Pol. J. Environ. Stud. Vol. 29, No. 2 (2020), 1009-1020 DOI: 10.15244/pjoes/108687 ONLINE PUBLICATION DATE: 2019-10-24

Review The Role of New Members of Phytohormones in Plant Amelioration under Abiotic Stress with an Emphasis on Heavy Metals

Abolghassem Emamverdian1, 3, Yulong Ding1, 3*, Yinfeng Xie1, 2

1Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China 2College of Biology and the Environment, Nanjing Forestry University, Nanjing, China 3Bamboo Research Institute, Nanjing Forestry University, Nanjing, China

Received: 27 February 2019 Accepted: 22 April 2019

Abstract

In addition to regulating plant growth and development, phytohormones play an essential role in the response to abiotic and – especially heavy metal stress. In response to environmental stressors, phytohormones act as signaling molecules in both exogenous and endogenous signaling pathways. In parts of the rhizosphere, phytohormones have an exogenous role, and when regulating plant growth and development, they have an endogenous role. Phytohormones and their associated signaling pathway network are involved in plant responses to heavy metal stress. These molecules can improve the plant defense system by increasing antioxidant enzyme activity and degrading lipoperoxidation and

H2O2. Phytohormones are divided into classical phytohormones such as , , , and , that have been investigated for many years and the new members, such as , , and , which have been little studied. In this review article, we investigated the main mechanisms involved in the amelioration of heavy metals by the three new phytohormones to provide more knowledge about their detoxification mechanisms.

Keywords: abiotic stress, heavy metals, jasmonates, brassinosteroids, strigolactones

Introduction stress [1, 5]. Phytohormones are the vital components of complicated signaling networks in the current Phytohormones, as a signaling molecule, regulate stress response models, which include endogenous plant growth, as well as influence the (SA), ethylene (Et), (ABA) [6], and the metabolism and physiological processes of a plant [1]. new members (JA), brassinosteroids Plants have adapted to biotic and abiotic stresses with (BRs), and strigolactones (SLs) [7]. Phytohormones are the mediating role of phytohormone in the regulation known as a regulator of plant growth and development of stress [2-4]. Phytohormones alter their levels upon and play an important role in response to abiotic and the encounter with abiotic stress, such as heavy metal biotic stresses [8]. They are a small molecule with low concentration, but play an important role as a chemical messenger in the regulation of cells in plants *e-mail: [email protected] [9]. There are two categories of phytohormones, which 1010 Emamverdian A., et al. are classical phytohormones such as auxins, ethylene, D14/DAD2 receptor and F-box protein (MAX2/D3) [25, gibberellins, and cytokinins, and the new members such 26]. The complex of SCF reducing the repressor with as jasmonates, brassinosteroids, and strigolactones [7], proteasome-mediation can be the main mechanism of which are discussed in this article. Strigolactones (SLs) phytohormones in the adjustment of gene expression are a member of the new phytohormone group, which [27]. Below are the mechanisms of new phytohormones are involved in important plant processes including and signaling pathway networks for scavenging of ROS seed germination, as well as the development of roots and metal stress. and plant architecture, which are exudates from roots [10]. Brassinosteroids are another new phytohormone Jasmonates (JAs) Via Heavy Metal Stress member, which are reported to be involved in many cell cycle processes, cellular expansion and plant Jasmonates (JAs) represent a new class of differentiation [11]. Jasmonic acid is also a small phytohormones. Jasmonates belong to cyclopentanone molecule that belongs to the new phytohormone compounds, and in the octadecanoic pathway they group that plays an important role in plant growth and are synthesized by linolenic acid. Jasmonates have development and the reduction of stress [12]. In this two recognized forms: methyl (MeJA) and review, we investigate the identification of these new jasmonic acid (JA) [28]. As a signaling molecule, Phytohormones and the mechanisms involved in the MeJA is a part of cyclopentanone compounds that play reduction of heavy metal stress by their applications. an important role in stress conditions by acting as a signal transduction pathway [29]. In the JA signaling network, MeJA and JA are bioactive small molecules Mechanisms Involved that are indicated by the isoleucine conjugated jasmonyl in New Phytohormones derivative [30]. MeJA is responsible for gene expression that leads to increased plant cell resistance in stress When plants encounter oxidative stress, plant conditions. Hanaka et al. [31] conducted research on resistance is increased by the stimulation of antioxidant the enhancement of endogenous levels of MeJA in activities. If the antioxidants are inadequate to cope response to different stressors, especially heavy metal with the stresses, plants increase their resistance by stress [30, 31]. mediates the regulation the enhancement of various signaling molecules via of metabolism and is involved in gene expression in exogenous treatment [13, 14]. Alternatively, plants responses to stress, cell communication, activation can also alter endogenous levels of phytohormones of plant defense mechanisms, and plant growth and in response to stressful conditions [15]. It has been development [32]. These molecules can increase the reported that phytohormones, including ABA, JAs, Et production of biomass and reduced malondialdehyde and salicylic acid, are involved in the signaling pathways content and fluorescence in leaf chlorophyll following that can play an important role in crosstalk of the stress- the exposure of plants to heavy metals; they can also signaling pathways [16]. Additionally, phytohormones reduce oxidative stress induced by reactive are involved in signaling pathways, which shows species (ROS) by degrading ROS derivatives such as OH that JAs play an essential role in the activation of the and H2O2 in leaves, and control transcriptional pathways pathway that is involved in signal transduction [17]. through oxidative stress [33]. There are two hypotheses

In phytohormones, signaling pathways have a vital regarding how JA can reduce H2O2 and MDA. The first role in the reduction of purposeful proteins through one is related to antioxidant activity; with increasing the ubiquitin-proteasome [18]. The phytohormones are antioxidant activity, JA leads to scavenging of ROS also known to interact with each other to ameliorate derivatives and reduces H2O2 production in cells. These the stress conditions [19]. Crosstalk between ABA and changes lead to degradation of H2O2 and MDA in cells. SLs is involved in the regulation of stress signaling, The second hypothesis is related to another endogenous which improves stomatal efficiency [20]. The SKP1- phytohormone. JA can induce other phytohormones CULLIN-F-BOX complex (SCF) is a major element for scavenging of ROS generated by oxidative stress in the signaling pathway of phytohormones [21]. Also, in plants [34]. Many studies have shown that applying the development of the root and shoot result from the jasmones (JA) can ameliorate complete (Chl) content crosstalk between IAA and SLs [22, 23]. Additionally, under heavy metal stress, which has been reported every phytohormone and its signals have an F-box in many plants, including soybean [35], capsicum protein component that belongs to the SCF, and its frutescens and Kandelia obovata [28]. Therefore, JA binding with the target protein results in its degradation can preserve a pigment system in photosynthesis and [24]. The mechanisms reported for the binding of SLs with increasing Chl content can enhance chlorophyll with target F-box proteins include binding via Skp1 [21]. biosynthesis and ultimately prevent the damaging Data obtained from genetic analyses of SL-insensitive impact of ROS on cell membrane structures such as mutants in A. thaliana and rice revealed three pathways [36]. Jasmonates (JAs) play an essential that are involved in SL signal transduction, which role in stress-signaling networks in plants under include a repressor and receptor that belong to the abiotic and biotic stresses [12] by acting as a signaling SCF complex, namely the D53/SMXL6 repressor to 8, molecule involved in the rising resistance to stress The Role of New Members of Phytohormones... 1011 via the activation of related genes [37]. The protective metal stress in intercellular parts of the plant, but role of JA against the stress of heavy metals involves scientists have reported that increased accumulation of stimulation of antioxidant enzymes, reduction of H2O2 endogenous JA in intercellular plant organs can be a and malondialdehyde (MDA) (protection of the cell strong reason for the amelioration of heavy metals in the membrane lipids), and providing a protective role for intercellular parts of plants, which are directly increased photosynthetic pigments (reducing oxidative damage) by the effect of exogenous MeJA in plants [28-45]. In [38]. This protective role is indicated by the effect of rice seedlings, exposure to Cu [46] and exposure of pea 0.1 µmol L−1 JA on Wolffia arrhiza under Pb stress [39] plants to Cd [47], as well as exposure of P. coccineus and and by the effect of 10 µmol L−1 MeJA on soybeans A. thaliana to Cd and Cu [48], resulted in a structural under Cd stress [40]. The results obtained for the effect alteration of JA that was dynamic and transient under of 0.1 µmol L−1 JA on Wolffia arrhiza under Pb stress abiotic stresses [48]. The role of jasmonate signaling show that JA protects the plant by increasing the level of on the stimulation of OsDOX gene expression in the primary metabolites, which help to restore plant growth, stress condition has been previously studied, with the prevent Pb accumulation in the plant, and activate plant results showing that exogenous MeJA leads to OsDOX defense mechanisms (enzymatic and nonenzymatic expression in the rice shoot, which evoked enhanced activities), including POD, CAT, NADH peroxidase, reactive oxygen species (ROS) [46]. The Jasmonates glutathione, and ascorbate [39]. JA can also reduce signaling pathway that induces ᾁ -dioxygenases (DOXs) translocation of heavy metals from the root to the shoot, (OsDOX gene expression) is a regulation mechanism which prevents the accumulation of heavy metals in in response to oxidative stress caused by heavy metals plants. This reduced translocation was confirmed by the [46]. A previous study showed that MeJA significantly effect of the Cd on K. obovata [28] and by the effect impacts the toxicity of Cu and Cd in Arabidopsis plants, of Pb on W. arrhiza [28, 39]; however, it occurs at a which depends on the jasmonic acid concentration and low concentration of JA (JA at 0.1 µmol L−1), which its focus on a specific point (external or internal) [45]. indicates the role of JA concentration in the amelioration Additionally, studies have shown that gene expression in of heavy metals [39]. A previous study showed that Cd2+ plant mechanisms, including phytochelatins (PCs) and MeJA with a low concentration of JA maintained plant metallothioneins (MTs), can raise plant resistance under membrane degradation and helped rice seedlings under heavy metal stress such that plant MT genes, such as the stress [41]. Methyl jasmonate also regulates stimulation KoMT2 gene, play an essential role in the degradation of stomatal closure, leading to an effective role in plant of oxidative stress and heavy metal detoxification via transpiration [28, 42], which can reduce metal uptake the influence on Cd accumulation in K. obovata leaves in the shoot and xylem sap [43], hence reducing the [28]. This has been reported in various plants exposed to loading of heavy metals in the xylem and shoot [44]. heavy metals [49-50-51]. Evidence shows that exogenous Jasmonates can be elevated in response to heavy metal JA/MeJA can increase synthesis of PCs and MTs at the stress as a one-second messenger when the plant defense transcript level during the heavy metal stress condition mechanism is stimulated [37]. This process is related to [28]; however, the exact mechanisms remain unclear and the stimulation of antioxidant activity [35]. A previous hence require future research. study investigating the effect of the Cd on Capsicum frutescens var. fasciculatum seedlings showed that under Brassinosteroids (BRs) Via Heavy Metal Stress Cd, a low concentration of methyl jasmonate exposes the plant to increased antioxidant activity, such as SOD Brassinosteroids (BRs) as a member of phytosteroidal and CAT, in the leaf, decreases MDA concentrations hormones [11] are known as a new application of and lipoperoxidation [35]. Additionally, APX in rice [17] plant hormones that belong to the polyhydroxy and increased GR in rice seedlings indicate that MeJA steroidal group [52-53]. Among the 70 BRs that exist is a protective tool to cope with the damaging effects of in plants, three types, including 24-epibrassinolide, oxidative stress [41]. In other studies, exogenous methyl 28-homobrassinolide and brassinolide, have been jasmonate (MeJA) increased the activity of antioxidant underinvestigated in regard to their role in the plant enzymes (APX and CAT), and reduced MDA and growth and development process because they have lipoperoxidation in Kandelia obovate. It was also been identified as top bioactive brassinosteroids [52-54]. reported that MeJA prevents Cd accumulation in leaves, BRs play an important role in many growth processes which occurs because of the influence on stomatal in plants, including the growth of fruit, flowers, pollen, closure and reduction of transpiration by exogenous seeds and fiber, as well as rhizogenesis, abscission, and methyl jasmonate (MeJA). And it can show other aspects senescence. They also play a role in the regulation of of the jasmonate mechanism in the face of heavy metal cellular expansion and plant differentiation, which stress [28]. In particular, it was reported by Keramat et are conducted by several genes involved in stimulated al. (2009) that the effect of 10 to 100 µmol L−1 JA on the plant signaling [11]. Further, BRs are involved in many soybean plant (Glycine max L.) increased antioxidant important cell cycle process such as cell division, cell activity, such as SOD, APX, and CAT, under Cd stress elongation, senescence and vascular differentiation; [40]. There is not an exact explanation for how exogenous as such, they are very important for plant growth [55]. MeJA acts on antioxidant mechanisms to remove heavy Additionally, it is indicated that BRs provide protective 1012 Emamverdian A., et al. activity for plants under environmental stress [52]. BRs vacuoles or the chelation of metal in the cytosol [52]. are involved in the regulation of expression of more than Bioabsorption of metals is another mechanism that can a hundred genes and influence many metabolic pathways degrade heavy metals. It occurs by metals-linking in that are involved in plant responses to environmental deference mechanisms including chemical and physical stress [56]. Additionally, BRs have the ability to stimulate adsorption, as well as complexation and ion exchange, antioxidant activity in stress conditions such as heavy which involve a process where metals interact with metal, drought, and salinity [57]. Brassinosteroids (BRs) hydroxyl, carboxyl, phosphoryl and amino groups. can increase plant resistance with some plant defense Further, the pH of the solution plays an important role mechanism, such as the reduction of lipoperoxidation, in removing the metals, with an optimum pH between stimulation of antioxidant activity and improvement of 4-6 [69]. Brassinosteroids can reduce pH in the cell wall phytochelatin synthesis [52]. Additionally, the efficiency and help plant growth, which has been reported in C. of photosynthesis is improved with the mechanisms vulgaris [68]. Additionally, BRs can influence water involved in the photochemical pathways involving BRs. deficits. A previous study reported that excess Cd alters These mechanisms include amelioration of electron the biological function of the membrane in cell wall so transport efficiency, improved damage of reaction that it has reduced capacity to maintain its water stage, centers and complexes of O2 evolution, which have been leading to a water deficit in the plant [70]. However, reported for winter rape under Cd stress [58]. Many BRs were found to improve the leaf water potential and studies have reported that BRs can decrease heavy ameliorated water deficits in the plant [70]. It has also metal stress in plants [52-59-60]. In plants exposed to been reported that BRs improve the levels of pigments/ heavy metals, BRs as a regulator play an essential role carotenoids (reduction of β-carotene and lycopene) in in the morphogenetic and physiological responses that ripening fruits exposed to Cd heavy metals, which can reduce biotic and abiotic stresses [61]. BRs can also indicates a positive role of BRs in the photosynthesis reduce the accumulation and uptake of heavy metals, process [70]. which was shown in a study on Brassica juncea seeds exposed to Cu, where the results indicated that BRs Strigolactones (SLs) Via Heavy Metal Stress improved shoot and biomass production and decreased the accumulation and uptake of copper in plants [62]. Strigolactones (SLs) are known as new plant The results of previous studies have indicated that BR hormones (Phytohormones) [71-72-73], and they play a has a strong impact on plant growth and biomass, which role in root architecture, rhizosphere structure and seed was specifically reported for mung beans exposed to germination in parasitic plants [2-74-75-76]. It has also aluminum stress [56-63]. BR also plays a vital role in been reported that SLs are involved in the senescence of the regulation of the elongation of shoots and roots, the leaf [77], reaction to nutrient stress [78-79], response as well as seed germination [64]. Exogenous BRs can to biotic stress [80], regulation of the development scavenge ROS compounds with mechanisms such of roots [81-82], and development and branching of as stimulation of antioxidants and accumulation of shoots; they also play a signaling role in the interaction

H2O2, which can improve plant resistance to oxidative between plants [73]. In this signaling role, SLs are stress caused by heavy metals [52]. BRs preserve the referred to as rhizosphere signaling molecules [83-84] regulation of the cellular redox state by adjusting and because in the rhizosphere, Strigolactones are involved stimulating antioxidant enzymes such as SOD, CAT, in detection signals in plant roots and fungi [85]. The DHAR, MDHAR GR and APOX, which maintain generation of strigolactones (SLs) usually occurs in the cell membrane and cell integrity by decreasing roots and some stem parts; however, they flow and are phospholipid peroxidation or the accumulation of secreted in the rhizosphere and are then involved in osmoprotectant [52]. It is not clear how BRs can protect biosynthesis throughout the plant, although this amount the cell, but BRs regulate protein and enzyme activity is minimal [86-87]. The pathways of CL biosynthesis in the membrane and interact with sterols and proteins occur in the plastid, and during the transferring process in the membrane [65]. Thus, the BR1 encoded protein (ring closures, oxidation, and functionalizations in complex (leucine-rich repeat receptor-like kinase) the membrane), it moves into the cytoplasm [88]. that is conducted through the signaling network by Recently, caprolactone (CL) has been identified as one related genes can regulate plant responses to stress of the intermediates in the biosynthesis of SLs and [66]. Therefore, BRs can regulate the expression of SL-like compounds [89-90-91]. There are more than various genes responsible for encoding plant defense 1000 SLs in nature; however, only 19 SLs have yet been mechanisms including phytochelatins (PCs), antioxidant identified [92-93]. Generally, SLs play a coordinating enzymes [60-67] and metallothioneins (MTs) [52]. role in the regulation of below- and above-ground plant BRs can facilitate and stimulate the syntheses of architecture, senescence of the leaf, root and shoot phytochelatins (PCs) in the plant cell in heavy metal formation, reproductive development and secondary stress conditions, which has been reported in plants growth in plants [94-95-96-97]. Strigolactones (SLs) exposed to Pb [68]. PCs are cysteine-rich compounds have been identified as a multifunctional molecule with the ability of metal binding, which plays an of new phytohormones that can play an important important role in the compartmentalization of metal in role in improving plant development when exposed The Role of New Members of Phytohormones... 1013 to stress and deficient conditions. Phytohormones of the ubiquitin-dependent repressor [74]. The SL are very important for phosphorus deficiencies and mutants, including the SL signaling mutant max2 and nutrient shortages [98]. Strigolactones (SLs) play an SL biosynthesis mutants max4 and max3, comprise the important role in plant mechanisms against water and link between SL and ABA phytohormones, which are nutrient deficiencies [99-100], and can be linked with more sensitive to drought stress conditions with the abiotic stresses such as nutrients and metals [78]. The regulation of the stomata [110-20]. Additionally, the mechanism of strigolactones in the encounter with root and shoot of branching strigolactones (SLs) play metals and nutrients are bilateral, which is related an essential role in cellular redox homeostasis. It has to the structure and architecture of the root system been shown that mutant formation (ore9) is involved [73]. A previous study on Pi (an inorganic form of in MAX2 and could prevent senescence and oxidative phosphorus) reported that strigolactones can regulate stress in comparison with wildtype [111]. GR24, a root systems by improving development of lateral synthesized , is known to be a defense root formation with a suitable concentration of Pi mechanism in stress conditions. Exogenous GR24 leads and conversely inhibit the emergence of lateral roots to increasing plant tolerance against salt and drought with a high concentration of Pi. Thus, reducing the stress in Arabidopsis [74-20]. When placed in the root uptake of heavy metals in the plant by decreasing the access, it is transferred to the shoots [19-112], creating length and density of root hairs is one of the avoidance a positive role in coping with stress [101]. A previous mechanism of strigolactones for coping with heavy experiment found that GR24 reduced MDA content and metals [95-101]. Recent research has confirmed the role chloroplast damage and increased the photosynthetic of strigolactones (SLs) on the LR (latest root) formation capacity and plant defense mechanism against ROS with process, which occurs in synthetic strigolactone stages the stimulation of antioxidant enzyme activity (SOD and [27]. In roots, SLs are responsible for altering actin POD) caused by salinity stresses [1]. Additionally, SLs dynamics, and the structure of the plasma membrane have the ability to regulate the development of shoot involved in the displacement of the transporter of PIN- branching in plants, which can be a positive mechanism FORMED [7], with rising degradation speed of to cope with the adverse effect of heavy metals on shoot PIN-FORMED1 (PIN 1) [22]. There are 15 types of branching. Additionally, SLs prevent shoot branching strigolactones that have been introduced and identified caused by heavy metal modulation, auxin transport and by researchers, which have been analyzed in a variety their biosynthesis processes by which the involved metal of studies [102]. The biosynthesis of strigolactones has levels can regulate shoot branching and increase plant been conducted in all parts of the plants [73], especially biomass. Further, SLs are involved in the regulation in the later parts of the stem and root [87], but usually of the development root and root hairs, which can a small amount is generated in the primary roots of ameliorate the negative effect of nutrients and heavy all varieties of plants, including single plant species metals, including calcium (Ca), N, Iron (Fe), sulfur (S), and primitive plants (Charales and Embryophyta) Pi, and aluminum (Al), on root development process [73], which is transferred to the apex shoot vertically such as primary root elongation, lateral root initiation, (to acropetally) [103]. It has also been reported that and root-hair formation [113]. Low concentrations of symbiotic arbuscular mycorrhizal fungi (AM) and some metals, including N and Pi, leads to increased SLs root-parasitic plants are classic sites for strigolactones in plant roots; thus, it has been reported that SLs can (SLs) as rhizospheric hosts [104]. Carotenoid synthesis enhance root-hair length and root-hair elongation and is the only pathway that is known to be involved in consequently improve nutrient absorption in plants [114]. strigolactones biosynthesis. It is controlled with three Strigolactones (SLs) are known as signaling plastid-localized proteins [105] that begin with changes molecules that are involved in the response to of all-trans-β-carotene into carlactone (CL). Previous environment stress [23]. Furthermore, SLs act as studies investigating essential proteins in SL signaling both exogenous and endogenous signaling molecules and biosynthesis on mutant species, including Oryza in response to environmental stresses [115]. Thus, sativa L. Petunia hybrida, Pisum sativum L, and SLs act exogenously in parts of the rhizosphere and Arabidopsis thaliana L [106], have reported that this endogenously as phytohormones that regulate plant process occurs with alteration in a cytochrome P450 growth and development [115]. SLs have been reported monooxygenase class III case by enhancement in growth as signaling pathways in several species, including pea, of AXILLARY GROWTH1 (MAX1) [107-108]. The role petunia, Arabidopsis, and rice [86], which can regulate of enzymes of carotenoid cleavage dioxygenase (CCD) plant development and interactions between the plant in different species of plants [109] is demonstrated by and the environment [71-72]. There is also evidence that the essential roles of CCD7 and CCD8 in SL synthesis the signaling pathways of SLs and auxin are involved in [71-72]. Strigolactone structures include one enol ether the adjustment of root architecture, which is influenced that plays the linking role between two ring systems, by GSH. Specifically, there is a signaling link between including the butenolide D and ABC ring [86]. These SLs, auxin and GSH that prevents GSH synthesis and molecules have some signaling pathways that include degradation of the adverse role of GSH on the root interactions between protein structure and degradation structure [116]. 1014 Emamverdian A., et al.

Table 1. Impact of new phytohormones on different species under various heavy metals by describing the involved mechanisms. Heavy metal Applications of new phy- Impact Plant Mechanism Reference stress tohormones on stress Inhibition from accumulation and uptake Indian mustard Cu BRs + of copper and aid in shoot generation [62] (Brassica juncea) and biomass Enhancement of photosynthetic pigments-reduction of H O , Lp and, Radish (Raphanus 2 2 Zn BRs + electrolyte leakage (ELP)- increasing [117] sativus L.) catalase (SOD), (CAT), (APX) - (ASA), (GSH), and proline Increasing in phytochelatins (PCs)- increasing enzyme activities of GSH Radish (Raphanus 28-Homobrassinolide Zn2+ + metabolism (GR, GPX and GST) and [118] sativus L.) (HBR) GSH biosynthesis (γ-ECS and GS) and reduction of MDA and H2O2 Tomato cultivars 28-homobrassinolide Improving photosynthetic perform- (cv. K-25 and Sar- Cd (HBL) or 24-epibrassino- + ance- increasing antioxidant activity and [119] vodya) lide (EBL) proline content Enhancement of antioxidative enzymes Bean (Phaseolus Cd and Nacl 24-epibrassinolide (EBL) + and proline-improving water content and [120] vulgaris L.) the membrane stability index (MSI) Increasing antioxidant enzymes activity Radish (Raphanus 24-epibrassinolide and Cd + including SOD, CAT, GPX, and APOX– [121] sativus L.) 28-homobrassinolide the reduction of lipid peroxidation Tomato cultivars 28-homobrassinolide/24- Improving photosynthetic and the in- (K-25 and Cd epibrassinolide (HBL/ + creasing antioxidant enzyme activity and [122] Sarvodya) EBL) proline content Tomato Cd + Increasing antioxidant activity [70] Brassica napus L. Increasing gene expression and enzy- cultivars (ZS 758–a matic activities (POD, SOD, APX, CAT, black seed type, and As Methyl jasmonate (MJ) + [33] CAD, PPO, and PAL). Degradation of Zheda 622–a yellow As contents seed type) Reduction of uptake of Na and Na2CO3- induced oxidative damage by degrada- seedlings Na CO -stress Jasmonic acid (JA) + [123] 2 3 tion of ROS accumulation and malondi- aldehyde Enhancement of S-assimilation and Mustard (Brassica production of decreasing glutathione Cd Methyl jasmonate (MeJA) + [124] juncea L.) (GSH) and ameliorated of functions in photosynthetic Increasing antioxidant activity SOD, Faba bean (Vicia CAT, glutathione reductase and ascorbate Cd Jasmonic acid (JA) + [125] faba L.) peroxidase Accumulation of Cd in shoots, roots, and leaves Influence on chlorophyll efficiency and Arabidopsis plants Cu and Cd Jasmonic acid (JAMe) + [45] photosynthetic activity Decreasing of H2O2 and MDA content Soybean plant (Gly- Cd Methyl jasmonate + and enhancement of antioxidant enzymes [40] cine max L.) activity MeJA ameliorated Cd stress by medi- Foxtail millet Cd Methyl jasmonate + ated of endogenous sodium hydrosulfide [126]

(H2S) Exogenous synthetic SLs Switchgrass (Pani- Reducing Cadmium uptake-activation of Cd analog, + [127] cum virgatum) activities of antioxidant enzymes GR24 The Role of New Members of Phytohormones... 1015

Table 1. Continued. Gene expression regulation related to GR24, a synthesized strig- plant defense mechanism, signal trans- Brassica napus L NaCl + [10] olactone duction of phytohormones and increas- ing photosynthesis Regulation of development of rice root, Rice (Oryza sativa Phosphate and SL analogue GR24 + which is faced with nitrate and phos- [128] L) Nitrate phate and limitation Pea (Pisum sativum Phosphate and Regulates development of mycorrhizal Strigolactone synthesis + [129] L.) Nitrate and regulates of nodulation in roots The adjustment of shoot architectural Arabidopsis (Arabi- Phosphate Strigolactone production + in the face to phosphate deficiency with [130] dopsis thaliana), deficiency xylem-transported strigolactones Low Pi condi- synthetic strigolactone Transmitted via the MAX2 component Arabidopsis + [131] tions GR24 of SL signaling First as a signal of rhizosphere to maxi- mize AM fungi symbiosis for improved Phosphate (Pi) Pi acquisition and the second one is the Rice seedlings Strigolactones (SLs) + [132] and nitrate endogenous hormone or its biosynthetic precursor to optimizing shoot branching for efficient Pi utilization

Discussion which is related to the structure and architecture of the root system. In addition to root and shoot branching, The identification and determination of detoxification SLs play an essential role in cellular redox homeostasis. factors to reduce heavy metal stress can be a good option It has been shown that compared with wildtype for coping with this harmful stress. Among these factors formation, mutant formation (ore9), which is involved are phytohormones, which play an important role in in MAX2, could prevent senescence and oxidative plant growth and development and the cell cycle process stress. GR24, a synthesized strigolactone, is known to in plants and can help to reduce heavy metal stress. be a defense mechanism in stress conditions. Exogenous These small molecules can regulate stress signaling GR24 leads to increased plant tolerance against salt, through signaling pathway networks in plants and can drought and metal stress, reduced MDA content and improve plant defense systems by increasing antioxidant chloroplast damage, and increased photosynthetic enzyme activity and degrading lipoperoxidation and capacity and plant defense mechanisms against ROS

H2O2. There are two categories of phytohormones, which via stimulation of antioxidant enzyme activity (SOD consist of classical phytohormones such as auxins, and POD) caused by salinity stresses. Additionally, SLs ethylene, gibberellins, and cytokinins, and the newest have the ability to regulate the development of shoot members of phytohormones such as strigolactones, branching in plants, which can be a positive mechanism brassinosteroids, and jasmonates. Jasmonic acid (JA) for coping with the adverse effects of heavy metals is an important member of the plant growth regulator on shoot branching. Brassinosteroids (BRs), as a new (PGR) family, which can act as a signaling molecule group of phytohormones, are involved in many growth in plants exposed to heavy metal stress. JA acts as processes in plants including growing of the fruit, signaling molecules involved in the rising resistance flower, pollen, seed, and fiber, as well as rhizogenesis, to stress by activation of related genes. The protective abscission, and senescence. Additionally, BRs have a role of JA against the stress of heavy metals involves role in the regulation of cellular expansion and plant the stimulation of antioxidant enzymes, reduction of differentiation. Brassinosteroids (BRs) can improve

H2O2 and malondialdehyde (MDA) (to protect the cell plant resistance with some plant defense mechanisms membrane lipid) and providing a protective role for such as the reduction of lipoperoxidation, stimulation photosynthetic pigments (reducing oxidative damage). of antioxidant activity and improving phytochelatin SLs are defined as a new class of multifunctional synthesis. Brassinosteroids also improve photosynthesis phytohormone molecules that are produced by plant root efficiency via mechanisms involved in photochemical exudation and play an important role in some process pathways and ameliorate electron transport efficiency involved in plant growth, including seed germination, to improve damage of reaction centers and evolving the formation of the root and hypocotyl growth. SLs play complexes of O2. Furthermore, BRs can regulate the an important role in plant mechanisms against water expression of a variety of genes encoding plant defense and nutrient deficiencies and can be linked with abiotic mechanism including PC, antioxidant enzymes and stresses such as nutrients and meals. The mechanisms of metallothioneins. Brassinosteroids can also facilitate SLs when faced with metals and nutrients are bilateral, and stimulate the synthesis of PC in the plant cell 1016 Emamverdian A., et al. in heavy metal stress conditions. Phytochelatins regulation of proline metabolism. Environ. Exp. Bot. 100, are cysteine-rich compounds with the ability of 34, 2014. metal binding, which play an important role in the 2. Van Zeijl A., Liu W., Xiao T.T., Kohlen W., Yang compartmentalization of metal in vacuoles or chelation W., Bisseling T. The strigolactone biosynthesis gene DWARF27 is co-opted in rhizobium symbiosis. BMC of metals in the cytosol. 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Physiological and genetic responses The signaling pathways networks involved in to pesticide mixture treatment of Veronica beccabunga. phytohormones play an essential role in regulating Water, Air Soil Pollut. 223, 6201, 2012. the integrity of plants coping with stress. These 6. Egamberdieva D., Wirth S.J., Alqarawi A.A., networks regulate and stimulate gene expression Abd_Allah E.F., Hashem A. Phytohormones and related to plant defense systems, such as antioxidant Beneficial Microbes: Essential Components for Plants to activities, phytochelatins (PCs), metallothioneins Balance Stress and Fitness. Front Microbiol. 8, 2017. (MTs) and other pathways. Despite numerous studies, 7. Wani S.H., Kumar V., Shriram V., Kumar ambiguous issues remain, for example how exogenous Sah S. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants, Crop J. 4, 162, JA/MeJA can increase the synthesis of PCs and MTs at 2016. a transcript level during heavy metal stress conditions. 8. Peleg Z., Blumwald E. Hormone balance and abiotic Additionally, we know that BR is a regulated protein stress tolerance in crop plants. Curr. Opin. Plant Biol. 14, that interacts with enzyme activity in the membrane 290, 2011. and with sterols and proteins in membranes. However, 9. Vob U., Bishopp A., Farcot E., Bennett M.J. it remains unknown how BRs can protect the cell Modelling hormonal response and development. Trends and which mechanisms are involved in BR efficiency Plant Sci. 19, 311, 2014. in aiding plant cells in oxidative stress. Thus, this 10. Ma N., Hu C., Wan L., Hu Q., Xiong J., Zhang C. questions should be considered in future studies. 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