The Jasmonate Pathway

A special issue of Plants (ISSN 2223-7747).

Deadline for manuscript submissions: closed (31 October 2015) | Viewed by 95043

Special Issue Editor


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Guest Editor
Jasmonate Signaling Group, Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120 Halle (Saale), Germany
Interests: Arabidopsis, plant genetics, jasmonate, plant defense, root growth

Special Issue Information

Dear Colleagues,

Throughout the entire life cycle of higher plants, the jasmonate (JA) pathway regulates a wide range of processes, which range from growth and defense to reproductive development. In response to developmental or environmental cues, bioactive JAs accumulate and induce extensive transcriptional reprogramming that promotes plant fitness. Plants subjected to mechanical wounding or herbivore attack represent some of the most characterized and better understood examples of these phenomena, thus highlighting the importance of the JA pathway in controlling resource allocation for defense at the expense of growth. Furthermore, intense research efforts have extended our knowledge regarding the role of JAs in seed germination, tuber formation, senescence, mycorrhization, cross-talk interactions with other hormones and light signaling, seedling and flower development, and adaptive responses in leaves and roots.

For this Special Issue, review and research papers are invited from scientists working on diverse aspects of JA biology across plant species. Topics include, but are not limited to, JA biosynthesis, metabolism, perception, signal transduction, short- and long-distance signaling, plant-insect, plant-pathogen, and plant-symbiotic interactions, the regulation of plant secondary metabolism, integration with other pathways, development, and plant adaptation and evolution. Contributions from breeders and scientists working on the JA pathway in crop species and the utilization of genetically improved materials are also welcome.

Dr. Debora Gasperini
Guest Editor

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Keywords

  • jasmonic acid
  • JA-Ile
  • plant immunity
  • fertility
  • growth inhibition
  • hormone crosstalk
  • regulation of gene expression

Published Papers (12 papers)

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Research

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4210 KiB  
Article
Paired Hierarchical Organization of 13-Lipoxygenases in Arabidopsis
by Adeline Chauvin, Aurore Lenglet, Jean-Luc Wolfender and Edward E. Farmer
Plants 2016, 5(2), 16; https://doi.org/10.3390/plants5020016 - 24 Mar 2016
Cited by 45 | Viewed by 7606
Abstract
Embryophyte genomes typically encode multiple 13-lipoxygenases (13-LOXs) that initiate the synthesis of wound-inducible mediators called jasmonates. Little is known about how the activities of these different LOX genes are coordinated. We found that the four 13-LOX genes in Arabidopsis thaliana have different basal [...] Read more.
Embryophyte genomes typically encode multiple 13-lipoxygenases (13-LOXs) that initiate the synthesis of wound-inducible mediators called jasmonates. Little is known about how the activities of these different LOX genes are coordinated. We found that the four 13-LOX genes in Arabidopsis thaliana have different basal expression patterns. LOX2 expression was strong in soft aerial tissues, but was excluded both within and proximal to maturing veins. LOX3 was expressed most strongly in circumfasicular parenchyma. LOX4 was expressed in phloem-associated cells, in contrast to LOX6, which is expressed in xylem contact cells. To investigate how the activities of these genes are coordinated after wounding, we carried out gene expression analyses in 13-lox mutants. This revealed a two-tiered, paired hierarchy in which LOX6, and to a lesser extent LOX2, control most of the early-phase of jasmonate response gene expression. Jasmonates precursors produced by these two LOXs in wounded leaves are converted to active jasmonates that regulate LOX3 and LOX4 gene expression. Together with LOX2 and LOX6, and working downstream of them, LOX3 and LOX4 contribute to jasmonate synthesis that leads to the expression of the defense gene VEGETATIVE STORAGE PROTEIN2 (VSP2). LOX3 and LOX4 were also found to contribute to defense against the generalist herbivore Spodoptera littoralis. Our results reveal that 13-LOX genes are organised in a regulatory network, and the data herein raise the possibility that other genomes may encode LOXs that act as pairs. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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2177 KiB  
Article
Effect of Drought on Herbivore-Induced Plant Gene Expression: Population Comparison for Range Limit Inferences
by Gunbharpur Singh Gill, Riston Haugen, Steven L. Matzner, Abdelali Barakat and David H. Siemens
Plants 2016, 5(1), 13; https://doi.org/10.3390/plants5010013 - 11 Mar 2016
Cited by 4 | Viewed by 5527
Abstract
Low elevation “trailing edge” range margin populations typically face increases in both abiotic and biotic stressors that may contribute to range limit development. We hypothesize that selection may act on ABA and JA signaling pathways for more stable expression needed for range expansion, [...] Read more.
Low elevation “trailing edge” range margin populations typically face increases in both abiotic and biotic stressors that may contribute to range limit development. We hypothesize that selection may act on ABA and JA signaling pathways for more stable expression needed for range expansion, but that antagonistic crosstalk prevents their simultaneous co-option. To test this hypothesis, we compared high and low elevation populations of Boechera stricta that have diverged with respect to constitutive levels of glucosinolate defenses and root:shoot ratios; neither population has high levels of both traits. If constraints imposed by antagonistic signaling underlie this divergence, one would predict that high constitutive levels of traits would coincide with lower plasticity. To test this prediction, we compared the genetically diverged populations in a double challenge drought-herbivory growth chamber experiment. Although a glucosinolate defense response to the generalist insect herbivore Spodoptera exigua was attenuated under drought conditions, the plastic defense response did not differ significantly between populations. Similarly, although several potential drought tolerance traits were measured, only stomatal aperture behavior, as measured by carbon isotope ratios, was less plastic as predicted in the high elevation population. However, RNAseq results on a small subset of plants indicated differential expression of relevant genes between populations as predicted. We suggest that the ambiguity in our results stems from a weaker link between the pathways and the functional traits compared to transcripts. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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Communication
Jasmonate Signalling and Defence Responses in the Model Legume Medicago truncatula—A Focus on Responses to Fusarium Wilt Disease
by Louise F. Thatcher, Ling-Ling Gao and Karam B. Singh
Plants 2016, 5(1), 11; https://doi.org/10.3390/plants5010011 - 05 Feb 2016
Cited by 11 | Viewed by 6546
Abstract
Jasmonate (JA)-mediated defences play important roles in host responses to pathogen attack, in particular to necrotrophic fungal pathogens that kill host cells in order to extract nutrients and live off the dead plant tissue. The root-infecting fungal pathogen Fusarium oxysporum initiates a necrotrophic [...] Read more.
Jasmonate (JA)-mediated defences play important roles in host responses to pathogen attack, in particular to necrotrophic fungal pathogens that kill host cells in order to extract nutrients and live off the dead plant tissue. The root-infecting fungal pathogen Fusarium oxysporum initiates a necrotrophic growth phase towards the later stages of its lifecycle and is responsible for devastating Fusarium wilt disease on numerous legume crops worldwide. Here we describe the use of the model legume Medicago truncatula to study legume–F. oxysporum interactions and compare and contrast this against knowledge from other model pathosystems, in particular Arabidopsis thaliana–F. oxysporum interactions. We describe publically-available genomic, transcriptomic and genetic (mutant) resources developed in M. truncatula that enable dissection of host jasmonate responses and apply aspects of these herein during the M. truncatula-–F. oxysporum interaction. Our initial results suggest not all components of JA-responses observed in M. truncatula are shared with Arabidopsis in response to F. oxysporum infection. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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Communication
The C2 Protein from the Geminivirus Tomato Yellow Leaf Curl Sardinia Virus Decreases Sensitivity to Jasmonates and Suppresses Jasmonate-Mediated Defences
by Tábata Rosas-Díaz, Alberto P. Macho, Carmen R. Beuzón, Rosa Lozano-Durán and Eduardo R. Bejarano
Plants 2016, 5(1), 8; https://doi.org/10.3390/plants5010008 - 15 Jan 2016
Cited by 32 | Viewed by 7723
Abstract
An increasing body of evidence points at a role of the plant hormones jasmonates (JAs) in determining the outcome of plant-virus interactions. Geminiviruses, small DNA viruses infecting a wide range of plant species worldwide, encode a multifunctional protein, C2, which is essential for [...] Read more.
An increasing body of evidence points at a role of the plant hormones jasmonates (JAs) in determining the outcome of plant-virus interactions. Geminiviruses, small DNA viruses infecting a wide range of plant species worldwide, encode a multifunctional protein, C2, which is essential for full pathogenicity. The C2 protein has been shown to suppress the JA response, although the current view on the extent of this effect and the underlying molecular mechanisms is incomplete. In this work, we use a combination of exogenous hormone treatments, microarray analysis, and pathogen infections to analyze, in detail, the suppression of the JA response exerted by C2. Our results indicate that C2 specifically affects certain JA-induced responses, namely defence and secondary metabolism, and show that plants expressing C2 are more susceptible to pathogen attack. We propose a model in which C2 might interfere with the JA response at several levels. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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Article
Defense Priming and Jasmonates: A Role for Free Fatty Acids in Insect Elicitor-Induced Long Distance Signaling
by Ting Li, Tristan Cofer, Marie Engelberth and Jurgen Engelberth
Plants 2016, 5(1), 5; https://doi.org/10.3390/plants5010005 - 08 Jan 2016
Cited by 20 | Viewed by 6869
Abstract
Green leaf volatiles (GLV) prime plants against insect herbivore attack resulting in stronger and faster signaling by jasmonic acid (JA). In maize this response is specifically linked to insect elicitor (IE)-induced signaling processes, which cause JA accumulation not only around the damage site, [...] Read more.
Green leaf volatiles (GLV) prime plants against insect herbivore attack resulting in stronger and faster signaling by jasmonic acid (JA). In maize this response is specifically linked to insect elicitor (IE)-induced signaling processes, which cause JA accumulation not only around the damage site, but also in distant tissues, presumably through the activation of electrical signals. Here, we present additional data further characterizing these distal signaling events in maize. Also, we describe how exposure to GLV increases free fatty acid (fFA) levels in maize seedlings, but also in other plants, and how increased fFA levels affect IE-induced JA accumulation. Increased fFA, in particular α-linolenic acid (LnA), caused a significant increase in JA accumulation after IE treatment, while JA induced by mechanical wounding (MW) alone was not affected. We also identified treatments that significantly decreased certain fFA level including simulated wind and rain. In such treated plants, IE-induced JA accumulation was significantly reduced when compared to un-moved control plants, while MW-induced JA accumulation was not significantly affected. Since only IE-induced JA accumulation was altered by changes in the fFA composition, we conclude that changing levels of fFA affect primarily IE-induced signaling processes rather than serving as a substrate for JA. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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Article
Dynamics of Jasmonate Metabolism upon Flowering and across Leaf Stress Responses in Arabidopsis thaliana
by Emilie Widemann, Ekaterina Smirnova, Yann Aubert, Laurence Miesch and Thierry Heitz
Plants 2016, 5(1), 4; https://doi.org/10.3390/plants5010004 - 06 Jan 2016
Cited by 28 | Viewed by 6810
Abstract
The jasmonic acid (JA) signaling pathway plays important roles in adaptation of plants to environmental cues and in specific steps of their development, particularly in reproduction. Recent advances in metabolic studies have highlighted intricate mechanisms that govern enzymatic conversions within the jasmonate family. [...] Read more.
The jasmonic acid (JA) signaling pathway plays important roles in adaptation of plants to environmental cues and in specific steps of their development, particularly in reproduction. Recent advances in metabolic studies have highlighted intricate mechanisms that govern enzymatic conversions within the jasmonate family. Here we analyzed jasmonate profile changes upon Arabidopsis thaliana flower development and investigated the contribution of catabolic pathways that were known to turnover the active hormonal compound jasmonoyl-isoleucine (JA-Ile) upon leaf stress. We report a rapid decline of JA-Ile upon flower opening, concomitant with the massive accumulation of its most oxidized catabolite, 12COOH-JA-Ile. Detailed genetic analysis identified CYP94C1 as the major player in this process. CYP94C1 is one out of three characterized cytochrome P450 enzymes that define an oxidative JA-Ile turnover pathway, besides a second, hydrolytic pathway represented by the amido-hydrolases IAR3 and ILL6. Expression studies combined with reporter gene analysis revealed the dominant expression of CYP94C1 in mature anthers, consistent with the established role of JA signaling in male fertility. Significant CYP94B1 expression was also evidenced in stamen filaments, but surprisingly, CYP94B1 deficiency was not associated with significant changes in JA profiles. Finally, we compared global flower JA profiles with those previously reported in leaves reacting to mechanical wounding or submitted to infection by the necrotrophic fungus Botrytis cinerea. These comparisons revealed distinct dynamics of JA accumulation and conversions in these three biological systems. Leaf injury boosts a strong and transient JA and JA-Ile accumulation that evolves rapidly into a profile dominated by ω-oxidized and/or Ile-conjugated derivatives. In contrast, B. cinerea-infected leaves contain mostly unconjugated jasmonates, about half of this content being ω-oxidized. Finally, developing flowers present an intermediate situation where young flower buds show detectable jasmonate oxidation (probably originating from stamen metabolism) which becomes exacerbated upon flower opening. Our data illustrate that in spite conserved enzymatic routes, the jasmonate metabolic grid shows considerable flexibility and dynamically equilibrates into specific blends in different physiological situations. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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1965 KiB  
Article
Activity Regulation by Heteromerization of Arabidopsis Allene Oxide Cyclase Family Members
by Markus Otto, Christin Naumann, Wolfgang Brandt, Claus Wasternack and Bettina Hause
Plants 2016, 5(1), 3; https://doi.org/10.3390/plants5010003 - 06 Jan 2016
Cited by 23 | Viewed by 7321
Abstract
Jasmonates (JAs) are lipid-derived signals in plant stress responses and development. A crucial step in JA biosynthesis is catalyzed by allene oxide cyclase (AOC). Four genes encoding functional AOCs (AOC1, AOC2, AOC3 and AOC4) have been characterized for Arabidopsis thaliana in terms of [...] Read more.
Jasmonates (JAs) are lipid-derived signals in plant stress responses and development. A crucial step in JA biosynthesis is catalyzed by allene oxide cyclase (AOC). Four genes encoding functional AOCs (AOC1, AOC2, AOC3 and AOC4) have been characterized for Arabidopsis thaliana in terms of organ- and tissue-specific expression, mutant phenotypes, promoter activities and initial in vivo protein interaction studies suggesting functional redundancy and diversification, including first hints at enzyme activity control by protein-protein interaction. Here, these analyses were extended by detailed analysis of recombinant proteins produced in Escherichia coli. Treatment of purified AOC2 with SDS at different temperatures, chemical cross-linking experiments and protein structure analysis by molecular modelling approaches were performed. Several salt bridges between monomers and a hydrophobic core within the AOC2 trimer were identified and functionally proven by site-directed mutagenesis. The data obtained showed that AOC2 acts as a trimer. Finally, AOC activity was determined in heteromers formed by pairwise combinations of the four AOC isoforms. The highest activities were found for heteromers containing AOC4 + AOC1 and AOC4 + AOC2, respectively. All data are in line with an enzyme activity control of all four AOCs by heteromerization, thereby supporting a putative fine-tuning in JA formation by various regulatory principles. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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Review

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1228 KiB  
Review
Functional Analysis of Jasmonates in Rice through Mutant Approaches
by Rohit Dhakarey, Preshobha Kodackattumannil Peethambaran and Michael Riemann
Plants 2016, 5(1), 15; https://doi.org/10.3390/plants5010015 - 18 Mar 2016
Cited by 21 | Viewed by 9445
Abstract
Jasmonic acid, one of the major plant hormones, is, unlike other hormones, a lipid-derived compound that is synthesized from the fatty acid linolenic acid. It has been studied intensively in many plant species including Arabidopsis thaliana, in which most of the enzymes [...] Read more.
Jasmonic acid, one of the major plant hormones, is, unlike other hormones, a lipid-derived compound that is synthesized from the fatty acid linolenic acid. It has been studied intensively in many plant species including Arabidopsis thaliana, in which most of the enzymes participating in its biosynthesis were characterized. In the past 15 years, mutants and transgenic plants affected in the jasmonate pathway became available in rice and facilitate studies on the functions of this hormone in an important crop. Those functions are partially conserved compared to other plant species, and include roles in fertility, response to mechanical wounding and defense against herbivores. However, new and surprising functions have also been uncovered by mutant approaches, such as a close link between light perception and the jasmonate pathway. This was not only useful to show a phenomenon that is unique to rice but also helped to establish this role in plant species where such links are less obvious. This review aims to provide an overview of currently available rice mutants and transgenic plants in the jasmonate pathway and highlights some selected roles of jasmonate in this species, such as photomorphogenesis, and abiotic and biotic stress. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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661 KiB  
Review
Beyond the Canon: Within-Plant and Population-Level Heterogeneity in Jasmonate Signaling Engaged by Plant-Insect Interactions
by Dapeng Li, Ian T. Baldwin and Emmanuel Gaquerel
Plants 2016, 5(1), 14; https://doi.org/10.3390/plants5010014 - 16 Mar 2016
Cited by 10 | Viewed by 6597
Abstract
Plants have evolved sophisticated communication and defense systems with which they interact with insects. Jasmonates are synthesized from the oxylipin pathway and act as pivotal cellular orchestrators of many of the metabolic and physiological processes that mediate these interactions. Many of these jasmonate-dependent [...] Read more.
Plants have evolved sophisticated communication and defense systems with which they interact with insects. Jasmonates are synthesized from the oxylipin pathway and act as pivotal cellular orchestrators of many of the metabolic and physiological processes that mediate these interactions. Many of these jasmonate-dependent responses are tissue-specific and translate from modulations of the canonical jasmonate signaling pathway. Here we provide a short overview of within-plant heterogeneities in jasmonate signaling and dependent responses in the context of plant-insect interactions as illuminated by examples from recent work with the ecological model, Nicotiana attenuata. We then discuss means of manipulating jasmonate signaling by creating tissue-specific jasmonate sinks, and the micrografting of different transgenic plants. The metabolic phenotyping of these manipulations provides an integrative understanding of the functional significance of deviations from the canonical model of this hormonal pathway. Additionally, natural variation in jasmonate biosynthesis and signaling both among and within species can explain polymorphisms in resistance to insects in nature. In this respect, insect-guided explorations of population-level variations in jasmonate metabolism have revealed more complexity than previously realized and we discuss how different “omic” techniques can be used to exploit the natural variation that occurs in this important signaling pathway. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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572 KiB  
Review
How Microbes Twist Jasmonate Signaling around Their Little Fingers
by Selena Gimenez-Ibanez, Andrea Chini and Roberto Solano
Plants 2016, 5(1), 9; https://doi.org/10.3390/plants5010009 - 19 Jan 2016
Cited by 60 | Viewed by 9249
Abstract
Plant immunity relies on a complex network of hormone signaling pathways in which jasmonic acid (JA) plays a central role. Successful microbial pathogens or symbionts have developed strategies to manipulate plant hormone signaling pathways to cause hormonal imbalances for their own benefit. These [...] Read more.
Plant immunity relies on a complex network of hormone signaling pathways in which jasmonic acid (JA) plays a central role. Successful microbial pathogens or symbionts have developed strategies to manipulate plant hormone signaling pathways to cause hormonal imbalances for their own benefit. These strategies include the production of plant hormones, phytohormone mimics, or effector proteins that target host components to disrupt hormonal signaling pathways and enhance virulence. Here, we describe the molecular details of the most recent and best-characterized examples of specific JA hormonal manipulation by microbes, which exemplify the ingenious ways by which pathogens can take control over the plant’s hormone signaling network to suppress host immunity. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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740 KiB  
Review
Control of Carbon Assimilation and Partitioning by Jasmonate: An Accounting of Growth–Defense Tradeoffs
by Nathan E. Havko, Ian T. Major, Jeremy B. Jewell, Elham Attaran, John Browse and Gregg A. Howe
Plants 2016, 5(1), 7; https://doi.org/10.3390/plants5010007 - 15 Jan 2016
Cited by 79 | Viewed by 10911
Abstract
Plant growth is often constrained by the limited availability of resources in the microenvironment. Despite the continuous threat of attack from insect herbivores and pathogens, investment in defense represents a lost opportunity to expand photosynthetic capacity in leaves and absorption of nutrients and [...] Read more.
Plant growth is often constrained by the limited availability of resources in the microenvironment. Despite the continuous threat of attack from insect herbivores and pathogens, investment in defense represents a lost opportunity to expand photosynthetic capacity in leaves and absorption of nutrients and water by roots. To mitigate the metabolic expenditure on defense, plants have evolved inducible defense strategies. The plant hormone jasmonate (JA) is a key regulator of many inducible defenses. Synthesis of JA in response to perceived danger leads to the deployment of a variety of defensive structures and compounds, along with a potent inhibition of growth. Genetic studies have established an important role for JA in mediating tradeoffs between growth and defense. However, several gaps remain in understanding of how JA signaling inhibits growth, either through direct transcriptional control of JA-response genes or crosstalk with other signaling pathways. Here, we highlight recent progress in uncovering the role of JA in controlling growth-defense balance and its relationship to resource acquisition and allocation. We also discuss tradeoffs in the context of the ability of JA to promote increased leaf mass per area (LMA), which is a key indicator of leaf construction costs and leaf life span. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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1568 KiB  
Review
The Ubiquitin System and Jasmonate Signaling
by Astrid Nagels Durand, Laurens Pauwels and Alain Goossens
Plants 2016, 5(1), 6; https://doi.org/10.3390/plants5010006 - 09 Jan 2016
Cited by 40 | Viewed by 9345
Abstract
The ubiquitin (Ub) system is involved in most, if not all, biological processes in eukaryotes. The major specificity determinants of this system are the E3 ligases, which bind and ubiquitinate specific sets of proteins and are thereby responsible for target recruitment to the [...] Read more.
The ubiquitin (Ub) system is involved in most, if not all, biological processes in eukaryotes. The major specificity determinants of this system are the E3 ligases, which bind and ubiquitinate specific sets of proteins and are thereby responsible for target recruitment to the proteasome or other cellular processing machineries. The Ub system contributes to the regulation of the production, perception and signal transduction of plant hormones. Jasmonic acid (JA) and its derivatives, known as jasmonates (JAs), act as signaling compounds regulating plant development and plant responses to various biotic and abiotic stress conditions. We provide here an overview of the current understanding of the Ub system involved in JA signaling. Full article
(This article belongs to the Special Issue The Jasmonate Pathway)
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