Introduction

Plants are threatened by several biotic and abiotic stresses that endanger their life. As sessile beings, evolution has helped plants to develop many mechanisms and behaviors to cope with predators and unfavorable life conditions. Perception of threat by cellular receptors is transduced into signals within seconds. Those signals are called second messengers such as Ca2+, reactive oxygen species (ROS), hydrogen sulfide (H2S), inositol trisphosphate (IP3), nitrogen oxide (NO) which interacts with several proteins to enhance plant response to a given stress (Agurla et al. 2018). ROS-Ca2+ hub have been extensively studied in plants in response to many environmental constraints and controls lots of mechanisms such as osmotic adjustment, hormonal signal transduction (HST), osmoregulation, mineral nutrition, cell elongation and development as well as programmed cell death (Demidchik and Shabala 2017). It has been suggested that ROS-Ca2+ hub/phytohormone signaling simultaneously activates the plant stress signaling cascades (Sewelam et al. 2016). Moreover, ROS, as the main source of signaling in plants under unfavorable conditions, interacts with other second messengers and signaling components such as Mitogen Activated protein Kinases (MAPKs), plant hormones, and transcription factors (Sewelam et al. 2016). In another hand, plant growth, development, and survival are strictly interconnected in a complex biological network that is disturbed by environmental conditions, such as soil condition and salinity, extreme temperatures, and pathogen attacks (Altaf-Ul-Amin et al. 2015). Hence, a relevant number of intermediate compounds, such as ROS and their derivatives, might accumulate in the cytoplasm and disturb signaling pathways especially when they are converted into toxic compounds and affect cell survival (Ayala et al. 2014). Phytohormones which are involved in ROS-Ca2+ mediated signals include abscisic acid (ABA), cytokinins (CKs), auxins (IAA), gibberellins (GA), ethylene (ET), salicylic acid (SA), brassinosteroids (BRs), jasmonic acid (JA) and strigolactones (Pottosin et al. 2014; Deng et al. 2018). All those hormones have different effect and can act with an antagonist or synergistic action in response to a stressor.

Among those phytohormones, JA and its derivatives, such as jasmonyl isoleucine (JA-Ile), methyl jasmonate (MeJA), 12-hydroxyjasmonic acid sulfate (12-HSO4-JA), cis-jasmone, JA-glucosyl ester, JA-Ile methyl ester, jasmonoyl-amino acid, 12-carboxy-JA-IIe, 12-O-glucosyl-JA-IIe, 12-O-glucosyl-JA, JA-Ile glucosyl ester, are known as jasmonates (JAs). JAs are lipid-derived signaling molecules that control many developmental processes. They are implicated in plant response to biotic and abiotic stress and they are detected in almost all plants (Sun et al. 2011). JAs are fatty acids that belong to oxidized lipids family. Those molecules are synthesized from cyclo-pentanones and known as oxylipins (Wasternack and Feussner 2018). The oxylipins signaling molecules are biologically active components produced either through auto-oxidation of poly-unsaturated fatty acids or by the activity of lipoxygenases enzymes or alpha-dioxygenases enzymes (Göbel and Feussner 2009). JAs regulates many crucial biological processes in planta, including stamen and trichome development, stomatal opening, leaf expansion, hook formation, cell cycle regulation, and glucose transport (Wasternack and Hause 2007; Yoshida et al. 2009).

In this review, we intend to describe the most recent updates in JA biosynthesis and signaling pathways, and we focus on the crosstalk between JA and others phytohormones to understand the mechanism of plant responses different stresses.

JA metabolism

JAs are ubiquitous molecules detected in higher plant species (Yang et al. 2019). The endogen level of JA in plants is higher in reproductive organs as well as in flowers but it is very low in roots and mature leaves (Dar et al. 2015). In recent years, the role of JA as an important phytohormone implicated in plant development under normal and stress conditions has emerged (Jang et al. 2019, 2020). Different studies have been conducted on plants belonging to different families such as Brassicacea (the model plant Arabidopsis thaliana), Solanaceae (tobacco: Nicotiana spp., tomato (Lycopersicum esculentum), and monocotyledons (Delker et al. 2006; Kazan and Manners 2013). Many groups described that wounding and systemin increases the endogenous level of JAs including the metabolic precursor, 12-oxo-phytodienoic acid (12-OPDA) and its derivatives JA and MeJA to activate the defense response machinery (Wang et al. 2016).

Reactions in the chloroplast

The JA biosynthetic pathway was studied in Arabidopsis (Ishiguro et al. 2001; Schaller 2001; Feussner and Wasternack 2002; Turner et al. 2002). JA is originally synthetized from a ω-3 fatty acid called linoleinc acid (ALA) (C18:39,12,15). Briefly, the reaction starts when phospholipases (PLDs) separates phospholipids such as linolenic (18:2) and α-linolenic (18:3) acid from chloroplast membranes (Bargmann et al. 2009). ALA constitutes the most abundant leaf lipids and can be found as galactolipids forming the main lipid components of chloroplasts: monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) of the chloroplast (Nilsson et al. 2016). Though the first substrate of the pathway is yet to be identified, it has been suggested that an esterification then oxygenation of ALA into galactolipid occurs via 13-lipoxygenase (13-LOX; Fig. 1; (Nilsson et al. 2016)). Moreover, other findings suggest that the ALA could be hydrolyzed then converted into 13-HPL (Wang et al. 2019). Allene oxide synthase (AOS) is the next acting enzyme in the octadecanoid pathway. Allene oxide synthase (AOS) is a cytochrome P450 (CYP) enzyme that belongs to the CYP74A family. AOS converts galactolipids into 12,13-epoxylinolenic acid which is rapidly transformed to cis (+)-12-oxo-phytodienoic acid (OPDA) by allene oxide cyclase (AOC) (Wasternack and Feussner 2018). In tomato, systemin activates a phospholipase A2 (PLA2) that operates the release of LA from membrane lipids after leaves are wounded (Narvaez-Vasquez et al. 1999). For example, systemin a peptide which is involved in the expression of JA-, wound- and insect-inducible proteinase inhibitors (PIs) was found in tomato but not in tobacco or Arabidopsis (Sun et al. 2011). Mechanisms of JA biosynthesis in Arabidopsis are summarized in Fig. 1.

Fig. 1
figure 1

A proposed model of JA biosynthesis in Arabidopsis. AOS enzyme is encoded by a single gene while four genes encode for the cyclase (AOC1–4). Growth and development processes as well as extracellular stimuli activate the octadecanoid pathway for JA biosynthesis with a so-far unknown mechanism. The first step in JA biosynthesis takes place in the choloroplast where we notice a sequential activity of several enzymes involved in the initial steps of JA biosynthesis including lipoxygenase (LOX), allene oxide synthase (AOS), and allene oxide cyclase (AOC) led to the production of 12-oxo-phytodienoic acid (12-OPDA). 12-OPDA is then translocated from chloroplasts via JASSY proteins and penetrates into peroxysome via CTS channels where it is reduced to 3-oxo-2(29[Z]-pentenyl)-cyclopentane-1-octanoic acid (OPC:8). OPC:8 undergoes three rounds of b-oxidation to yield JA. After biosynthesis, JA is conjugates with ILE and transported to the cytoplasm where is could be transported all over the plant or could be inactivated via CYP94B3 proteins

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In monocotyledons, JA biosynthetic pathway is almost conserved with dicotyledons. In fact, some works confirmed the involvement of many enzymes such as PLDs in JA biosynthetic (Nahar et al. 2011). Knockdown of PLD enzymes involved in JA biosynthetic pathway such as OsPLDα4 (Os06g0604200) and OsPLDα5 (Os06g0 604300) confers herbivory susceptibility to rice (Qi et al. 2011). As enzymes implicated in the reduction of ODPA are located in the peroxisomes, this cyclopentenone must be exported from chloroplast and transported to peroxisomes. This is ensured by an ABC transporter located in the peroxisomal membrane called COMATOSE (CTS) and a possible implication of an ion trapping mechanism was proposed (Theodoulou et al. 2005). Recently, a novel protein called JASSY was described and it presented an export activity toward OPDA (Guan et al. 2019) and was found in the chloroplast outer envelope (OE) membranes (Simm et al. 2013). JASSY proteins, which are exclusively located in the chloroplastic OE, could have a role in binding and/or transport of hydrophobic molecules as it contains a steroid acute regulatory protein-related lipid transfer (START) domain. JASSY mutants represent an altered phenotype (growth inhibition and decrease in cold stress tolerance) is correlated with a decreased level of transcription factors INDUCER OF CBF EXPRESSION1 (ICE1) and C-REPEAT BINDING FACTOR 3 (CBF3) involved in the cold acclimation response). Moreover, jassy mutant had an increased susceptibility to infection by the necrotrophic pathogen Botrytis cinerea and decreased expression of corresponding marker genes, such as PLANT DEFENSIN1.2 (PDF1.2). In conclusion, after wounding, a lack of JA response (associated with reduced level of JA biosynthesis) and a reduced JA biosynthesis genes activation, as well as transcription factors involved in JA responses, were observed in the jassy mutant (Guan et al. 2019). In jassy mutant plants, ODPA synthesis is normal but its export out of the chloroplast was defected. However, evidence that ODPA pass through a JASSY channel with OPDA-regulated voltage-dependent gating is still missing. Furthermore, little information is available about specificity for OPDA-related compounds (Wasternack and Hause 2019). Thus, a link between JASSY proteins and JA biosynthesis genes was suggested.

Reactions in peroxisomes

The OPDA cyclopentenone component (12-oxo-phytodienoic acid) is scaled down to cyclopentanone using the OPDA reductase (OPDR; 12-oxo-phytodienoic acid reductase). The cyclopentenone ring is reduced by the AOC enzyme (Fig. 1). The (9S,13S)-OPDA [cis-(+)-OPDA] is the only natural component synthetized in nature (Wasternack and Feussner 2018). In another hand, OPDA could act as a signaling molecule and thus activates gene transcription independently of its conversion into JA (Taki et al. 2005). Another JA synthetic pathway was also revealed using Arabidopsis OPDA reductase 3 (OPR3) mutant which revealed another independent JA pathway using 4,5-didehydrojasmonate (Fig. 1; Chini et al. 2018). OPR could also regulate seed germination in Arabidopsis (Dave et al. 2011). In maize, it has been shown that OPR proteins are crucial for plant development and immunity (to pathogens and insects; Dave et al. 2011). Once synthetized, JA (or its active forms, e.g. MeJA) are transported all over the plant and in the phloem and xylem of vascular bundles. This transport is ensured via a protein transporter called GTR1 (Ishimaru et al. 2017; Matsu et al. 2017).

Reactions in cytoplasm

In Arabidopsis, works conducted on jar1-1, a JA-insensitive mutant revealed that the active form of JA was an amino acid conjugate. The isoleucine is the principal amino acid that conjugates with JA to form JA (JA-Ile) synthetized in the cytoplasm (Fig. 1). Other amino acid could rarely conjugate with JA such as valine, leucine, and phenylalanine (Staswick and Tiryaki 2004).

JA catabolism

JA-Ile metabolism is ensured by two major routes: hydrolyzation and oxidation (Fig. 2; Bruckhoff et al. 2016). JA-Ile hydrolyzation allows the liberation JA and Ile from JA-Ile. This is controlled by an aminohydrolase (AMH) enzyme. After that, JA is subjected to a hydroxylation, controlled by a P450 enzyme to generate 12-hydroxy-JA-Ile that could be oxidized later to generate carboxy-derivative. In another hand, JA-Ile could also be subjected to different oxidations of the ω-end of the pentenyl sidechain catalyzed by specific enzyme, CYP94 (Kitaoka et al. 2014). In the first step, JA-Ile is hydroxylated to 12-hydroxy JA-Ile. This can then either undergo further oxidation to produce the 12-carboxy-JA-Ile (Koo et al. 2014), or else can be glycosylated to generate 12-O-glycosyl-JA-Ile (Fig. 2; Haroth et al. 2019).

Fig. 2
figure 2

Catabolism of jasmonic acid (JA). JA could be inactivated via two major pathways: hydrolysation (I) and oxydation (II). Hydrolyzes is unsured by amidohydrolase (AMH) to release Ile and JA. Then JA could be either hydroxylated (to 12-hydroxy-JA), glycosylated, methylated to form methyl JA (Me-JA) or decarboxylated to synthesize cis-jasmone (CJ). JA-Ile could also undergo sequential oxidation reaction to generate 12-carboxy-JA-Ile. JA could also be glycosylated to generate 12-O-glycosyl-JA-Ile. Enzymes that catalyses the reactions are shown in red (colour figure online)

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JA conversion into signaling molecules

Me-JA

Me-JA is synthesized via the acceptation of methyl group from S-adenosyl-l-methionine (SAM) to JA. This reaction is catalyzed by the SAM: JA carboxyl methyl-transferase enzyme. This esteric compound formed is volatile in contrast to JA (Sanchez-Aguayo et al. 2004). Me-JA has been detected in plant leaves after an herbivore attack. Interestingly, this molecule is detected only in leaves that have not been predated. Thus, this molecule can serve as an airborne warning molecule signal (Wasternack and Feussner 2018). In plants like potato and tomato, the production of PIN II protease inhibitor is one of the common markers for JA pathway activation (Singh et al. 2020). Those inhibitors act as an anti-feedant compound as it interferes with digestive proteins in the insect gut leading to lower food availability for the insect and hence the insect take more time to grow and complete its life cycle (Singh et al. 2020).

The consequence of insect growth delay is that weather changes may occur and hence reduce the survival of the insect (Bayram and Tonga 2018). In addition, Me-JA is one of complex volatiles compounds released during plant infection that could play the role of chemical attractor for insect predators such as wasps as demonstrated for Triticum aestivum (Bayram and Tonga 2018). Moreover, treatment with Me-JA stimulates phytoalexins compounds such as alkaloids terpenoids and glycosteroids which have an antimicrobial activity (Shi et al. 2015), enhances carotenoid biosynthesis as demonstrated for maize (Luo et al. 2019, 2020) or stimulates sucrose degradation. Moreover, MeJA changes enzymatic activity of many enzymes of the phenylpropanoid pathway (Sadeghnezhad et al. 2020). Me-JA also decreased the amino acid biosynthesis rate thus it controls the cell growth rate (Sadeghnezhad et al. 2020).

cis-Jasmone (CJ)

CJ is used in perfume industry as an important ingredient. This natural compound is liberated from flowers of different species such as jasmine, neroli (Citrus bigaradia; Matsu et al. 2017), jonquil (Narcissus jonquilla L.; Dabrowska and Boland 2007), bergamot (Citrus bergamia), and members of the Pittosporum family (Griffiths 2020). After plant infection, CJ is released, and it could act like JA. It can act as an insect repellent or it could participate to attract insect predators (Matthes et al. 2010). In fact, exogenous application of CJ to wheat was effective against cereal aphids and some phytophagous thrips species as well as wheat stem sawflies Bayram and Tonga 2018). Moreover, foliar application of CJ increased volatile organic compounds (VOCs) production as well as the upregulation of genes encoding them. Besides, CJ negatively affect tomato pest Spodoptera exigua reproduction (Disi et al. 2017).

The signaling pathway of JA

The SCFCOI1 protein and JA signaling

Experiments conducted with the Arabidopsis mutant coi1 (coronatine insensitive 1) add knowledge on the comprehension of the JA response pathway (Feys et al. 1994). COI1 was identified as an F-box protein; it is closely related to the auxin receptor/F-box protein TIR1 (Xie et al. 1998). Thus, the authors suggested that it could act as part of an SCF (Skp/Cullin/F-box) E3 ubiquitin ligase to mediate JA signaling (Xie et al. 1998). In fact, COI1 was demonstrated to be associated with components of the SCF complex, including ASK1, ASK2, CUL1, and RBX1 (Xu et al. 2002). Moreover, in Arabidopsis, other works suggest that SCFCOI1 protein targets the repressor proteins of JA signaling for degradation and, therefore, activates JA-modulated changes at transcriptional level. The same founding was also reported in tobacco, tomato, and soybean (Scheer and Ryan 2002; Li et al. 2004).

The AtMYC2: master regulator of JA signaling

MYC2 structure

Several works have classified the basic helix-loop-helix (bHLH) transcription factor (TF) as the greater JA signaling pathway in Arabidopsis (Browse 2009; Chini et al. 2009a; Howe 2010; Pauwels and Goossens 2011; Wager and Browse 2012). The best characterized TF in this group and the most multifunctional in the JA signaling pathway in Arabidopsis is MYC2 (Kazan and Manners 2013). This nucleolar protein (Chini et al. 2009b) presents the general characteristics of bHLH TF protein family (Toledo-Ortiz et al. 2003; Pires and Dolan 2010) such as the conserved bHLH domain at its carboxyl domain. Those domains are formed by two amphipathic alpha-helices consisting of hydrophobic amino acids united by a loop region important to form homo/heterodimers with other TFs like the most closed TFs MYC3 and MYC4 (Fernandez-Calvo et al. 2011). It has been suggested that the C-terminal leucine zipper domain could function as a supplementary dimerization domain to increase the specificity of cooperation with other TFs (Amoutzias et al. 2008). Moreover, the 15–20 mostly basic amino acids are involved in linking to the G-box (5′-CACGTG-3′) found in MYC2 target promoters (Toledo-Ortiz et al. 2003; Pires and Dolan 2010; Fernandez-Calvo et al. 2011; Amoutzias et al. 2008; Carretero-Paulet et al. 2010). In the N-terminal part of the MYC2 TF, a putative transcriptional activation domain (TAD) is found, which is important for transcription initiation (Fernandez-Calvo et al. 2011; Amoutzias et al. 2008; Carretero-Paulet et al. 2010). Moreover, MYC2 and their closely related proteins, MYC3, and MYC4, interplay with the C-terminal part of JAZ proteins (JAS domain) through JID domain (JAZ Interaction Domain) (Fernandez-Calvo et al. 2011; Amoutzias et al. 2008; Carretero-Paulet et al. 2010; Chini et al. 2007). Some works proposed that protein phosphorylation is involved in the modulation of JA signaling (Hiruma et al. 2011). Though MYC2 was shown to be phosphorylated, the identity of kinase protein implicated in this phosphorylation is still unknown (Zhai et al. 2013).

MYC2 and JA response

MYC2 orchestrates the JA pathway by controlling several mechanisms such as plant response to pathogen infection, abiotic stress applications and developmental processes (Kazan and Manners 2013). It tightly regulates the expression of downstream transcriptional activators as well as JAZ repressors that, in turn, act upstream from MYC2. In fact, myc2 mutant Arabidopsis seedlings had reduced expression of JAZ genes comparing with wild-type proteins in response to JA treatment (Chini et al. 2007; Grunewald et al. 2009). Later, it has been demonstrated that MYC2 directly binds to the promoter of JAZ3 (Chini et al. 2007) and JAZ2 (Figueroa and Browse 2012) confirming that the MYC2 TF is a regulator of JAZ gene expression. MYC2-mediated transcriptional activation and JAZ repressors synthesis coordinate to degrade the JAZ proteins (Chini et al. 2007; Demianski et al. 2012). MYC2 TF controls the expression of a high number of JA-responsive genes including TFs (Guo et al. 2012; Dombrecht et al. 2007). In fact, several researchers have identified that MYC2 presented a dual effect on the JA signaling pathways as it acts as a transcriptional activator as well as a repressor in the regulation of JA signaling network (Fig. 3). In fact, it has been demonstrated that a comparative microarray analysis using JA-treated and untreated myc2 and wild-type plants. The analysis identified many JA-responsive genes that are directly or indirectly managed by MYC2 all along JA signaling (Dombrecht et al. 2007). Moreover, bioinformatic analyzes showed that MYC2 interacts with at least 100 proteins as revealed by The Arabidopsis thaliana Promoter Analysis Net, network (AtPAN) (http://atpan.itps.ncku.edu.tw/), conclude more than 100 different MYC2 cooperator (Chen et al. 2012). The most important studied interactome are resumed in Table 1.

Fig. 3
figure 3

A simplified schematic presentation of jasmonate (JA) signaling. After its biosynthesis in plastids, JA is conjugated with aa, especially Ile by JAR under the control of JAR enzymes in the cytoplasm. In some conditions, JAZ interacts with NINJA, TOPLESS (TPL), and histone deacetylase (HAD) proteins to repress JA gene expression via inhibiting MYC2 TF. It also inhibits many negative regulators of JA signaling such as IIId bHLH factors. In presence of extracellular stimuli or in growth and development processes, JA-Ile enhances the CORONATINE INSENSITIVE1 (COI1)/JA ZIM-domain (JAZ) family proteins interaction. This leads to JAZ ubiquitination and degradation with the 26S proteasome. MYC2 TFs interacts with the MED25 subunit of the moderator complex then interacts with the G-box motif of the target promoters, which allows the activation of JA-responsive genes. In another hand, IIId bHLH factors antagonize MYC2 action via competitive binding to the G-box motif and inhibiting JA-responsive genes. Thus, succeeding transcription factors are stimulated, allowing them to enhance JA-responsive early genes activities and JA responses

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Table 1 The most identified MYC2 interacting proteins in Arabidopsis thaliana
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Jasmonate ZIM-domain proteins: inhibitor of JA response

Eight different JAZ proteins (jasmonate ZIM-domain proteins) were identified in opr3 mutants during JA response (Thines et al. 2007). Those proteins harbor two conserved interaction domains, called ZIM and Jas (Thireault et al. 2015). The Jas domain controls JAZ interaction with COI1 and with other TFs as well (Gimenez-Ibanez et al. 2014). Moreover, the ZIM (TIFY) domain regulates the JAZ dimerization and interaction with other interactives of JAZ (NINJA) proteins which requires TOPLESS (TPL) proteins, transcriptional co-suppressor, via the interaction with the conserved EAR domain (Zhang et al. 2015). Importantly, in vitro and in vivo assays demonstrated that JA-Ile, not other derivatives, mediates direct JAZ1 and COI1 interaction (Thines et al. 2007). In response to JA, many JAZ proteins, such as JAZ3, are fixed with SCFCOI1 to mediate their proteasome degradation (Chini et al. 2007). Moreover, in absence of JA, JAZ directly interacts with AtMYC2 which leads to transcriptional repression of JA-responsive genes (Chini et al. 2007).

Identification of NINJA proteins

As discussed above, physical interplay between JAZ repressor proteins and AtMYC2 regulates JA-responsive gene expression. This requires the interaction between NINJA proteins and Groucho/Tup1-type co-repressor TOPLESS (TPL) and TPL-related proteins (TPRs) with the presence of unknown adaptor protein. TPL and NINJA proteins act as negative regulators in the JA signaling pathway. NINJA acts as a transcriptional repressor whose activity is mediated by a functional TPL-binding EAR repression motif (Pauwels et al. 2010).

SCFCOI1/JAZ/ AtMYC2 complex: the JA Core Signaling Module

Generally, JA-Ile endogenous level is low in normal conditions, but they can rapidly increase in presence of a given stimuli. This increase in sensed by a JA receptor called COI1 which constitute a fundamental component of SCFCOI1. COI1 lie to JAZ proteins and enhances JAZ ubiquitination and degradation through the 26S proteasome pathway. Thus, downstream TFs (e.g.: MYCs) can be released to activate JA responses (Gimenez-Ibanez et al. 2014; Dubois et al. 2018). As a result, many works identified MYC, JAZ, and COI1 protein as the core signal transduction mechanism of JA signaling. Those proteins play a crucial role in plant extension and maturing as well as its reply to environmental stresses (Gimenez-Ibanez et al. 2014; Dubois et al. 2018). JAZ interact with many TFs and specifically regulate many responses (Chini et al. 2016). In Arabidopsis thaliana, when endogenous jasmonate concentration increase, JAZ proteins interact with SCFCOI1 ubiquitin ligase which leads to JAZ degradation by proteasome 26S (Chini et al. 2007). Thus, degradation of JAZ protein liberates COI1 and AtMYC2 to enhance jasmonate-dependent gene expression (Chini et al. 2007; Thines et al. 2007). Defense compounds increases in presence of JAZ-MYC module. Thus, this could stimulate defense response against pathogen infection or inhibit plant growth (Havko et al. 2016). Moreover, COI1/JAZ2/MYC2, 3,4/ANAC19,55,72 and other modules have been identified to enhance plant response to endogenous or exogenous stimuli (Gimenez-Ibanez et al. 2014; Mao et al. 2017). MYCs–JAZs interactions could trigger the hormonal cross talk pathways like ET-mediated cell division throughout ET RESPONSE Transcription factor (ERF) (Gimenez-Ibanez et al. 2014; Zhang et al. 2015; Dubois et al. 2018).

Involvement of JA in plant growth and development

Phytohormones control internal developmental interactions with entourage stimuli to regulate plant maturation and survival. In the last decade, a huge body of studies focused on understanding the role of JA in plant maturation and development. An important number of works have shown that jasmonates are involved in a huge number of plants expanding events, such as primary root growth, leaf senescence, and reproductive development (Wasternack and Hause 2007; Kim et al. 2015). Moreover, JA is implicated into the regulation of various metabolites production, such as phytoalexins and terpenoids.

Effects on seed germination

It has been described that some phytohormones like ABA, IAA, and JA play important roles during seed germination (Xiao et al. 2018). Both ABA and JA inhibit seed germination but their interactions during this process are still elusive (Tang et al. 2020). In Arabidopsis, JA inhibition occurs in a COI1-independent manner (Dave et al. 2011). In Triticum aestivum plants, cold-stimulated germination of seeds resulted in an increase in endogenous level of JA after upregulation of JA biosynthesis-related gene and JA promotes cold-stimulated germination (Xu et al. 2016; Avramova 2017). Recently, a novel SAPK10-bZIP72-AOC’ pathway was identified in rice. In this pathway, ABA stimulates JA biosynthesis to synergically inhibit the germination of rice seeds (Wang et al. 2020). Some authors demonstrated that SAPK10 was activated by auto-phosphorylation, then this molecule stabilizes by phosphorylation bZIP72 TF and promotes it’s binding to the G-box cis-element of AOC promoter to enhance AOC transcription in presence of elevated concentrations of JA. Interestingly, alleviation of ABA sensitivity was recorded after blocking of JA biosynthesis (Wang et al. 2020).

Inhibition of root growth

Mutations in the co-receptor for JA-Ile COI1 make plants insensitive to the prevention of primary root maturation by JAs (Yan et al. 2009). Moreover, inositol pentakisphosphate (InsP5) enhances COI1–JAZ9 interactions and thus the blocking effect of JAs on root expansion and maturation (Mosblech et al. 2011). In another hand, coronatine-O-methyloxime, a competitive JA antagonist obstruct COI1–JAZs interactions and thus suppress the inhibitory outcome of coronatine on primitive root growth (Monte et al. 2014). In Arabidopsis, most JAZ proteins (13 members) lack the ERF-associated amphiphilic repression (EAR) domain. Thus, they should interact with TPL and TPL-related proteins (TPRs) via the EAR of NINJA proteins to crush JA responses. Interestingly, the non-canonical JAZ proteins, JAZ8 and JAZ13 do not require NINJA protein to interact with TPLs /TPRs but use directly their one EAR domain (Thireault et al. 2015; Chini et al. 2016). Interestingly, overexpressed NINJA proteins or modified JAZ proteins (carrying a deletion, mutation) in Jas domain suppressed the inhibitory effect of JA on primary root growth. But this inhibitory effect was stimulated by the NINJA/TPL or combined mutations in JAZ7, JAZ8, JAZ10, and JAZ13 (Thireault et al. 2015; Thatcher et al. 2016). In Arabidopsis, bHLH type transcription factors (MYC2 and its homologs MYC3/4/5), interact with JAZ proteins (Qi et al. 2015). MYC2/3/4 are in the primary root apex; make place to the primary root growth inhibition by JAs (Gasperini et al. 2015). Moreover, MYC2 inhibits PLETHORA genes (PLT1 and PLT2) expression to minimize the activity of root meristematic cells and suppress primary root growth (Chen et al. 2011). Besides, MYC2 interacts with MED25 subunit to unsure this inhibitory effect by inhibiting RNA polymerase II (Chen et al. 2011). It has been demonstrated that JAZ9 handicaps MYC3–MED25 interactions (Gimenez-Ibanez et al. 2014). MYC2 ubiquitination via PLANT U-BOX PROTEIN10 and its phosphorylation of MYC2 in presence of mitogen-activated protein kinase 3/6 suppresses JA-mediated root maturation inhibition (Chico et al. 2014; Sethi et al. 2014).

In Arabidopsis, ETHYLENE INSENSITIVE (EIN) 3 and EIN3-LIKE1 (EIL1) are primordial TFs acting in ethylene signaling. Those TFs interact with JAZ proteins and positively mediate the JA-dependent primary root growth inhibition as well as JA-induced root hair formation (Zhu et al. 2011). In Arabidopsis, JA stimulates also the lateral root formation as it upregulates ERF109 expression which stimulates ANTHRANILATE SYNTHASE Α1 (ASA1) and YUCCA2 genes implicated in auxin biosynthesizes (Cai et al. 2014). In contrast, JA negatively regulates adventitious root formation via the COI1-MYC2/3/4 cascade (Gutierrez et al. 2012).

Regulation of stomatal closure

Stomata control gas exchange, water loss in plants. It also regulates plant immunity against phytopathogens. Stomatal closure is also mediated by JA. In fact, Methyl-JA/ COI1 activate a plasma membrane H+-ATPase. Membrane depolarization generates an influx of Ca2+ and an efflux of H+ (Yin et al. 2016). Methyl-JA/ COI1 induces also the production of ROS, the stimulation of Cl– channels (which engender an efflux of Cl–) and the stimulation of K+ efflux (via K+ channels), causing turgor guard cell loss and stomatal closure (Yan et al. 2015) Drought and salt stress conditions induce stomatal closure in plants. It has been proven that JA and ABA pathways control stomatal closure in Arabidopsis through the stimulation of OPEN STOMATA1 protein kinase (Yin et al. 2016). Moreover, in drought conditions, plants synthesizes OPDA rather than jasmonate. This molecule is more efficient than JA in such conditions. OPDA interplay with ABA to enhance stomatal closure in Arabidopsis (Savchenko et al. 2014).

Plant infection with Pseudomonas syringae induces also stomatal closure to limit bacterial invasion (Melotto et al. 2006). To protect themselves, many P. syringae strains synthesize coronatine which interferes with COI1-JAZ-MYC signaling and prohibits SA intensification via NAC019/NAC055/NAC072 and JA2L, enhancing stomatal reopening to help bacterial infection (Zhu et al. 2015). Moreover, HopX1 and HopZ1a, effectors of P. syringae, deplete JAZ proteins in a COI1-independent manner, and maintain stomatal apertures to promote infection (Gimenez-Ibanez et al. 2014).

Delay of flowering

In Arabidopsis, vegetative-reproductive maturation transition is inhibited by JA. COI1–JAZ interaction inhibits flowering. In fact, coi1 mutant as well as JAZ1Δ3A transgenic plants presented an early flowering. Moreover, TARGET OF EAT TFs (TOE1 and TOE2), APETALA2/ERF domain TFs type, control plant flowering. In fact, their interaction with JAZ proteins inactivates the transcription of FLOWERING LOCUS T and thus inhibits flowering. In another hand, overexpression of TOE1 and/or TOE2 inhibits coi1 early flowering phenotype (Zhai et al. 2015).

Inhibition of hypocotyl growth

In Arabidopsis, JA inhibits hypocotyl elongation in many light stress conditions such as far-red and blue wavelengths. This is ensured through COI1 (Chen et al. 2013). Studies showed that JA-deficient mutant jar1 plants grown in far-red light conditions represented elongated hypocotyls (Robson et al. 2010). Moreover, coi1 mutants have longer hypocotyls compared to WT plants when they were grown in dark or under fared lights conditions (Chen et al. 2013) or under red light or low R/FR light ratio (Chen et al. 2013; Robson et al. 2010). The same observation was registered for the myc2/jin1 mutant grown under far-red light and a low R/FR light ratio (Robson et al. 2010), but those plants show a shorter hypocotyl under blue light (Yadav et al. 2005). Authors suggest that bHLH type TF MYC2 plays a role in plant response to red or far-red light and positively regulates the repression of hypocotyls expansion, but it negatively controls the inhibition of hypocotyls elongation by blue light. In rice, JA represses coleoptiles maturation and plant height. In Zea mays, JA inhibits ear shoot maturation (Yan et al. 2012; Yang et al. 2012).

Stamen development in Arabidopsis

In Arabidopsis, many male sterile plants were described. Among those mutants, JA-deficient mutants were described. In fact, coi1, lox3 lox4, aos, opr3; fad3 fad7 fad8, defective in anther dehiscence1 (dad1), JAZ1Δ3A and JAZ10.4 mutants as well as CYP94B3 overexpression lines represented incomplete stamen development (Song et al. 2013). Interestingly, exogenous application of JA restores stamen development only in plants deficient in JA biosynthesis but not in JA signaling mutants (Jewell and Browse 2016). Moreover, in coi1 background, re-imposed COI1 expression in many tissues such as filaments epidermis or anthers can retrieve anther dehiscence, filament elongation, and pollen maturation (Jewell et al. 2016). R2R3-MYB TFs such as MYB21, MYB24, and MYB57 interact directly with JAZs (Song et al. 2011). The myb21 myb24 double mutant represents a delayed anther dehiscence, a non-viable pollen grains and short filaments. Coi1-1 plants overexpressing MYB21 proteins represent a restored stamen development (Song et al. 2011). MYB21 and MYB24 connect physically with MYC2, MYC3, MYC4, and MYC5 to control stamen development (Qi et al. 2015). Interestingly, overexpression of MYC5 and MYC3 in coi1-1 plants can restore stamen maturation and productivity (Qi et al. 2015).

Inhibition of petal expansion

In Arabidopsis, JA inhibits petal expansion via COI1 pathway. In fact, coi1 mutants represent larger petals comparing with wild type at plant anthesis. The same observation was registered for Arabidopsis JA-deficient mutants’ aos and opr3 (Reeves et al. 2012; Brioudes et al. 2009). JA represses MYB21 and MYB24 proteins during sexual organs formation which lead to the restriction of petal growth confirming that MYB21 and MYB24 are important for petal expansion (Reeves et al. 2012). Interestingly, aos and coi1 plants showed an increased MYB21 expression level in petals leading to continuous petal extension and thus grand petals (Reeves et al. 2012). Moreover, opr3 plants represent an increased bHLH TF BIGPETALp expression level. This TF controls post-mitotic cell expansion and unsure larger petals and larger cells in this mutant (Brioudes et al. 2009).

Promotion of trichome formation

Trichomes are barriers or sensors that protect plants from herbivore attack. They can also release volatile compounds. In Arabidopsis, it has been demonstrated that defect in JA biosynthesis or perception can block trichome formation after wounding (Yoshida et al. 2009). At low endogen JA level in cells, JAZ proteins physically connect with WD-repeat/bHLH/MYB complexes to inhibit their transcriptional activity (Qi et al. 2011). After wounding or pathogen attack, endogenous JA concentration increase leading to JAZ proteins turn over. In such situations, WD-repeat/bHLH/MYB complexes enhance trichome formation. Subgroup IIIdbHLH TFs inhibits WD-repeat/bHLH/MYB complexes action by binding to the promoters of their putative target genes competitively leading to the inhibition of trichome formation (Nakata et al. 2013).

Inhibition of apical hook formation

COI1-JAZs-MYC2/3/4 cascade inhibits the formation of apical hook of dark grown plants (Song et al. 2014). In dark stress conditions, MYC2, MYC3, and MYC4 TFs are activated by JA and physically interact with and repress the transcriptional activity of EIN3/EIL1. This leads to downregulation of HOOKLESS1 gene that controls apical hook formation and to the inhibition of apical hook curvature (Song et al. 2014; Zhang et al. 2014). Besides, MYC2 activates EIN3 BINDING F-BOX PROTEIN1 expression which leads to EIN3 degradation (Zhang et al. 2014).

Induction of leaf senescence and chlorophyll degradation

JA stimulates leaf senescence in Arabidopsis. This effect occurs in COI1-dependent manner (Qi et al. 2015). Moreover, JAZ7 represses leaf senescence in dark grown plants (Yu et al. 2015). Many NAC TFs members (such as NAC019, NAC055, and NAC072) act downstream of MYC2/3/4 to enhance chlorophyll degradation (Melotto et al. 2006). In another hand, Subgroup IIIdbHLH TFs antagonize MYC2/3/4 actions as they bind competitively to their target promoters and inhibit leaf senescence (Qi et al. 2015). WRKY57 interacts physically with JAZ4/8 and act as a negative regulator of leaf senescence in presence of JA (Jiang et al. 2014). YABBY1 and YABBY3 proteins interact with JAZs leading to chlorophyll degradation promotion (Boter et al. 2015).

Involvement of JA in plant abiotic and biotic stress responses

Role of JA in plant drought and oxidative stress response

JAs and MeJAs are known to take part in various physiological processes. Exogenous application of JAs so far tested on different plants under abiotic stresses particularly salinity, drought, and temperature (low/high) conditions have proved effective in improving plant stress tolerance (Ahmad et al. 2016). Several studies conducted on Arabidopsis, barley, wheat, maize, and pearl millet showed that both ABA and JA positively control plant tolerance to drought stress (Awan et al. 2020; Wang et al. 2021). In rice and Arabidopsis, both ABA and JA-connected genes were controlled in the first drought constraint subjection, but showed different figure under the next drought stress cycles, underlying a potential role of those hormones in stress memory (Li et al. 2019). In pearl millet, water deficit conditions diminish root and shoot length as well as their fresh- and dry weight comparing with control plants (Awan et al. 2020). Exogenous application of ABA and JA weaken drought stress effects on pearl millet plantlet by increasing the fresh and dry weight of seedlings, root length and shoot length with a pronounced effect of JA comparing to ABA (Awan et al. 2020) as also shown for soybean and wheat under drought stress (Ruan et al. 2019). Authors showed that JA have a more pronounced effect of JA comparing with ABA in plant stress alleviation (Awan et al., 2020). This indicates the signaling interaction between ABA and JA in response to environmental stresses.

Moreover, JA intensifies the antioxidant enzyme (SOD, CAT, and APX) activities with a pronounced effect comparing with ABA hormone treatment in pearl millet (Awan et al. 2020). In contrast, in the absence of allene oxide cyclase (AOC) gene, which encodes the enzyme involved in JA biosynthesis, rice showed enhanced tolerance to water deficit stress in term of stomatal conductance, water content, and shoot ABA content compared to the wild type (Dhakarey et al. 2017). Besides, both hormones, ABA and JA, reveal drought stress effects by minimizing oxidative damage (serious oxidative impairment of cell membrane), in the leaves. In fact, exogenously applied ABA and JA improved drought stress in Arabidopsis (de Ollas et al. 2015), wheat (Siddiqi and Husen 2019), and pearl millet (Awan et al. 2020) which positively raise MDA and H2O2 contents in those plants.

JA alleviates negative impacts of heavy metals stress

Heavy metals [manganese (Mn), nickel (Ni), cadmium (Cd), and lead (Pb)] damage the environment and reduce plant growth and maturation (Zhang et al. 2018). Many foundings revealed that JA controls plant responses to heavy metal applications by modulating their antioxidant systems (Noriega et al. 2012; Carvalho et al. 2013; Ali et al. 2018). In tomato, it has been demonstrated that spr2, a JA-deficient mutant accumulated more Cd in roots and leaves comparing with wild-type plants (Zhao et al. 2016). Furthermore, in Vicia faba, external JA supplementation enhanced plant growth and biomass yielding, restores total chlorophyll content and carotenoid concentrations, enhances glutathione reductase activity and proline accumulation (Ahmad et al. 2017), reduces Cd accumulation in roots, shoots, and leaves by stimulating antioxidant activity and inhibiting MDA and H2O2 accumulation (Carvalho et al. 2013; Ahmad et al. 2017). Moreover, JA activated ascorbate or glutathione antioxidant machinery in soybean to inhibit lipid peroxidase activity (Noriega et al. 2012). In Brassica napus, JA minimized the Cd uptake in leaves, which ensured a reduction in membrane damage and MDA content. This facilitated also essential nutrient uptake by roots and increases gas exchange and photosynthetic pigment contents by protecting chloroplasts from damaging effects of Cd (Ali et al. 2018).

Exogenous JA application on Glycine max seeding before NiCl2 stress could enhance tolerance to Ni2+ stress. This positive effect of JA is ensured by protecting total protein contents and controlling the antioxidant machinery (Sirhindi et al. 2015). In Zea mays, external application of JA protects plant from Ni toxicity by stimulating antioxidant enzyme activity (Azeem 2018).

Jasmonic acid alleviates also the nefast effect of lead (Pb) stress. Pb minimizes macro and micronutrients uptake by plants roots (Sharma and Dubey 2005). It prevents the penetration of many essential cations (such as K+, Zn2+, Mn2+, Mg2+, Cu2+, Ca2+, Fe3+), and anions (NO3−) in the roots (Bali et al. 2019a). Pb causes also a decline in roots and shoots lengths in many plants such as tobacco ((Alkhatib et al. 2012) and tomato (Bali et al. 2019a). Bali et al. (2018) showed that JA alleviates Pb effects by enhancing tomato growth. External JA application minimizes Pb uptake by tomato roots. Moreover, this hormone helps plants to improve their photosynthetic efficiency and gaseous exchange. Furthermore, JA-treated plants exhibits an increased content of osmolytes (glycine betaine, proline, polyamine, and total carbohydrates). Besides, JA-treated tomato cultivated under Pb stress presented an enhanced accumulation of metal chelating compounds (total thiols, non-protein thiols, and protein thiols) (Bali et al. 2018, 2019b).

Role of JA in plant resistance against nematodes

Recently, the infection of watermelon plants (Citrullus lanatus L.) by a soil-dwelling, microscopic nematode called Meloidogyne incognita was investigated. Plants infection leads to apparition of galls on roots which can enhance plant sensitivity to infection by other pathogens (Kyndt et al. 2013). After nematodes invasion, plants activate different defense strategies such as ROS, hormones, and activation of appropriate defense-related genes (Melillo et al. 2006; Martìnez-Medina et al. 2017; Song et al. 2017). In Arabidopsis thaliana, ROS production is mediated by RbohD and RbohF genes after nematodes infections leading to galls formation and cell death (Siddique et al. 2014). Moreover, SA, JA, ET, BRs, and ABA are involved in plant response to nematodes (Nahar et al. 2011; Kammerhofer et al. 2015; Kyndt et al. 2017; Song et al. 2017). Notably, JA is implicated in systemic defense induction of rice (Nahar et al. 2011), watermelon (Yang et al. 2018) and tomato (Sun et al. 2010) against nematodes. Recently, it has been demonstrated that implication of JA in plant defense against Root Knot nematode is related to the alterations of antioxidative protection and photosynthetic processes (Bali et al. 2017). Moreover, application of exogenous SA alleviates plant infections by nematodes (Molinari et al. 2014; Martìnez-Medina et al. 2017). In another hand, biotrophic and necrotrophic pathogens infections are positively regulated by red lights in several plants (Mutar and Fattah 2013; Yang et al. 2015). Recent founding showed that the incidence of Root Knot nematodes in watermelon was inhibited by diurnal red lights comparing to white lights. This plant defense was closely related to a remarkable increase of many genes (AOS, PRI, ICS, WRKY70, and LOX) in association with a pronounced increase in SA, JA, and H2O2 contents in various tissues of watermelon plants (Yang et al. 2018). JA and SA participate to plant defense against nematodes such as M. incognita (Kammerhofer et al. 2015). This pathogen forces plants to activate SA pathways and to inhibit JA pathway in leaves to allow a successful pathogen invasion (Martìnez-Medina et al. 2017). Interestingly, JA has a higher accumulation in roots after root knot nematodes infection which is transported later to the leaves which helps plants to trigger their defense against nematodes (Zhang and Baldwin 1997). Furthermore, plant treatment by red lights enhances JA accumulation in roots and leaves (Yang et al. 2018) confirming the importance of JA signaling in rhizo-bacteria-induced systemic resistance (Fujimoto et al. 2011). Besides, studies conducted on tomato and watermelon confirms that exogenous MeJA application reduced root knot nematodes infections (Fujimoto et al. 2011; Yang et al. 2018). Moreover, due to the antagonistic roles between SA and JA, red lights inhibit SA accumulation in leaves (Yang et al. 2018) but stimulated its accumulation in roots after nematode infection underlying the positive effect of red lights on SA accumulation on roots (Branch et al. 2004; Yang et al. 2018). Meanwhile, red lights stimulate JA accumulation in roots demonstrating a positive regulation of JA biosynthesis genes by red lights; such results could indicate a synergic interaction (van Wees et al. 2000; Yang et al. 2018). This is shown at the molecular level by transcript accumulation of ICS gene (for SA biosynthesis) and LOX and AOS genes (for JA biosynthesis). In parallel, red lights induces accumulation of WRKY70 transcript and H2O2 particles after root knot nematode infections in both roots and shoots of watermelon (Yang et al. 2018) suggesting a pivotal role of WRKY70 TFs and ROS signaling in red lights-induced plant defense against Root Knot nematodes in watermelon plants. Accumulation of WRKY70 in roots only could suggest that this TF acts as a point of convergence between JA-mediated and SA-mediated signals in plant defense (Li et al. 2004; Yang et al. 2018).

Interaction between JA and other plant growth regulators

Plant genomes encodes for plant growth regulators which are implicated in plant growth and development and are also implicated in plant response to biotic and abiotic stresses. Thousands of works have described biosynthesis of those endogenous organic compounds (Liu et al. 2017; Chandler and Werr 2015; Kazan 2015; Li et al. 2019). They also underline the way to modulate plant response at molecular and physiological levels. Interactions between phytohormones are crucial for prompt and efficient plant responses to biotic and abiotic stress factors. The endogenous concentrations of those natural compounds are low, and it changes depending of the applied stress. Those observations suggest that plant hormones interact with each other to modulate plant development as revealed for IAA/CKs interplay (Liu et al. 2017; Chandler and Werr 2015). Some works demonstrated that JA interacts with salicylic acid (Liu et al. 2016a), ethylene (Kazan 2015; Li et al. 2019), GA (Wasternack and Hause 2007), IAA (Chen et al. 2011), BR (Choudhary et al. 2012) and ABA (Aleman et al. 2016) to unsure plant response to biotic and abiotic stress. Moreover, it has been demonstrated that stress imposition involves usually the activation/inhibition of a high number of genes as a response to the biosynthesis of phytohormones. For example, in response to drought stress ABA, IAA, JA, GA, SA, and ET orchestrate to upregulate almost 859 genes in Arabidopsis as revealed by transcriptomic studies (Ding et al. 2013). In this section, we describe the crosstalk between JA and other phytohomones GA, CKs, SA, ABA, BR, ET, and auxin to modulate plant growth and development.

The JA–GA interaction

GAs are crucial hormones controlling many aspects of plant growth and development, such as leaf expansion, stem elongation, root development, seed germination, and stamen and flower development (Um et al. 2018). In another hand, several studies suggest that GA is crucial for growth inhibition in stress conditions (Liu and Hou 2018). In unfavorable stress conditions, plants inhibit their growth by activating their defense systems and inhibiting developmental programs. Many works suggest an antagonistic role between GA and JA to coordinate plant development under normal and stress conditions (Jang et al. 2017). This is ensured by the direct interaction between DELLA (GA signaling repressor) and JAZ (JA signaling repressor) proteins (Fig. 4; Yang et al. 2012; Hou et al. 2010). It has recently shown that rice OsJAZ9 acts as the key JAZ protein in mediating crosstalk between JA and GA (Um et al. 2018). It interacts with a DELLA protein called SLENDER RICE 1 (SLR1). Overexpression of OsJAZ9 enhanced rice GA response. Thus, we can speculate that JA acts as an essential hormone that modulates plant growth under stress conditions due to its antagonistic interaction with GA.

Fig. 4
figure 4

Schematic representation of antagonistic action between JA and GA. a In Free JA conditions, the GA concentrations in cell increase to unsure growth programs. The direct interaction between JAZs and DELLA proteins is abolished by degradation of DELLAs, and JAZ proteins inhibit the activity of MYC2 TF. This activates PIF TFs to interact with responsive gene inducing GA responses. b In GA-free situation, JA concentration increases. Ile-JA/JAZ1/COI1 complex is released by the ubiquitation and degradation of JAZs by proteosome 26. Thus, the MYC2 TF is activated and enhanced transcription of JA-induced genes

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The JA–CKs interaction

Cytokinin (CKs) control a plethora of aspects related to plant growth and development by maintaining stem cell integrity as well as cell proliferation. In higher plants, zeatin is the most abundant form of CKs and occurs as two isomers, trans-zeatin (tZ), the active form and cis-zeatin (cZ); less active form. Trans-zeatin is synthetized under the control of several hormones such as Isopentenyl transferases (IPTs), and cytochrome P450 CYP735A1 and CYP735A2 (Kieber and Schaller 2018). JA and JA-dependent stress response genes affect the expression of CKs gene response (Argueso et al. 2009). CKs deficient plant mutants are tolerant to stress and respond to stress application in a manner like transgenic plants having high JA concentrations (Qi et al. 2014). In higher plants, CKs receptors, called histidine phosphotransferase-proteins transcription factors, regulates CKs responses in plants. Many works suggest that JA and CKs act antagonistically controlling various plant development aspects. In fact, in soybean, the CKs induced callus Growth is inhibited by JA (Ueda and Kato 1982). Furthermore, JA has an antagonistic effect on CKs as JA inhibits the expression of genes implicated in chlorophyll development (Liu et al. 2016b). In another hand, it has been demonstrated that JA positively controls xylem differentiation in Arabidopsis roots and eliminates the specific procambium response to CKs application (Jang et al. 2017). In contrast, CKs acts as a negative regulator of xylem differentiation in Arabidopsis roots. Taken together, those results approve the idea that CKs interacts antagonistically with JA in xylem development in Arabidopsis roots. Interestingly, myc2 mutant did not show extra xylem formation in response to exogenous JA. Moreover, the expression of CKs signaling inhibitor, AHP6, was inhibited in this mutant. Those results suggest that MYC2 transcription factor is involved in this process by promoting AHP6 expression. Nevertheless, it has been demonstrated that JA and CKs antagonistically interact in the plant response to circadian stress (Nitschke et al. 2016). In fact, plants with reduced or defective CKs levels present a JA-dependent cell death phenotype in response to circadian modification, in contrast to wild types (Nitschke et al. 2016).

The JA–auxin interaction

Auxin is a crucial phytohormone implicated in plant growth and development (Figueiredo and Köhler 2018). In plants, the predominant form is called IAA (Indole-3-acetic-acid). IAA biosynthesis could take place through two different pathways: tryptophan-dependent and -independent pathways (Wang et al. 2019). The JA–IAA interaction controls many aspects of plant physiology and development such as production of secondary metabolites, tendril coiling and cell elongation (Saniewski et al. 2002). Unfortunately, those interactions have never been demonstrated at the molecular level. The most studied aspect of JA–IAA interaction is the regulation of plant roots development. In fact, the apical roots growth was inhibited by JA. This was demonstrated by wild-type plants treated by JA. They form much shorter roots comparing with non-treated plants. In contrast, JA defective mutant plants presents roots with similar length comparing with wild type mainly in presence of JA treatment (Jang et al. 2017). Meanwhile, auxin is crucial hormone implicated in the control of root growth. Auxin deficient mutants or signaling mutants develop shorter roots in comparison with wild-type plants as demonstrated for (trp2-12) and auxin resistant 3 (arx3-1) (Zhang et al. 2019). Those findings suggest that JA–IAA interaction could mediate root growth inhibition as revealed by (Chen et al. 2011). The group showed that JA inhibits root growth by reducing root meristem activity as exogenous JA application inhibits PLETHORAs (PLTs) expression, auxin-responsive transcription factors controlling cell proliferation (Mahonem et al. 2014). Interestingly, PLTs expression level was not modified in JA signaling mutants, such as coi1-1 and myc2. Authors suggest then that COI1 could be implicated in controlling root phenotype, whereas MYC2 directly binds to the PTLS promoters and inhibits their expression. This suggests that auxin and JA antagonistically interact in the regulation of apical root growth (Fig. 5).

Fig. 5
figure 5

Role of JA/Auxin crosstalk in plant growth and development. JA and IAA signaling pathways positively regulate flowering via MYB21/MYB24 Tfs but negatively regulate root growth through JAZs-MYC2

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The development of floral organs is another physiological process controlled by JA–IAA interaction (Reeves et al. 2012). An interaction between IAA and JA modulates petals and stamens development under the control of R2R3 MYB transcription factors especially MYB21 and MYB24 TFs which are considered as key regulators of petal and stamen growth (Reeves et al. 2012). Moreover, ARF6 and ARF8 TFs control the regulation of expression of MYB21 and MYB24 JA-responsive TFs (Fig. 5). Nevertheless, the regulation of leaves senescence is also controlled by IAA–JA interaction. In fact, JA acts as a positive regulator of leaf senescence as JAZ7 proteins suppress dark-induced leaf senescence and MYCs TFs, such as MYC2, promote senescence by activating the senescence-associated genes expression as well as chlorophyll degradating-related genes, demonstrating that JA stimulates leaf senescence pathway in a COI1-dependent manner (Yu et al. 2015). In this pathway, JAZ4, JAZ8 and WRKY57 act as negative regulators contrarily to JAZ7 and the auxin signaling repressor IAA29 functions as a positive regulator. Moreover, WRKY57 negatively regulates senescence-associated gene expression by interacting with JAZ4/8 and IAA29. Authors speculate that competition between the WRKY57–JAZ4/8 WRKY57-IAA29 implies the adequate response to the physiological stimulus. Thus, an antagonistic JA–IAA interaction is involved in leaf senescence (Fig. 5; Jiang et al. 2014).

JA–Brassinosteroids crosstalk

Brassinosteroids (BR) are implicated in different aspects of plant growth and development. They are also involved in the modulation of JA signaling and JA-dependent growth inhibition.

In contrast to JA, BR promotes above-ground plant growth. Thus, JA-BR crosstalk is insured by the balance between plant growth and defense resistance (Yang et al. 2019). For example, low BR concentrations induce OsDI1 and OsDWARF expression at early and late stages of BR biosynthesis, which activate the defense pathway (Yang et al. 2019). Moreover, DWARF4 encodes a key enzyme responsible for BR biosynthesis and a leaky mutation of DWARF4 restored JA sensitivity in the coi1 mutant background and showed JA hypersensitivity in the wild-type background. Furthermore, expression of DWARF4 was down regulated by JA in a COI1-dependent manner, and exogenous BR treatment attenuated the effects of JA on root growth inhibition (Ren et al. 2009). These results indicate that a BR–JA interaction is involved in the modulation of JA signaling. A low BR concentration activates BR signaling pathways such as BR receptor BRI1, BR-related kinase BAK1, and BR-related TFs. This induces the activation of several downstream genes such as BES1 and BZR1, which activate plant response to many abiotic stresses (Yang et al. 2019).

The JA–SA crosstalk

After stress perception, JA rapidly regulates plant gene defense (Genva et al. 2019). The A. thaliana coronatine insensitive 1 (coi1) mutants presented a blocked JA response (Feys et al. 1994). COI1 is a JA receptor that belongs to the F-box protein family. It acts as an E3-ubiquitin ligase-mediated proteolysis of target proteins (Hiruma et al. 2011) such as JASMONATE ZIM-DOMAIN (JAZ) proteins. JA is essentially involved in plant response against necrotrophic pathogens. SA mediates plant resistance against biotrophic and hemibiotrophic pathogens (Fu et al. 2012). JA signaling modulates many NAC Tfs activities (such as ANAC019/055/072) to block SA accumulation through modulation of multiple NAC TFs. Briefly, physical interaction between MYC2 and several NACs promoter activates their transcription. Expressed NAC TFs inhibits the expression of SA biosynthesis gene called ISOCHORISMATE SYNTHASE 1 (ICS1) but stimulate the expression of a SA methylation gene, BENZOIC ACID/SA CARBOXYL METHYLTRANSFERASE 1 (BSMT1) (Zheng et al. 2012). In addition, many other components are involved in SA-JA crosstalk such as MYC2, TGAs, and PDF 1.2 (Gatz 2013); mitogen-activated protein kinase (MAPK) (Suarez-Rodriguez et al. 2010), redox regulators glutathione (GRX) and thioredoxin (TRX) (Sopel and Gary 2011) and WRKY70 (Shim et al. 2013). GRXs genes can block TGA-mediated JA response gene expression, such as ORA59 confirming SA–JA antagonism (Zander et al. 2010). MPK4 is a positive regulator of GRX480 (SA signaling pathway) and acts as a negative regulator of MYC2 (JA signaling pathway) (Wasternack and Hause 2007). Meanwhile, TRX enzyme transforms NPR1 polymers to monomers in presence of SA. Those monomers such as GRX480 are transported to the nucleus and specifically bind to TGAs, which also directly regulate the expression of PR1 (Fu et al. 2012; Gatz 2013; Zander et al. 2010). A schematic presentation of JA–SA crosstalk component is presented in Fig. 6.

Fig. 6
figure 6

JA-SA crosstalk in plants in response to pathogen infection. Plant infection by a pathogen leads to the increase in the endogenous SA concentration and the activation of NONEXPRESSOR OF PR GENES1 (NPR1), which induces WRKY70 transcriptional activity. In turn, WRKY70 promotes PR1 gene expression and thus enhancing pathogen response

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In addition to its crucial role in ensuring plant defense against pathogens, other important roles of SA in regulating many physiological processes and responding to adverse environmental situations have emerged. SA is implicated in plant response to salinity (Khan et al. 2012), light (Tuteja and Gill 2013) and cold (Gornik et al. 2014). In fact, plant treatment with JA or SA improves plant resistance to chilling (Gornik et al. 2014). Moreover, MeJA and MeSA present a protective effect against chilling injury in pomegranates fruits (Sayyari et al. 2010). SA and JA are also implicated in plant tolerance to drought (Ilyas et al. 2017). In another hand, several studies concentrated on the role of SA and JA in plant tolerance to salinity. In fact, some researches demonstrated that JA and SA protect plants from negative effects of salinity by the induction of gene encoding effective proteins expression (Khan et al. 2012). Moreover, it has been found that exogenous SA and JA application decreased Na+ concentrations in soybean cells under different salt stress levels and that JA has a greater effect on Na+ reduction than SA (Farhangi-Abriz and Ghassemi-Golezani 2018). Therefore, a regulatory protein called glutaredoxin GRX480 is a key protein in JA and SA signaling. This protein mediates redox regulation of proteins by catalyzing disulfide transitions (Meldau et al. 2012). In Nicotiana attenuata plants, researches demonstrated that mitogen-activated protein kinase 4 (MPK4) have a dual role in plant signaling. In fact, in response to light stress, this kinase acts as a negative regulator during the SA signaling pathway, but it plays a positive role during the JA signaling pathway (Tuteja and Gill 2013). To coordinate regulation between SA and JA, cells involve several factors such as GRX480 or MAPK4. Moreover, exogenous application of SA and/or JA can enhance abiotic stress responses (Tuteja and Gill 2013).

JA–ABA crosstalk

Upon external stimuli application on plants, an immense signaling network of events occurs in cells. Ca2+ sensors act in the first line of defense to decode and then transducer signals through the suitable stress hormone pathways to activate the appropriate signaling cascade. ABA is a well-studied phytohormone implicated in plant response to abiotic stress. Many studies described that ABA and JA presents an antagonistic role in plant growth and development (Chen et al. 2011). In another hand, those hormones act synergistically in response to environmental stress and MYC2 unsure that crosstalk (Chen et al. 2011). In A. thaliana as well as tobacco plants, PYRABACTIN RESISTANCE1-Like proteins (PYLs) known as ABA receptor proteins control metabolic reprogramming via JA signaling pathway. Thus, JA/ABA crosstalk can control plant metabolism and growth (Per et al. 2018). When endogenous ABA concentration increases in response to external (salt stress, drought…) or internal (growth and development) conditions, ABA interacts with many members of the PYL/RCAR ABA receptor family to inhibit 2C protein phosphatases (PP2C proteins) thus to initiate signal transduction. Recently, a direct interaction between the ABA receptor PYL6 RCAR9 and MYC2 TF has been demonstrated (Aleman et al. 2016). This interaction is enhanced in presence of ABA. Moreover, ABA receptor PYL6 forms a complex with JAZ6 and JAZ8 to stimulate the transcriptional activity of MYC2. In fact, MYC2 stimulate VSP2 expression, inhibits PTL1 and PTL2 expression and root development.

JA–ET crosstalk in plants

Many researchers found that JA and ET could antagonize or coordinate to regulate plant stress response (Zhu and Lee 2015). In fact, MYC2 (JA signaling) and (EIN3-like 1 (EIL1) and ET INSENSITIVE3 (EIN3) involved in ET signaling pathway are implicated in JA/ET crosstalk (Zhang et al. 2014). Recent findings showed that when plants are exposed to a necrotrophic or hemibiotrophic pathogen attacks, JA signaling pathway act in synergy with the ET signaling pathway to activate defense proteins such as PDF1.2 expression by activating ERF1 and ORA59 expression. Thus, JA and ET control plant response to nectrophic pathogens through JAZs-MYC2 and EIN3/EIL1 (Pieterse 2012). Moreover, JA enhances the degradation of JAZ, so MYC2 is activated to regulate ORA59/ERF1 expression and VSP2, a wound responsive gene to respond to herbivorous insect attacks (Yang et al. 2019). Besides, JAZ inhibits EIL2/EIN3 transcriptional activity downstream ORA59/ERF1 that targets the promoter of PLANT DEFENSIN 1.2 (PDF1.2) and induces its expression thereby resisting the infection of necrotrophic pathogens and hemibiotrophic pathogens (Pieterse 2012). In Arabidopsis, JA inhibits apical hook formation via activation of MYC2:3:4 TFs. ET stabilizes EIN3/ EIL1 complex leading to the inhibition of the transcriptional function of MYCs, and it attenuates MYC-mediated plant defenses against insect attack (Song et al. 2014).

In the lights of those findings, we can conclude that hormonal interactions play a critical role for insuring plant physiology and growth (Yang et al. 2019). The cross talk of JA with other hormones (IAA, GA, CKs, BR, JA ABA and SA) ensures plant growth and defense. Direct JA–GA, JA–IAA, JA–BR, and JA–CKs interactions play important role in modulating physiological role such as root and floral organs development and can help plant to optimize their growth and development in stressful conditions. However, this interaction is almost antagonistic but in some cases it is synergic. In fact, despite JA–GA interaction antagonistically control stem elongation, it plays a positive role to control stamen development (Qi et al. 2014). In the same way of idea, JA–IAA interaction negatively regulates apical roots growth but positively regulate lateral root growth (Cai et al. 2014).

Conclusion and prospects

Jasmonic acid and its derivatives have pivotal roles in the establishing plant defense and resistance in response to environmental stimuli. The mechanisms of action of JA are specific when plants are subjected to different environmental constraints due to the diversification of plant hormone interplay. Several genes (e.g. JAZ, AOS1, AOC, LOX2, and COI1) and TFs (MYC2 and bHLH) are involved in the core JA signaling pathway as activators or repressors, thereby modulating the responses to stimuli received by the plants from the surrounding environment. The JAZ-MYC module has a key role in the JA signaling pathway through the assimilation of regulatory TFs and associated genes. Plant hormone signaling systems are complicated and unstable, especially under complex environmental conditions. Over the years, JA crosstalk with other phytohormones has been elucidated. However, information in plants is still limited. Crosstalk nodes between those hormones have to be investigated. In presence of abiotic constraints, JA orchestrate plant stress responses by stimulating the plant’s defense apparatus, which mainly involves phytohormones and other defensive compounds such as antioxidative enzymes. JA functions synergistically and antagonistically with ABA, ET, SA, and other plant hormones to accomodate environmental constraints. The process is usually accompanied by the regulation of plant maturation and development hormones. Future studies can spot how plant distinguish between different environmental signals to activate a specific signaling pathway to respond to stress as well as to synthesis Jas and TFs/JAZ repressors interactions during JA action. Future studies can also clarify the molecular control of JA interaction with its transporter to control it’s moving through plants. Furthermore, crosstalk between JA and other phytohormones is not linear and researches should focus on the spatio-temporal relationships between hormones using new chemicals that act as targets of JA in vivo or using high-throughput nucleotide sequencing techniques as well CRISPR-CAS technology to generate specific mutant that allows underlying mechanisms of plant tolerance to unfavorable environments. Thus, understanding the signal transduction mechanism of JA under environmental stress is essential to promote plant resistance, with potential improvements in plant survival and crop yield.