Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding

A new metabolite profiling approach combined with an ultrarapid sample preparation procedure was used to study the temporal and spatial dynamics of the wound-induced accumulation of jasmonic acid (JA) and its oxygenated derivatives in Arabidopsis thaliana. In addition to well known jasmonates, including hydroxyjasmonates (HOJAs), jasmonoyl-isoleucine (JA-Ile), and its 12-hydroxy derivative (12-HOJA-Ile), a new wound-induced dicarboxyjasmonate, 12-carboxyjasmonoyl-l-isoleucine (12-HOOCJA-Ile) was discovered. HOJAs and 12-HOOCJA-Ile were enriched in the midveins of wounded leaves, strongly differentiating them from the other jasmonate metabolites studied. The polarity of these oxylipins at physiological pH correlated with their appearance in midveins. When the time points of accumulation of different jasmonates were determined, JA levels were found to increase within 2-5 min of wounding. Remarkably, these changes occurred throughout the plant and were not restricted to wounded leaves. The speed of the stimulus leading to JA accumulation in leaves distal to a wound is at least 3 cm/min. The data give new insights into the spatial and temporal accumulation of jasmonates and have implications in the understanding of long-distance wound signaling in plants.     

Jasmonoyl isoleucine accumulation is needed for abscisic acid build‐up in roots of Arabidopsis under water stress conditions

Phytohormones are central players in sensing and signalling numerous environmental conditions like drought. In this work, hormone profiling together with gene expression of key enzymes involved in abscisic acid (ABA) and jasmonate biosynthesis were studied in desiccating Arabidopsis roots. Jasmonic acid (JA) content transiently increased after stress imposition whereas progressive and concomitant ABA and Jasmonoyl Isoleucine (JA‐Ile) accumulations were detected. Molecular data suggest that, at least, part of the hormonal regulation takes place at the biosynthetic level. These observations also point to a possible involvement of jasmonates on ABA biosynthesis under stress. To test this hypothesis, mutants impaired in jasmonate biosynthesis (opr3, lox6 and jar1‐1) and in JA‐dependent signalling (coi1) were employed. Results showed that the early JA accumulation leading to JA‐Ile build up was necessary for an ABA increase in roots under two different water stress conditions. Signal transduction between water stress‐induced JA‐Ile accumulation and COI1 is necessary for a full induction of the ABA biosynthesis pathway and subsequent hormone accumulation in roots of Arabidopsis plants. The present work adds a level of interaction between jasmonates and ABA at the biosynthetic level.     

Silicon: a duo synergy for regulating crop growth and hormonal signaling under abiotic stress conditions

Abiotic stresses, such as salinity, heavy metals and drought, are some of the most devastating factors hindering sustainable crop production today. Plants use their own defensive strategies to cope with the adverse effects of these stresses, via the regulation of the expression of essential phytohormones, such as gibberellins (GA), salicylic acid (SA), jasmonates (JA), abscisic acid (ABA) and ethylene (ET). However, the efficacy of the endogenous defensive arsenals of plants often falls short if the stress persists over an extended period. Various strategies are developed to improve stress tolerance in plants. For example, silicon (Si) is widely considered to possess significant potential as a substance which ameliorate the negative effects of abiotic stresses, and improves plant growth and biomass accumulation. This review aims to explain how Si application influences the signaling of the endogenous hormones GA, SA, ABA, JA and ET during salinity, wounding, drought and metal stresses in crop plants. Phytohormonal cross talk plays an important role in the regulation of induced defences against stress. However, detailed molecular and proteomic research into these interactions is needed in order to identify the underlying mechanisms of stress tolerance that is imparted by Si application and uptake.     

Jasmonates induce Nod factor production by Bradyrhizobium japonicum

Jasmonates are signaling molecules involved in induced systemic resistance, wounding and stress responses of plants. We have previously demonstrated that jasmonates can induce nod genes of Bradyrhizobium japonicum when measured by beta-galactosidase activity. In order to test whether jasmonates can effectively induce the production and secretion of Nod factors (lipo-chitooligosaccharides, LCOs) from B. japonicum, we induced two B. japonicum strains, 532C and USDA3, with jasmonic acid (JA), methyl jasmonate (MeJA) and genistein (Ge). As genistein is well characterized as an inducer of nod genes it was used a positive control. The high-performance liquid chromatography (HPLC) profile of LCOs isolated following treatment with jasmonates or genistein showed that both JA and MeJA effectively induced nod genes and caused production of LCOs from bacterial cultures. JA and MeJA are more efficacious inducers of LCO production than genistein. Genistein plus JA or MeJA resulted in greater LCO production than either alone. A soybean root hair deformation assay showed that jasmonate induced LCOs were as effective as those induced by genistein. This is the first report that jasmonates induce Nod factor production by B. japonicum. This report establishes the role of jasmonates as a new class of signaling molecules in the Bradyrhizobium-soybean symbiosis.     

Wound and insect‐induced jasmonate accumulation in carnivorous Drosera capensis: two sides of the same coin

Carnivorous sundew plants catch and digest insect prey for their own nutrition. The sundew species Drosera capensis shows a pronounced leaf bending reaction upon prey capture in order to form an ‘outer stomach’. This formation is triggered by jasmonates, phytohormones typically involved in defence reactions against herbivory and wounding. Whether jasmonates still have this function in D. capensis in addition to mediating the leaf bending reaction was investigated here. Wounded, insect prey‐fed and insect‐derived oral secretion‐treated leaves of D. capensis were analysed for jasmonates (jasmonic acid, JA; jasmonic acid‐isoleucine conjugate, JA‐Ile) using LC‐MS/MS. Prey‐induced jasmonate accumulation in D. capensis leaves was persistent, and showed high levels of JA and JA‐Ile (575 and 55.7 pmol·g·FW^?1, respectively), whereas wounding induced a transient increase of JA (maximum 500 pmol·g·FW^?1) and only low (3.1 pmol·g·FW^?1) accumulation of JA‐Ile. Herbivory, mimicked with a combined treatment of wounding plus oral secretion (W+OS) obtained from Spodoptera littoralis larvae induced both JA (4000 pmol·g·FW^?1) and JA‐Ile (25 pmol·g·FW^?1) accumulation, with kinetics similar to prey treatment. Only prey and W+OS, but not wounding alone or OS, induced leaf bending. The results indicate that both mechanical and chemical stimuli trigger JA and JA‐Ile synthesis. Differences in kinetics and induced jasmonate levels suggest different sensing and signalling events upon injury and insect‐dependent challenge. Thus, in Drosera, jasmonates are still part of the response to wounding. Jasmonates are also employed in insect‐induced reactions, including responses to herbivory and carnivory.     

Possible involvement of jasmonates in various morphogenic events

Jasmonates (jasmonic acid and related compounds) seem to be involved in various morphogenic events of plants, such as tuberization (potato, yam and Jerusalem artichoke), tuberous root formation (sweet potato), bulb formation (onion and garlic), determination of plant structure (soybean) and thigmomorphogenesis (coiling of tendrils of Bryonia dioica ). The involvement of jasmonates in tuberization in these plants was inferred from their ability to induce tubers in vitro, and from changes in the levels of endogenous jasmonates during the growth of the plants, which can account for the initiation of tuberization. As to potato tuberization, jasmonic acid (JA) and its methyl ester (JA-Me) have strong tuber-inducing activity. These compounds seem to exert their tuber-inducing effects by elicting the expansion of cells, because JA and JA-Me are capable of causing the expansion of cells in potato tubers. The JA-induced expansion of cells is attributable to both an increase in osmotic pressure due to the accumulation of sucrose and changes in cell wall architecture that appear to affect the extensibility of the wall. And, moreover, the synthesis of cellulose might be indispensable for the JA-induced expansion. The tuberization and the expansion of cells induced by JA always involve the reorientation of cortical microtubules (MTs), suggesting that JA controls the direction of cell expansion by changing the arrangement of MTs. However, the reorientation of MTs itself seems to be insufficient for the induction of expansion of cells.
Involvement of jasmonates in bulb formation and tuberous root formation is presumed from the fact that JA is able to induce these in vitro. The exact nature of the control that the jasmonates exert on morphogenesis remains to be elucidated.     

Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis

Jasmonic acid (JA) and methyl jasmonate (MeJA), collectively termed jasmonates, are ubiquitous plant signalling compounds. Several types of stress conditions, such as wounding and pathogen infection, cause endogenous JA accumulation and the expression of jasmonate-responsive genes. Although jasmonates are important signalling components for the stress response in plants, the mechanism by which jasmonate signalling contributes to stress tolerance has not been clearly defined. A comprehensive analysis of jasmonate-regulated metabolic pathways in Arabidopsis was performed using cDNA macroarrays containing 13516 expressed sequence tags (ESTs) covering 8384 loci. The results showed that jasmonates activate the coordinated gene expression of factors involved in nine metabolic pathways belonging to two functionally related groups: (i) ascorbate and glutathione metabolic pathways, which are important in defence responses to oxidative stress, and (ii) biosynthesis of indole glucosinolate, which is a defence compound occurring in the Brassicaceae family. We confirmed that JA induces the accumulation of ascorbate, glutathione and cysteine and increases the activity of dehydroascorbate reductase, an enzyme in the ascorbate recycling pathway. These antioxidant metabolic pathways are known to be activated under oxidative stress conditions. Ozone (O3) exposure, a representative oxidative stress, is known to cause activation of antioxidant metabolism. We showed that O3 exposure caused the induction of several genes involved in antioxidant metabolism in the wild type. However, in jasmonate-deficient Arabidopsis 12-oxophytodienoate reductase 3 (opr3) mutants, the induction of antioxidant genes was abolished. Compared with the wild type, opr3 mutants were more sensitive to O3 exposure. These results suggest that the coordinated activation of the metabolic pathways mediated by jasmonates provides resistance to environmental stresses.     

Production and function of jasmonates in nodulated roots of soybean plants inoculated with Bradyrhizobium japonicum

Little is known regarding production and function of endogenous jasmonates (JAs) in root nodules of soybean plants inoculated with Bradyrhizobium japonicum. We investigated (1) production of jasmonic acid (JA) and 12-oxophytodienoic acid (OPDA) in roots of control and inoculated plants and in isolated nodules; (2) correlations between JAs levels, nodule number, and plant growth during the symbiotic process; and (3) effects of exogenous JA and OPDA on nodule cell number and size. In roots of control plants, JA and OPDA levels reached a maximum at day 18 after inoculation; OPDA level was 1.24 times that of JA. In roots of inoculated plants, OPDA peaked at day 15, whereas JA level did not change appreciably. Shoot dry matter of inoculated plants was higher than that of control at day 21. Chlorophyll a decreased more abruptly in control plants than in inoculated plants, whereas b decreased gradually in both cases. Exogenous JA or OPDA changed number and size of nodule central cells and peripheral cells. Findings from this and previous studies suggest that increased levels of JA and OPDA in control plants are related to senescence induced by nutritional stress. OPDA accumulation in nodulated roots suggests its involvement in "autoregulation of nodulation."     

Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae)

The present study was undertaken to test the influence of exogenously applied jasmonic acid (JA) upon the growth and metabolism of Wolffia arrhiza (Lemnaceae), the smallest vessel aquatic plant exposed to lead (Pb) stress. It was found, that JA acted in a concentration-dependent manner. Treatment with JA at the highest concentration 100 μM resulted in the enhancement of heavy metal toxicity leading to increase in metal biosorption and formation of lipid peroxides as well as decrease in fresh weight, chlorophyll a, carotenoid, monosaccharide and soluble protein content. In contrast, this phytohormone applied at 0.1 μM protected W. arrhiza fronds against Pb stress inhibiting heavy metal accumulation, restoring plant growth and primary metabolite level. Moreover, JA at 0.1 μM activated enzymatic (catalase, ascorbate peroxidase, NADH peroxidase) and non-enzymatic antioxidant (ascorbate, glutathione) system in W. arrhiza, and therefore, suppressed oxidative destruction of cellular components induced by heavy metal. The data suggest that JA plays an important role in the growth and metabolism of W. arrhiza exposed to abiotic stressor and its high adaptation ability to metal contamination of aquatic environment.     

Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae)

The present study was undertaken to test the influence of exogenously applied jasmonic acid (JA) upon the growth and metabolism of Wolffia arrhiza (Lemnaceae), the smallest vessel aquatic plant exposed to lead (Pb) stress. It was found, that JA acted in a concentration-dependent manner. Treatment with JA at the highest concentration 100 μM resulted in the enhancement of heavy metal toxicity leading to increase in metal biosorption and formation of lipid peroxides as well as decrease in fresh weight, chlorophyll a, carotenoid, monosaccharide and soluble protein content. In contrast, this phytohormone applied at 0.1 μM protected W. arrhiza fronds against Pb stress inhibiting heavy metal accumulation, restoring plant growth and primary metabolite level. Moreover, JA at 0.1 μM activated enzymatic (catalase, ascorbate peroxidase, NADH peroxidase) and non-enzymatic antioxidant (ascorbate, glutathione) system in W. arrhiza, and therefore, suppressed oxidative destruction of cellular components induced by heavy metal. The data suggest that JA plays an important role in the growth and metabolism of W. arrhiza exposed to abiotic stressor and its high adaptation ability to metal contamination of aquatic environment.     

Jasmonic acid is involved in the water-stress-induced betaine accumulation in pear leaves

Jasmonic acid (JA) is known to be involved in the response of plants to environmental stresses such as drought, and betaine (glycinebetaine) is an osmopretectant accumulated in plants under environmental stresses including drought. However, it remains currently unclear whether JA is involved in the water‐stress‐induced betaine accumulation in plant leaves. The present experiment, performed with the whole pear plant (Pyrus bretschneideri Redh. cv. Suli), revealed that the exogenously applied JA induced a significant increase of the betaine level in the pear leaves when the plants were not yet stressed by drought, and when the plants were subjected to water stress, the ‘JA plus drought’ treatment induced a significant higher betaine level than did the drought treatment alone. Meanwhile, the ‘JA plus drought’ treatment induced higher levels of betaine aldehyde dehydrogenase (BADH, E C 1.2.1.8) and activities in the leaves than did the drought treatment alone. These results obtained in the whole plant experiments were supported by the results of detached leaf experiments. In detached leaves JA induced significant increases in betaine levels, BADH activities and BADH protein amounts in a time‐ and concentration‐dependent manner. These data demonstrate that JA is involved in the drought‐induced betaine accumulation in pear leaves.     

Changes in the polypeptide patterns of barley seedlings exposed to jasmonic Acid and salinity

Soluble and thylakoid membrane proteins of jasmonic acid (JA)-treated and salt-stressed barley (Hordeum vulgare L.) seedlings were investigated using 15% sodium dodecyl sulfate-polyacrylamide slab gel electrophoresis. High JA concentrations induced marked quantitative and qualitative changes in polypeptide profiles concerning mainly the proteins with approximately equal mobility, as in NaCl-stressed plants. The most obvious increase in thylakoid polypeptide band intensity was at 55 to 57 kilodaltons (kD). The relative share of some polypeptides with apparent molecular masses above 66 kD and of polypeptides with lower molecular masses in the region of 20.5 to 15 kD was enhanced. At the same time, one new band at 31 to 31.5 kD was well expressed at 25 and 250 micromolar JA concentrations and became discernible in the 100 micromolar NaCl-treated plants. The intensity of some polypeptides of soluble proteins (molecular masses of 60, 47, 37, 30, and 23.4 kD) increased with increasing JA concentration, whereas the intensities of other polypeptide bands (55, 21.4, and 15 kD) decreased. Enhanced levels of 60-, 47-, 34-, and 30-kD polypeptides and reduced levels of 55- and 15-kD polypeptides were present in NaCl-treated plants. The appearance of one new polypeptide, of 25.1 kD, was observed only in NaCl-treated plants. At 100 millimolar NaCl, an eightfold increase in proline content was observed while at 250 micromolar JA, the proline content was threefold over the control. It is hypothesized that exogenously applied jasmonates act as stress agents. As such, they provoke alterations in the proline content and they can modulate typical stress responses by induction of stress proteins.     

Octadecanoid-derived alteration of gene expression and the "oxylipin signature" in stressed barley leaves. Implications for different signaling pathways

Stress-induced gene expression in barley (Hordeum vulgare cv Salome) leaves has been correlated with temporally changing levels of octadecanoids and jasmonates, quantified by means of gas chromatography/mass spectrometry-single ion monitoring. Application of sorbitol-induced stress led to a low and transient rise of jasmonic acid (JA), its precursor 12-oxophytodienoic acid (OPDA), and the methyl esters JAME and OPDAME, respectively, followed by a large increase in their levels. JA and JAME peaked between 12 and 16 h, about 4 h before OPDA and OPDAME. However, OPDA accumulated up to a 2.5-fold higher level than the other compounds. Dihomo-JA and 9, 13-didehydro-OPDA were identified as minor components. Kinetic analyses revealed that a transient threshold of jasmonates or octadecanoids is necessary and sufficient to initiate JA-responsive gene expression. Although OPDA and OPDAME applied exogenously were metabolized to JA in considerable amounts, both of them can induce gene expression, as evidenced by those genes that did not respond to endogenously formed JA. Also, coronatine induces JA-responsive genes independently from endogenous JA. Application of deuterated JA showed that endogenous synthesis of JA is not induced by JA treatment. The data are discussed in terms of distinct signaling pathways.     

Phytohormone responses in pepper (Capsicum annuum L.) leaves under a high density of aphid infestation

The time course response of selected phytohormones has been evaluated in sweet pepper plants (Capsicum annuum L.) submitted to a high density (200 aphids/plant) of aphid (Myzus persicae Sulzer) infestation. Abscisic acid (ABA), salicylic acid (SA), indole-3-acetic acid (IAA), and jasmonates (JAs), including jasmonic acid (JA), jasmonoyl-l -isoleucine (JA-Ile), and cis-OPDA have been simultaneously identified and quantitated by UHPLC–MS/MS in pepper leaf tissue harvested at 3, 8 hours post-infestation (hpi), 1, 2, 4 and 7 days post-infestation (dpi). Infested plants showed a reduction in stem length at 7 dpi and in the number of leaves and leaf width from 4 dpi onwards. JA and JA-Ile significantly increased very early (from 3 hpi) while SA only accumulated at 7 dpi. Despite the high density of infestation, the aphid-induced accumulation of JAs was much lower than the burst typically induced by chewing herbivores. On the other side, ABA peaked in aphid-infested plants at 2 and 4 dpi, while IAA content did not change significantly at any time point. Growth inhibition may be partially explained by the high levels of JAs found in aphid-infested plants. The possibility that the obtained results support the hypothesis of the aphid manipulation of plant metabolism is discussed.     

Regulation of stress hormones jasmonates and ethylene by MAPK pathways in plants

Plant stress hormones, such as jasmonates (JAs) and ethylene (ET) are essential in plant defence against stress conditions. JAs are used in cosmetics and food flavouring, and the recently demonstrated anti-cancer activity of JAs highlights their potential in health protection. It reinforces the need for a better understanding of biosynthetic regulation of JAs. Which mechanisms are involved in the regulation of the biosynthesis of JAs and ET? Production of stress hormones is induced in plants after wounding or herbivore attack. ET is a gaseous compound and plant JAs are oxylipins structurally similar to prostaglandins that are induced upon inflammation or injury in mammals. Wounding activates protein phosphorylation cascades involving mitogen-activated protein kinases (MAPKs). MAPKs regulate ET production. The induction of JA biosynthesis was suggested to require MAPK activation; however the defined roles of MAPKs in JA production remain unclear. Here we will highlight the most recent findings suggesting the regulation of JA biosynthesis and ethylene production by stress activated MAPKs and phosphatases that inactivate these MAPKs.