Abstract
Jasmonates (JAs), such as jasmonic acid and its methyl ester, are lipid-derived compounds with signal functions in plant growth and development, as well as in responses to stress. JAs are widely distributed in plants as natural plant growth regulators. JAs do not work independently but work as a part of a complex signaling network with other phytohormones. They are deployed to induce response during wounding and are often used for elicitation and stimulation of secondary metabolites production in different in vitro culture systems. Application of JAs seems to be promising during different steps of the micropropagation system for different species. JAs stimulate proliferation rate of shoots, roots, callus and induce microtubers and bulblets formation. However, negative effects of JAs on the condition of plant tissues are also reported, e.g. leaf senescence, reduced growth and inhibited somatic embryogenesis. This review summarizes the current knowledge of the application and properties of jasmonates under in vitro conditions in terms of cell division, explant growth, proliferation ability, storage organ formation and stress response.
Key message
The review summarized in detail the results achieved for plants cultivated in vitro in the presence of jasmonates and their possible mechanisms of action.
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Introduction
Jasmonates (JAs) are widely distributed in plant tissues with high activity and growth rate, such as the stem tips, root tips, young leaves, flowers and unripe fruits. Endogenous JAs levels increase in response to the external stimuli, including mechanical damage, pathogen attack and osmotic stress (Sembdner and Parthier 1993; Creelman and Mullet 1995).
Jasmonic acid (JA) and its methyl ester (methyl jasmonates, MeJA) are linolenic acid (LA)-derived cyclopentanone-based compounds that belong to oxylipins (Creelman and Mullet 1995). It is believed that JA and MeJA represent a separate group of plant growth regulators with hormone-like properties (Sembdner et al. 1990). The initiation of JAs biosynthesis begins with the release of α-linolenic acid (Fig. 1) from chloroplast membranes, which undergoes multistage reactions catalyzed by enzymes present in plastids, peroxisomes and cytoplasm (Ghasemi Pirbalouti et al. 2014; Sharma and Laxmi 2016) and is regulated by light conditions (Zhai et al. 2007). Among exogenous JAs it was showed that more effective is MeJA due to its easier cell membrane crossing ability in comparison to JA and quick demethylation to free JA (Fattorini et al. 2018).
Bioactive form of JAs synthesized by JAR1 (Jasmonyl-L-amino acid synthetase; Fig. 1) is (7S,3R)-JA-Ile perceived by the COI1 receptor (the F-box protein CORONATINE INSENSITIVE 1) (Staswick and Tiryaki 2004; Fonseca et al. 2009; Wasternack and Hause 2013; Ueda et al. 2020). However, biochemical analysis indicated that OsJAR1 encodes an enzyme conjugating JA not only to isoleucine (Ile) but also to tryptophane (Trp), leucine (Leu), methionine (Met), phenylalanine (Phe) and valine (Val) (Staswick 2009). JA-Ile binds to the Skp1-Cullin-F-box (SCF)COI1E3 ubiquitin ligase complex which further recruits JAZ (JASMONATE ZIM-DOMAIN) transcriptional repressors for degradation through 26S proteasome, allowing the expression of JA-responsive genes (Zhai et al. 2017; Hyde et al. 2018; Fig. 1). JAZ repressors bind and inhibit the MYC family of transcription factors which ultimately leads to the growth promotion of leaves. However, JAZ-MYC interaction also takes part in plant growth inhibition during defense responses (Major et al. 2017; Guo et al. 2018). JA-Trp acts as an endogenous auxin inhibitor in A. thaliana and exogenously caused agravitropic root growth (Staswick 2009). The biological functions of other JA-amino acid conjugates are still unclear, although different COI1 homologs with variable preference perceive those bioactive molecules (Xiao et al. 2014; Yan et al. 2016).
The presence of JAs is associated with different changes in plant development and structure. Many studies have shown that JA and MeJA are involved in leaf senescence by stimulation of chlorophyll degradation. JA exposure causes damage to chloroplasts, decreases photosynthetic activity as a result of stimulation of RuBisCO degradation, stimulates destruction of cell membrane structure in the lipid peroxidation process and increases expression of senescence associated genes. The application of MeJA in turn, leads to an increase in the rate of cellular respiration, proteolytic and peroxidase activity in the leaves (Parthier 1990; Creelman and Mullet 1997; Liu et al. 2016). However, JAs are also involved in the defense responses to herbivore attack, promotion of shoot growth, storage organ formation: bulblets and tubers, flowering processes, fruit and inflorescence number (Rohwer and Erwin 2008; Hummel et al. 2009).
Many studies on JAs effect were carried out on field or pot-grown plants, while its potential in in vitro culture need to be fully understood. The aim of this review is to summarize studies investigating the role of jasmonates in micropropagation, explants growth, storage organ formation and somatic embryogenesis in plants under in vitro conditions. This review might provide a starting point for further research using jasmonates.
Use of JAs during plant micropropagation
Basal culture medium provides all nutrients, energy and water necessary for plantlets, organs, tissues or cells growth. Regulation of developmental processes in plant tissue culture generally requires the addition of plant growth regulators (PGRs). Successful micropropagation strictly depends on a selection of appropriate PGRs and their concentration. The most commonly used PGRs are auxins and cytokinins which regulate growth and organize development of a plant tissue. In general, auxin mediates cell division and cytokinin mediates cell differentiation (Moubayidin et al. 2009). However, cultured plant tissues are also influenced by gibberellins (GAs), brassinosteroids (BRs), ethylene (ET), abscisic acid (ABA), salicylic acid (SA), jasmonates (JAs) and interactions among them (Gaspar et al. 1996; Phillips and Garda 2019). Exogenous application of JAs can affect a great variety of morphological and physiological responses in plants. Jasmonates, like all growth regulators, do not work independently but they are involved in a complex signaling network of interactions among multiple plant hormone signaling pathways (Yang et al. 2019). Different effects of exogenously applied PGRs, including JAs, may arise from modification of synthesis, catabolism, activation, sequestration, transport, or sensitivity to endogenous phytohormones of the same or other type (Gaspar et al. 1996).
A large number of studies conducted in different in vitro conditions have shown that exogenous JAs inhibit plant growth by suppression of the cell proliferation and expansion (Patil et al. 2014). However, high level of endogenous JAs was observed especially in young organs with high rate of cell division, therefore growth-promoting activity of JAs cannot be excluded and it was proposed that JAs-mediated physiological response might be a consequence of changes in endogenous cytokinins level which affects and regulates cell cycle (Avalbaev et al. 2016). Cell cycle is also under the gibberellins signaling control (Achard et al. 2009). Analysis of Nicotiana attenuata plants treated with exogenous JA and GA showed that JAs might indirectly repress shoot growth by antagonizing the GA pathway through specific DELLA-JAZ interactions and down regulation of photosynthesis (Machado et al. 2017). The GA signal is perceived by GID1 (GA-insensitive dwarf1). The GID1-GA complex stimulates plant growth and development by down-regulating DELLA repressors. In the absence of GA DELLAs compete with MYC2 for binding to JAZs, thereby releasing MYC2 to activate expression of MYC2-regulated genes. In the presence of GA DELLAs are degraded through SCFGID2E3 complex leading to inhibitory JAZ-MYC2 interactions (Fig. 1; De Bruyne et al. 2014).
Cell cycle and cell proliferation
One of the first characterized physiological ex vivo effect of JAs was growth inhibition of the potted Vicia faba pericarp as a result of a cell cycle disturbance (Dathe et al. 1981). On this basis, a number of studies focused on the inhibitory effect of JAs on plant growth have been developed also under in vitro conditions. Ueda and Kato (1982) reported that JA and MeJA were powerful inhibitors of kinetin‐ and N‐phenyl‐N′‐(2‐chloro‐4‐pyridyl)urea‐induced callus growth of Glycine max. Plant growth and development are related to cell expansion and cell differentiation, but also are strictly linked with cell division (Perrot-Rechenmann 2010). Świątek et al. (2002) compared the effect of JA with ABA on the cell cycle using Nicotiana tabacum BY-2 cell line. Their results showed that these phytohormones disturbed cell cycle progression by preventing DNA replication. Exogenous application of both compounds before the G1/S transition caused retention of cells in the G1 phase of the cell cycle. ABA application at a later stages did not affect further progression of the cell cycle, whereas JA effectively prevented cells from entering mitosis (cells arrested in G2 phase; Fig. 2). Those observations showed that the growth inhibition in response to JA might not resulted from a cell expansion in the elongation zone, but from a disruption of meristem activity (Świątek et al. 2002). Continued research confirmed that JA application led to tobacco BY-2 cell arrest in both G1 and G2 phases (Świątek et al. 2004). Analysis of a gene expression of Arabidopsis genome showed that also MeJA inhibited the activation of the M phase genes thus cells were arrested in the G2 phase of the cell cycle (Pauwels et al. 2008; Fig. 2). However, JAs treatment leads to reprogramming cells through the activity of specific transcription factors and proteins activity. It was indicated that MeJA primarily activates expression of the genes involved in jasmonate synthesis, thus cell cycle genes expression is suppressed in the later stages (Gumerova et al. 2015; Pauwels et al. 2008).
In asynchronously dividing Taxus cuspidata cultures addition of MeJA resulted in turn in four effects on the cell cycle: transient increase in G2 phase cells, transient decrease in S phase cells, and at later stages post-elicitation, increase in G0/G1 phase cells and decrease in G2 and S phase cells. After 96 h of elicitation with MeJA, percentage of cells in the G2 and S phases decreased but in the G1/G0 phases increased, therefore it was suggested that cells treated with MeJA were not arrested in the G2/M transition but progression through the cell cycle was slowed down. A time lag between MeJA-mediated growth inhibition and cell death in asynchronously dividing T. cuspidate cell culture suggested that observed growth suppression in response to MeJA was not due to necrosis and/or rupturing of cell membranes, although the evidence indicated that JAs might affect cell walls (Capitani et al. 2005; Patil et al. 2014). Northern analysis and in situ hybridization using cDNA probes of the G1/S phase-specific genes confirmed enhanced proliferation growth of N. tabacum cells in response to relatively low concentrations of MeJA, whereas in highest concentration (10 μM) MeJA indicated transient effect and was more effective in enhancing defense-related processes such as cell wall thickening (Capitani et al. 2005). It was reported that MeJA elicitation increases content of cellular monolignols in A. thaliana (Pauwels et al. 2008) which polymerize into lignin according to the cell-wall class III peroxidases generating reactive oxygen species (ROS) from hydrogen peroxide. Peroxidase expression and activity is also stimulated by JA. These changes in response to JA are associated with a cessation of a growth and decreased cell expansion as a result of increased cross-linking of primary cell-wall components (Almagro et al. 2009; Napoleao et al. 2017; Hyde et al. 2018). An earlier report indicated that JAs delayed regeneration of the cell wall in protoplast of Solanum tuberosum (Ravnikar et al. 1992). In contrary to all these observations, it was reported that JA promotes division of mitotically less active cells in the root apical meristem named quiescent center (QC) in A. thaliana. Furthermore, JA pre-treatment increased number of new columella cell layer between QC and ablated cells, which suggest that JA stimulates stem cell replacement after ablation (Chen et al. 2011). JA-dependent regeneration network is highly important for plant response to parasitic infection (Zhou et al. 2019).
Effect of JAs on the cell division was also indirectly visualized during callus propagation under in vitro conditions. In higher concentration (5–50 μM) both JA and MeJA inhibited callus growth of Medicago sativa during differentiation stage (Ruduś et al. 2001; Table 1; Fig. 3). Elicitation with 10–100 μM MeJA significantly decreased cell viability of T. cuspidata and Taxus baccata suspension culture on WB/A medium supplemented with 6-benzylaminopurine (BA) and 1-naphthaleneacetic acid (NAA) (Bulgakov et al. 2011). Also 100 µM MeJA significantly decreased cell viability in protoplast culture of A. thaliana due to the rapid accumulation of H2O2 (Zhang and Xing 2008). Enhanced hydrogen peroxide and superoxide radical production was also detected in Salvia miltiorrhiza hairy roots (Liang et al. 2012) and Panax ginseng roots (Ali et al. 2006). In Ricinus communis gradual accumulation of H2O2 was indicated between 1 and 6 h after MeJA treatment of plants germinated under ex vivo conditions (Soares et al. 2010). High level of accumulated ROS leads to lipid peroxidation in cell membranes that might cause membrane damages, imbalance of cell homeostasis and further cell death (Pérez-Pérez et al. 2012). Correlation between oxidative stress and JAs is very complex. It was proposed that JA at a definite concentration can directly modify superoxide dismutase (SOD) structure that stimulates its activity (Maksymiec and Krupa 2006), thus JAs indicated both antioxidative and pro-oxidative activity (Ho et al. 2020). Exposure to JA and MeJA (50–200 µM) of Mentha × piperita cell suspension culture resulted in a less biomass accumulation than that of the control. Both elicitors suppressed growth of the cell suspension culture, although stronger inhibition was noted for MeJA application. Furthermore elicitation resulted in cultures color change from greenish to brown. Authors mentioned that this effect might be caused by increased accumulation of phenolic compounds and their oxidation what correlates with stimulatory effect of JAs on secondary metabolites accumulation (Krzyzanowska et al. 2011).
Earlier reports indicated that JAs not only have suppressing effect, but also have stimulating effect on cell division in various culture conditions or plant species, thus effect of JAs depends on its concentration, interaction with a specific PGRs and type of explant. In S. tuberosum JA (0.01–1.0 μM) combined with BA and 2,4-dichlorophenoxyacetic acid (2,4-D) stimulated cell division manifested by increased number of microcalli (Ravnikar et al. 1992). Similar results were obtained for Prunus avium and Vigna mungo callus cultures propagated on B5 and MS medium, respectively, supplemented with JA in the comparable concentrations (Table 1), although without any other hormonal additives (Kondo et al. 2002; Lingakumar et al. 2014). Addition of the ester derivative of JA also affected callus growth. MeJA (10–40 μM) combined with 2,4-D and kinetin (Kin) increased callus growth rate from Dianthus caryophyllus leaf explants (Matter et al. 2017). Even ten times higher concentration (118.9–475.6 μM) of MeJA in MS medium with BA and NAA increased fresh and dry weight of Catharanthus roseus callus (Al-Zuhairi and Ghanm 2017). The JAs effect might also depend on the growth stage of the plants. In Malus pumila growing in an open field, the endogenous level of JA is high in the early stages of pulp development, thus effect of exogenous JA under in vitro conditions varied between samples from ex vivo plants collected in different days after blooming (DAFB). It was indicated that only at 15 DAFB, when the plant tissue was still in the cell division stage, JA promoted callus formation. At 25 and 35 DAFB, JA in turn inhibited callus formation probably because endogenous JA concentrations increase with time of fruit growth. These results indicated that only low endogenous JA level promotes callus formation, whereas increasing JA concentration inhibits this process (Kondo et al. 2001).
Organogenesis
Analyzing JAs addition during plant micropropagation, it was reported that these compounds perform varied effects, either promoting or inhibitory. For example, JA in concentrations of 0.5–2.0 μM shortened time for shoot initiation, increased shoot and root elongation, number of nodes, leaves and roots in stem nodes of S. tuberosum placed onto MS medium (Kumlay 2016; Table 1). In turn, growth of the Oryza sativa seedling was inhibited with increasing concentration of JA in MS medium, even in the presence of 1 μM JA root growth was reduced twofold over the control (Cho et al. 2007). As it was noticed role of JAs seems to be species- and context-dependent (Lakehal and Bellini 2018) and mentioned JA and GA growth-defense balance should be considered during analyzing the JAs effect on the propagation effectiveness. Generally it is presupposed that JA prioritizes defense, in turn GA—prioritizes growth. Inhibited plant growth as a results of JA treatment is probably related with suppression of GA-mediated pathway (Hou et al. 2013; Nguyen et al. 2019a). It was indicated that MeJA-mediated growth inhibition might results also from the perturbations in mitochondrial membrane integrity, decreases in the biosynthesis of ATP and proteins involved in energy metabolism (Ruiz-May et al. 2011; Cho et al. 2007).
Shoots proliferation and growth of the aerial parts
In the shoot induction, development and proliferation cytokinins play a vital role. In S. tuberosum stem node cultures it was indicated that exogenous JA increased the ratio between physiologically active and inactive cytokinins without changing its total content (Dermastia et al. 1994). In turn, Triticum aestivum seedlings treated with MeJA showed two-fold increased accumulation of cytokinins without changes in ABA and auxins levels (Avalbaev et al. 2016). It was also reported that MeJA increased accumulation of cytokinins, despite the antagonistic interaction between JA and cytokinin noted in xylem development of A. thaliana (Jang et al. 2017). JAs were considered as inhibitors of cytokinin-induced plant growth manifested by reduced biomass in A. thaliana (Yan et al. 2007,2009; Zhang and Turner 2008; Noir et al. 2013; Attaran et al. 2014; Table 1; Fig. 3) and in O. sativa (Yang et al. 2012; Hibara et al. 2016). JA suppresses cell proliferation in wounded A. thaliana plants leading to a reduced leaf size with fewer and smaller epidermal cells giving a “bonsai effect” (Zhang and Turner 2008; Noir et al. 2013; Yang et al. 2019). JAs act as a growth inhibitors even in combination with exogenous BA. Repressed growth of the shoots was observed for Pinus radiata (Tampe et al. 2001), Curcuma longa (Cousins and Adelberg 2008) and Withania somnifera (Sivanandhan et al. 2013). No shoot production was observed for Lavandula angustifolia treated with 4.78 μM JA (Miclea et al. 2020). Addition of JA even in concentrations lower than 1 μM into MS medium with BA reduced multiple formation and elongation of Pistacia lentiscus shoots (Koç et al. 2014). JA in concentrations up to 0.05 μM increased dry weight of shoots, leaves and roots developed from single nodes explants and number of leaves of Brassica oleracea cultivated in MS medium. In higher concentrations (1.25–6. μM) JA inhibited explant growth (Toro et al. 2003). MeJA in concentrations 0.1–1.0 μM also increased explant fresh weight but in higher concentration decreased number of developed shoots in N. tabacum cultured on MS medium supplemented with BA and IAA. Histological analyzes indicated that loss of the thin layer tobacco explants ability to regenerate in response to MeJA treatment was due to a strong hypertrophy of the cells and disappearance of meristemoids (Biondi et al. 2001) and reduced shoot primordial development (Capitani et al. 2005).
For various species JA stimulated shoot proliferation rate and growth when it was added into a medium in concentrations up to 10 μM (Table 1). JA supplementation of a medium containing N6-(2-Isopentenyl)adenine (2-iP) increased shoot multiplication and development in Allium sativum (0.1–10 μM JA) and Narcissus triandrus (4.8 μM JA) (Ravnikar et al. 1993; Santos and Salema 2000). Combined with Kin, 10 μM JA increased shoot number of Dioscorea cayenensis—D. rotundata (Ovono et al. 2007). In Pyrus communis and P. cerasus × P. canescens shoots addition of 1–10 μM JA into MS medium supplemented with BA and IBA or NAA increased leaf growth, fresh and dry weight of shoots (Ružić et al. 2013). MeJA (0.3–3.2 μM) also improved shoot multiplication and favored leaf development of Pistacia vera propagated onto MSPV medium containing BA and IBA, although 10 μM MeJA led to the leaf senescence and decreased shoot proliferation (Dolcet-Sanjuan and Claveria 1995). On the other hand in Musa acuminata increasing concentration of MeJA up to 100 µM also stimulated proliferation rate of shoots in presence of BA (Mahmood et al. 2012). Similarly proliferation rate of Taraxacum pieninicum shoots on MS medium supplemented with BA and NAA was stimulated by JA in higher concentrations (24–96 μM). However, it was reported that increasing concentration of JA limited the growth of the obtained shoots (Kamińska et al. 2018). The opposite effect was obtained for Ziziphora persica multiplied shoots on MS medium supplemented with the same PGRs, where MeJA decreased shoot proliferation rate but stimulated its elongation (Zare-Hassani et al. 2019). Increased height and dry weight of the seedlings probably by a rapid and significant increase of cytokinins level was observed also for T. aestivum and Artemisia annua treated with only MeJA in low concentrations (0.01–1 µM and 2–5 µM, respectively) (Avalbaev et al. 2016; Alam and Albalawi 2020), but high MeJA concentrations (10 and 100 µM) inhibited wheat seedlings growth (Avalbaev et al. 2016). Reduced growth of the shoots in response to JA or MeJA alone in MS medium was also reported in S. tuberosum (Ravnikar et al. 1992), O. sativa (Cho et al. 2007), Centella asiatica and Galphimia glauca (Mangas et al. 2006). In A. thaliana inhibited leaf growth as a result of treatment with 50 µM MeJA was manifested by both cell number and cell size reduction (Noir et al. 2013). Furthermore, it was indicated that exogenous MeJA suppresses hypocotyl elongation in a SCF COI1-dependent pathway in Arabidopsis under various light conditions, particularly effectively under red light (Chen et al. 2013). Signal cross-talk between JA and the red-light receptor phytochrome B (phyB) is thought to intermediate growth stimulation in neighboring plants competing for light. However, in further research it was shown that growth restriction at high level of endogenous JA was independent of phyB but involved dysregulation of Trp biosynthesis (Major et al. 2020).
Rooting of the plantlets
The most important PGRs during rooting process of in vitro derived shoots are auxins, especially indole-3-butyric acid (IBA) and indole-3-acetic acid (IAA) (Goel et al. 2018). Increased accumulation of endogenous JA might be stimulated during adventitious root (AR) formation by conversion of the IBA to IAA in NO-mediated upregulation of JA biosynthetic genes (Fattorini et al. 2017). It was suggested that MeJA acts during dedifferentiation phase by increasing sensitivity to auxin of the founder cells which divide and the descendent cells become increasingly determined to root formation under the auxin signal (De Klerk 2002). However, it was documented that JA and auxins antagonize root growth through interaction between JAZ protein and transcription factor MYC2 (Yang et al. 2019; Fig. 1). Furthermore, MeJA induced root growth inhibition through the reduction of Arabidopsis root cell length with involvement of COI1 in this process (Adams and Turner 2010). These results suggest that JAs modulates root formation via whole JAs pathway COI1-JAZs-MYC2 (Chini et al. 2009), but it was also reported that JA inhibits auxin-induced lateral root (LR) formation independently of the COI1 receptor (Ishimaru et al. 2018). Inhibition of AR initiation induced by JAs involve cytokinin-dependent pathway in A. thaliana (Lakehal et al. 2020). In turn auxin increases JA conjugation efficiency lowering free JA level. This auxin-JA interaction supports the hypothesis that JA signaling pathway negatively regulates AR in Arabidopsis hypocotyls (Gutierrez et al. 2012). Other studies indicated that JAs inhibits primary root (PR) elongation but promotes LR formation (Lakehal and Bellini 2018) and it was reported that IAA biosynthesis is required for MeJA to promote LR formation (Sun et al. 2009; Cai et al. 2014). Furthermore, it was shown that JA affect PR and LR growth by an auxin-independent pathway. The inhibiting effect of JA on a root system was found to be caused by a reduced cortex cell length and the low rate of the root-meristem cell formation in Helianthus annuus seedlings (Monzón et al. 2012). It was also suggested that the effect of JAs on the root growth may result from the reorganization of the root meristem, decreased cell division, inhibited cell elongation and premature cell maturation (Xue and Zhang 2007; Tung et al. 1996).
As for all micropropagation steps concentration of PGR does matter, but for some species, e.g. O. sativa, JA regardless of its concentration reduced root growth (Cho et al. 2007). In Medicago truncatula in turn only 0.1–10 μM JA inhibited nodulation and suppressed roots elongation growth (Sun et al. 2006). Similarly MeJA (5–16 µM) decreased root biomass in Curcuma longa plantlets (Cousins and Adelberg 2008). However, suppressed rooting process was mainly associated with the high concentrations of JAs (Table 1). Addition of 100 µM MeJA into MS medium reduced roots growth of C. asiatica, Ruscus aculeatus and G. glauca (Mangas et al. 2006). Furthermore, MeJA (50–100 µM) inhibited hairy roots growth of C. asiatica (Nguyen et al. 2019b). Supplementation of WPM medium with MeJA in concentrations of 50–200 µM led to decreased roots and shoots development and growth on nodal explants of Stevia rebaudiana (Moharramnejad et al. 2019). In turn in Z. persica 100 µM MeJA decreased number of roots, although at higher concentration (150 µM) stimulated root elongation (Zare-Hassani et al. 2019). Stimulation of root formation by JAs was also noted for low concentrations (up to 1.0 μM) in S. tuberosum, B. oleracea and Lycopersicum esculentum (Ravnikar et al. 1992; Tung et al. 1996; Toro et al. 2003; Zhang et al. 2006; Table 1). In Cymbidium kanran 1 μM JA increased number of rhizome branches (Shimasaki et al. 2003). Even in lower concentrations (4.76 × 10−5 to 4.76 × 10−3 μM) JA induced minirhizomes formation in shoot clusters of Rheum rhabarbarum (Rayirath et al. 2011). JA also stimulated root primordium and subsequent root formation with lateral branches in V. mungo hypocotyls placed onto MS medium (Lingakumar et al. 2014). Addition of 10.65 µM MeJA into MS medium supplemented with Gamborg’s B5 vitamins, BA and NAA increased number of regenerated roots in Cymbopogon schoenanthus seedlings but showed negative effect on a shoot production (Abdelsalam et al. 2018).
It was indicated that JA derived by the demethylation of MeJA, applied at 0.01 μM in combination with IBA and Kin enhanced AR in N. tabacum and A. thaliana seedlings and thin cell layers (TCLs) under dark conditions. The endogenous IAA levels increased in the TCLs at the time of the first AR-cell cluster formation under MeJA treatment. Furthermore, it was shown that also xylogenesis in Arabidopsis TCLs is under the JAs control. Role of JAs in these processes was related to crosstalk between JA- and ET-signalling (Fattorini et al. 2009, 2018). It was proposed that JA at high concentrations promote xylogenesis rather than AR formation, and mentioned cross-talk between JA and ET may decide which of these competing processes will occur (Druege et al. 2019). These results were confirmed by Betti et al. (2019) who showed that during AR formation in Arabidopsis stem explants cultured with IBA the antagonism between JA and ET is based on an involvement of the EIN2 (Ethylene Insensitive2) and COI1 cross-talk. It was also assumed that JAs cooperate with cytokinins to repress initiation of AR formation in Arabidopsis under constant red light conditions thus JAs effect on AR formation might also depend on light conditions during culture (Lakehal et al. 2020; Fig. 3).
Somatic embryogenesis
Somatic embryogenesis (SE) is the developmental process in which a competent cell or a cell group undergoes biochemical and molecular changes resulting in the formation of a somatic embryo (Yang and Zhang 2010). Somatic embryos are bipolar structures with an apical pole (the future shoot) and a basal pole (the future root), both with its own meristem (Horstman et al. 2017). This regeneration system is preferred over organogenesis due to a low frequency of chimeras, a high number of regenerants and a limited level of somatic variation (Gaj 2001; Carra et al. 2019). One of the determining factors during induction of SE is IAA metabolism in the cells. Acquisition the embryogenic potential by pro-embryogenic mass is dependent on auxin homeostasis at a specific level (Nic-Can and Loyola-Vargas 2016). In Arabidopsis SE is a two-step process. In the first step early cotyledonary zygotic embryos are placed on medium supplemented with auxins to stimulate formation of the embryogenic tissue. In the next step formation of the somatic embryos is stimulated by the removal of auxins from the medium. JA is a key component of embryogenesis regulation in the pathway including phytoglobin 2 (PGB2), NO and several JA-responsive intermediates (Bassuner et al. 2007; Mira et al. 2016). It was suggested that JAs inhibit embryo germination in angiosperm (Białecka and Kępczyński 2003), although high endogenous level of JA is essential for somatic embryo formation in M. sativa. A relatively high and stable JA content was reported in somatic embryos developed from globular through torpedo till early-cotyledonary stage (Ruduś et al. 2009). Exogenous MeJA not only inhibited callus growth of this species during differentiation stage, but also negatively affected the proliferation of embryogenic suspension and reduced somatic embryos production (Ruduś et al. 2001, 2006; Table 1; Fig. 3). Tokuji et al. (1995) showed that MeJA markedly delayed somatic embryo differentiation from cell clusters to torpedo stage and repressed their further regeneration in Daucus carota. Cells of Fagopyrum tataricum from suspension culture after MeJA treatment were almost completely unable to produce somatic embryos. Proposed explanation was based on possible suppression of the cell cycle genes expression and cells arrest of entry into mitosis. On the other hand it cannot be excluded that exogenous MeJA induced perturbations in the level of endogenous hormones which after cells transfer onto hormone-free medium prevent activation of the embryogenesis process (Gumerova et al. 2015). In contrast to these results, Reinbothe et al. (1994) indicated that MeJA induces embryogenesis-related proteins and mRNA in Nicotiana plumbaginifolia. Improved microspore embryogenesis was obtained for Brassica napus treated with 4.8 μM JA for 24 h. At higher level (9.5 and 23.8 μM) JA improved embryogenesis and callogenesis only after 6 h incubation. Longer incubation decreased microspore embryogenesis and microspore-derived embryos germination (Ahmadi et al. 2014). Blázquez et al. (2004) indicated that JA also in low concentration (2.4 μM) significantly improved SE and plant regeneration in Crocus sativus. Equivalent to somatic embryos in orchids, protocorm-like bodies (PLBs) formation was improved as a result of a MeJA treatment, although PLBs formation decreased as MeJA level increased (Teixeira da Silva 2012). Similar results were obtained in shoots culture of Cymbidium eburneum where addition of MeJA into MS medium stimulated PLBs formation with simultaneous decreased shoot formation (Shimasaki et al. 2003).
Microtuber and bulblet formation
For some species culture through bulblets or microtubers has become a more effective method of propagation due to the genetic purity (Wang and Hu 1982; Sultana et al. 2010). Formation of this both storage organs under in vitro conditions might be affected by several factors such as sucrose levels, photoperiods and PGRs and is controlled by biochemical and genetic factors (Gheisari and Miri 2017; Islam et al. 2017).
Several phytohormones are associated with the processes associated with the tuberization. Especially significant role was assigned to GA3 which regulates the change in cell growth orientation from longitudinal to radial swelling of the stolon tip what is characteristic step during tuber formation (Hannapel et al. 2017). JAs also induce changes of the cell division marked by cortical microtubules reorientation and radial expansion direction during initiation of storage organs formation (Shibaoka 1991; Matsuki et al. 1992; Podwyszyńska et al. 2015). JAs involvement in this process was repeatedly confirmed not only in tuber formation from stolon apex in plants from soil cultivation (Koda 1997; Cenzano et al. 2003) but also during further cell expansion of medullary tissue in S. tuberosum microtuber discs cultured in vitro (Takahashi et al. 1994; Table 2). Pruski et al. (2002) pointed out that JA induction of tuberization and microtuber bulking on S. tuberosum nodal cuttings was most pronounced under tuberization-inhibiting 16 h photoperiod. As can be seen different studies indicated that JA and its derivatives stimulated microtuber formation (Hamberg and Gardner 1992; Fig. 3) not only in potato, but also in D. rotundata (Jasik and Mantell 2000), D. cayenensis (Ovono et al. 2007) and Pterostylis sanguinea (Debeljak et al. 2002), although a number of studies indicated that JA was not directly involved in process of tuberization in Solanum spp. (Helder et al. 1993; Jackson and Willmitzer 1994; Jackson 1999). This process is also controlled by light, temperature and GA (Lin et al. 2013). It suggests that tuberization is indirectly controlled by JAs through crosstalk with GA signaling (Koda 1997; Wasternack and Hause 2013; Siddiqi and Husen 2019). However, increased accumulation of JA in pretuberous roots of Manihot esculenta planted in the field inhibited tuberous root formation. Those inconsistencies might be due to the differences between potato (i.e., stem tuber) and cassava (i.e., root tuber) and contrasting JAs impact on the cell processes in tissues that differ e.g. in sensitivity to this phytohormone and endogenous level of other PGRs (Utsumi et al. 2020), e.g. cytokinins which were reported to antagonize the JAs effect on S. tuberosum microtuber growth after induction. Furthermore JAs effect on microtuber formation is also maturity-specific. The late maturing cultivar may have lower response to JAs (Sarkar et al. 2006).
Commercially grown cultivars are also propagated by other vegetative tissue, such as bulbs. Conventionally bulbs are produced from scales since a long period of time. Micropropagation is similar to the scaling, although under in vitro conditions small scale-explants are used and excised scales from the new bulblets can be used as initial material thus propagation cycles can be performed few times per year (Askari et al. 2018). It was shown that increased JAs level occurs also in bulb forming plants suggesting that this phytohormone is involved in the formation of storage organs other than tubers. JAs plays role in the formation and enlargement of bulblets on N. triandus (Santos and Salema 2000), A. sativum (Bekheet 2006), Allium victorialis (Park et al. 2004) shoot explants placed on MS medium, and A. sativum basal plates transferred onto B5 medium (Ravnikar et al. 1993) (Table 2; Fig. 3). For A. sativum and Narcissus papyraceus it was also noted that JA and MeJA, respectively, stimulated bulblet formation and increased number and weight of bulblets in combination with NAA (Kim et al. 2003; Hosseini et al. 2013), although in N. papyraceus MeJA showed an inhibitory effect on a size of bulblets (Hosseini et al. 2013). Interestingly JA combined with cytokinin 2-iP stimulated bulblets production and its growth in Hyacinthus orientalis (Doğan et al. 2020), although Saniewski and Puchalski (1987) reported that 0.5% MeJA inhibited benzyladenine-induced bulblet formation in Muscari armeniacum and in lower concentration (0.1% and 0.2%) MeJA delayed development and growth of the bulblets. MeJA decreased bulblet number also in Tulipa gesneriana, although in one of the four studied cultivars (P14) MeJA combined with 500 μM Arg increased number of bulblets, their size and weight (Podwyszyńska et al. 2015).
Development of gametophyte and sporophyte
JA may be involved in alternation of generations in ferns by activating the ontogenesis phases. The JA effect on the growth of gametophyte is age-dependent. JA at 0.1–1.0 μM promoted early Platycerium bifurcatum gametophyte development and its transition from a filamentous to a spatulate growth. In turn, after 40 days of culture JA inhibited growth of the gametophyte of this species. Authors proposed that maturation of the gametophytes leads to differences in response to JA (Camloh et al. 1996, 2001). In protoplast culture of a sporophyte 0.01 μM JA stimulated initial divisions of the cells (Camloh et al. 1996). JA, especially in concentration of 10 μM, promoted rhizoids and adventitious shoots development on leaves of this species. Stimulatory effect on rhizoid development was observed even in the presence of 100 μM JA (Camloh et al. 1999). Exogenous JA activated growth of the gametophyte and the further sporophytes development on the thallus surface of Anemia tomentosa. It was also observed that JA was able to remain in the gametophyte stage even when sporophytes were already developed (Castilho et al. 2018). However, in horsetail Equisetum arvense JA inhibited growth of gametophytic and sporophytic tissues and also suppressed initiation of sporophytic shoots in vitro (Kuriyama et al. 1993).
JAs as a stimulator of secondary metabolism
JAs have been widely used as elicitors to induce secondary metabolite production in a variety of plant in vitro cultures. Increased secondary metabolites accumulation was often associated with decreased explants growth. Treatment of Calendula officinalis hairy roots with JA led to slightly decreased growth of the explants, but stimulated secretion of oleanolic acid glycosides into the medium (Alsoufi et al. 2019). Similar correlation was reported for C. asiatica. MeJA inhibited shoot, callus and cell suspension culture growth with simultaneous stimulation of asiaticoside (in shoot and callus culture) and asiatic acid (callus culture) biosynthesis (Krishnan et al. 2019). However treatment of adventitious roots of Ajuga bracteosa with NAA and MeJA led to increased maximum dry biomass formation and enhanced total phenolic content (Saeed et al. 2017). Similar results were obtained for Castilleja tenuiflora thirty-day-old in vitro plants elicited by foliar spraying with MeJA (Rubio-Rodríguez et al. 2021). Effect of jasmonates, as for all growth regulators, strictly depends on the used concentration. Treatment of Vitis vinifera with MeJA showed that 100 μM and 50 μM concentrations enhanced and lowered hairy roots biomass and secretion of resveratrol into the culture medium, respectively (Hoseinpanahi et al. 2020). The wider examples of the JAs usage for elicitation under in vitro conditions can be found in other reviews (Giri and Zaheer 2016; Singh and Dwivedi 2018; Ho et al. 2020).
JAs under stress conditions
A few studies are available on the effect of JAs on in vitro cultivated plant tissue subjected to stress conditions. Significantly more observations and conclusions were made and reached in pots and fields experiments with foliar application of JAs, e.g. under salinity stress (Manan et al. 2016; Taheri et al. 2020), drought stress (Sadeghipour 2018; Tayyab et al. 2020), heavy metal stress (Ahmad et al. 2017; Ali et al. 2018), heat stress (Lee et al. 2019), cold stress (Connolly and Orrock 2018; Ghanbari et al. 2018) and under biotic stress (Burdziej et al. 2021). Under in vitro conditions JAs were studied under drought, salt and cold stress conditions (Table 3). To simulate drought stress in plants mostly a high molecular weight polyethylene glycol (PEG) has been used as a non-penetrating osmotic agent which lowers the water potential of the medium (Bressan et al. 1981). Improved explants growth under water stress in response to MeJA and JA was reported for M. acuminata and Fragaria × ananassa (Mahmood et al. 2012; Yosefi et al. 2020). Protective role of JAs might be correlated with a mitigation of oxidative stress by increased activity of POD and SOD enzymes (Yosefi et al. 2020), although contradictory effects of JAs in significantly higher concentration (200 µM) were obtained for Verbascum nudicuale seedlings (Ghasemlou et al. 2019). Induced activity of antioxidant enzymes was also observed in T. aestivum under water stress in presence of a low MeJA concentrations (0.25–2.5 µM) with simultaneous increase in the level of H2O2 (Ma et al. 2015), which suggests that JAs might also play role during induction of the oxidative stress. JAs also decreased proline accumulation in B. napus and Saccharum species under water stress. Increased proline level might indicate high stress level or high stress responsivity (Huguet-Robert et al. 2003; Nieves et al. 2001). Bandurska et al. (2003) indicated that exogenous JA increased endogenous level of ABA in Hordeum vulgare and H. spontaneum plantlets. ABA is the principal mediator in physiological outcome of drought avoidance, tolerance and resistance. JA and ABA seem to share common targets in a signaling pathway related to drought (de Ollas and Dodd 2016). The linkage of these two phytohormones was also indicated in a cold stress (Wang et al. 2016). In Malus × domestica cultivated in 8 °C MeJA improved callus growth and increased expression level of the genes involved in cold-signal response (Wang et al. 2019). Encapsulated shoot tips of Taraxacum pieninicum in a calcium alginate matrix showed growth inhibition during cold-storage in the presence of JA, although JA limited proline accumulation and oxidative stress by decreased lipid peroxidation (Kamińska et al. 2018). Application of JAs improved explants condition also under salinity stress, e.g. JAs stimulated growth of the G. max and S. tuberosum explants (Yoon et al. 2009; Efimova et al. 2019) and development of S. melongena embryos (Manar et al. 2013) treated with 60–100 mM NaCl (Table 3). At molecular level it was reported that JA-inducible salt stress related genes were not activated in presence of ABA in O. sativa roots, although some evidence of a crosstalk between these phytohormones for regulating salt stress was proposed (Ryu and Cho 2015).
Conclusions
Jasmonates can differentially affect explants growth under optimal and stress conditions. More detailed works are needed to determine what mechanisms decide about physiological effect of JAs. JA is best studied as an elicitor and undoubtedly plays an important role in a secondary metabolite biosynthesis. The detailed role of JAs in a whole plant or explants growth is still unknown. JAs are often described as a growth retardant during defense related to biotic stresses, however they have also stimulatory effect on explants growth, especially microtubers and bulblets. The crosstalks between JAs and other phytohormone (mainly cytokinins, auxins and gibberellins) seems to be crucial for shoot proliferation, rooting and embryogenesis efficiency of different species. Particularly interaction linking JAs responses with gibberellins signaling pathway is a key factor determining explant growth and tuberization process. Knowledge about the mechanism of JA action in explants will provide useful information, especially important for species with problematic propagation and microprapagation system.
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Kamińska, M. Role and activity of jasmonates in plants under in vitro conditions. Plant Cell Tiss Organ Cult 146, 425–447 (2021). https://doi.org/10.1007/s11240-021-02091-6
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DOI: https://doi.org/10.1007/s11240-021-02091-6