Transient pulse formation in jasmonate signaling pathway

Ever since their discovery as key regulators of the jasmonate (JA) signaling pathway, repressor proteins of the JASMONATE ZIM-domain (JAZ) family are rising stars in research on hormonal regulation of plant growth and defense. In plant cells, JAZ repressor proteins interact with an E3 ubiquitin ligase complex (SCFCOI1) that together functions as a JA receptor. In uninduced cells, JAZs block the activity of transcriptional regulators of JA responses by physically binding to them. Upon perception of bioactive JAs, JAZ proteins are rapidly degraded via the ubiquitin/26S proteasome-dependent proteolytic pathway. This releases the JAZ-bound transcription factors, resulting in the activation of downstream JA responses. JAs play a dominant role in regulating defense responses against herbivorous insects and necrotrophic pathogens, and in adaptive responses to beneficial soil-borne microbes. In addition, JAs have a signal function in a myriad of other processes, including abiotic stress reactions and plant growth responses to environmental cues. The JA pathway functions in the context of a complex network of hormone-regulated signaling pathways that, depending on the environmental or developmental condition, can act antagonistically or synergistically on each other to finely balance resource allocation between growth and defense and minimize fitness tradeoffs. In the process of balancing plant growth and defense, gibberellins (GAs) emerged as dominant antagonists of the JA signaling output. GAs regulate different aspects of plant growth via DELLA repressor proteins that block the activity of transcriptional regulators of GA responses by physically binding to them. Analogous to the role of JAZs in the JA pathway, DELLAs are degraded upon perception of GAs, resulting in the activation of downstream growth responses. Interestingly, DELLAs also interact with JAZs, thereby mutually limiting the cellular binding capacity to their cognate transcription factors. Consequently, GA-mediated degradation of DELLAs enhances the cellular binding capacity of JAZs to their cognate transcription factors, thus reducing the potential JA signaling output. This GA-mediated antagonistic effect on the JA pathway becomes apparent during the shade-avoidance response of plants that grow in dense vegetation stands. Shade-intolerant plant species respond to competition for light by increasing apical dominance and accelerating stem and petiole elongation. These growth and developmental responses occur in response to a drop in the red:far-red (R:FR) light ratio that is sensed by the phytochrome photoreceptors, predominantly phyB, and are GA-dependent through GA-mediated degradation of DELLA proteins. This allows them to outgrow neighboring plants, but at the cost of a reduced defensive capacity against necrotrophic pathogens and insect herbivores. In this issue of New Phytologist, Leone and co-workers zoomed in on the specific role of the Arabidopsis thaliana (Arabidopsis) JAZ10 protein in this process and shed light on the involvement of DELLAs in GA-JA crosstalk during the shade avoidance response. Besides growth-related hormones, also effector proteins of pathogens and plant growth-promoting mycorrhizal fungi have recently been shown to target JAZ repressor proteins, thereby changing the defense-related signaling circuitry for their own benefit. Hence, JAZ repressor proteins are emerging as central targets in the rewiring of the hormone-regulated signaling circuitry that regulates growth and defense.

JASMONATE ZIM-DOMAIN (JAZ) proteins are primary transcriptional repressors in the jasmonate (JA) signaling pathway that regulate a broad range of JA-dependent responses. A mechanistic mode of action is well established, but what are the biological roles of individual JAZs, and how do they contribute to the specification of JA signaling outputs? Two recent articles in Journal of Experimental Botany reveal roles of JAZ7 in regulating dark-induced senescence and susceptibility to fungal pathogens. Jasmonates (JAs) regulate a broad range of processes, from growth and development to biotic and abiotic stress responses. JASMONATE ZIM-DOMAIN (JAZ) proteins are key regulators in controlling JA signaling outputs. Since the discovery of JAZs in 2007, over 100 research articles have been published on the characterization of JAZ functions, genomic or transcriptomic analyses of JAZs, or the identification of down-stream transcription factors in the JA signaling pathway through yeast two-hybrid screens using JAZs as bait (reviewed in Pauwels and Goossens, 2011; Shyu and Brutnell, 2015). Biochemical and molecular functions of JAZ proteins have been extensively studied, but surprisingly little is known about the biological role of JAZs and how they contribute to specific JA signaling outputs.

The Harpin protein Hpa1 can induce defense responses in plant. This study aimed at investigating the role of jasmonate (JA) signal pathway in the process of biosynthesis of secondary metabolite in Sorbus aucuparia cell eliciting by Hpa1 crude extract (Hpa1 CE). The results showed that Hpa1 crude extract (Hpa1 CE) could induce phytoalexin synthesis in S. aucuparia cell， most of which was noraucuparin and its glycosides. Meanwhile Hpa1 CE treatment resulted in methyl jasmonate (MeJA) production increased and noraucuparin was de novo synthesized in large quantities. Combination of Hpa1 CE and salicylhydroxamic acid (SHAM, JA signaling inhibitor) caused the decreased MeJA and noraucuparin in the S. aucuparia cell compared with that in Hpa1 CE group. Real-time PCR results indicated that Hpa1 CE treatment caused down-regulation of JAZ and up-regulation of mcy2 in transcription level. Therefore Hpa1 CE elicited defense mechanism and JA signaling pathway involved in phytoalexin biosynthesis in S. aucuparia cell. It presented information to elucidate the role of JA signal pathway in stress response in the perspective of secondary metabolism of plant.

Roles of jasmonate and ethylene signalling and their interaction in yeast elicitor-induced biosynthesis of a phytoalexin, beta-thujaplicin, were investigated in Cupressus lusitanica cell cultures. Yeast elicitor, methyl jasmonate, and ethylene all induce the production of beta-thujaplicin. Elicitor also stimulates the biosynthesis of jasmonate and ethylene before the induction of beta-thujaplicin accumulation. The elicitor-induced beta-thujaplicin accumulation can be partly blocked by inhibitors of jasmonate and ethylene biosynthesis or signal transduction. These results indicate that the jasmonate and ethylene signalling pathways are integral parts of the elicitor signal transduction leading to beta-thujaplicin accumulation. Methyl jasmonate treatment can induce ethylene production, whereas ethylene does not induce jasmonate biosynthesis; methyl jasmonate-induced beta-thujaplicin accumulation can be partly blocked by inhibitors of ethylene biosynthesis and signalling, while blocking jasmonate biosynthesis inhibits almost all ethylene-induced beta-thujaplicin accumulation. These results indicate that the ethylene and jasmonate pathways interact in mediating beta-thujaplicin production, with the jasmonate pathway working as a main control and the ethylene pathway as a fine modulator for beta-thujaplicin accumulation. Both the ethylene and jasmonate signalling pathways can be regulated upstream by Ca(2+). Ca(2+) influx negatively regulates ethylene production, and differentially regulates elicitor- or methyl jasmonate-stimulated ethylene production.

Multigenic families of Plant Defensin type 1 (PDF1) have been described in several species, including the model plant Arabidopsis thaliana as well as zinc tolerant and hyperaccumulator A. halleri. In A. thaliana, PDF1 transcripts (AtPDF1) accumulate in response to pathogen attack following synergic activation of ethylene/jasmonate pathways. However, in A. halleri, PDF1 transcripts (AhPDF1) are constitutively highly accumulated. Through an evolutionary approach, we investigated the possibility of A. halleri or A. thaliana species specialization in different PDF1s in conveying zinc tolerance and/or the response to pathogen attack via activation of the jasmonate (JA) signaling pathway. The accumulation of each PDF1 from both A. halleri and A. thaliana was thus compared in response to zinc excess and MeJA application. In both species, PDF1 paralogues were barely or not at all responsive to zinc. However, regarding the PDF1 response to JA signaling activation, A. thaliana had a higher number of PDF1s responding to JA signaling activation. Remarkably, in A. thaliana, a slight but significant increase in zinc tolerance was correlated with activation of the JA signaling pathway. In addition, A. halleri was found to be more tolerant to the necrotrophic pathogen Botrytis cinerea than A. thaliana. Since PDF1s are known to be promiscuous antifungal proteins able to convey zinc tolerance, we propose, on the basis of the findings of this study, that high constitutive PDF1 transcript accumulation in A. halleri is a potential way to skip the JA signaling activation step required to increase the PDF1 transcript level in the A. thaliana model species. This could ultimately represent an adaptive evolutionary process that would promote a PDF1 joint effect on both zinc tolerance and the response to pathogens in the A. halleri extremophile species.

Jasmonates (JAs) are lipid-derived regulators that play crucial roles in both host immunity and development. We recently identified the NAC transcription factor RIM1 as a host factor involved in multiplication of rice dwarf virus (RDV). Here, we report that RIM1 functions as a transcriptional regulator of JA signaling and is degraded in response to JA treatment via a 26S proteasome-dependent pathway. Plants carrying rim1 mutations show a phenotype of root growth inhibition. The expression profiles of the mutants were significantly correlated with those of JA-treated wild-type plants without accumulation of endogenous JA, indicating that RIM1 functions as a component of JA signaling. The expression of genes encoding JA biosynthetic enzymes (lipoxygenase (LOX), allene oxide synthase 2 (AOS2) and OPDA reductase 7 (OPR7)) was up-regulated in the rim1 mutants under normal conditions, and a rapid and massive accumulation of endogenous JA was detected in the mutants after wounding. These results suggest that RIM1 may represent a new molecular link in jasmonate signaling, and may thereby provide new insights into the well-established coronatine-insensitive 1 (COI1)-Jasmonate ZIM-domain (JAZ) JA signaling pathway.

Jasmonate (JA) is an important phytohormone regulating growth, development, and environmental response in plants, particularly defense response against herbivorous insects. Recently, completion of the draft genome of the mulberry (Morus notabilis) in conjunction with genome sequencing of silkworm (Bombyx mori) provides an opportunity to study this unique plant-herbivore interaction. Here, we identified genes involved in JA biosynthetic and signaling pathways in the genome of mulberry for the first time, with the majority of samples showing a tissue-biased expression pattern. The analysis of the representative genes 12-oxophytodienoic acid reductase (OPRs) and jasmonate ZIM-domain (JAZs) was performed and the results indicated that the mulberry genome contains a relatively small number of JA biosynthetic and signaling pathway genes. A gene encoding an important repressor, MnNINJA, was identified as an alternative splicing variant lacking an ethylene-responsive element binding factor-associated amphiphilic repression motif. Having this fundamental information will facilitate future functional study of JA-related genes pertaining to mulberry-silkworm interactions.

Heat stress is a major environmental challenge affecting agricultural productivity and food security. The jasmonate (JA)-myelocytomatosis protein 2 (MYC2) pathway plays a critical role in plant growth and stress response. However, the mechanisms of how the JA-MYC2 pathway participates in the heat stress response in tomato remain unclear. Here, using approaches of reverse genetics, biochemical and molecular biology, we explore the molecular mechanism by which the JA signaling pathway and the histone demethylase Jumonji C domain - containing protein C3 (JMJC3)synergistically regulate thermotolerance in tomato. The JA biosynthetic mutant spr2 exhibited reduced thermotolerance, which was rescued by exogenous methyl jasmonate. Further analysis revealed that the transcription factor MYC2, a key JA signaling component, directly binds to the promoters of heat shock proteins (HSPs), activating their expression under heat stress. Moreover, MYC2 interacts with the histone demethylase JMJC3, which specifically removes repressive histone marks (H3K9me1/3 and H3K27me3) at HSP loci, facilitating their transcription. Genetic evidence showed that JMJC3 silencing compromises MYC2-mediated thermotolerance and HSP induction. Notably, MYC2 also transcriptionally activates JMJC3, forming a positive feedback loop. Collectively, the study unveiled a JA-MYC2-JMJC3 module that integrates hormonal signaling and epigenetic regulation to enhance HSP expression and thermotolerance in tomato, providing insights into plant adaptation to heat stress.

Herbivory by mites often activates both jasmonate and salicylate signaling pathways in plants. While the role of jasmonic acid (JA) pathway in inducing plant defenses against mites is well established, the contribution of salicylic acid (SA) remains under debate. In previous studies, we found that herbivory by the mite Oligonychus ilicis (McGregor) (Acari: Tetranychidae) triggered the accumulation of both SA and JA, but increased plants susceptibility to subsequent herbivores. Here, we investigated the relative importance of SA and JA signaling pathways in coffee resistance to O. ilicis by applying methyl jasmonate (MeJA) and methyl salicylate (MeSA) as elicitors. To address this question, we combined behavioral assays (host selection and performance) with chemical analyses to attempt to identify and quantify secondary metabolites in plants treated with two concentrations of the elicitors (1.5 mM and 3.0 mM). Treatment with MeSA at 3.0 mM increased mite attraction but did not affect their performance. In contrast, treatment with MeJA at 3.0 mM reduced mite performance without altering mite preference, confirming the defensive role of the JA pathway. Levels of total phenolic compounds were not affected, but target analyses revealed that some phenolics were up-regulated by the elicitor treatments, such as syringic acid and coumaric acids in MeSA-treated plants and o-coumaric acid in MeJA-treated plants. By demonstrating the contrasting effects of MeJA and MeSA on the responses of coffee plants, our study extends the understanding of phytohormone-mediated defenses, providing guidance for sustainable pest management and deepening our comprehension of arthropod-plant interactions.

The F-box protein Coronatine Insensitive (COI) is a receptor for the jasmonic acid signaling pathway in plants. To investigate the functions of the 6 maize (Zea mays) COI proteins (COI1a, COI1b, COI1c, COI1d, COI2a, and COI2b), we generated single, double, and quadruple loss-of-function mutants. The pollen of the coi2a coi2b double mutant was inviable. The coi1 quadruple mutant (coi1-4x) exhibited shorter internodes, decreased photosynthesis, leaf discoloration, microelement deficiencies, and accumulation of DWARF8 and/or DWARF9, 2 DELLA family proteins that repress the gibberellic acid (GA) signaling pathway. Coexpression of COI and DELLA in Nicotiana benthamiana showed that the COI proteins trigger proteasome-dependent DELLA degradation. Many genes that are downregulated in the coi1-4x mutant are GA-inducible. In addition, most of the proteins encoded by the downregulated genes are predicted to be bundle sheath- or mesophyll-enriched, including those encoding C4-specific photosynthetic enzymes. Heterologous expression of maize Coi genes in N. benthamiana showed that COI2a is nucleus-localized and interacts with maize jasmonate zinc-finger inflorescence meristem domain (JAZ) proteins, the canonical COI repressor partners. However, maize COI1a and COI1c showed only partial nuclear localization and reduced binding efficiency to the tested JAZ proteins. Together, these results show the divergent functions of the 6 COI proteins in regulating maize growth and defense pathways.

Phytohormones such as ethylene and auxin are involved in the regulation of the aluminum (Al)-induced root growth inhibition. Although jasmonate (JA) has been reported to play a crucial role in the regulation of root growth and development in response to environmental stresses through interplay with ethylene and auxin, its role in the regulation of root growth response to Al stress is not yet known. In an attempt to elucidate the role of JA, we found that exogenous application of JA enhanced the Al-induced root growth inhibition. Furthermore, phenotype analysis with mutants defective in either JA biosynthesis or signaling suggests that JA is involved in the regulation of Al-induced root growth inhibition. The expression of the JA receptor CORONATINE INSENSITIVE1 (COI1) and the key JA signaling regulator MYC2 was up-regulated in response to Al stress in the root tips. This process together with COI1-mediated Al-induced root growth inhibition under Al stress was controlled by ethylene but not auxin. Transcriptomic analysis revealed that many responsive genes under Al stress were regulated by JA signaling. The differential responsive of microtubule organization-related genes between the wild-type and coi1-2 mutant is consistent with the changed depolymerization of cortical microtubules in coi1 under Al stress. In addition, ALMT-mediated malate exudation and thus Al exclusion from roots in response to Al stress was also regulated by COI1-mediated JA signaling. Together, this study suggests that root growth inhibition is regulated by COI1-mediated JA signaling independent from auxin signaling and provides novel insights into the phytohormone-mediated root growth inhibition in response to Al stress.

BackgroundTIFY is a large plant-specific transcription factor gene family. A subgroup of TIFY genes named JAZ (Jasmonate-ZIM domain) has been identified as repressors of jasmonate (JA)-regulated transcription in Arabidopsis and other plants. JA signaling is involved in many aspects of plant growth/development and in defense responses to biotic and abiotic stresses. Here, we identified the TIFY genes (designated PvTIFY) from the legume common bean (Phaseolus vulgaris) and functionally characterized PvTIFY10C as a transcriptional regulator.ResultsNineteen genes from the PvTIFY gene family were identified through whole-genome sequence analysis. Most of these were induced upon methyl-JA elicitation. We selected PvTIFY10C as a representative JA-responsive PvTIFY gene for further functional analysis. Transcriptome analysis via microarray hybridization using the newly designed Bean Custom Array 90 K was performed on transgenic roots of composite plants with modulated (RNAi-silencing or over-expression) PvTIFY10C gene expression. Data were interpreted using Gene Ontology and MapMan adapted to common bean. Microarray differential gene expression data were validated by real-time qRT-PCR expression analysis. Comparative global gene expression analysis revealed opposite regulatory changes in processes such as RNA and protein regulation, stress responses and metabolism in PvTIFY10C silenced vs. over-expressing roots. These data point to transcript reprogramming (mainly repression) orchestrated by PvTIFY10C. In addition, we found that several PvTIFY genes, as well as genes from the JA biosynthetic pathway, responded to P-deficiency. Relevant P-responsive genes that participate in carbon metabolic pathways, cell wall synthesis, lipid metabolism, transport, DNA, RNA and protein regulation, and signaling were oppositely-regulated in control vs. PvTIFY10C-silenced roots of composite plants under P-stress. These data indicate that PvTIFY10C regulates, directly or indirectly, the expression of some P-responsive genes; this process could be mediated by JA-signaling.ConclusionOur work contributes to the functional characterization of PvTIFY transcriptional regulators in common bean, an agronomically important legume. Members from the large PvTIFY gene family are important global transcriptional regulators that could participate as repressors in the JA signaling pathway. In addition, we propose that the JA-signaling pathway involving PvTIFY genes might play a role in regulating the plant response/adaptation to P-starvation.

ERF4 affects fruit ripening by acting as a JAZ interactor between ethylene and jasmonic acid hormone signaling pathways

The phytohormones jasmonates (JAs) constitute an important class of elicitors for many plant secondary metabolic pathways. However, JAs do not act independently but operate in complex networks with crosstalk to several other phytohormonal signaling pathways. Here, crosstalk was detected between the JA and abscisic acid (ABA) signaling pathways in the regulation of tobacco (Nicotiana tabacum) alkaloid biosynthesis. A tobacco gene from the PYR/PYL/RCAR family, NtPYL4, the expression of which is regulated by JAs, was found to encode a functional ABA receptor. NtPYL4 inhibited the type-2C protein phosphatases known to be key negative regulators of ABA signaling in an ABA-dependent manner. Overexpression of NtPYL4 in tobacco hairy roots caused a reprogramming of the cellular metabolism that resulted in a decreased alkaloid accumulation and conferred ABA sensitivity to the production of alkaloids. In contrast, the alkaloid biosynthetic pathway was not responsive to ABA in control tobacco roots. Functional analysis of the Arabidopsis (Arabidopsis thaliana) homologs of NtPYL4, PYL4 and PYL5, indicated that also in Arabidopsis altered PYL expression affected the JA response, both in terms of biomass and anthocyanin production. These findings define a connection between a component of the core ABA signaling pathway and the JA responses and contribute to the understanding of the role of JAs in balancing tradeoffs between growth and defense.

Jasmonates (JAs), which can exogenously induce anti-herbivore defensive reaction in plants, are important in the field of plant physiology and plant protection. We summarized the ecological effects of exogenous JAs applied on 40 species of plants on various herbivores (such as Lepidoptera and Hemipteran) and their natural enemies in the past 20 years. We systematically genera-lized the research status about the direct and indirect antiherbivore defense induced by JAs, induced systemic defense, induction methods, induced performance in field, and the application status of JAs. Moreover, combining with the latest literatures, we reviewed the effects of JAs on plant growth-defense trade-offs from the cross-talk between phytohormone signaling pathways, and the regulation of nodes in the JA signaling pathway. Finally, we proposed the future directions and key aspects of the research on the plant anti-herbivore defense induced by exogenous JAs, which would promote the development of the related research and the application of JAs in field.