Hewedy et al.

Download as pdf or txt
Download as pdf or txt
You are on page 1of 14

Environmental and Experimental Botany 208 (2023) 105260

Contents lists available at ScienceDirect

Environmental and Experimental Botany


journal homepage: www.elsevier.com/locate/envexpbot

Jasmonic acid regulates plant development and orchestrates stress response


during tough times
Omar A. Hewedy a, b, *, Nabil I. Elsheery c, **, Ali M. Karkour d, Neveen Elhamouly e,
Ramadan A. Arafa f, g, Ghada Abd-Elmonsef Mahmoud h, Mona F.-A. Dawood h,
Walaa E. Hussein i, j, Abdelaziz Mansour k, Dina H. Amin l, Suleyman I. Allakhverdiev m, n,
Marek Zivcak o, **, Marian Brestic o, **
a
Department of Plant Agriculture, University of Guelph, 50 Stone Road East, Guelph, ON N1G 2W1, Canada
b
Department of Genetics, Faculty of Agriculture, Menoufia University, Shibin El-Kom 32514, Egypt
c
Agricultural Botany Department, Faculty of Agriculture, Tanta University, Tanta 31527, Egypt
d
Microbiology Department, Faculty of Science, Tanta University, Tanta, Egypt
e
Department of Botany, Faculty of Agriculture, Menoufia University, Shibin El-Kom 32514, Egypt
f
Plant Pathology Research Institute, Agricultural Research Center, 12619 Giza, Egypt
g
Japan International Research Center for Agricultural Sciences (JIRCAS), Tsukuba, Ibaraki 305-8686, Japan
h
Botany and Microbiology Department, Faculty of Science, Assiut University, PO 71516, Assiut, Egypt
i
Department of Food Science and Technology, The Ohio State University, Columbus, OH, United States
j
Department of Microbiology and Immunology, National Research Center, Giza, Egypt
k
Department of Economic Entomology and Pesticides, Faculty of Agriculture, Cairo University, Giza, Egypt
l
Department of Microbiology, Faculty of Agriculture, Ain Shams University, Abbasiya, Cairo 1566, Egypt
m
K.A. Timiryazev Institute of Plant Physiology RAS, Botanicheskaya St. 35, 127276 Moscow, Russia
n
Faculty of Engineering and Natural Sciences, Bahcesehir University, Istanbul, Turkey
o
Institut of Plant and Environmental Sciences, Slovak University of Agriculture, A. Hlinku 2, 94976 Nitra, Slovakia

A R T I C L E I N F O A B S T R A C T

Keywords: Jasmonic acid (JA) or methyl jasmonate (MeJA) are master regulators of plant development and stress response
Jasmonic acid against pathogens and environmental fluctuations. Thus, JA is an important stress-associated phytohormone that
Abiotic stress can promote various defense interactions, regulate stomatal openness, synthesis of antimicrobial substances, or
Jasmonate-responsive genes
plant cell reprogramming. Numerous studies also demonstrated that plants thriving under environmental fluc­
Plant development
Phytohormones
tuations stresses are linked to the JA response, revealing that JA application can alleviate the damage of abiotic
Transcription factors stress by improving plant tolerance. Therefore, jasmonic acid and amino acid conjugate (JA-Ile) represent stress
hormones that improve crop resilience under environmental fluctuations. In addition, JA modulates the plant
growth and developmental stages by regulating the crosstalk between JA and the main plant hormone groups,
balancing plant development and defense mechanism against pathogen attacks. The effects on various processes
and plant structures, such as seed germination, primary root/root hair growth, fruit development, pollen
maturation, senescence, and regeneration, have been documented for jasmonates. Therefore, we reviewed the
functional influence of jasmonates, involving sensing and regulating their signaling under harsh conditions,
which is becoming a top priority for agriculture. In addition, the crosstalks with other phytohormones, such as
auxin, salicylic acid, ethylene, and the plant-pathogen interactions, are discussed.

* Corresponding author at: Department of Plant Agriculture, University of Guelph, 50 Stone Road East, Guelph, ON N1G 2W1, Canada.
** Corresponding authors.
E-mail addresses: ohewedy@uoguelph.ca (O.A. Hewedy), nshery@yahoo.com (N.I. Elsheery), marek.zivcak@uniag.sk (M. Zivcak), marian.brestic@gmail.com
(M. Brestic).

https://doi.org/10.1016/j.envexpbot.2023.105260
Received 3 August 2022; Received in revised form 4 February 2023; Accepted 6 February 2023
Available online 8 February 2023
0098-8472/© 2023 Elsevier B.V. All rights reserved.
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

1. Introduction systems against insect attacks. In seeds, the exogenous application of JA


to JA biosynthesis-deficient mutants enables their stamen maturation
Abiotic stresses and continuous exposure to unfavorable conditions since the development of stamens is critical for plant fertilization (Jewell
such as pathogens and insect attacks cause significant yield crop losses and Browse, 2016). Interestingly, stamen development in coi1–1 plants
worldwide, especially concerning climate change (Chakraborty and was restored during the overexpression of MYB21 since the mutant
Newton, 2011; Chaudhry and Sidhu, 2022; Mosa et al., 2017). There­ MYB21 and MYB24 regulate jasmonate-mediated stamen maturation
fore, the documentation of candidate mechanisms positioned by plants (Song et al., 2011). Additionally, the MYB108 MYB24 cascade regulated
as a reaction to various stresses is essential for conserving their life cy­ pollen maturation and anther dehiscence regulation in response to JA
cles. Since the 1990 s, there have been significantly more articles (Mandaokar and Browse, 2009). In the flowers of myc2 myc3 myc4
studying JA and much more to learn about JA signaling in plants (Ali myc5 plants, a downregulation in MYB57, MYB108, MYB21, and
and Baek, 2020; Creelman and Mullet, 1995; Hou et al., 2013; Per et al., MYB24 expressions was observed. In coi1–1, MYC3 and MYC5 over­
2018; Pernas et al., 2000). Jasmonic acid (JA) and Jasmonoyl isoleucine expression can partly reestablish the formation of stamen and fertility
(JA-Ile) are hormonal molecules controlling plant development and (Qi et al., 2015a). In Arabidopsis, ectopic expression of MYC2 or JAZ1
defense. JA has also been identified as a stress hormone controlling how mutation accelerates somatic embryogenesis through stimulation of the
plants react to environmental challenges, such as salt, drought, tem­ biosynthesis of indole-3-acetic acid (Mira et al., 2016). JA pathway is
perature fluctuations, and the toxicity of heavy metals (Raza et al., essential in the stamen formation in Arabidopsis (Yuan and Zhang,
2022). Therefore, there is a need to understand and review the 2015). Gibberellic acid (GA) inhibited DELLA repressor proteins, which
comprehensive studies that showed the functional impact of jasmonic increased JA accumulation and the gene expression of DAD1. Conse­
acid in that era. In addition, recent studies in the plant physiology quently, MYB expression increased, elongating the filament growth
domain have demonstrated that plant growth regulators or hormones, (Cheng et al., 2009). Furthermore, MYB orchestrates JA biosynthesis
particularly JA, have introduced dramatic new insights regarding the expression by controlling the elongation of filament growth and the
signaling pathways of plants under unfavorable environmental developmental process of anther dehiscence. AUXIN RESPONSE FAC­
conditions. TOR6 (ARF6)/ARF8, INDOLE-3-ACETIC ACID 8 (IAA8), and TRANS­
Interestingly, JA participates in various cellular and biological pro­ PORT INHIBITOR RESPONSE1 (TIR1)/AUXIN SIGNALING F-BOX
cesses (e.g., molecular, biochemical, and physiological pathways), PROTEINs - Auxin signaling components - had a crucial impact on this
significantly impacting the resistance mechanisms versus phytopatho­ process (Nagpal et al., 2005; Wang et al., 2013). Interestingly, the
genic microorganisms and insect outbreaks and stages of plant devel­ development of the maize floral head and the tassel was a noticeable
opment (Sun et al., 2022). In this review, we summarize recent findings influence on JA in Zea mays. Due to jasmonate deficiency, the devel­
relating to the role of jasmonic acid (JA) and methyl jasmonate (MeJA) opment of tassel lox8 mutants (tasselseed1, ts-1) was regulated in the
in response to environmental fluctuations and how this plant stress tasselseed mutant phenotype. While cross-pollination allows these mu­
hormone can mediate the effect of abiotic stressors (Günther et al., 2022; tants to produce viable seeds, they are male sterile. Additionally, it was
Shikha et al., 2022). Furthermore, JA stimulates other hormones to reported that the various mutated allele was repaired by JA treatment,
improve crop resilience under adverse stressors (Rivero et al., 2022). such as male floret-deficient masculinization in lox8 single (Acosta et al.,
This review also discusses the JA signaling pathways in response to 2009), opr7opr8 double mutants (Yan et al., 2012b), and tasselseed2
environmental challenges by upregulating the transcription factors (ts2) mutants.
(TFs) and stress-defense genes that regulate JA biosynthesis pathways. Remarkably, the ear shoots of growing opr7opr8 ears are 3–4 times
longer than those of WT. Treatment with JA successfully reversed the
1.1. Jasmonate: a critical frontier in productive plant stages, reproductive abnormal female sexual organ phenotype, like chemical complementa­
organs, and seed development tion rescue for the conventional tassel. In rice, JAZ1 acts with MYC2 and
controls spikelet development by the OsG1, OsMADS6, and OsMADS5
Jasmonic acid (JA) and amino acid conjugate (e.g., JA-Ile) emerged floral identity genes (Zhang et al., 2016). It has been discovered that an
in the last decades as essential phytohormones in response to stressful OsPEX5 gene mutation, which produces the PTS1 receptor protein,
conditions and plant development (Browse, 2009; Ghorbel et al., 2021; causes an abnormal spikelet shape by preventing JA production. By
Wasternack, 2007). A crucial role in floral development, tuberization in introducing the OsOPR7 enzyme responsible for JA biosynthesis into
potatoes (Solanum tuberosum L.), trichome formation, and arbuscular peroxisomes, OsPEX5 regulates spikelet development. OsOPR7 diffuses
mycorrhizal colonization was observed after JA application (Balbi and in the cytoplasm instead of being limited to peroxisomes in the ospex5
Devoto, 2008; Browse, 2005; Yoshida et al., 2009). Begum et al. (2022) mutant, which disrupts JA biosynthesis (You et al., 2019). Jasmonates
examined the roles of JA transcriptional repressor (JAZ), signaling influence rice fertility by regulating the development of rice spikelets
suppressor subtype JAZ1, in potato tuberization. Its overexpression led through the key conserved signaling module constituting
to the inhibition of tuber formation. StJAZ1-like modulated the tran­ JA-Ile/COI/JAZ/TFs. According to this conserved paradigm, the
scriptomic responses associated with the activity of phytohormones, endogenous content of JA-Ile in the flower parts must be higher than the
cytoskeleton, and overall cell cycle. threshold level for the JAZ repressor to break down and enable
JA concentrations vary according to tissue type, developmental TF-mediated transcription of the genes associated with flowering. In
stage, and environmental stimuli. Flowers and reproductive tissues have rice, the reduction of fertility was observed with altered spikelet struc­
the highest JA levels, whereas roots and mature leaves have the lowest ture caused by overexpression of the JASMONIC ACID CARBOXYL
concentrations. A remarkable role of Jasmonates was observed and well- METHYL TRANSFERASE (AtJMT) or mutations of the JASMONYL-L-I­
described in the fertility process and plant development regulation as SOLEUCINE SYNTHASES 1 (OSJAR1) gene (Kim et al., 2009; Xiao et al.,
well as reproductive organ differentiation. The abnormalities in floral 2014). In addition, Oxylipin (bioactive lipid metabolites), including
structure and sterility exhibited in JA biosynthetic mutants have been jasmonates, had a critical role in tomato embryo development; they
identified in several crops, including tomato Solanum lycopersicum L. represent signaling compounds in plant growth and development.
(Solanaecae) (Li et al., 2004; Schubert et al., 2019), maize (Zea mays) However, the JA-insensitive tomato (Solanum lycopersicum) mutant jai1
(Acosta et al., 2009; Yan et al., 2012b), cotton (Gossypium hirsutum) (Li is female sterile. Most mutants affected by jasmonic acid (JA) biosyn­
et al., 2013), and Arabidopsis (Arabidopsis thaliana) (Park et al., 2002; thesis and signaling are male sterile in Arabidopsis thaliana (Goetz et al.,
Shih et al., 2014). 2012). The 35 S::SlAOC-RNAi lines and the female-sterile jai1 plants
Generally, JA regulates plant developmental stages, as broadly showed a similar phenotype. It implies that a compound is required for
reviewed by Huang et al. (2017). It also governs the plant immune typical embryo development upstream of the AOC-catalyzed process.

2
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

However, the poor seed set limited any proof based on examining those peroxide and superoxide anions were inhibited after MeJA treatment by
lines. The mutation spr2 affecting 7-fatty acid desaturase enzyme ac­ improving the activities of the antioxidant enzymes (Fu et al., 2023).
tivity led to poor embryo development, embryos with a smaller endo­ Important knowledge on the effects of jasmonates on growth and
sperm, or embryo abortions (Wasternack et al., 2012). In the case of development processes has been obtained under in vitro conditions, as
mutant acx1, the normal development of seeds was observed, identical reviewed by Kaminska (Kamińska, 2021). The multiple results demon­
to the wild type. Because ACX1 is responsible for the catalysis of the step strate the strict links between cell division, plant growth and develop­
downstream of JA precursor 12-oxophytodienoic acid (OPDA), it was ment, and cell differentiation and expansion. For example, researchers
assumed that this compound was necessary for embryo development. used the Nicotiana tabacum BY-2 cell line to examine the roles of JA and
Surprisingly, OPDA accumulated primarily in the seed coat throughout ABA on cell development (Swiatek et al., 2002). According to their
embryo development. findings, these growth regulators inhibit the replication process, dis­
In contrast, in the testa, endosperm, and embryo, the downstream rupting cell cycle development. However, exogenous administration of
compounds like 12-OH-JA and JA occurred in trace amounts only, and both substances before the G1/S transition resulted in cell cycle reten­
the seeds of the acx1 mutant had higher OPDA levels than wild-type tion in the G1 phase. At the later stage, ABA treatment had little effect on
seeds. A TUNEL assay revealed enhanced programmed cell death in cell cycle progression, while JA efficiently inhibited triggering mitosis of
the endosperm tissues and the seed coat of spr2, indicating that low the cells (i.e., cells were stopped in the G2 phase). These findings sug­
OPDA levels impact both tissues. This substance was believed to regulate gested that growth reduction in response to JA was caused by a distur­
the embryo’s development because of its high content in the testa of wild bance in meristem activity rather than BY inhibition of the cell
type seed and the capacity of the acx1 mutants to synthesize it (Li et al., expansion in the elongation zone (Krajnčič and Nemec, 1995). In addi­
2019; Wasternack et al., 2013). Nevertheless, a small amount of tion, MeJA also blocked the activation of M-phase genes, inhibiting cell
JA/JA-Ile in acx1 seeds may ensure normal development of the embryo. division during the G2 phase of the cell cycle, according to an exami­
To distinguish the effects of OPDA and JA/JA-Ile, the jai1 mutation was nation of the gene expression in the Arabidopsis genome (Pauwels et al.,
used. Despite being JA-insensitive, this mutant can detect OPDA (Sheard 2008).
et al., 2010). Indeed, in jai1 plants repeatedly injured during embryo Abdelsalam et al. (2021) observed that adding MeJA (10–400 µM) in
development, the embryo growth was partly restored, indicating the growth medium significantly improved somatic embryogenesis at
increased OPDA content in fruits compared to the unwounded different developmental stages, leading to higher numbers of somatic
individuals. and mature embryos and embryogenic shoots. On the other hand, its
Contrary to expectations, the OPDA rise does not correspond to the effects on the organogenesis of shoots and roots were adverse. In turn,
broadly accepted assumption that JA biosynthesis is controlled by COI1- the positive effects of JA on biomass were observed in cultures of Salacia
and JA-dependent genes (Reymond et al., 2000). However, there ap­ chinensis L. when the callus was treated with 75 µM JA. Moreover, the
pears to be some remaining COI1-independent JA production since the JA-treated callus supplemented with 2,4-D (2.0 mg/l), BAP (1.5 mg/l)
immunocytochemical analyses identified AOC in ovules of jai1 mutant showed higher contents of flavonoids, total phenolics, and mangiferin
(Goetz et al., 2012). One of the hypothesized mechanisms of OPDA ac­ (Chavan et al., 2021). Nandy et al. (2021) observed in the medicinal
tivity is the influence of OPDA on carbon availability. It has also been crop Hemidesmus indicus (L.) grown in-vitro induction of growth pro­
hypothesized that JA has a physiological function in tuber formation. moted by MeJA treatment (25–75 μM). In addition to the overall
Therefore, JA may accelerate tuber growth by breaking intracellular biomass increase, the treatment upregulated nodular meristemoids’
microtubules and promoting radial cell expansion, which occurs before growth and stimulated the accumulation of root-specific bioactive al­
tuber development. kaloids. Unlike these two studies, Yazdanian et al. (2022) observed in­
Furthermore, the tuber-inducing stimulus in potatoes (Solanum hibition of callus growth under higher concentrations of MeJA treatment
tuberosum) is considered a member of the jasmonate family. Even in Allium jesdianum grown in vitro, while the content of secondary me­
modest amounts of tuberonic acid-β-glucosidase offer a strong signal for tabolites was enhanced.
tuber development. This substance is produced in the leaves and By activating transcription factors and proteins, JA application
transferred down to the stolons (Kolomiets et al., 2001). Furthermore, stimulates cell reprogramming. MeJA primarily boosts gene expression
jasmonates influenced bulblet production in onion (Allium cepa L.) and in jasmonate production; thus, gene expression in the later stages of the
garlic (Allium sativum L.). In the cultivating medium, the presence of JA cell cycle was decreased (Gumerova et al., 2015). Adding MeJA to the
(0.01–10 µM) enhanced the quantity of garlic bulbs (Ravnikar et al., suspension cultures of Taxus cuspidata with asynchronous cell division
1993), and in conditions of higher JA concentration (10 µM), the pro­ led to a series of effects on mitogenesis. During the in vitro propagation
duction of bulbs in onion was upregulated (Koda and Kikuta, 1991). In of calluses, the indirect JA effects on cytokinesis were also observed. In
vitro cultivation of Narcissus triandrus L. shoots in a JA-enriched medium the differentiation stage of Medicago sativa, larger doses (5–50 µM) of JA
led to better quality and a higher quantity of bulbs (Santos and Salema, and MeJA inhibited the development of calluses. Induction with 10–100
2000). Furthermore, in Hyacinthus orientalis, JA combining with cyto­ µM MeJA significantly reduced the vitality of Taxus baccata and Taxus
kinin 2-iP (isopentyl-adenine) enhanced the generation and develop­ cuspidata cell cultures on WB/A media with the addition of a 6-benzyl
ment of bulblets (Doğan et al., 2020). However, (Saniewski and amino purine (BAP) and 1-naphthaleneacetic acid (NAA) (Bulgakov
Puchalski, 1987) observed that in Muscari armeniacum, 0.5% MeJA et al., 2011). Due to the rapid buildup of H2O2 caused by 100 µM MeJA,
prevented benzyl adenine-induced bulblet formation, but lower con­ cell viability in the A. thaliana protoplast culture was significantly
centrations of MeJA (0.1% and 0.2%) led to slower bulblet growth and reduced (Zhang and Xing, 2008). Moreover, glucoraphanin (GRA) and
delayed development. In similar, the number of Tulipa gesneriana bulb­ sulforaphane (SF) biosynthesis after MeJA treatment led to the effective
lets was lowered by MeJA. In turn, one genotype responded to the regulation of broccoli hairy roots (Bao et al., 2022).
combined treatment of MeJA and Arg (500 µM) by stimulated bulblet
growth (Podwyszyńska et al., 2015). 1.2. JA functions to close the stomata and combat pathogens
Recently, it was shown that MeJA induced the accumulation of JA in
response to Botrytis cinerea in tomato fruit. It was demonstrated that Plant species closely control stomatal apertures and guard cells in
0.05 mM MeJA treatment during the tomato storage led to upregulating response to various stressors. Production of jasmonate and other plant
the disease resistance enzyme activities and the expression of hormones elicited various physiological processes in crop plants via
pathogenesis-related (PR) genes. In addition, the transcriptional factors signaling intermediates and other molecules to enhance plant health
of genes (SlCOI1 and SlMYC2) were induced that upregulate the disease- (Turner et al., 2002). Furthermore, jasmonate induced stomatal closure
responsive genes such as SlPI I and SlPI II. Furthermore, hydrogen in various plants, including Nicotiana glauca, Arabidopsis thaliana, Vicia

3
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

faba, and Paphiopedilum tonsum (Suhita et al., 2004). Diverse essential complex then binds JA-Ile, which is made up of the
signal processes were discovered in MeJA and JA-induced stomatal coronatine-insensitive 1 (COI1) F-box protein and leads to stomatal
closure and signal crosstalk with other plant hormones (Munemasa closure, development responsibility, and internal defense (Sheard et al.,
et al., 2007). Surprisingly, MeJA causes guard cells to release reactive 2010) (Fig. 1).
oxygen species (ROS) and nitric oxide (NO) to induce stomatal closure. Surprisingly, JA can use a COI1-independent strategy to control the
However, diphenylene iodonium, an NAD(P)H oxidase inhibitor, plays a closure and opening of plant stomata. Plants are constantly attacked by
crucial role in ROS generation and the MeJA-induced guard cell potentially phytopathogenic microorganisms, including biotrophic,
response (Munemasa et al., 2007). hemibiotrophic, and necrotrophic microbes. Plant pathogens can stim­
Furthermore, disrupting the AtrbohD and AtrbohF genes producing ulate immunological signaling pathways, defense interactions, and
NADPH oxidase eliminates closing stomata caused by MeJA and related other circumstances. For example, extensive gene expression reprog­
production of ROS (Suhita et al., 2004). Exogenous application of JA or ramming after JA proliferation is associated with many JA activities in
MeJA to crop plants can be followed by their conversion to the physi­ plant tissues. The JA signaling pathway appears necessary in internal
ologically active form 7-iso-jasmonoyl-L-isoleucine (JA-Ile). The SCFCOI plant immunity under biotic stress, such as in necrotrophic diseases (e.

Fig. 1. The molecular mechanism and physiological and biochemical impact of Jasmonic acid (JA) on plants which controls stomatal closure and internal defense.
JA-Ile = Jasmonoyl isoleucine; ROS = Reactive oxygen species; NO = nitric oxide.

4
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

g., Botrytis cinerea, Plectosphaerella cucumerina, and Pythium spp.) Takken and Goverse, 2012). As a result, JA governs biological processes
(Campos et al., 2014; Yan and Xie, 2015). The mutants fad3fad7fad8, for plant development and contact, translaminar, and systemic pathogen
jar1, and coi1–1 showed susceptibility to Alternaria brassicicola, resistance reactions.
P. cucumerina, and B. cinerea in Arabidopsis (Hu et al., 2017; Stintzi et al.,
2001). Recently, Chen et al. (2021) reported that the JA signaling 1.3. The functions of JA in root behavior and development
pathway played a role in the positive activation of defense mechanisms
in Arabidopsis vs. A. brassicicola and B. cinerea via the transcription factor Plant species, as sessile organisms, must be very efficient in adjusting
WRKY75 and the target gene ORA59. In addition, the biosynthetic en­ to the various climate scenarios by modifying their growth and devel­
zymes ACX2 and ACX3 of JA were activated by an interaction between opment. Plant roots represent the underground part that absorbs mac­
IQ-MOTIF-CONTAINING PROTEIN 1 (AtIQM1), a Ca2+-independent ronutrients, micronutrients, and water. Depending on plant families and
CaMBP, and CATALASE2 (CAT2) in Arabidopsis, resulting in an increase species, the architecture of plant roots displays a high level of
in JA levels and resistance to B. cinerea (Lv et al., 2019). Through the morphological variability. Improved root systems can increase the ab­
degradation of JAZ1 and the release of RcMYB84 and RcMYB123, JA sorption of all necessary elements for the life cycle and water, increasing
consistently causes basal resistance in Rosa chinensis plants against crop productivity. In addition, several biotic and abiotic parameters can
B. cinerea (Ren et al., 2020). influence root architecture with high plastic characteristics. The plas­
In addition, Pseudomonas syringae pv. tomato is a bacterium speck ticity and its molecular mechanisms have been studied in model plants,
disease that produces coronatine (COR) as a virulent molecule to acti­ such as Arabidopsis thaliana (Motte et al., 2019; Osmont et al., 2007).
vate the JA signaling pathway. Finally, JAZ2-COI1 complexes activate Since numerous phytohormones are essential in the development of
and deteriorate JAZ, resulting in stomata opening induction and plant root systems, JA regulates other plant organ development,
allowing the pathogen to enter and colonize the host (Gimenez-Ibanez including seed development and germination, root regeneration, and
et al., 2017). Indeed, the innate immunity systems in plants consist of flower evolution (Ye et al., 2020; Zhang et al., 2019). JA impacts root
both effector-triggered immunity (ETI) and pathogen-associated mo­ growth, including primary root disincentive, root regeneration, and
lecular patterns (PAMPs) (Jones and Dangl, 2006). Moreover, PRRs, the reducing adventitious root formation. In addition, it encourages lateral
pattern recognition receptors, are considered the first line of defense root construction, where all these physiological procedures are regu­
against PAMPs (Macho and Zipfel, 2014) (Fig. 2). lated by crosstalk with other plant hormones (Lakehal et al., 2019;
The promotion of MAPK, induction of ROS, pathogen-related protein Zhang et al., 2019). The JA signaling pathway includes some of the
activation, and the biosynthesis of phytohormones associated with stress regulatory factors, such as JASMONATE-RESISTANT 1 (JAR1) and
(e.g., JA, SA) are among the physiological processes and communication JASMONATE-INSENSITIVE 1 (MYC2/JAI1), as well as
components involved in the early defense interaction (Ahuja et al., CORONATINE-INSENSITIVE 1 (COI1), which are associated with the
2012; Torres et al., 2006; Tsuda et al., 2013). Consequently, stomatal JA-mediated plant root system (Berger et al., 1996). Additionally, plant
closure, antimicrobial component synthesis, and plant cell reprogram­ root elongation can be decreased by JA application by reducing the
ming promote defense interactions (Dixon, 2001). Effector-triggered number of cells and dimensions, an intricate process, along with the root
immunity (ETI) can also be stimulated when plant-adapted microor­ architecture (Chen et al., 2011a), as shown in Fig. 3.
ganisms insert effector proteins to disrupt PAMP-triggered immunity Furthermore, the exogenous application of JA at different doses to
(PTI) response signaling pathways (Dodds and Rathjen, 2010; Hann the growth media of sunflower seedlings revealed a repressing effect on
et al., 2010). These proteins are recognized via resistance genes of the the root architecture through inhibition of the primary root growth and
host tissues and lead to incompatible responses (Spoel and Dong, 2012; reducing the number of lateral roots (Corti Monzón et al., 2012; Sun

Fig. 2. Schematic representation of crop-pathogen interactions showing the plant immunity system including two main defence components, effector-triggered
immunity (ETI) and PAMP-triggered immunity (PTI). Incompatible response (resistance) due to specific receptors and resistance genes, PAMP – pathogen-
associated molecular pattern; NB-LRRs – nucleotide-binding and leucine-rich repeats; PRRs – pattern recognition receptors; JA – jasmonic acid; PR-proteins –
pathogenesis-related proteins, MAPK – mitogen-activated protein kinase.

5
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

Fig. 3. Diagram depicting the influence of JA application on the root system of crop plants. An increased JA dose represses the formation of primary and lateral roots.

et al., 2009). A biological pathway of JA can be involved in lateral root 1.5. JA and drought stress
regulation, where the application of MeJA to the wild-type of Arabi­
dopsis induced lateral root formation. In contrast, another mutant Water scarcity is a significant constraint affecting development,
(asa1–1) did not generate these roots (Sun et al., 2009). Similarly, physiological, biochemical, molecular aspects, and productivity.
(Raya-González et al., 2012) reported that the receptor COI1 of JA is Numerous reports showed the negative impacts of drought stress on
vital in the production of the lateral root, whereas, in the case of the plant tissues by changing membrane stability, inducing reactive oxygen
coi1–1 mutant, JA failed to promote more roots. Similarly, Jing et al. species, and decreasing turgor pressure. In addition, the attenuation of
(2022) found that the suppressor of JA signaling, StJAZ1-like, decreases gas exchange by stimulating stomatal closure causes a decline in
drought tolerance by downregulating the formation of adventitious photosynthetic efficiency (Seleiman et al., 2021; Sharma et al., 2020;
roots. Barboričová et al., 2022). JA production is also stimulated in response to
Additionally, one of the underlying molecular mechanisms for water deficit, demonstrating that JA is associated with the dehydration
crosstalk between JA and other hormones is the transcription of various response. Drought stress also alters the endogenous content of phyto­
genes associated with the biosynthesis of auxins, such as ASA1, hormones. For instance, the content of JA in tomato roots exposed to
YUCCA2, and NITRILASE 3 (NIT3), and ASB1, which can be triggered by water shortage for 12 h was almost 10-fold higher than that of
MeJA (Cheng et al., 2006; Kutz et al., 2002; Stepanova et al., 2005). In non-stressed plants. The leaf JA contents were also elevated (Zhang and
addition, MeJA activates YUC8 and YUC9 in auxin-mediated lateral root Huang, 2013). In addition, JA accumulation in wheat (Triticum aestivum)
initiation and primary root development. Likewise, the compatible was upregulated in response to water limitations, and the cellular JA
interaction between JA and auxin pathways induces the regeneration of concentration was 5-fold higher for 24 h (Kamran et al., 2021).
plant roots, where JA activates ERF109, CYCLIN D6;1 (CYCD6;1), and Furthermore, drought stress stimulated the JA biosynthesis-
ERF115 expression (Hentrich et al., 2013; Zhou et al., 2019). associated gene expression in wheat, including LOX1, AOS1, AOC1,
and OPR3. It suggests that the water deficit supports the production of
1.4. Jasmonic acid orchestrates abiotic stress responses JA, which is connected with the upregulation of related genes (Kim
et al., 2021). Increases in the concentrations of endogenous JA in
Jasmonic Acid, as a phytohormone mediates plant responses to un­ drought-stressed A. thaliana and citrus (Citrus paradisi × Poncirus trifo­
favorable environmental conditions at low concentrations. It alleviates liata) were fast and transient (Balbi and Devoto, 2008; de Ollas et al.,
abiotic stresses via physiological and molecular responses, as shown in 2013). On the other hand, the prolonged stress led to JA decreasing
(Fig. 4). Triggering the antioxidant system (Karpets et al., 2014), soluble basal levels.
carbohydrates (Wasternack, 2014), and increasing the content of the The functions of exogenous JA in plant stress response and tolerance
amino acids (isoleucine and methionine) was the physiological re­ to water deficit were observed in multiple studies. For instance, MeJA
sponses to JA application (Acharya and Assmann, 2009). Besides, the treatment in peanuts (Arachis hypogaea), soybean, and rice led to
modulation of the closing and opening of stomata during photosyn­ enhanced drought resistance (Todaka et al., 2015; Fu et al., 2017;
thesis. Interestingly, high concentrations inhibit growth and photosyn­ Mohamed and Latif, 2017). JA-treated soybean, pearl millet (Pennise­
thesis while accelerating senescence (Kamran et al., 2021). Moreover, tum glaucum), and maize led to a more resistant response to water
the role of JA in mediating molecular responses is the upregulation of deficit (Riemann et al., 2015; Abdelgawad et al., 2014; Awan et al.,
expression of related genes (AOC, JAZ, COI1, AOS1, and LOX2) inter­ 2021). In addition, JA increased proline accumulation and reduced
acting with various phytohormones (IAA, GA, ABA, ET, SA, BR). Finally, plant ROS levels (Fugate et al., 2018; Sirhindi et al., 2015). In this
it interacts with transcription factors (MYC2 and bHLH148) (Hu et al., respect, JA was shown to regulate the ROS scavenging system and
2017; Ku et al., 2018; Yang et al., 2019; Zhao et al., 2013). proline metabolism by gene expression regulation (Abdelgawad et al.,
2014; Awan et al., 2021). The methyl jasmonate treatment of maize
enhanced drought tolerance which was associated with the

6
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

Fig. 4. Jasmonic acid (JA)-mediated various plant stress responses, including high temperature, heavy metals, salinity, drought, and phytopathogenic microor­
ganisms. Implementing JA can regulate many advantageous biological processes in plants at different levels to confer protection and adaptation against undesirable
biotic and abiotic factors. The sections show the impact of JA (stress hormone) on modulating the physiological responses to various stresses.

accumulation of different metabolites, such as soluble sugars, poly­ hormonal imbalance, causing growth and yield suppression (Arif et al.,
saccharides, proteins, free amino acids, or proline (Abdelgawad et al., 2020; Ibrahimova et al., 2021; Hewedy et al., 2022). JA is one of the
2014). essential phytohormones reported to be affected by salinity stress. A.
thaliana (Friero et al., 2022; Li et al., 2022) and tomato (Altaf et al.,
2022; Pedranzani et al., 2003) had increased JA content in response to
1.6. JA and salt stress salt stress. Several studies have started improving the JA content and
JA-biosynthesizing genes of maize and sweet potato (Ipomoea batatas)
Salt stress is a significant constraint on agricultural soil caused by (Zhang et al., 2017) in response to salt stress. In addition, the JA
high salt levels in the soil or water supply. Salinization of soil severely biosynthetic genes MtAOS1 and MtAOS2 were enhanced by salt treat­
impacts plants by restricting water uptake and the accumulation of Na ment of Medicago truncatula compared to control plants (De Domenico
and Cl, causing ionic toxicity. It harms plants’ physiological and et al., 2019). Thus, many studies have reported the effect of exogenous
biochemical attributes, such as photosynthetic inhibition, water-relation JA on plants as an antistress salt agent. In this regard, the exogenous
imbalance, ROS accumulation, membrane disorders, failure of the application of JA restrained the reduction in chlorophyll mediated by
antioxidant system, deregulation of secondary metabolites, and

7
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

saline conditions in soybean, almond (Prunus dulcis), and pepper accumulation under boron toxicity led to the activation of the antioxi­
(Capsicum annuum), supporting the role of JA in salt stress response dant system of Artemisia annua that reduced lipid peroxidation (Aftab
(Tavallali and Karimi, 2019; Yoon et al., 2009). In addition, the exog­ et al., 2011).
enous application of JA on leaves of plants exposed to salt stress was Furthermore, by stimulating the antioxidant system, JA mitigated
shown to regulate oxidative stress and promote the synthesis of osmo­ the harmful effects of oxidative stress on plant growth, biomass, and
protective compounds, thus supporting plant tolerance (Farhangi-Abriz protein levels in Ni-treated plants (Azeem, 2018). Jasmonates, ethylene,
and Ghassemi-Golezani, 2018). and brassinosteroids regulated the root system (e.g., lateral roots) under
Ion toxicity was considered the main problem of salt stress; the heavy metals (Betti et al., 2021). In Arabidopsis, JA levels in roots were
negative impacts of salt stress might depend on reducing Na accumu­ increased due to the induction of genes that promote endogenous JA
lation (Dawood et al., 2022). For example, a decline in Na+ content by production under Cd accumulation. JAs, both produced or applied
applying JA in soybean under various levels of salt stress significantly exogenously, lowered the Cd concentration in root cell sap and reduced
affected the changes in Na+ uptake and translocation from roots to Cd stress by downregulating gene expression that promotes Cd uptake
shoots (Farhangi-Abriz and Ghassemi-Golezani, 2018). Furthermore, in and long-distance translocation (Lei et al., 2020).
two maize genotypes, JA could improve Na+ exclusion in the root by Moreover, JA plays a role in reducing the oxidative stress on plants
decreasing Na+ uptake and facilitating surface salt stress tolerance and induction of genes encoding antioxidants and secondary metabolites
(Shahzad et al., 2015). Furthermore, the exogenous application of JA in B. napus (Farooq et al., 2016). Furthermore, in response to increased
decreased plant salt-mediated damage by increasing photosynthetic osmotic pressure, external JA accumulation might reduce Cd toxicity
rates, proline contents, and antioxidant enzyme activity (Walia et al., rates in roots, shoots, and leaves, restricting H2O2 (Noriega et al., 2012).
2007). In addition, the endogenous JA improved salt tolerance by Such reports illustrated that JA improved the plant tolerance against
maintaining the homeostasis of reactive oxygen species (ROS) in tomato heavy metal stress by triggering the secondary metabolism and antiox­
crops (Abouelsaad and Renault, 2018). idant system to minimize heavy metal uptake.
Furthermore, (Jiang et al., 2016) reported that the application of
MeJA to black locust trees (Robinia pseudoacacia) mitigated the nega­ 2. JA orchestrates other phytohormones
tive impacts of salinity by stimulating the antioxidant system, namely,
SOD and APX. In addition, (Faghih et al., 2017) stated that APX, POD, 2.1. JA–ABA
and SOD were stimulated in salt-stressed plants by MeJA. Moreover, the
exogenous application of JA reduced the lipid peroxidation and ABA is a critical regulator of plant responses to stressful conditions
hydrogen peroxide accumulation of wheat plants, which enhanced the (Gomez-Cadenas et al., 2015). ABA crosstalks with JA, mediated
tolerance of wheat to salinity stress. Furthermore, the levels of the through JAZs-MYC2, regulate plant growth, defense against herbivorous
transcripts of SOD, POD, CAT, and APX activities were increased insect feeding, and respond to drought, cold, salt, and water stress (Hu
significantly. In addition, the transcriptional levels of the FeSOD, POD, et al., 2013; Chen et al., 2011a; Wang et al., 2020a). For example, the
CAT, and APX genes and the ascorbate content improved under NaCl regulation of ABA and JA signaling pathways is mediated mainly
salinity and JA treatments (Qiu et al., 2014; Sheteiwy et al., 2021). through MYC2 and AOC1 under adverse abiotic stresses (e.g., drought)
These studies suggest a role for JA in improving salt stress by increasing (Browse, 2009). Both ABA and JA were increased in response to low
the level of antioxidants. temperatures in Z. japonica leaves (Li et al., 2018). Interestingly, the
concentration of ABA increased simultaneously with the increase in JA
1.7. JA and heavy metal stress concentration under salt stress (Wang et al., 2001). Proline accumula­
tion in A. thaliana lines was reported independent of ABA under water
Industrialization emits various metalloids and metals that mediate scarcity. At the same time, JA-insensitive (jai1) and JA-deficient
ecotoxicity or potential phytotoxic impacts on plants. Alteration of some (jar1–1) proteins accumulate at the same levels (de Ollas et al., 2015).
phytohormones is one of the adaptive responses of plants to heavy Moreover, ORA47 functions as a genetic target in ABA/JA biosynthesis
metals toxicity. Jasmonates improve different plant species under heavy under drought stress (Chen et al., 2016). Arabidopsis thaliana and to­
metal stress, and various heavy metals influence the endogenous level of bacco metabolic reprogramming are regulated through signaling be­
jasmonate. Copper (Cu) or cadmium (Cd) stresses rapidly enhance the tween JA and PYRABACTIN RESISTANCE 1-like proteins (PYLs), ABA
endogenous level of JA (Ojuederie and Babalola, 2017). In response to receptors. Plant resistance to herbivorous insect feeding is mediated by
100 µM Cu or 100 µM Cd (Maksymiec et al., 2005), JA increased by 4- forming the PYL-JAZ complex that activates MYC2, which increases the
and 6-fold, respectively. An accumulation of JA 2-fold in response to the JA-responsive gene expression VSP2 by mediating MED25. Additionally,
Cd stress of pepper plants was observed (Yan et al., 2013, 2015). In root initiation and the expression of PTL1 and PTL 2 are inhibited by
addition, increasing the susceptibility of tomato plants to Cd stress was MYC2; moreover, ABA induces JAZ12 degradation, playing a significant
correlated with the lack of endogenous JA. These findings suggested that role in JA/ABA crosstalk (Pauwels et al., 2015).
heavy metal stress influences JA levels. This hypothesis supported the Yan and coworkers reported (Yan et al., 2012a) that mutant OPR7
observations that heavy metal conditions impacted the activation of and OPR8 exhibited propagative deficiency and robust progression ab­
gene expression involved in JA response or biosynthesis. normalities, particularly with substantially reduced JA perception,
The JA-mediated improvement of the growth performance of Choy which were rescued by exogenous JA treatment. One of the crops’ most
sum (Brassica chinensis var. parachinensis L.) under Cr stress was asso­ important adaptation problems and methods to ensure reproductive
ciated with its positive role in cellular redox balance, upregulation of success in either wild-type or developed crops is seed germination time.
water and nutrient uptake, and carbohydrate metabolism. JA improved Furthermore, phytohormones are essential in seed dormancy regulation
the Cr-mediated phytotoxic effects on gas exchange and photosynthetic via compatible and incompatible (antagonistic) interactions. As cross­
pigments on the growth of Choy sum plants (Kamran et al., 2021). In talk with abscisic acid (ABA), JA has a twofold function in seed germi­
response to heavy metal stresses, improving plant tolerance by nation. First, in cold-stimulated seed germination, the level of JA in
increasing the activity of antioxidants was also a practical approach germinating wheat seeds increased considerably after induction of JA
stimulated by JA under heavy metal stress (Raza et al., 2021a). In biosynthesis-associated gene expression, and TaNCED1 and TaNCED2,
addition, JA improved some antioxidants, including ascorbate/gluta­ two critical genes for the ABA pathway, were inhibited (Xu et al., 2016).
thione and glyoxalase, to stimulate plant defense. Moreover, antioxi­ Alternatively, crosstalk between JA and ABA inhibits rice seed germi­
dants efficiently decreased the negative impact of oxidative and nation via the control of the SAPK10-bZIP72-AOC biosynthetic pathway,
carbonyl stresses on Brassica under Cr stress (Kamran et al., 2021). JA which includes phosphorylation of bZIP72 and promotes AOC

8
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

transcription (Wang et al., 2020b). due to JA biosynthesis failure (JA receptor COI1 (coi1–1)), which
resulted in male sterility (Raza et al., 2021b). Liu et al. (2022) observed
2.2. JA–auxin inhibition of the pollen tube formation by exogenous JA and MeJA at
1.0 mM concentration. JA upregulated JA-signal transduction genes
Auxin is a necessary plant hormone to initiate seed development and CoJAZ1, and CoMYC2, especially in self-pollinated styles. The results
regulate cell division (Figueiredo and Köhler, 2018). Plant development suggest that JA signal transduction plays a role in the process of pro­
and physiology are regulated through the coordinated signaling path­ tection against self-pollination, where the JA signal triggers the molec­
ways of JA and auxin. Although auxin deficiency results in the devel­ ular mechanism of inhibiting the growth of self-pollinating pollen tubes.
opment of very short roots, root growth inhibition might be mediated
through JA-auxin (Ursache et al., 2014). JA and auxin antagonize root 2.4. Transcription factors regulating plant stress responses
growth through JAZ–MYC2 activity. Exogenously applied auxin induces
the signaling of auxin–TIR–AUX/IAA–ARF and the JA biosynthesis. The Plant tolerance in response to stressful conditions is regulated by
endogenously produced JA initiates auxin biosynthesis through auxin transcription factors (TFs). They play crucial roles in mediating JA
synthase gene (ASA1) expression, mediating JAZ1 expression and root crosstalk and JA signaling pathways (Fig. 5). The mechanistic roles of
growth. In addition, JA initiates COI1-JAZ complex formation, which ORA59, OsGSK2, and MYC2 TFs and the various JA-associated functions
results in degradation, hence, MYB21/MYB24 transcriptional activities regulated by these TFs are discussed in this review as significant targets
and flower development (Yang et al., 2019). PLETHORA (PTL1 and for phytohormone modulation.
PTL2) gene expression is inhibited by MYC2, which signals aux­
in–TIR–AUX/IAA–ARF to counteract root growth (Chen et al., 2011b). 2.5. ORA59
The development of stamens and petals is regulated by the interactions
between auxin signaling pathway components (ARF6/ARF8), JAZ in JA JA and ethylene (ET) signaling pathways impact the synergistic
signaling pathway components (MYB21/MYB24), and the level of regulation of plant defense under biotic stress. As a critical component of
endogenous JA (Qi et al., 2015b). Additionally, leaf senescence is plant immunity, phytohormone signaling necessitates the interaction of
regulated through JA positive regulation and JA-auxin antagonistic in­ transcription factors and transcriptional reprogramming. Octadecanoid-
teractions. JA promotes senescence through COI1, while MYC2 induces responsive Arabidopsis 59 (ORA59) functions as a critical regulator in the
leaf senescence by expressing senescence-related genes and chlorophyll interplay between JA and ET. ORA59 is a transcription factor of the IX
degradation-associated genes (Qi et al., 2015b; Zhu and Lee, 2015). ethylene response factor (IX ERF) family. It has been suggested that
Moreover, IAA29 and auxin signaling repressors positively regulated ORA59 functions as an integrator in JA/ET signaling pathways and
senescence, while JAZ4, JAZ8, and WRKY57 negatively regulated mediates defense against necrotrophic pathogens (Kim et al., 2018).
senescence (Jiang et al., 2014). The interactions of JA with phytohor­ Resistance to Botrytis cinerea was enhanced through the overexpression
mones are summarized in Table 1. of ORA59, which JA and ethylene regulate to induce plant defense
(Berrocal-Lobo et al., 2002). In addition, a yeast two-hybrid system was
2.3. JA-ethylene used to unravel the molecular function of ORA59 and identify another
VII ERF family member RELATED TO AP2.3 (RAP2.3) (Kim et al., 2018).
Recently, additional JA functions for enhancing plant regeneration Additionally, they elucidated an ethylene-dependent nuclear localiza­
have been discovered (Zhang et al., 2021). For example, JA perception tion that plays an essential role in resistance to Pectobacterium
could reduce quiescent center (QC) quiescence in the root stem cell carotovorum.
niche (SCN) in the model plant Arabidopsis thaliana via the RBR-SCR Moreover, the overexpression of ORA59 antagonizes the SA-
stress protein ETHYLENE RESPONSE FACTOR115 network (ERF115) counteracting effect on PDF1.2 expression mediated through JA (He
(Zhou et al., 2019). Thus, plant growth activation may be induced et al., 2017). ORA59 was reported to regulate the synergistic JA and
during stress circumstances via the JA biological pathway and stem cell ethylene induction of basic chitinase (b-CHI) and PDF1.2 expression
regeneration stimulation. In terms of reproductive growth, JA is essen­ (Pré et al., 2008). Additionally, ORA59 is activated through the synergy
tial for pollen capability, dehiscence, and stamen filament elongation between JA and ethylene. Both JA and ET promote the phosphorylation
(Thines and Mandaokar, 2013). Interestingly, male sterility in plant of ORA59, which is essential for ORA59 activity and specificity (Yang
species is a typical feature of JA deficiency. However, the opr3 and aos et al., 2021). The synergistic action in response to JA and ethylene was
mutants exhibited flaws in Arabidopsis anther and pollen development promoted through the direct binding of ORA59 to GCC boxes of the
PDF1.2 promoter (Zarei et al., 2011).
Table 1
Overview of the crosstalk among phytohormones and their functions of plant 2.6. OsGSK2
growth regulation, development, and biotic or abiotic stress responses.
Phytohormone Responses Components involved The interplay between JA and the signaling pathways of brassinos­
teroids (BRs) is also critical for the developmental stages of plant and
JA–SA Biotic stress (pathogenic MAPK, MYC2, PDF 1.2, GRX,
diseases) TGAs, WRKY70, NAC TFs defense mechanisms. The glycogen synthase kinase 3 (GSK3)–like and
JA–ABA Environmental factors JAZs, MYC2, AOC1, ORA47, kinase OsGSK2 (also named OsGSK7, OsSK22) function as a suppressors
(drought, cold, salinity) PYLs, VSP2, MED25, PTL1, PTL 2 of BR signaling through interactions with variable protein substrates
JA–auxin Growth and development JAZs, MYC2, TIR, AUX, IAA, such as OsBZR1, OsDLT, OsLIC, OsOFP8, and RLA1/SMOS1 (Qiao et al.,
ARF6, ARF8, ASA1, COI1,
MYB21, MYB24, IAA29,
2017; Tong et al., 2012; Yang et al., 2016). BR signaling pathways
WRKY57 regulate plant development through the phosphorylation of OsGSK2 to
JA–GA Plant defense JAZs, DELLAs, MYC2, PIF, OsOFP8, which is critical for its nuclear export to the cytoplasm and
DAD1, LOX subsequent proteasomal degradation (Yang et al., 2016). Either over­
MYB21, MYB24, RGA3
expression of OsGSK2 or the inhibited expression of OsGSK2 through
JA–ET Stress responses (drought, ERFs, AP2, ORA59, ORCA, JAZs,
salinity, cold, and resistance MYC2 iRNA technology were correlated with increasing OsBZR1 phosphory­
to pathogens) EIN3, EIL1, VSP2, PDF1.2., lated form levels (Tong et al., 2012). OsGSK2 acts as a positive regulator
JA-BR Growth and defense OsDI1, OsDWARF, TFs, BAK1, and enhancer of antiviral plant defense by activating JA signaling in rice
BRI1, (Oryza sativa) (He et al., 2020). In addition, OsGSK2 interacts directly
BES1, BZR1, COI1, VSP2, MYC2
with and phosphorylates OsJAZ4. That led to OsJAZ4–OsNINJA and

9
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

Fig. 5. An integrated view of JA biosynthesis at the molecular levels, gene expression regulation, and functional role of JA in helping plant species respond to
stressful conditions.

OsJAZ4–OsJAZ11 disruption, resulting in OsJAZ4 destabilization and JA crosstalk with other plant hormones regulates numerous enzymes
degradation. High levels of BR enhanced rice susceptibility to the and proteins, complex biological pathways, gene networks, and anti­
black-streaked dwarf virus through increasing OsGSK2 activity, result­ oxidants that protect plant cells and tissues against destructive factors in
ing in increased levels of OsJAZ4 and decreased JA signaling (He et al., the surrounding environment. Moreover, thanks to the next-generation
2017). sequencing (NGS) technologies, novel functions of JA, and innovative
signaling pathways have been discovered, providing a new approach to
3. Summary and conclusions the function of JA in response to stressful conditions and plant devel­
opmental processes. However, the signaling pathway of JA is still
Biotic and abiotic stressors affect crop quality and quantity, causing incomplete, similar to a puzzle with some missing pieces. Tran­
losses globally. Therefore, plants must identify and establish critical scriptomics, proteomics, and metabolomics studies will help to under­
mechanisms to tolerate these harmful factors and sustain their devel­ stand the signal pathways of plant hormones and defensive gene
opment and persistence. Essentially, phytohormones (e.g., JA, IAA, SA) expression. Thus, knowledge of genomic clustering and plant stress
participate in plant stress defense and developmental stages by regu­ defense cascades will provide a better knowledge of the capability
lating stress-responsive genes and synthetic hormone pathways. In mitigation of plants under unfavorable conditions. In addition, this
addition, JA plays crucial roles in crop development at different growth knowledge will improve plant adaptability and resilience under climate
stages, including seed germination, root system formation, anther, pol­ change, increasing crop yield and providing novel future green agri­
len development, tissue regeneration, flowering time, and stomatal culture opportunities.
closure and reopening. In general, due to the diversity of phytohormone
signalings and the numerous genes (i.e., JAZ, AOS1) involved in the JA Funding
synthetic pathways and TFs (MYC2). Therefore, further research on the
interactions among plant hormones under various environmental stress Marek Zivcak and Marian Brestic were supported by the Science
is needed to study the underlying mechanisms controlling the inhibitors Grant Agency (VEGA) of The Ministry of Education, Science, Research
and activators of JA pathways. and Sport of the Slovak Republic under the grant no. VEGA 1/0664/22.

10
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

The results (Fig. 4) were obtained within the state assignment of the enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma
248, 601–612.
Ministry of Science and Higher Education of the Russian Federation,
Ahuja, I., Kissen, R., Bones, A.M., 2012. Phytoalexins in defense against pathogens.
Russia (theme No. 122050400128–1). Trends Plant Sci. 17, 73–90.
Ali, M.S., Baek, K.-H., 2020. Jasmonic acid signaling pathway in response to abiotic
stresses in plants. Int. J. Mol. Sci. 21, 621.
CRediT authorship contribution statement Altaf, M.A., Shahid, R., Kumar, R., Altaf, M.M., Kumar, A., Khan, L.U., Saqib, M.,
Nawaz, M.A., Saddiq, B., Bahadur, S., 2022. Phytohormones mediated modulation of
Omar A. Hewedy, Nabil I. Elsheery, Ali M. Karkour: Conceptu­ abiotic stress tolerance and potential crosstalk in horticultural crops. J. Plant Growth
Regul. 1–27.
alization. Ramadan A. Arafa, Ghada Abd-Elmonsef Mahmoud:
Arif, Y., Singh, P., Siddiqui, H., Bajguz, A., Hayat, S., 2020. Salinity induced
Methodology. Neveen Elhamouly: Software. Ghada Abd-Elmonsef physiological and biochemical changes in plants: An omic approach towards salt
Mahmoud, Mona F.-A. Dawood, Walaa E. Hussein: Validation. stress tolerance. Plant Physiol. Biochem. 156, 64–77.
Awan, S.A., Khan, I., Rizwan, M., Zhang, X., Brestic, M., Khan, A., El-Sheikh, M.A.,
Omar A. Hewedy, Nabil I. Elsheery, Ali M. Karkour, Neveen Elha­
Alyemeni, M.N., Ali, S., Huang, L., 2021. Exogenous abscisic acid and jasmonic acid
mouly, Ramadan A. Arafa, Ghada Abd-Elmonsef Mahmoud: Formal restrain polyethylene glycol-induced drought by improving the growth and
analysis. Omar A. Hewedy, Nabil I. Elsheery, Ali M. Karkour, Ghada antioxidative enzyme activities in pearl millet. Physiol. Plant. 172, 809–819.
Abd-Elmonsef Mahmoud, Mona F.-A. Dawood, Walaa E. Hussein, Azeem, U., 2018. Ameliorating Nickel stress by Jasmonic acid treatment in Zea mays L.
Russ. Agric. Sci. 44, 209–215.
Abdelaziz Mansour: Investigation. Omar A. Hewedy, Nabil I. Balbi, V., Devoto, A., 2008. Jasmonate signalling network in Arabidopsis thaliana:
Elsheery, Ali M. Karkour, Neveen Elhamouly, Ramadan A. Arafa, crucial regulatory nodes and new physiological scenarios. N. Phytol. 177, 301–318.
Ghada Abd-Elmonsef Mahmoud, Mona F.-A. Dawood: Resources. Bao, J., Lu, X., Ma, L., Zhang, X., Tian, P., Zhang, X., Li, S., Ma, S., Yang, J., Lu, Y.,
Wei, Y., Zhang, C., Shi, X., 2022. Transcriptome analysis of genes related to
Omar A. Hewedy, Ghada Abd-Elmonsef Mahmoud, Mona F.-A. glucoraphanin and sulforaphane synthesis in methyl jasmonate treated broccoli
Dawood, Walaa E. Hussein, Abdelaziz Mansour, Dina H. Amin: (Brassica oleracea var. italica) hairy roots. J. Plant Res. 135, 757–770. https://doi.
Data curation. Omar A. Hewedy: Writing − original draft preparation. org/10.1007/s10265-022-01407-7.
Barboričová, M., Filaček, A., Mlynáriková Vysoká, D., Gašparovič, K., Živčák, M.,
Omar A. Hewedy, Abdelaziz Mansour, Dina H. Amin, Marian Brestič, M., 2022. Sensitivity of fast chlorophyll fluorescence parameters to
Brestic, Suleyman I. Allakhverdiev, Marek Zivcak: Writing − review combined heat and drought stress in wheat genotypes. Plant Soil Environ. 68,
& editing. Omar A. Hewedy, Neveen Elhamouly, Ramadan A. Arafa, 309–316.
Begum, S., Jing, S.L., Yu, L., Sun, X., Wang, E., Kawochar, M.A., Qin, J., Liu, J., Song, B.,
Ghada Abd-Elmonsef Mahmoud, Mona F.-A. Dawood, Walaa E.
2022. Modulation of JA signalling reveals the influence of StJAZ1-like on tuber
Hussein, Abdelaziz Mansour: Visualization. Nabil I. Elsheery, Mona initiation and tuber bulking in potato. Plant J. 109 (4), 952–964.
F.-A. Dawood, Omar A. Hewedy, Suleyman I. Allakhverdiev, Berger, S., Bell, E., Mullet, J.E., 1996. Two methyl jasmonate-insensitive mutants show
altered expression of AtVsp in response to methyl jasmonate and wounding. Plant
Marian Brestic, Marek Zivcak: Supervision. Nabil I. Elsheery: Project
Physiol. 111, 525–531.
administration. Neveen Elhamouly, Abdelaziz Mansour, Dina H. Berrocal-Lobo, M., Molina, A., Solano, R., 2002. Constitutive expression of ETHYLENE-
Amin, Marian Brestic, Suleyman I. Allakhverdiev, Marek Zivcak, RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic
Nabil I. Elsheery: Funding acquisition. All authors have read and fungi. Plant J. 29, 23–32.
Betti, C., Della Rovere, F., Piacentini, D., Fattorini, L., Falasca, G., Altamura, M.M., 2021.
agreed with the final version. Jasmonates, ethylene and brassinosteroids control adventitious and lateral rooting as
stress avoidance responses to heavy metals and metalloids. Biomolecules 11, 77.
Browse, J., 2005. Jasmonate: an oxylipin signal with many roles in plants. Vitam. Horm.
Declaration of Competing Interest 72, 431–456.
Browse, J., 2009. Jasmonate passes muster: a receptor and targets for the defense
hormone. Annu. Rev. Plant Biol. 60, 183–205.
The authors declare the following financial interests/personal re­ Bulgakov, V.P., Tchernoded, G.K., Veselova, M.V., Fedoreyev, S.A., Muzarok, T.I.,
lationships which may be considered as potential competing interests. Zhuravlev, Y.N., 2011. Catechin production in cultured cells of Taxus cuspidata and
Marek Zivcak, Marian Brestic reports financial support was provided by Taxus baccata. Biotechnol. Lett. 33, 1879–1883.
Campos, M.L., Kang, J.-H., Howe, G.A., 2014. Jasmonate-triggered plant immunity.
Cultural and Educational Grant Agency of the Ministry of Education J. Chem. Ecol. 40, 657–675.
Science Research and Sport of the Slovak Republic. Suleyman I. Chakraborty, S., Newton, A.C., 2011. Climate change, plant diseases and food security:
Allakhverdiev reports financial support was provided by Ministry of an overview. Plant Pathol. 60, 2–14.
Chaudhry, S., Sidhu, G.P.S., 2022. Climate change regulated abiotic stress mechanisms in
Science and Higher Education of the Russian Federation.
plants: a comprehensive review. Plant Cell Rep. 41, 1–31.
Chavan, J.J., Kshirsagar, P.R., Jadhav, S.G., Nalavade, V.M., Gurme, S.T., Pai, S.R., 2021.
Data availability Elicitor-mediated enhancement of biomass, polyphenols, mangiferin production and
antioxidant activities in callus cultures of Salacia chinensis L. 3 Biotech 11, 1–11.
Chen, H.-Y., Hsieh, E.-J., Cheng, M.-C., Chen, C.-Y., Hwang, S.-Y., Lin, T.-P., 2016.
No data was used for the research described in the article. ORA47 (octadecanoid-responsive AP2/ERF-domain transcription factor 47)
regulates jasmonic acid and abscisic acid biosynthesis and signaling through binding
to a novel cis-element. N. Phytol. 211, 599–613. https://doi.org/10.1111/
Acknowledgment nph.13914.
Chen, Q., Sun, J., Zhai, Q., Zhou, W., Qi, L., Xu, L., Wang, B., Chen, R., Jiang, H., Qi, J.,
Omar A. Hewedy was supported by a generous scholarship from the 2011a. The basic helix-loop-helix transcription factor MYC2 directly represses
PLETHORA expression during jasmonate-mediated modulation of the root stem cell
Government of Egypt.
niche in Arabidopsis. Plant Cell 23, 3335–3352.
Chen, Q., Sun, J., Zhai, Q., Zhou, W., Qi, L., Xu, L., Wang, B., Chen, R., Jiang, H., Qi, J.,
References Li, X., Palme, K., Li, C., 2011b. The Basic Helix-Loop-Helix Transcription Factor
MYC2 Directly Represses PLETHORA Expression during Jasmonate-Mediated
Modulation of the Root Stem Cell Niche in Arabidopsis. Plant Cell 23, 3335–3352.
Abdelgawad, Z., Khalafaallah, A.A., Abdallah, M., 2014. Impact of methyl jasmonate on
https://doi.org/10.1105/tpc.111.089870.
antioxidant activity and some biochemical aspects of maize plant grown under water
Cheng, H., Song, S., Xiao, L., Soo, H.M., Cheng, Z., Xie, D., Peng, J., 2009. Gibberellin
stress condition. Agric. Sci. 5, 1077.
acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to
Abdelsalam, A., Mahran, E., Chowdhury, K., Boroujerdi, A., El-Bakry, A., 2021. Effect of
promote stamen filament growth in Arabidopsis. PLoS Genet. 5, e1000440.
exogenous methyl jasmonate on in vitro propagation, metabolic profiling and
Corti Monzón, G., Pinedo, M., Lamattina, L., De La Canal, L., 2012. Sunflower root
proximadiol production from Cymbopogon schoenanthus subsp. proximus. Plant
growth regulation: the role of jasmonic acid and its relation with auxins. Plant
Physiol. Rep. 26, 548–560.
Growth Regul. 66, 129–136.
Abouelsaad, I., Renault, S., 2018. Enhanced oxidative stress in the jasmonic acid-
Creelman, R.A., Mullet, J.E., 1995. Jasmonic acid distribution and action in plants:
deficient tomato mutant def-1 exposed to NaCl stress. J. Plant Physiol. 226, 136–144.
regulation during development and response to biotic and abiotic stress. Proc. Natl.
Acharya, B.R., Assmann, S.M., 2009. Hormone interactions in stomatal function. Plant
Acad. Sci. 92, 4114–4119.
Mol. Biol. 69, 451–462.
Dawood, M.F., Zaid, A., Latef, A.A.H.A., 2022. Salicylic acid spraying-induced resilience
Acosta, I.F., Laparra, H., Romero, S.P., Schmelz, E., Hamberg, M., Mottinger, J.P.,
strategies against the damaging impacts of drought and/or salinity stress in two
Moreno, M.A., Dellaporta, S.L., 2009. Tasselseed1 is a lipoxygenase affecting
varieties of Vicia faba L. seedlings. J. Plant Growth Regul. 41, 1919–1942.
jasmonic acid signaling in sex determination of maize. Science 323, 262–265.
Aftab, T., Khan, M., Idrees, M., Naeem, M., Hashmi, N., 2011. Methyl jasmonate
counteracts boron toxicity by preventing oxidative stress and regulating antioxidant

11
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

De Domenico, S., Taurino, M., Gallo, A., Poltronieri, P., Pastor, V., Flors, V., Santino, A., Jiang, M., Xu, F., Peng, M., Huang, F., Meng, F., 2016. Methyl jasmonate regulated
2019. Oxylipin dynamics in Medicago truncatula in response to salt and wounding diploid and tetraploid black locust (Robinia pseudoacacia L.) tolerance to salt stress.
stresses. Physiol. Plant. 165, 198–208. Acta Physiol. Plant. 38, 1–13.
Dixon, R.A., 2001. Natural products and plant disease resistance. Nature 411, 843–847. Jiang, Y., Liang, G., Yang, S., Yu, D., 2014. Arabidopsis WRKY57 Functions as a Node of
Dodds, P.N., Rathjen, J.P., 2010. Plant immunity: towards an integrated view of Convergence for Jasmonic Acid– and Auxin-Mediated Signaling in Jasmonic
plant–pathogen interactions. Nat. Rev. Genet. 11, 539–548. Acid–Induced Leaf Senescence. Plant Cell 26, 230–245. https://doi.org/10.1105/
Doğan, S., Çağlar, G., Palaz, E.B., 2020. The effect of different applications on in vitro tpc.113.117838.
bulb development of an endemic hyacinth plant (Hyacinthus orientalis l. subsp. Jing, S., Begum, S., Yu, L., Kawochar, M.A., Wang, E., Chen, Y., Song, B., 2022. StJAZ1-
chionophyllus Wendelbo) grown in Turkey. Turk. J. Agric. -Food Sci. Technol. 8, like mediated root architecture plays critical roles in drought susceptibility in potato.
1713–1719. Environ. Exp. Bot. 202, 105008.
Faghih, S., Ghobadi, C., Zarei, A., 2017. Response of strawberry plant cv. ’Camarosa’to Jones, J.D., Dangl, J.L., 2006. The plant immune system. Nature 444, 323–329.
salicylic acid and methyl jasmonate application under salt stress condition. J. Plant Kamińska, M., 2021. Role and activity of jasmonates in plants under in vitro conditions.
Growth Regul. 36, 651–659. Plant Cell, Tissue Organ Cult. (PCTOC) 146 (3), 425–447.
Farhangi-Abriz, S., Ghassemi-Golezani, K., 2018. How can salicylic acid and jasmonic Kamran, M., Wang, D., Alhaithloul, H.A.S., Alghanem, S.M., Aftab, T., Xie, K., Lu, Y.,
acid mitigate salt toxicity in soybean plants? Ecotoxicol. Environ. Saf. 147, Shi, C., Sun, J., Gu, W., 2021. Jasmonic acid-mediated enhanced regulation of
1010–1016. oxidative, glyoxalase defense system and reduced chromium uptake contributes to
Farooq, M.A., Gill, R.A., Islam, F., Ali, B., Liu, H., Xu, J., He, S., Zhou, W., 2016. Methyl alleviation of chromium (VI) toxicity in choysum (Brassica parachinensis L.).
jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica Ecotoxicol. Environ. Saf. 208, 111758.
napus L. Front. Plant Sci. 7, 468. Karpets, Y.V., Kolupaev, Y.E., Lugovaya, A.A., Oboznyi, A.I., 2014. Effect of jasmonic
Figueiredo, D.D., Köhler, C., 2018. Auxin: a molecular trigger of seed development. acid on the pro-/antioxidant system of wheat coleoptiles as related to hyperthermia
Genes Dev. 32, 479–490. tolerance. Russ. J. Plant Physiol. 61, 339–346. https://doi.org/10.1134/
Friero, I., Larriba, E., Martínez-Melgarejo, P.A., Justamante, M.S., Alarcón, M.V., S102144371402006X.
Albacete, A., Salguero, J., Pérez-Pérez, J.M., 2022. Transcriptomic and hormonal Kim, E.H., Kim, Y.S., Park, S.-H., Koo, Y.J., Choi, Y.D., Chung, Y.-Y., Lee, I.-J., Kim, J.-K.,
analysis of the roots of maize seedlings grown hydroponically at low temperature. 2009. Methyl jasmonate reduces grain yield by mediating stress signals to alter
Plant Sci., 111525 spikelet development in rice. Plant Physiol. 149, 1751–1760.
Fu, J., Wu, H., Ma, S., Xiang, D., Liu, R., Xiong, L., 2017. OsJAZ1 attenuates drought Kim, H., Seomun, S., Yoon, Y., Jang, G., 2021. Jasmonic acid in plant abiotic stress
resistance by regulating JA and ABA signaling in rice. Front. Plant Sci. 8, 2108. tolerance and interaction with abscisic acid. Agronomy 11, 1886.
Fu, X., Li, X., Ali, M., Zhao, X., Min, D., Liu, J., Li, F., Zhang, X., 2023. Methionine Kim, N.Y., Jang, Y.J., Park, O.K., 2018. AP2/ERF family transcription factors ORA59 and
sulfoxide reductase B5 plays vital roles in tomato fruit defense response against RAP2. 3 interact in the nucleus and function together in ethylene responses. Front.
Botrytis cinerea induced by methyl jasmonate. Postharvest Biol. Technol. 196, Plant Sci. 9, 1675.
112165 https://doi.org/10.1016/j.postharvbio.2022.112165. Koda, Y., Kikuta, Y., 1991. Possible involvement of jasmonic acid in tuberization of yam
Fugate, K.K., Lafta, A.M., Eide, J.D., Li, G., Lulai, E.C., Olson, L.L., Deckard, E.L., plants. Plant Cell Physiol. 32, 629–633.
Khan, M.F., Finger, F.L., 2018. Methyl jasmonate alleviates drought stress in young Kolomiets, M.V., Hannapel, D.J., Chen, H., Tymeson, M., Gladon, R.J., 2001.
sugar beet (Beta vulgaris L.) plants. J. Agron. Crop Sci. 204, 566–576. Lipoxygenase is involved in the control of potato tuber development. Plant Cell 13,
Ghorbel, M., Brini, F., Sharma, A., Landi, M., 2021. Role of jasmonic acid in plants: The 613–626.
molecular point of view. Plant Cell Rep. 40, 1471–1494. Krajnčič, B., Nemec, J., 1995. The effect of jasmonic acid on flowering in Spirodela
Gimenez-Ibanez, S., Boter, M., Ortigosa, A., García-Casado, G., Chini, A., Lewsey, M.G., polyrrhiza (L.) Schleiden. J. Plant Physiol. 146, 754–756.
Ecker, J.R., Ntoukakis, V., Solano, R., 2017. JAZ 2 controls stomata dynamics during Ku, Y.-S., Sintaha, M., Cheung, M.-Y., Lam, H.-M., 2018. Plant hormone signaling
bacterial invasion. N. Phytol. 213, 1378–1392. crosstalks between biotic and abiotic stress responses. Int. J. Mol. Sci. 19, 3206.
Goetz, S., Hellwege, A., Stenzel, I., Kutter, C., Hauptmann, V., Forner, S., McCaig, B., Lakehal, A., Chaabouni, S., Cavel, E., Le Hir, R., Ranjan, A., Raneshan, Z., Novák, O.,
Hause, G., Miersch, O., Wasternack, C., 2012. Role of cis-12-oxo-phytodienoic acid Păcurar, D.I., Perrone, I., Jobert, F., 2019. A molecular framework for the control of
in tomato embryo development. Plant Physiol. 158, 1715–1727. adventitious rooting by TIR1/AFB2-Aux/IAA-dependent auxin signaling in
Gomez-Cadenas, A., Vives, V., I Zandalinas, S., Manzi, M., M Sanchez-Perez, A., M Perez- Arabidopsis. Mol. Plant 12, 1499–1514.
Clemente, R., Arbona, V., 2015. Abscisic acid: a versatile phytohormone in plant Lei, G.J., Sun, L., Sun, Y., Zhu, X.F., Li, G.X., Zheng, S.J., 2020. Jasmonic acid alleviates
signaling and beyond. Curr. Protein Pept. Sci. 16, 413–434. cadmium toxicity in Arabidopsis via suppression of cadmium uptake and
Gumerova, E., Akulov, A., Rumyantseva, N., 2015. Effect of methyl jasmonate on growth translocation. J. Integr. Plant Biol. 62, 218–227.
characteristics and accumulation of phenolic compounds in suspension culture of Li, C., Shi, L., Li, X., Wang, Y., Bi, Y., Li, W., Ma, H., Chen, B., Zhu, L., Fu, Y., 2022. ECAP
tartary buckwheat. Russ. J. Plant Physiol. 62, 195–203. is a key negative regulator mediating different pathways to modulate salt stress-
Günther, C.S., Plunkett, B.J., Cooney, J.M., Jensen, D.J., Trower, T.M., Elborough, C., induced anthocyanin biosynthesis in Arabidopsis. N. Phytol. 233, 2216–2231.
Nguyen, H.M., Deng, C.H., Lafferty, D.J., Albert, N.W., 2022. Biotic stress-induced Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E.,
and ripening-related anthocyanin biosynthesis are regulated by alternate Howe, G.A., 2004. The tomato homolog of CORONATINE-INSENSITIVE1 is required
phytohormone signals in blueberries. Environ. Exp. Bot. 203, 105065. for the maternal control of seed maturation, jasmonate-signaled defense responses,
Hann, D.R., Gimenez-Ibanez, S., Rathjen, J.P., 2010. Bacterial virulence effectors and and glandular trichome development. Plant Cell 16, 126–143.
their activities. Curr. Opin. Plant Biol. 13, 388–393. Li, S., Yang, Y., Zhang, Q., Liu, N., Xu, Q., Hu, L., 2018. Differential physiological and
He, X., Jiang, J., Wang, C.Q., Dehesh, K., 2017. ORA59 and EIN3 interaction couples metabolic response to low temperature in two zoysiagrass genotypes native to high
jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF and low latitude. PLoS One 13, e0198885.
expression. J. Integr. Plant Biol. 59, 275–287. Li, Y., Jiang, J., Du, M.-L., Li, L., Wang, X.-L., Li, X.-B., 2013. A cotton gene encoding
He, Y., Hong, G., Zhang, H., Tan, X., Li, L., Kong, Y., Sang, T., Xie, K., Wei, J., Li, J., 2020. MYB-like transcription factor is specifically expressed in pollen and is involved in
The OsGSK2 kinase integrates brassinosteroid and jasmonic acid signaling by regulation of late anther/pollen development. Plant Cell Physiol. 54, 893–906.
interacting with OsJAZ4. Plant Cell 32, 2806–2822. Li, Y., Xu, J., Li, G., Wan, S., Batistič, O., Sun, M., Zhang, Y., Scott, R., Qi, B., 2019.
Hentrich, M., Böttcher, C., Düchting, P., Cheng, Y., Zhao, Y., Berkowitz, O., Masle, J., Protein S-acyl transferase 15 is involved in seed triacylglycerol catabolism during
Medina, J., Pollmann, S., 2013. The jasmonic acid signaling pathway is linked to early seedling growth in Arabidopsis. J. Exp. Bot. 70, 5205–5216.
auxin homeostasis through the modulation of YUCCA 8 and YUCCA 9 gene Liu, Y., Zhou, J., Lu, M., Yang, J., Tan, X., 2022. The core jasmonic acid-signalling
expression. Plant J. 74, 626–637. module CoCOI1/CoJAZ1/CoMYC2 are involved in jas mediated growth of the pollen
Hewedy, O.A., Mahmoud, G.A.-E., Elshafey, N.F., Khamis, G., Karkour, A.M., Lateif, K.S. tube in Camellia oleifera. Curr. Iss Molec Biol. 44 (11), 5405–5415.
A., Amin, B.H., Chiab, N., El-Taher, A.M., Elsheery, N.I., 2022. Plants take action to Lv, T., Li, X., Fan, T., Luo, H., Xie, C., Zhou, Y., Tian, C.-e, 2019. The calmodulin-binding
mitigate salt stress: Ask microbe for help, phytohormones, and genetic approaches. protein IQM1 interacts with CATALASE2 to affect pathogen defense. Plant Physiol.
J. Water Land Dev. 1-16-11-16. 181, 1314–1327.
Hou, X., Ding, L., Yu, H., 2013. Crosstalk between GA and JA signaling mediates plant Macho, A.P., Zipfel, C., 2014. Plant PRRs and the activation of innate immune signaling.
growth and defense. Plant Cell Rep. 32, 1067–1074. Mol. Cell 54, 263–272.
Hu, Y., Jiang, L., Wang, F., Yu, D., 2013. Jasmonate regulates the inducer of CBF Maksymiec, W., Wianowska, D., Dawidowicz, A.L., Radkiewicz, S., Mardarowicz, M.,
expression–c-repeat binding factor/DRE binding factor1 cascade and freezing Krupa, Z., 2005. The level of jasmonic acid in Arabidopsis thaliana and Phaseolus
tolerance in Arabidopsis. Plant Cell 25, 2907–2924. coccineus plants under heavy metal stress. J. Plant Physiol. 162, 1338–1346.
Hu, Y., Jiang, Y., Han, X., Wang, H., Pan, J., Yu, D., 2017. Jasmonate regulates leaf Mandaokar, A., Browse, J., 2009. MYB108 acts together with MYB24 to regulate
senescence and tolerance to cold stress: crosstalk with other phytohormones. J. Exp. jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol. 149, 851–862.
Bot. 68, 1361–1369. Mira, M.M., Wally, O.S., Elhiti, M., El-Shanshory, A., Reddy, D.S., Hill, R.D., Stasolla, C.,
Huang, H., Liu, B., Liu, L., Song, S., 2017. Jasmonate action in plant growth and 2016. Jasmonic acid is a downstream component in the modulation of somatic
development. J. Exp. Bot. 68 (6), 1349–1359. embryogenesis by Arabidopsis Class 2 phytoglobin. J. Exp. Bot. 67, 2231–2246.
Ibrahimova, U., Zivcak, M., Gasparovic, K., Rastogi, A., Allakhverdiev, S.I., Yang, X., Mohamed, H.I., Latif, H.H., 2017. Improvement of drought tolerance of soybean plants
Brestic, M., 2021. Electron and proton transport in wheat exposed to salt stress: is the by using methyl jasmonate. Physiology and Molecular Biology of Plants, 23,
increase of the thylakoid membrane proton conductivity responsible for decreasing 545–556.
the photosynthetic activity in sensitive genotypes? Photosynth. Res. 150, 195–211. Mosa, K.A., Ismail, A., Helmy, M., 2017. Introduction to plant stresses. Plant Stress
Jewell, J.B., Browse, J., 2016. Epidermal jasmonate perception is sufficient for all aspects Tolerance. Springer,, pp. 1–19.
of jasmonate-mediated male fertility in Arabidopsis. Plant J. 85, 634–647. Motte, H., Vanneste, S., Beeckman, T., 2019. Molecular and environmental regulation of
root development. Annu. Rev. Plant Biol. 70, 465–488.

12
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

Munemasa, S., Oda, K., Watanabe-Sugimoto, M., Nakamura, Y., Shimoishi, Y., Reymond, P., Weber, H., Damond, M., Farmer, E.E., 2000. Differential gene expression in
Murata, Y., 2007. The coronatine-insensitive 1 mutation reveals the hormonal response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12,
signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis 707–719.
guard cells. Specific impairment of ion channel activation and second messenger Riemann, M., Dhakarey, R., Hazman, M., Miro, B., Kohli, A., Nick, P., 2015. Exploring
production. Plant Physiol. 143, 1398–1407. jasmonates in the hormonal network of drought and salinity responses. Front. Plant
Nagpal, P., Ellis, C.M., Weber, H., Ploense, S.E., Barkawi, L.S., Guilfoyle, T.J., Hagen, G., Sci. 6, 1077.
Alonso, J.M., Cohen, J.D., Farmer, E.E., 2005. Auxin response factors ARF6 and Rivero, R.M., Mittler, R., Blumwald, E., Zandalinas, S.I., 2022. Developing climate-
ARF8 promote jasmonic acid production and flower maturation. Development 132, resilient crops: improving plant tolerance to stress combination. Plant J. 109,
4107–4118. 373–389.
Nandy, S., Hazra, A.K., Pandey, D.K., Ray, P., Dey, A., 2021. Elicitation of industrially Saniewski, M., Puchalski, J., 1987. The effect of methyl jasmonate and abscisic acid on
promising vanillin type aromatic compound 2-hydroxy 4-methoxy benzaldehyde differentiation of benzyladenine-induced bulblets inMuscari bulbs. Biol. Plant. 29,
(MBAlD) yield in the in-vitro raised medicinal crop Hemidesmus indicus (L) R. Br. by 63–65.
methyl jasmonate and salicylic acid. Ind. Crops Prod. 164, 113375. Santos, I., Salema, R., 2000. Promotion by Jasmonic acid of bulb formation in shoot
Noriega, G., Cruz, D.S., Batlle, A., Tomaro, M., Balestrasse, K., 2012. Heme oxygenase is cultures of Narcissus triandrus L. Plant Growth Regul. 30, 133–138.
involved in the protection exerted by jasmonic acid against cadmium stress in Schubert, R., Dobritzsch, S., Gruber, C., Hause, G., Athmer, B., Schreiber, T.,
soybean roots. J. Plant Growth Regul. 31, 79–89. Marillonnet, S., Okabe, Y., Ezura, H., Acosta, I.F., 2019. Tomato MYB21 acts in
Ojuederie, O.B., Babalola, O.O., 2017. Microbial and plant-assisted bioremediation of ovules to mediate jasmonate-regulated fertility. Plant Cell 31, 1043–1062.
heavy metal polluted environments: a review. Int. J. Environ. Res. Public Health 14, Seleiman, M.F., Al-Suhaibani, N., Ali, N., Akmal, M., Alotaibi, M., Refay, Y.,
1504. Dindaroglu, T., Abdul-Wajid, H.H., Battaglia, M.L., 2021. Drought stress impacts on
de Ollas, C., Hernando, B., Arbona, V., Gómez-Cadenas, A., 2013. Jasmonic acid transient plants and different approaches to alleviate its adverse effects. Plants 10, 259.
accumulation is needed for abscisic acid increase in citrus roots under drought stress Shahzad, A., Pitann, B., Ali, H., Qayyum, M., Fatima, A., Bakhat, H., 2015. Maize
conditions. Physiol. Plant. 147, 296–306. genotypes differing in salt resistance vary in jasmonic acid accumulation during the
de Ollas, C., Arbona, V., Gómez-Cadenas, A., 2015. Jasmonic acid interacts with abscisic first phase of salt stress. J. Agron. Crop Sci. 201, 443–451.
acid to regulate plant responses to water stress conditions. Plant Signal. Behav. 10, Sharma, A., Kumar, V., Shahzad, B., Ramakrishnan, M., Singh Sidhu, G.P., Bali, A.S.,
e1078953 https://doi.org/10.1080/15592324.2015.1078953. Handa, N., Kapoor, D., Yadav, P., Khanna, K., 2020. Photosynthetic response of
Osmont, K.S., Sibout, R., Hardtke, C.S., 2007. Hidden branches: developments in root plants under different abiotic stresses: a review. J. Plant Growth Regul. 39, 509–531.
system architecture. Annu. Rev. Plant Biol. 58, 93–113. Sheard, L.B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T.R., Kobayashi, Y.,
Park, J.H., Halitschke, R., Kim, H.B., Baldwin, I.T., Feldmann, K.A., Feyereisen, R., 2002. Hsu, F.-F., Sharon, M., Browse, J., 2010. Jasmonate perception by inositol-
A knock-out mutation in allene oxide synthase results in male sterility and defective phosphate-potentiated COI1–JAZ co-receptor. Nature 468, 400–405.
wound signal transduction in Arabidopsis due to a block in jasmonic acid Sheteiwy, M.S., Shao, H., Qi, W., Daly, P., Sharma, A., Shaghaleh, H., Hamoud, Y.A., El-
biosynthesis. Plant J. 31, 1–12. Esawi, M.A., Pan, R., Wan, Q., 2021. Seed priming and foliar application with
Pauwels, L., Morreel, K., De Witte, E., Lammertyn, F., Van Montagu, M., Boerjan, W., jasmonic acid enhance salinity stress tolerance of soybean (Glycine max L.)
Inzé, D., Goossens, A., 2008. Mapping methyl jasmonate-mediated transcriptional seedlings. J. Sci. Food Agric. 101, 2027–2041.
reprogramming of metabolism and cell cycle progression in cultured Arabidopsis Shih, C.-F., Hsu, W.-H., Peng, Y.-J., Yang, C.-H., 2014. The NAC-like gene ANTHER
cells. Proc. Natl. Acad. Sci. 105, 1380–1385. INDEHISCENCE FACTOR acts as a repressor that controls anther dehiscence by
Pauwels, L., Ritter, A., Goossens, J., Durand, A.N., Liu, H., Gu, Y., Geerinck, J., Boter, M., regulating genes in the jasmonate biosynthesis pathway in Arabidopsis. J. Exp. Bot.
Vanden Bossche, R., De Clercq, R., Van Leene, J., Gevaert, K., De Jaeger, G., 65, 621–639.
Solano, R., Stone, S., Innes, R.W., Callis, J., Goossens, A., 2015. The RING E3 Ligase Shikha, D., Jakhar, P., Satbhai, S.B., 2022, Role of Jasmonate signaling in regulation of
KEEP ON GOING Modulates JASMONATE ZIM-DOMAIN12 Stability. Plant Physiol. plant responses to nutrient deficiency stresses. Journal of Experimental Botany.
169, 1405–1417. https://doi.org/10.1104/pp.15.00479. Sirhindi, G., Mir, M.A., Sharma, P., Gill, S.S., Kaur, H., Mushtaq, R., 2015. Modulatory
Pedranzani, H., Racagni, G., Alemano, S., Miersch, O., Ramírez, I., Peña-Cortés, H., role of jasmonic acid on photosynthetic pigments, antioxidants and stress markers of
Taleisnik, E., Machado-Domenech, E., Abdala, G., 2003. Salt tolerant tomato plants Glycine max L. under nickel stress. Physiol. Mol. Biol. Plants 21, 559–565.
show increased levels of jasmonic acid. Plant Growth Regul. 41, 149–158. https:// Song, S., Qi, T., Huang, H., Ren, Q., Wu, D., Chang, C., Peng, W., Liu, Y., Peng, J., Xie, D.,
doi.org/10.1023/A:1027311319940. 2011. The jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription
Per, T.S., Khan, M.I.R., Anjum, N.A., Masood, A., Hussain, S.J., Khan, N.A., 2018. factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in
Jasmonates in plants under abiotic stresses: Crosstalk with other phytohormones Arabidopsis. Plant Cell 23, 1000–1013.
matters. Environ. Exp. Bot. 145, 104–120. Spoel, S.H., Dong, X., 2012. How do plants achieve immunity? Defence without
Pernas, M., Sánchez-Monge, R., Salcedo, G., 2000. Biotic and abiotic stress can induce specialized immune cells. Nat. Rev. Immunol. 12, 89–100.
cystatin expression in chestnut. FEBS Lett. 467, 206–210. Stintzi, A., Weber, H., Reymond, P., Browse, J., Farmer, E.E., 2001, Plant defense in the
Podwyszyńska, M., Kosson, R., Treder, J., 2015. Polyamines and methyl jasmonate in absence of jasmonic acid: the role of cyclopentenones. Proceedings of the National
bulb formation of in vitro propagated tulips. Plant Cell, Tissue Organ Cult. (PCTOC) Academy of Sciences 98, 12837–12842.
123, 591–605. Suhita, D., Raghavendra, A.S., Kwak, J.M., Vavasseur, A., 2004. Cytoplasmic alkalization
Pré, M., Atallah, M., Champion, A., De Vos, M., Pieterse, C.M., Memelink, J., 2008. The precedes reactive oxygen species production during methyl jasmonate-and abscisic
AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene acid-induced stomatal closure. Plant Physiol. 134, 1536–1545.
signals in plant defense. Plant Physiol. 147, 1347–1357. Sun, J., Xu, Y., Ye, S., Jiang, H., Chen, Q., Liu, F., Zhou, W., Chen, R., Li, X., Tietz, O.,
Qi, T., Huang, H., Song, S., Xie, D., 2015a. Regulation of jasmonate-mediated stamen 2009. Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin
development and seed production by a bHLH-MYB complex in Arabidopsis. Plant biosynthesis and transport during lateral root formation. Plant Cell 21, 1495–1511.
Cell 27, 1620–1633. Sun, T., Zhang, J., Zhang, Q., Li, X., Li, M., Yang, Y., Zhou, J., Wei, Q., Zhou, B., 2022.
Qi, T., Wang, J., Huang, H., Liu, B., Gao, H., Liu, Y., Song, S., Xie, D., 2015b. Regulation Exogenous application of acetic acid enhances drought tolerance by influencing the
of Jasmonate-Induced Leaf Senescence by Antagonism between bHLH Subgroup IIIe MAPK signaling pathway induced by ABA and JA in apple plants. Tree Physiol.
and IIId Factors in Arabidopsis. Plant Cell 27, 1634–1649. https://doi.org/10.1105/ Swiatek, A., Lenjou, M., Van Bockstaele, D., Inzé, D., Van Onckelen, H., 2002.
tpc.15.00110. Differential effect of jasmonic acid and abscisic acid on cell cycle progression in
Qiao, S., Sun, S., Wang, L., Wu, Z., Li, C., Li, X., Wang, T., Leng, L., Tian, W., Lu, T., 2017. tobacco BY-2 cells. Plant Physiol. 128, 201–211.
The RLA1/SMOS1 transcription factor functions with OsBZR1 to regulate Takken, F.L., Goverse, A., 2012. How to build a pathogen detector: structural basis of NB-
brassinosteroid signaling and rice architecture. Plant Cell 29, 292–309. LRR function. Curr. Opin. Plant Biol. 15, 375–384.
Qiu, Z., Guo, J., Zhu, A., Zhang, L., Zhang, M., 2014. Exogenous jasmonic acid can Tavallali, V., Karimi, S., 2019. Methyl jasmonate enhances salt tolerance of almond
enhance tolerance of wheat seedlings to salt stress. Ecotoxicol. Environ. Saf. 104, rootstocks by regulating endogenous phytohormones, antioxidant activity and gas-
202–208. exchange. J. Plant Physiol. 234, 98–105.
Ravnikar, M., Žel, J., Plaper, I., Špacapan, A., 1993. Jasmonic acid stimulates shoot and Thines, B., Mandaokar, A., 2013. Characterizing jasmonate regulation of male fertility in
bulb formation of garlic in vitro. J. Plant Growth Regul. 12, 73–77. Arabidopsis. Jasmonate Signal. Springe 13–23.
Raya-González, J., Pelagio-Flores, R., López-Bucio, J., 2012. The jasmonate receptor Todaka, D., Shinozaki, K., Yamaguchi-Shinozaki, K., 2015. Recent advances in the
COI1 plays a role in jasmonate-induced lateral root formation and lateral root dissection of drought-stress regulatory networks and strategies for development of
positioning in Arabidopsis thaliana. J. Plant Physiol. 169, 1348–1358. drought-tolerant transgenic rice plants. Front. Plant Sci. 6, 84.
Raza, A., Charagh, S., Najafi-Kakavand, S., Siddiqui, M.H., 2021a. The crucial role of Tong, H., Liu, L., Jin, Y., Du, L., Yin, Y., Qian, Q., Zhu, L., Chu, C., 2012. DWARF AND
jasmonates in enhancing heavy metals tolerance in plants. Jasmonates Sali Signal. LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase
Plants Springe 159–183. to mediate brassinosteroid responses in rice. Plant Cell 24, 2562–2577.
Raza, A., Charagh, S., Zahid, Z., Mubarik, M.S., Javed, R., Siddiqui, M.H., Torres, M.A., Jones, J.D., Dangl, J.L., 2006. Reactive oxygen species signaling in
Hasanuzzaman, M., 2021b. Jasmonic acid: a key frontier in conferring abiotic stress response to pathogens. Plant Physiol. 141, 373–378.
tolerance in plants. Plant Cell Rep. 40, 1513–1541. Tsuda, K., Mine, A., Bethke, G., Igarashi, D., Botanga, C.J., Tsuda, Y., Glazebrook, J.,
Raza, A., Salehi, H., Rahman, M.A., Zahid, Z., Madadkar Haghjou, M., Najafi- Sato, M., Katagiri, F., 2013. Dual regulation of gene expression mediated by
Kakavand, S., Charagh, S., Osman, H.S., Albaqami, M., Zhuang, Y., 2022. Plant extended MAPK activation and salicylic acid contributes to robust innate immunity
hormones and neurotransmitter interactions mediate antioxidant defenses under in Arabidopsis thaliana. PLoS Genet. 9, e1004015.
induced oxidative stress in plants. Front. Plant Sci. 13. Turner, J.G., Ellis, C., Devoto, A., 2002. The jasmonate signal pathway. Plant Cell 14,
Ren, H., Bai, M., Sun, J., Liu, J., Ren, M., Dong, Y., Wang, N., Ning, G., Wang, C., 2020. S153–S164.
RcMYB84 and RcMYB123 mediate jasmonate-induced defense responses against Ursache, R., Miyashima, S., Chen, Q., Vatén, A., Nakajima, K., Carlsbecker, A., Zhao, Y.,
Botrytis cinerea in rose (Rosa chinensis). Plant J. 103, 1839–1849. Helariutta, Y., Dettmer, J., 2014. Tryptophan-dependent auxin biosynthesis is

13
O.A. Hewedy et al. Environmental and Experimental Botany 208 (2023) 105260

required for HD-ZIP III-mediated xylem patterning. Development 141, 1250–1259. Yang, Y.N., Kim, Y., Kim, H., Kim, S.J., Cho, K.-M., Kim, Y., Lee, D.S., Lee, M.-H., Kim, S.
https://doi.org/10.1242/dev.103473. Y., Hong, J.C., 2021. The transcription factor ORA59 exhibits dual DNA binding
Walia, H., Wilson, C., Condamine, P., Liu, X., Ismail, A.M., Close, T.J., 2007. Large-scale specificity that differentially regulates ethylene-and jasmonic acid-induced genes in
expression profiling and physiological characterization of jasmonic acid-mediated plant immunity. Plant Physiol. 187, 2763–2784.
adaptation of barley to salinity stress. Plant, Cell Environ. 30, 410–421. Yazdanian, E., Golkar, P., Vahabi, M.R., Taghizadeh, M., 2022. Elicitation Effects on
Wang, J., Yan, D.-W., Yuan, T.-T., Gao, X., Lu, Y.-T., 2013. A gain-of-function mutation in Some Secondary Metabolites and Antioxidant Activity in Callus Cultures of Allium
IAA8 alters Arabidopsis floral organ development by change of jasmonic acid level. jesdianum Boiss. & Buhse.: Methyl Jasmonate and Putrescine. Appl. Biochem
Plant Mol. Biol. 82, 71–83. Biotech. 194, 601–619.
Wang, J., Song, L., Gong, X., Xu, J., Li, M., 2020a. Functions of jasmonic acid in plant Ye, B.-B., Shang, G.-D., Pan, Y., Xu, Z.-G., Zhou, C.-M., Mao, Y.-B., Bao, N., Sun, L., Xu, T.,
regulation and response to abiotic stress. Int. J. Mol. Sci. 21, 1446. Wang, J.-W., 2020. AP2/ERF transcription factors integrate age and wound signals
Wang, Y., Mopper, S., Hasenstein, K.H., 2001. Effects of salinity on endogenous ABA, for root regeneration. Plant Cell 32, 226–241.
IAA, JA, and SA in Iris hexagona. J. Chem. Ecol. 27, 327–342. Yoon, J.Y., Hamayun, M., Lee, S.-K., Lee, I.-J., 2009. Methyl jasmonate alleviated salinity
Wang, Y., Hou, Y., Qiu, J., Wang, H., Wang, S., Tang, L., Tong, X., Zhang, J., 2020b. stress in soybean. J. Crop Sci. Biotechnol. 12, 63–68.
Abscisic acid promotes jasmonic acid biosynthesis via a Yoshida, Y., Sano, R., Wada, T., Takabayashi, J., Okada, K., 2009, Jasmonic acid control
’SAPK10–bZIP72–AOC’pathway to synergistically inhibit seed germination in rice of GLABRA3 links inducible defense and trichome patterning in Arabidopsis.
(Oryza sativa). N. Phytol. 228, 1336–1353. You, X., Zhu, S., Zhang, W., Zhang, J., Wang, C., Jing, R., Chen, W., Wu, H., Cai, Y.,
Wasternack, C., 2007. Jasmonates: an update on biosynthesis, signal transduction and Feng, Z., 2019. Os PEX 5 regulates rice spikelet development through modulating
action in plant stress response, growth and development. Ann. Bot. 100, 681–697. jasmonic acid biosynthesis. N. Phytol. 224, 712–724.
Wasternack, C., 2014. Action of jasmonates in plant stress responses and development– Yuan, Z., Zhang, D., 2015. Roles of jasmonate signalling in plant inflorescence and flower
applied aspects. Biotechnol. Adv. 32, 31–39. https://doi.org/10.1016/j. development. Curr. Opin. Plant Biol. 27, 44–51.
biotechadv.2013.09.009. Zarei, A., Körbes, A.P., Younessi, P., Montiel, G., Champion, A., Memelink, J., 2011. Two
Wasternack, C., Goetz, S., Hellwege, A., Forner, S., Strnad, M., Hause, B., 2012. Another GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-
JA/COI1-independent role of OPDA detected in tomato embryo development. Plant mediated activation of the PDF1. 2 promoter in Arabidopsis. Plant Mol. Biol. 75,
Signal. Behav. 7, 1349–1353. 321–331.
Wasternack, C., Forner, S., Strnad, M., Hause, B., 2013. Jasmonates in flower and seed Zhang, B., Wu, S., Zhang, Ye, Xu, T., Guo, F., Tang, H., Li, X., Wang, P., Qian, W., Xue, Y.,
development. Biochimie 95, 79–85. 2016. A High Temperature-Dependent Mitochondrial Lipase EXTRA GLUME1
Xiao, Y., Chen, Y., Charnikhova, T., Mulder, P.P., Heijmans, J., Hoogenboom, A., Promotes Floral Phenotypic Robustness against Temperature Fluctuation in Rice
Agalou, A., Michel, C., Morel, J.-B., Dreni, L., 2014. OsJAR1 is required for JA- (Oryza sativa L.). PLOS Genet. 12, e1006152 https://doi.org/10.1371/journal.
regulated floret opening and anther dehiscence in rice. Plant Mol. Biol. 86, 19–33. pgen.1006152.
Xu, Q., Truong, T.T., Barrero, J.M., Jacobsen, J.V., Hocart, C.H., Gubler, F., 2016. A role Zhang, C., Huang, Z., 2013. Effects of endogenous abscisic acid, jasmonic acid,
for jasmonates in the release of dormancy by cold stratification in wheat. J. Exp. Bot. polyamines, and polyamine oxidase activity in tomato seedlings under drought
67, 3497–3508. stress. Sci. Hortic. 159, 172–177.
Yan, C., Xie, D., 2015. Jasmonate in plant defence: sentinel or double agent? Plant Zhang, G., Zhao, F., Chen, L., Pan, Y., Sun, L., Bao, N., Zhang, T., Cui, C.-X., Qiu, Z.,
Biotechnol. J. 13, 1233–1240. Zhang, Y., 2019. Jasmonate-mediated wound signalling promotes plant
Yan, Y., Christensen, S., Isakeit, T., Engelberth, J., Meeley, R., Hayward, A., Emery, R.J., regeneration. Nat. Plants 5, 491–497.
Kolomiets, M.V., 2012a. Disruption of OPR7 and OPR8 reveals the versatile Zhang, G., Liu, W., Gu, Z., Wu, S., Zhou, W., Lin, J., Xu, L., 2021, Roles of the wound
functions of jasmonic acid in maize development and defense. Plant Cell 24, hormone jasmonate in plant regeneration. Journal of Experimental Botany.
1420–1436. https://doi.org/10.1105/tpc.111.094151. Zhang, H., Zhang, Q., Zhai, H., Li, Y., Wang, X., Liu, Q., He, S., 2017. Transcript profile
Yan, Y., Christensen, S., Isakeit, T., Engelberth, J., Meeley, R., Hayward, A., Emery, R.N., analysis reveals important roles of jasmonic acid signalling pathway in the response
Kolomiets, M.V., 2012b. Disruption of OPR7 and OPR8 reveals the versatile of sweet potato to salt stress. Sci. Rep. 7, 40819. https://doi.org/10.1038/
functions of jasmonic acid in maize development and defense. Plant Cell 24, srep40819.
1420–1436. Zhang, L., Xing, D., 2008. Methyl jasmonate induces production of reactive oxygen
Yan, Z., Chen, J., Li, X., 2013. Methyl jasmonate as modulator of Cd toxicity in Capsicum species and alterations in mitochondrial dynamics that precede photosynthetic
frutescens var. fasciculatum seedlings. Ecotoxicol. Environ. Saf. 98, 203–209. dysfunction and subsequent cell death. Plant Cell Physiol. 49, 1092–1111.
Yan, Z., Zhang, W., Chen, J., Li, X., 2015. Methyl jasmonate alleviates cadmium toxicity Zhao, M.L., Wang, J.N., Shan, W., Fan, J.G., Kuang, J.F., Wu, K.Q., Li, X.P., Chen, W.X.,
in Solanum nigrum by regulating metal uptake and antioxidative capacity. Biol. He, F.Y., Chen, J.Y., 2013. Induction of jasmonate signalling regulators MaMYC2s
Plant. 59, 373–381. and their physical interactions with MaICE1 in methyl jasmonate-induced chilling
Yang, C., Shen, W., He, Y., Tian, Z., Li, J., 2016. OVATE family protein 8 positively tolerance in banana fruit. Plant, Cell Environ. 36, 30–51.
mediates brassinosteroid signaling through interacting with the GSK3-like kinase in Zhou, W., Lozano-Torres, J.L., Blilou, I., Zhang, X., Zhai, Q., Smant, G., Li, C., Scheres, B.,
rice. PLoS Genet. 12, e1006118. 2019. A jasmonate signaling network activates root stem cells and promotes
Yang, J., Duan, G., Li, C., Liu, L., Han, G., Zhang, Y., Wang, C., 2019. The Crosstalks regeneration. Cell 177, 942–956 e914.
Between Jasmonic Acid and Other Plant Hormone Signaling Highlight the Zhu, Z., Lee, B., 2015. Friends or foes: new insights in jasmonate and ethylene co-actions.
Involvement of Jasmonic Acid as a Core Component in Plant Response to Biotic and Plant Cell Physiol. 56, 414–420. https://doi.org/10.1093/pcp/pcu171.
Abiotic Stresses. Front. Plant Sci. 10. https://doi.org/10.3389/fpls.2019.01349.

14

You might also like

pFad - Phonifier reborn

Pfad - The Proxy pFad of © 2024 Garber Painting. All rights reserved.

Note: This service is not intended for secure transactions such as banking, social media, email, or purchasing. Use at your own risk. We assume no liability whatsoever for broken pages.


Alternative Proxies:

Alternative Proxy

pFad Proxy

pFad v3 Proxy

pFad v4 Proxy