering LR development in
response to low‐P conditions. This physiological effect of SLs on
Arabidopsis LR growth has been shown to be mediated through the
modulation of endogenous auxin status and/or auxin sensitivity in
plants (Ruyter‐Spira et al., 2011).
In Arabidopsis, the reduction in RH length was observed in both
SL‐biosynthetic max1 and max4, as well as SL‐signalling max2 mutants,
when compared with WT during vegetative growth under low‐P con-
ditions (Ito et al., 2015; Mayzlish‐Gati et al., 2012). In contrast, applica-
tion of GR24 restored the phenotypes of LR, RH, and seminal roots
only in SL‐biosynthetic mutants (max1, max4, d10, and d27) but not
in SL‐signalling mutants (d3 and max2) under P‐deficient conditions
(Ito et al., 2015; Mayzlish‐Gati et al., 2012; H. Sun et al., 2014). Taken
together, these results imply that SLs may help plants increase root
coverage, particularly by triggering the formation of crown roots, PR,
RH, and seminal roots to forage more soil surface for water and nutri-
ents under unfavorable nutritional conditions.
5.2 | Effects of SLs on aboveground structure of
plants under abiotic stresses
SLs can also shape aboveground architecture in response to P status in
growth medium. A suboptimal concentration of P inhibited shoot
branching and outgrowth of tiller buds in WT rice, whereas such
effects were not observed in SL‐biosynthetic d10 and SL‐signalling
d3 mutants (Table 1; Umehara et al., 2008; Umehara et al., 2010).
Thus, SLs have been suggested to play roles in configuring aerial archi-
tecture under P‐deficient conditions. Additionally, similar effects from
P starvation have also been observed in Arabidopsis (Table 1; Kohlen
et al., 2011). Specifically, a reduced number of secondary rosette
branches were observed in WT, whereas the numbers remained
unchanged in both SL‐biosynthetic max1 and max3, and SL‐signalling
max2 mutants (Kohlen et al., 2011). During exposure to P‐deficient
conditions, the observation of an increased expression of the SL trans-
porter PDR1 gene in petunia roots (Kretzschmar et al., 2012) and the
increased amount of SLs in xylem of Arabidopsis (Kohlen et al., 2011)
suggests that SLs are transported from roots to shoots. However,
because SLs are not found within xylem sap from a variety of plants,
including rice and Arabidopsis, and root‐applied SLs have been
detected in rice shoots, it was hypothesized that the shootward move-
ment of endogenous and exogenous SLs in plants happens through
the xylem‐associated parenchyma cells instead of the xylem itself
(Xie et al., 2015). Nevertheless, these findings clearly demonstrate that
SLs may act as a systemic signal in regulating shoot branching in
response to P deficiency in plants.
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2235
Under drought, reduced tillering phenotypes in tall fescue and rice
were associated with the enhanced expression of SL‐biosynthetic
genes (FaD17 and D10, D17, and D27 in tall fescue and rice, respec-
tively) and SL‐signalling genes (FaD14 and D14 in tall fescue and rice,
respectively; Table 1; Zhuang et al., 2017; Du et al., 2018), suggesting
that an SL‐dependent pathway might be involved in drought‐induced
reduction of tillering. The control over this phenotypic plasticity via
SLs indicates that they have the potential to enable plants to avoid
deleterious effects from severe drought by reducing vegetative
growth and by also saving energy for subsequent reproductive
development. By using SL mutants of pea (SL‐synthetic rms3 and
SL‐signalling rms4) and Arabidopsis (SL‐synthetic max3 and max4, and
SL‐signalling max2), Cooper et al. (2018) recently demonstrated the
roles of SLs in protecting photosynthesis under dark chilling condi-
tions, thereby enhancing shoot biomass production. In addition, SLs
also act as a positive regulator of leaf senescence by enabling plants
to reallocate the nutrients from old tissues to developing younger tis-
sues (Yamada & Umehara, 2015). Collectively, it is plausible that the
aforementioned SL‐mediated adjustments within aerial tissues, which
are dependent on nutrient and water statuses, may allow plants to
maximize the use of available resources for balancing biomass produc-
tion, particularly under adverse environmental conditions (Figure 2).
6 | I M P L I C A T I O N OF S L s I N P L A N T
RESPONSES AND ADAPTATION TO
D RO U G H T A N D S A L I N I T Y
6.1 | Drought
Generally, the primary response of plants to water deficit is the reduc-
tion of transpiration by inducing stomatal closure, in which ABA plays
crucial regulatory roles (Daszkowska‐Golec & Szarejko, 2013; Negin &
Moshelion, 2016). The first evidence on the direct involvement of SLs
in regulating the acclimatization of plants to drought and ABA‐
mediated stomatal closure was reported in Arabidopsis (C. V. Ha
et al., 2014). Specifically, the Arabidopsis SL‐biosynthetic max3 and
max4 and the SL‐response max2 mutants were more drought‐
susceptible than WT, which was further supported by water deficit‐
hypersensitive responses of the Arabidopsis SL‐biosynthetic max1
mutant plants (Y. Zhang et al., 2018), and the SL‐depleted L. japonicus
LjCCD7‐silenced and tomato SlCCD7‐silenced transgenic plants (Liu
et al., 2015; Visentin et al., 2016). In addition, C. V. Ha et al. (2014)
also observed that the leaves of the max2, max3, and max4 mutants
subjected to dehydration lost more water in comparison with WT
leaves. In the max mutants, the more rapid water loss was accompa-
nied by increased stomatal density, decreased ABA‐mediated stomatal
closure, and reduced sensitivity to ABA (C. V. Ha et al., 2014). In
response to treatment with ABA, a higher stomatal conductance was
also observed in the SL‐depleted LjCCD7‐ and SlCCD7‐silenced plants
(Liu et al., 2015; Visentin et al., 2016), which strongly supports the
contribution of SLs in regulating ABA‐mediated stomatal closure in
different plant species (Liu et al., 2015; Visentin et al., 2016). In com-
parison with WT shoots during water deficit, no significant change in
endogenous ABA content was observed in the shoots of SL‐deficient

2236
LjCCD7‐silenced plants (Liu et al., 2015) and SL‐signalling max2 mutant
(Bu et al., 2014). However, a reduction in ABA synthesis was noted in
SlCCD7‐silenced tomato plants (Visentin et al., 2016), suggesting that
the impairment in ABA‐mediated stomatal closure of these SL‐
depleted plants may be associated with a decrease in ABA responsive-
ness, ABA transport, and/or alteration in endogenous ABA content in
plant shoots (C. V. Ha et al., 2014; Liu et al., 2015; Visentin et al.,
2016). The data obtained from the studies of SL‐deficient mutants
clearly indicate a role for SLs in ABA‐mediated stomatal operation,
thereby regulating osmotic pressure during plant adaptation to water
deficit (Figure 3; C. V. Ha et al., 2014; Liu et al., 2015; Visentin et al.,
2016). Intriguingly, a recent study in rice reported that the d17/ccd7
mutant plants showed higher ABA accumulation in shoots under
drought; however, the authors did neither examine the ABA‐mediated
stomatal closure nor the ABA responsiveness of the d17 mutant
(Haider et al., 2018), which would allow us to make a valuable compar-
ison with what was observed in dicot plants, such as Arabidopsis,
L. japonicus, and tomato. It is worth mentioning that treatment of
broad bean (Vicia faba) with GR24 enhanced stomatal closure in a con-
centration‐dependent manner (Y. Zhang et al., 2018). Very recently, Lv
et al. (2018) reported that rac‐GR24 induced the production of H2O2
and NO that were required for promoting SL‐mediated stomatal
Osmotic
stresses
Modulation of endogenous SLs
Shoot
Photosynthesis branching
Stress-related
Leaf senescence
gene expresssion
Nutrient allocation
Stomatal closure
Osmolyte
Reduced water loss accumulation
Flavonoid
biosynthesis
Alleviation of water-stress
related symptoms ROS
metabolism
Reduction of negative
effects of osmotic stresses
Osmotic stress acclimatization
FIGURE 3 A schematic presentation of strigolactones (SLs)‐
mediated plant acclimatization to osmotic stresses. Modulation of
endogenous SL levels in plant shoots by osmotic stresses can regulate
a number of physiological and biochemical processes, which leads to
improvement of various stress‐related traits. SLs can induce stomatal
closure and biosynthesis of stress‐responsive proteins for alleviating
water deficit stress‐related symptoms. SLs can improve nutritional
status of plants by reallocating nutrients through the suppression of
photosynthesis, as well as by inhibiting shoot branching and
promoting leaf senescence. SLs are also involved in regulating
biosynthesis of secondary metabolites such as flavonoids to
strengthen plant protection against osmotic stresses. SLs might also
modulate the production of osmolytes and reactive oxygen species
metabolism, contributing to stress tolerance. Dotted arrows indicate
proposed roles for SLs in stress mitigation. Bar indicates the inhibitory
effect of SLs
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MOSTOFA ET AL.
closure in Arabidopsis. These results may imply a potential crosstalk
between SL or SL‐like compounds with H2O2/NO signalling pathways
in regulating plant acclimatization to external stresses (Figure 3). In
support of their roles in drought tolerance, SLs have also been known
to be positively involved in regulating the synthesis of flavonoids (Ito
et al., 2015; Lazar & Goodman, 2006), which are well known to play
crucial roles in osmoprotection under different stress conditions,
including drought (Nakabayashi et al., 2014; Nguyen et al., 2016).
Interestingly, although Bu et al. (2014) confirmed that max2
mutants are more sensitive to drought, they did not observe that the
SL‐biosynthetic max1, max3, and max4 mutants exhibited drought‐
sensitive phenotypes on soil upon withholding water for a period of
10 days when compared with WT. This result does not comply with
what reported by C. V. Ha et al. (2014) and Y. Zhang et al. (2018). It
is possible that this discrepancy in drought‐related attributes can be
explained by different growth conditions, seedling age, and different
periods of exposure to drought. Nevertheless, Bu et al. (2014) also
speculated that the SL‐biosynthetic max mutants (max3 and max4)
might still contain a detectable level of residual SLs, as was observed
in rice (Umehara et al., 2008), that could sustain drought responses
in these mutants as compared with max2. Moreover, because MAX2
is shared by both D14‐mediated SL signalling and KAI2‐mediated
karrikin signalling pathways (De Cuyper et al., 2017; Soundappan
et al., 2015), analysis of both D14‐ and KAI2‐mediated pathways
might explain why max2 showed a higher water loss rate than what
was observed in the SL‐biosynthetic max3 and max4 mutants during
dehydration (C. V. Ha et al., 2014). Indeed, a comparative drought tol-
erance test of the single d14 and kai2 mutants and kai2 d14 double
mutant revealed that all three mutants were sensitive to drought
and that the kai2 d14 double mutant plants were more sensitive to
drought stress than either of the single mutants under water depriva-
tion (W. Li et al., 2017). These findings suggest that both SLs, and the
yet‐unidentified KL, which binds to and is perceived through KAI2,
may act in concert through the checkpoint MAX2 to provide drought
tolerance in plants. Furthermore, in comparison with WT, the single
max2 and kai2 mutants, and the double kai2 d14 mutant, exhibited
reduced cuticle thickness in leaves; however, the single d14 mutant
did not (Bu et al., 2014; W. Li et al., 2017). This interesting observation
related to the difference in cuticle structure of examined mutants
raises an important question whether the D14‐ and KAI2‐mediated
signalling pathways execute additive effects by distinct mechanisms
in plant responses to drought. In the future, a detailed study compris-
ing physiological, biochemical, and molecular investigations using SL‐
and KAR‐specific mutants under water deficit conditions could be
employed to answer this question.
6.2 | Salinity
SLs have also been shown to play important roles in conferring salinity
tolerance in a MAX2‐dependent manner (C. V. Ha et al., 2014). Upon
exposure to high salinity at germination and vegetative stages, both
Arabidopsis SL‐deficient max3 and max4 and SL‐signalling max2
mutants exhibited salt‐sensitive phenotypes. However, no differences
in damage were observed between the roots of the examined max
mutant plants and WT (C. V. Ha et al., 2014). Similarly, max2 mutant

MOSTOFA ET AL.
plants exposed to salt stress showed a time‐ and concentration‐
dependent decrease in germinative greening rate in comparison with
WT (Bu et al., 2014). These results imply that reduction in endogenous
SL content, or impairment of SL signalling, compromises the ability of
plants to tolerate salt stress across developmental stages. However, as
observed in drought tolerance‐related studies, functional analyses of
D14 and KAI2 in the response of plants to salt stress need to be inves-
tigated in parallel to provide a proper mechanistic insight into how SL
signalling regulates plant tolerance to salt stress.
The role of SLs in salt tolerance was also evident in the presence
of AM symbiosis (Aroca et al., 2013). For example, in lettuce roots, SL
production was positively correlated with the enhancement of growth
and efficiency of the Photosystem II under a gradient of salt stress in
the presence of AMF (Aroca et al., 2013). The authors also observed
increased stomatal conductance in AMF‐colonized plants, which was
suggested to be associated with efficient CO2 fixation to support opti-
mum growth of lettuce plants (Aroca et al., 2013). In the roots of the
colonized plants, the production of ABA, and expression of the ABA‐
biosynthetic gene NINE‐CIS‐EPOXYCAROTENOID DIOXYGENASE2
(LsNCED2), showed a positive relation with the SL‐induced seed ger-
mination of Pasteuria ramosa (Aroca et al., 2013), suggesting an inter-
action between these two hormones in executing salt tolerance under
symbiotic conditions. Recently, an interaction of SLs with H2O2 in alle-
viating salt stress in the presence of AM symbiosis has been reported
in Sesbania cannabina seedlings (Kong, Ren, Li, Xie, & Wang, 2017).
The authors demonstrated that H2O2‐induced salt tolerance was
dependent on SL accumulation in AMF‐colonized S. cannabina seed-
lings. In Arabidopsis, it has also been reported that application of
GR24 caused a significant elevation of reduced glutathione levels in
the roots of WT, max3, and max4, but not in the max2 mutant plants,
even under nonstressed conditions (Marquez‐Garcia, Njo, Beeckman,
Goormachtig, & Foyer, 2014). These data suggest that a max2‐depen-
dent role of SLs exists in redox homeostasis. Although the precise
mechanism of the interaction between SLs and reactive oxygen
species (ROS) remains to be clarified, we hypothesize that the
SL‐regulated balance in plant architecture, together with ROS metab-
olism, may facilitate appropriate acclimatization of plants under
changing environmental conditions.
7 | I N T E R A C T I O N S O F S L s WI T H OT H E R
P H Y TOH O RM ON ES I N P L A NT R E SP O NS E S
T O A B I O T I C ST R E S S E S
Several findings have suggested that SLs, instead of working alone,
interact with other plant hormones to optimize growth and adaptive
responses under adverse environmental stresses (Brewer et al.,
2013; Cheng, Ruyter‐Spira, & Bouwmeester, 2013; Koltai, 2013;
Koltai, 2015; Liu, Lovisolo, Schubert, & Cardinale, 2013; López‐Ráez
et al., 2017). Accordingly, SL‐mediated plant acclimatization to
water‐related stresses was reported to occur through interactions
between SLs and ABA, especially by regulating stomatal sensitivity
to ABA (Figure 4; C. V. Ha et al., 2014; Liu et al., 2015). As evidenced
by the downregulation of CK catabolism‐related genes (CKX1, CKX2,
CKX3, and CKX5) in max2 mutant during dehydration (C. V. Ha et al.,
13653040, 2018, 10, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/pce.13364 by Readcube (Labtiva Inc.), Wiley Online Library on [10/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2237
(a)
SLs
ABA CK
Drought and salt tolerance
(b) (c)
Nutrient deficiency SLs
Auxin SLs ET ABA GA ET
Root hair growth Seed germination
under high temperature
Nutrient absorption
FIGURE 4 Interactions between strigolactones (SLs) and other
hormones in responses to different abiotic stresses. (a) SLs interact
with abscisic acid (ABA) and cytokinin (CK) in responses to drought
and salinity. (b) SLs function and interactions with ethylene (ET) and
auxin in the regulation of root hair growth under nutrient‐deficiency
stress (e.g., low‐phosphate stress). (c) Interactions among SL, ABA, ET,
and gibberellin (GA) in the regulation of seed germination under high
temperature. Solid arrow‐headed lines indicate positive regulation,
solid blunt‐ended lines indicate negative regulation. Dotted arrow‐
headed and blunt‐ended lines indicate proposed positive and negative
regulation, respectively
2014), it is possible that SLs may also negatively regulate CK levels
in plants under drought, which was not observed in the dehydrated
kai2 mutant (W. Li et al., 2017). In addition, the CK‐biosynthetic gene
AtIPT3 was also upregulated in max2 and max4 mutants (Chaudhary,
2013), adding additional evidence which supports the role of SLs in
the negative regulation of CK synthesis. Because CK acts as a negative
regulator of drought and salt tolerance (Lubovská, Dobrá, Štorchová,
Wilhelmová, & Vanková, 2014; Macková et al., 2013; Nishiyama
et al., 2011), we also hypothesize that SLs positively regulate plant
responses to these stresses through a reduction of CK levels and
thus inhibition of CK signalling in plants (Figure 4). Furthermore, a
relationship among SLs, ABA, and GA was evident from a study
of thermoinhibition on the seed germination of Striga and SL‐
biosynthetic (max1) and SL‐signalling (max2) mutants (Toh et al.,
2012). The authors reported that application of exogenous GR24 res-
cued the thermoinhibition on the germination of Arabidopsis and Striga
seeds by decreasing the ABA/GA ratio via suppression of the heat‐
induced increase of ABA and by inhibition of the heat‐induced
decrease in GA contents. This finding suggests that SLs can act as
endogenous modulators of ABA and GA to promote seed germination
under high temperatures, and this hormonal interaction is conserved
in both parasitic and nonparasitic seeds. However, it is not currently

2238
known how SLs impact profiles of other hormones under tempera-
ture‐related stresses at other developmental stages. Additionally, GA
can interfere with SL functions by downregulating the expression of
SL‐biosynthetic genes in rice roots (Ito et al., 2017). This GA‐triggered
decrease in SL production also leads to a reduced germination of
parasitic weed Striga (Ito et al., 2017), thereby suggesting a promising
parasitic weed management strategy by exploring the crosstalk
between GA and SLs.
Investigations in WT and various SL‐signalling mutants, including
d3 in rice and max2 in Arabidopsis, revealed that the regulatory func-
tions of SLs in root development under nutrient shortage are mainly
attributed to their crosstalk with auxin and ET signalling pathways
(Kapulnik, Resnick, et al., 2011; H. Sun et al., 2014). In rice, H. Sun
et al. (2014) demonstrated that the shoot‐to‐root movement of auxin
is crucial for determining the effect of SLs on the mediation of LR and
seminal root development under low‐P stress. It was also postulated
that a balance in the auxin‐SL interaction played the most important
role in the regulation of the root‐to‐shoot ratio in Arabidopsis under
P‐deficient stress conditions (Ruyter‐Spira et al., 2011). Auxin–SL
crosstalk is also known to be involved in the mediation of shoot
branching suppression in Arabidopsis and chrysanthemum under N‐
and P‐deficient conditions, respectively (de Jong et al., 2014; Xi
et al., 2015). SLs have also been implicated in regulating leaf senes-
cence in Arabidopsis through their crosstalk with ET (Ueda & Kusaba,
2015; Yamada & Umehara, 2015). In comparison with WT plants,
the Arabidopsis SL‐deficient mutant max1 exhibited a delayed dark‐
and ET‐induced senescence, and exogenous treatment with both ET
and GR24 more strongly triggered leaf senescence in max1 plants
when compared with ET treatment alone (Ueda & Kusaba, 2015).
These results clearly indicate an interaction between SLs and ET,
where the SL‐induced enhancement of ET action promotes leaf senes-
cence in Arabidopsis. Taken together, it is apparent that SLs exert their
crucial roles in controlling differential responses of plants toward various
abiotic stresses by forming a coordinated network with ABA, CK, GA, ET,
auxin, and perhaps with additional plant hormones as well (Figure 4).
8 | C O N CL U S I O N A N D F U T U R E
PERSPECTIVES
Although the ecological significance of SLs is ancient, the diversified
roles of SLs in the acclimatization of plants to environmental stresses
represent a new avenue in plant research. Research pertaining to SLs
is a cutting‐edge topic due to the major regulatory functions of SLs
on plant aspects and processes relevant for agronomical and ecologi-
cal purposes, including seed germination, hyphal branching, shoot
growth inhibition, root development, and parasitic plant control. Taken
together, all of these areas of impact indicate that advancements in
our understanding of SLs have a great potential in modern agriculture.
However, limited production, reduced bioavailability, and complex
diversified structures of SLs are all impediments for rapid advance-
ments for the research of SL biology (Screpanti et al., 2016). In addi-
tion, these factors also hinder prospective applications of SLs in
stress management. Therefore, overcoming technological limitations
for detecting natural SLs and developing synthetic SLs with simplified
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MOSTOFA ET AL.
structures, optimized bioactivity, and sizable amounts are essential for
deepening SL‐related research and formulating new chemicals for agri-
cultural applications. Because SLs function as important communica-
tors between host plants and beneficial microbes, it is possible that
this eco‐friendly chemical strategy could serve as an alternative over
traditional breeding or genetic engineering methods for developing
solutions to enable plants to better cope with the detrimental effects
of environmental stresses. Recently, SL receptors have been identified
in Striga, and their functional studies revealed that parasitic plants,
with a large binding pocket for SLs, are able to recognize a trace
amounts (picomolar) of SLs in the soils (Conn et al., 2015; Toh et al.,
2015; Tsuchiya et al., 2015). Therefore, the identification of SL recep-
tors in AMF and subsequent functional characterizations of these
receptors bear significant importance in designing SL analogues with
stronger affinities for AMFs than parasitic plants. These analogues
may assist in the establishment of effective symbioses by attracting
more AMFs toward host roots for helping crop plants to efficiently
explore existing resources and survive under suboptimal growth con-
ditions. Alternatively, it is also plausible to devise specific SL analogues
with supreme germination stimulating capacity for parasitic seeds that
may lead to suicidal germination of parasitic plants in the absence of
their host, thereby reducing parasitic infestations of host plants during
subsequent cultivation of plants in parasitic seed‐infested soils. More-
over, elucidation of the mechanistic modes of action of D14‐ and
KAI2‐mediated signalling pathways in symbiosis would increase the
speed of development for novel eco‐friendly agricultural opportunities
under abiotic stress conditions.
SL crosstalk with other phytohormones, such as ABA, CK, and
auxin, have been partly characterized under stress conditions. There-
fore, it is important to reveal how the interactions of SLs with other
hormones and signalling molecules are transformed into physiological,
biochemical, and molecular changes in order to gain further insight
into this complex regulatory network in plant responses to environ-
mental stresses. Hormonal interaction with ROS signalling is also an
integral part of stress‐responsive mechanisms. However, it remains
to be determined how SL signalling impacts the ROS signalling path-
way and vice versa. Thus, an important area of research has emerged
to further elucidate the roles of SLs in plant stress adaptation. Because
SLs have already been proven to be responsive to drought, salinity,
and chilling (Cooper et al., 2018; C. V. Ha et al., 2014; W. Li et al.,
2017; Liu et al., 2015; Visentin et al., 2016; Y. Zhang et al., 2018), it
would be interesting to investigate how SLs adjust osmotic imbalance
and oxidative stress by regulating the formation of compatible solutes
and antioxidant components.
In vitro and in vivo studies also revealed that modifications of the
structure (Quain et al., 2014) and signalling pathway (Islam et al., 2013)
of SLs significantly impact their roles in regulating the acclimatization
of plants to environmental stresses. Therefore, the identification of
exogenous chemicals that can modify in planta functions of SLs is an
important strategy for examining the mode of actions of SLs during
the management of environmental stress. Because SLs are known to
regulate phosphate transporters (Ito et al., 2015; Mayzlish‐Gati et al.,
2012), it would be very interesting to examine how SLs could impact
the transport of heavy metals, such as arsenic, as it also enters into
plant cells via phosphate transporters (N. Li, Wang, & Song, 2016).

MOSTOFA ET AL.
Moreover, it is still unknown whether the exudation of SLs into the
soils has any interaction with the uptake process of heavy metals by
plants when they are being grown in heavy metal‐contaminated soils.
Furthermore, it is possible that SLs could be indirectly used in a
phytoremediation strategy by exploiting their effects on promoting
the establishment of AM and/or rhizobial symbioses which can
enhance the efficiency of plants to remove excessive metals from
metal‐polluted ecosystems. Finally, as we continue to face increasing
concerns associated with plant production and global climate change,
comparative transcriptomic, proteomic, metabolomic, and functional
genomic approaches could provide inclusive knowledge on SL biology
which may speed up the design of SL‐engineered plants with the aim
to mitigate adverse effects associated with environmental stresses.
ACKNOWLEDGMENTS
M. G. M thankfully acknowledges postdoc fellowship from the Japan
Society for the Promotion of Science (JSPS). K. H. N. gratefully
acknowledges the “International Program Associate” of Rikagaku
Kenkyusho (Institute of Physical and Chemical Research, Japan) for
supporting his PhD study. L.‐S. P. T. is supported by a grant
(17K07459) from the JSPS.
CONF LICT OF INT E RE ST
The authors declare no conflict of interest.
ORCID
Lam‐Son Phan Tran http://orcid.org/0000-0001-9883-9768
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