The Jasmonate Pathway: New Actors, Mechanisms and Impacts

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (30 June 2019) | Viewed by 35169

Special Issue Editor

IBMP-CNRS, Université de Strasbourg, 67000 Strasbourg, France
Interests: Arabidopsis; rice; jasmonate metabolism; signaling regulation; plant defense

Special Issue Information

Dear Colleagues,

Jasmonates (JAs) define a multifaceted hormonal pathway that shapes numerous aspects of plant development, reproduction, and adaptation to environmental challenges. Since the successful 2015 Special Issue on “The Jasmonate Pathway” in Plants, research on JAs has remained extremely active and formerly emerging questions have attracted the spotlight and become major issues. Historically, JA synthesis and action was associated with plant responses to wounding/herbivory or necrotrophic microbial pathogens, and the range of defense responses and specialized metabolites under JA control is still expanding, particularly in crop species or plant providing health benefits. Interactions with other hormonal pathways are also being better understood, and the importance of JA signaling in the chemical interaction with rhizosphere microorganisms is increasingly established. Importantly, new exciting genetic and chemical approaches now allow to disentangle the mechanisms underlying conserved growth–defense tradeoffs and constitute promising tools to optimize plant adaptation to environmental stress while maintaining high biomass and yields. Furthermore, renewed interest in JA metabolism itself revealed new nodes of signaling regulation and disclosed unexpected modification steps. Finally, recent investigations of the JA pathway in early land plants has provided unprecedented understanding of the key features in pathway evolution and may guide future research directions.

The present Special Issue invites authors in the field to contribute review and research articles on new actors, mechanisms and impacts on the JA pathway in a diversity of plant species or even microorganisms. Topics include, but are not limited to, jasmonate metabolism and targeted modifications, perception, cellular and long-distance signaling mechanisms, hormonal crosstalk, roles in biotic and abiotic stress adaptation, growth inhibition, induction of specialized metabolism, beneficial interactions, reproduction, evolution. Epigenetic aspects of JA regulation are also welcome.

Dr. Thierry Heitz
Guest Editor

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Keywords

  • Jasmonic acid, JA-Ile
  • Jasmonate metabolism
  • Signaling pathway evolution
  • Structure–function
  • Hormonal interactions
  • Growth–defense tradeoff
  • Plant adaptation and immunity

Published Papers (8 papers)

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Research

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12 pages, 1534 KiB  
Article
Induction of Jasmonoyl-Isoleucine (JA-Ile)-Dependent JASMONATE ZIM-DOMAIN (JAZ) Genes in NaCl-Treated Arabidopsis thaliana Roots Can Occur at Very Low JA-Ile Levels and in the Absence of the JA/JA-Ile Transporter JAT1/AtABCG16
by Corinna Thurow, Markus Krischke, Martin J. Mueller and Christiane Gatz
Plants 2020, 9(12), 1635; https://doi.org/10.3390/plants9121635 - 24 Nov 2020
Cited by 5 | Viewed by 3047
Abstract
The plant hormone jasmonoyl-isoleucine (JA-Ile) is an important regulator of plant growth and defense in response to various biotic and abiotic stress cues. Under our experimental conditions, JA-Ile levels increased approximately seven-fold in NaCl-treated Arabidopsis thaliana roots. Although these levels were around 1000-fold [...] Read more.
The plant hormone jasmonoyl-isoleucine (JA-Ile) is an important regulator of plant growth and defense in response to various biotic and abiotic stress cues. Under our experimental conditions, JA-Ile levels increased approximately seven-fold in NaCl-treated Arabidopsis thaliana roots. Although these levels were around 1000-fold lower than in wounded leaves, genes of the JA-Ile signaling pathway were induced by a factor of 100 or more. Induction was severely compromised in plants lacking the JA-Ile receptor CORONATINE INSENSITIVE 1 or enzymes required for JA-Ile biosynthesis. To explain efficient gene expression at very low JA-Ile levels, we hypothesized that salt-induced expression of the JA/JA-Ile transporter JAT1/AtABCG16 would lead to increased nuclear levels of JA-Ile. However, mutant plants with different jat1 alleles were similar to wild-type ones with respect to salt-induced gene expression. The mechanism that allows COI1-dependent gene expression at very low JA-Ile levels remains to be elucidated. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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14 pages, 1794 KiB  
Article
Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway
by Nathan E. Havko, George Kapali, Michael R. Das and Gregg A. Howe
Plants 2020, 9(2), 172; https://doi.org/10.3390/plants9020172 - 01 Feb 2020
Cited by 10 | Viewed by 3815
Abstract
Rising global temperatures are associated with increases in the geographic range, population size, and feeding voracity of insect herbivores. Although it is well established that the plant hormone jasmonate (JA) promotes durable resistance to many ectothermic herbivores, little is known about how JA-mediated [...] Read more.
Rising global temperatures are associated with increases in the geographic range, population size, and feeding voracity of insect herbivores. Although it is well established that the plant hormone jasmonate (JA) promotes durable resistance to many ectothermic herbivores, little is known about how JA-mediated defense is influenced by rising temperatures. Here, we used the Arabidopsis-Trichoplusia ni (cabbage looper) interaction to investigate the relative contribution of JA and elevated temperature to host resistance. Video monitoring of T. ni larval behavior showed that elevated temperature greatly enhanced defoliation by increasing the bite rate and total time spent feeding, whereas loss of resistance in a JA-deficient mutant did not strongly affect these behaviors. The acceleration of insect feeding at elevated temperature was not attributed to decreases in wound-induced JA biosynthesis, expression of JA-responsive genes, or the accumulation of defensive glucosinolates prior to insect challenge. Quantitative proteomic analysis of insect frass, however, provided evidence for a temperature-dependent increase in the production of T. ni digestive enzymes. Our results demonstrate that temperature-driven stimulation of T. ni feeding outweighs the protective effects of JA-mediated resistance in Arabidopsis, thus highlighting a potential threat to plant resilience in a warming world. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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19 pages, 4021 KiB  
Article
SpitWorm, a Herbivorous Robot: Mechanical Leaf Wounding with Simultaneous Application of Salivary Components
by Guanjun Li, Stefan Bartram, Huijuan Guo, Axel Mithöfer, Maritta Kunert and Wilhelm Boland
Plants 2019, 8(9), 318; https://doi.org/10.3390/plants8090318 - 31 Aug 2019
Cited by 11 | Viewed by 3253
Abstract
Induction of jasmonate-mediated plant defense against insect herbivory is initiated by a combination of both mechanical wounding and chemical factors. In order to study both effects independently on plant defense induction, SpitWorm, a computer-controlled device which mimics the damage pattern of feeding insect [...] Read more.
Induction of jasmonate-mediated plant defense against insect herbivory is initiated by a combination of both mechanical wounding and chemical factors. In order to study both effects independently on plant defense induction, SpitWorm, a computer-controlled device which mimics the damage pattern of feeding insect larvae on leaves and, in addition, can apply oral secretions (OS) or other solutions to the ‘biting site’ during ‘feeding,’ was developed and evaluated. The amount of OS left by a Spodoptera littoralis larva during feeding on Phaseolus lunatus (lima bean) leaves was estimated by combining larval foregut volume, biting rate, and quantification of a fluorescent dye injected into the larvae’s foregut prior to feeding. For providing OS amounts by SpitWorm equivalent to larval feeding, dilution and delivery rate were optimized. The effectiveness of SpitWorm was tested by comparing volatile organic compounds (VOC) emissions of P. lunatus leaves treated with either SpitWorm, MecWorm, or S. littoralis larvae. Identification and quantification of emitted VOCs revealed that SpitWorm induced a volatile bouquet that is qualitatively and quantitatively similar to herbivory. Additionally, RT-qPCR of four jasmonic acid responsive genes showed that SpitWorm, in contrast to MecWorm, induces the same regulation pattern as insect feeding. Thus, SpitWorm mimics insect herbivory almost identically to real larvae feeding. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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14 pages, 1988 KiB  
Article
Effects of Jasmonate on Ethylene Function during the Development of Tomato Stamens
by Ramona Schubert, Stephan Grunewald, Lea von Sivers and Bettina Hause
Plants 2019, 8(8), 277; https://doi.org/10.3390/plants8080277 - 09 Aug 2019
Cited by 10 | Viewed by 3492
Abstract
The phenotype of the tomato mutant jasmonate-insensitive1-1 (jai1-1) mutated in the JA-Ile co-receptor COI1 demonstrates JA function in flower development, since it is female-sterile. In addition, jai1-1 exhibits a premature anther dehydration and pollen release, being in contrast to a delayed [...] Read more.
The phenotype of the tomato mutant jasmonate-insensitive1-1 (jai1-1) mutated in the JA-Ile co-receptor COI1 demonstrates JA function in flower development, since it is female-sterile. In addition, jai1-1 exhibits a premature anther dehydration and pollen release, being in contrast to a delayed anther dehiscence in the JA-insensitive Arabidopsis mutant coi1-1. The double mutant jai1-1 Never ripe (jai1-1 Nr), which is in addition insensitive to ethylene (ET), showed a rescue of the jai1-1 phenotype regarding pollen release. This suggests that JA inhibits a premature rise in ET to prevent premature stamen desiccation. To elucidate the interplay of JA and ET in more detail, stamen development in jai1-1 Nr was compared to wild type, jai1-1 and Nr regarding water content, pollen vitality, hormone levels, and accumulation of phenylpropanoids and transcripts encoding known JA- and ET-regulated genes. For the latter, RT-qPCR based on nanofluidic arrays was employed. The data showed that additional prominent phenotypic features of jai1-1, such as diminished water content and pollen vitality, and accumulation of phenylpropanoids were at least partially rescued by the ET-insensitivity. Hormone levels and accumulation of transcripts were not affected. The data revealed that strictly JA-regulated processes cannot be rescued by ET-insensitivity, thereby emphasizing a rather minor role of ET in JA-regulated stamen development. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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21 pages, 4784 KiB  
Article
Genome-Wide Identification and Characterization of JAZ Protein Family in Two Petunia Progenitors
by Shaoze Tian, Siyu Liu, Yu Wang, Kun Wang, Chaoqun Yin, Yuanzheng Yue and Huirong Hu
Plants 2019, 8(7), 203; https://doi.org/10.3390/plants8070203 - 03 Jul 2019
Cited by 9 | Viewed by 4066
Abstract
Jasmonate ZIM-domain (JAZ) family proteins are the key repressors in the jasmonate signaling pathway and play crucial roles in plant development, defenses, and responses to stresses. However, our knowledge about the JAZ protein family in petunia is limited. This research respectively identified 12 [...] Read more.
Jasmonate ZIM-domain (JAZ) family proteins are the key repressors in the jasmonate signaling pathway and play crucial roles in plant development, defenses, and responses to stresses. However, our knowledge about the JAZ protein family in petunia is limited. This research respectively identified 12 and 16 JAZ proteins in two Petunia progenitors, Petunia axillaris and Petunia inflata. Phylogenetic analysis showed that the 28 proteins could be divided into four groups (Groups A–D) and further classified into six subgroups (A1, A2, B1, B3, C, and D1); members in the same subgroup shared some similarities in motif composition and sequence structure. The Ka/Ks ratios of seven paralogous pairs were less than one, suggesting the petunia JAZ family might have principally undergone purifying selection. Quantitative real-time PCR (qRT-PCR) analysis revealed that PaJAZ genes presented differential expression patterns during the development of flower bud and anther in petunia, and the expression of PaJAZ5, 9, 12 genes was generally up-regulated after MeJA treatment. Subcellular localization assays demonstrated that proteins PaJAZ5, 9, 12 were localized in nucleus. Yeast two hybrid (Y2H) elucidated most PaJAZ proteins (PaJAZ1-7, 9, 12) might interact with transcription factor MYC2. This study provides insights for further investigation of functional analysis in petunia JAZ family proteins. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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Review

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19 pages, 1835 KiB  
Review
Jasmonates—the Master Regulator of Rice Development, Adaptation and Defense
by Hieu Trang Nguyen, Huong Thi Mai To, Michel Lebrun, Stephane Bellafiore and Antony Champion
Plants 2019, 8(9), 339; https://doi.org/10.3390/plants8090339 - 09 Sep 2019
Cited by 38 | Viewed by 7101
Abstract
Rice is one of the most important food crops worldwide, as well as the model plant in molecular studies on the cereals group. Many different biotic and abiotic agents often limit rice production and threaten food security. Understanding the molecular mechanism, by which [...] Read more.
Rice is one of the most important food crops worldwide, as well as the model plant in molecular studies on the cereals group. Many different biotic and abiotic agents often limit rice production and threaten food security. Understanding the molecular mechanism, by which the rice plant reacts and resists these constraints, is the key to improving rice production to meet the demand of an increasing population. The phytohormone jasmonic acid (JA) and related compounds, collectively called jasmonates, are key regulators in plant growth and development. They are also one of the central players in plant immunity against biotic attacks and adaptation to unfavorable environmental conditions. Here, we review the most recent knowledge about jasmonates signaling in the rice crop model. We highlight the functions of jasmonates signaling in many adaptive responses, and also in rice growth and development processes. We also draw special attention to different signaling modules that are controlled by jasmonates in rice. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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11 pages, 944 KiB  
Review
Arabidopsis Flowers Unlocked the Mechanism of Jasmonate Signaling
by John Browse and James G. Wallis
Plants 2019, 8(8), 285; https://doi.org/10.3390/plants8080285 - 14 Aug 2019
Cited by 22 | Viewed by 5128
Abstract
The Arabidopsis male-sterile phenotype has been a wonderful model for jasmonate action in plants. It has allowed us to identify transcription factors that control gene expression during stamen and pollen maturation and provided for the discovery of the JAZ repressor proteins and the [...] Read more.
The Arabidopsis male-sterile phenotype has been a wonderful model for jasmonate action in plants. It has allowed us to identify transcription factors that control gene expression during stamen and pollen maturation and provided for the discovery of the JAZ repressor proteins and the mechanism of jasmonate signaling. More recently, it has revealed intriguing details of the spatial localization of jasmonate synthesis and perception in stamen tissues. The extensive and thoughtful application of protein–protein interaction assays to identify JAZ-interacting partners has led to a much richer appreciation of the mechanisms by which jasmonate integrates with the actions of other hormones to regulate plant growth and physiological responses. This integration is strikingly evident in stamen and pollen development in Arabidopsis, which requires the actions of many hormones. Just as importantly, it is now evident that jasmonate has very different actions during flower development and reproduction in other plant species. This integration and diversity of action indicates that many exciting discoveries remain to be made in this area of jasmonate hormone signaling and response. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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14 pages, 1344 KiB  
Review
Circadian Network Interactions with Jasmonate Signaling and Defense
by Bryan Thines, Emily V. Parlan and Elena C. Fulton
Plants 2019, 8(8), 252; https://doi.org/10.3390/plants8080252 - 28 Jul 2019
Cited by 9 | Viewed by 4564
Abstract
Plants experience specific stresses at particular, but predictable, times of the day. The circadian clock is a molecular oscillator that increases plant survival by timing internal processes to optimally match these environmental challenges. Clock regulation of jasmonic acid (JA) action is important for [...] Read more.
Plants experience specific stresses at particular, but predictable, times of the day. The circadian clock is a molecular oscillator that increases plant survival by timing internal processes to optimally match these environmental challenges. Clock regulation of jasmonic acid (JA) action is important for effective defenses against fungal pathogens and generalist herbivores in multiple plant species. Endogenous JA levels are rhythmic and under clock control with peak JA abundance during the day, a time when plants are more likely to experience certain types of biotic stresses. The expression of many JA biosynthesis, signaling, and response genes is transcriptionally controlled by the clock and timed through direct connections with core clock proteins. For example, the promoter of Arabidopsis transcription factor MYC2, a master regulator for JA signaling, is directly bound by the clock evening complex (EC) to negatively affect JA processes, including leaf senescence, at the end of the day. Also, tobacco ZEITLUPE, a circadian photoreceptor, binds directly to JAZ proteins and stimulates their degradation with resulting effects on JA root-based defenses. Collectively, a model where JA processes are embedded within the circadian network at multiple levels is emerging, and these connections to the circadian network suggest multiple avenues for future research. Full article
(This article belongs to the Special Issue The Jasmonate Pathway: New Actors, Mechanisms and Impacts)
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