Oxylipins form a steadily growing group of signaling molecules that comprise oxygenated fatty acids and metabolites derived therefrom that can be found in all kingdoms of life. Prokaryotic organisms such as cyanobacteria form only simple oxylipin molecules, typically arising from only one or two metabolic steps, whereas eukaryotic organisms such as plants have evolved complex pathways leading to hundreds of different molecules (Wasternack and Feussner 2018). The most renowned and heavily studied oxylipins are indisputably the animal prostaglandins and the plant jasmonates (JAs).
In June 2009, Ted Farmer organized an international symposium on regulatory oxylipins at the University of Lausanne (Switzerland). The main focus of that symposium was on oxylipin discovery and signaling and the biology of nonenzymatic lipid oxidation in whole-organism responses to stress. Those days, the field was greatly marked by the fresh discovery of the JAZ repressor proteins as the direct targets of the JA receptor SCFCOI1 E3 ubiquitin ligase, which revealed the long-sought missing link in JA signaling (Browse 2009). Nonetheless, the oxylipin research presented at the 2009 symposium was not limited to JAs and signaling; on the contrary, it covered research on the identification of structurally diverse oxylipins in a wide variety of plant and nonplant species.
Ten years later, the understanding of biosynthesis, metabolism, perception and action of oxylipins has dramatically improved, especially that of land plant JAs. By 2019, this was further reinforced at the international meeting on Regulatory Oxylipins held at the VIB-Ghent University in Ghent, Belgium, and organized by Alain Goossens and Ted Farmer (Fig. 1). Rather unintentionally, it was evidenced that JAs have formed the focal point of plant oxylipin research; however, the diversity in JA research has dramatically increased. Indeed, during the conference, the debate arose as to which and how many JA derivatives may actually be bioactive (see the session on ‘Biochemistry and structural biology’). Similarly, the number of model species for plant oxylipin research is increasing rapidly and is now spanning the entire land plant kingdom—from the ancient liverworts to the classic model Arabidopsis thaliana and many major crops (see the session on ‘Regulatory oxylipins in emerging model systems’). Finally, although the role of the JA pathway in the control of one of the major limbs of the plant defense system is becoming further substantiated, it stands beyond doubt that JA can no longer be considered as ‘only’ a stress hormone. Indeed, more and more unexpected roles for JAs in all kinds of plant cellular processes are being revealed, including metabolism, growth, development and multiple forms of interaction with the environment (see the sessions on ‘Control of growth and defence’ and ‘Control of metabolism, reproduction, and ecology’). Accordingly, our deciphering of the molecular mechanisms and signaling cascades that steer these processes is reaching unprecedented levels of detail (see the session on ‘Jasmonate signalling mechanisms and long-distance signalling’), which can be exemplary for other phytohormones that have been studied longer and more extensively. Because of these collective assets, the JA community is clearly expanding and includes vibrant research from groups that have not necessarily started with JA as the focal point but rather serendipitously ‘bumped’ into this inevitable and crucial phytohormone. We were extremely pleased to note that the group of more established JA researchers, several of whom also attended the 2009 symposium, has been complemented by a versatile and energetic group of new (younger) faces.
A group photograph taken in front of the Aula of Ghent University in Belgium.
Below we provide an overview of the seminars given by our (keynote) speakers. For more details, we invite you to consult the already published papers of the speakers, and obviously keep an eye out for the many others that will hopefully be published soon, from which we were privileged to get a sneak preview.
Regulatory Oxylipins in Emerging Plant Model Systems
In contrast to the 2009 meeting in Lausanne, nonplant systems were not touched upon in the Regulatory Oxylipins 2019 meeting in Ghent. However, the range of species spanning the plant kingdom has greatly expanded this past decade. The power of including ancestral land plants in the study of oxylipin signaling was brilliantly illustrated by our opening keynote speaker, Roberto Solano (Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Spain), who has started including the liverwort Marchantia polymorpha, in addition to A. thaliana, in his research. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways (Fig. 2A), which has allowed the identification of the ancestral bioactive JA ligand and clarification of the phylogenetic history and role of JA signaling proteins in plant defense, growth and development (Fig. 2B, C; Monte et al. 2018, Monte et al. 2019). Similarly, Christiane Gatz (Georg-August-University Göttingen, Germany) presented the work of her group on COI1 proteins from leptosporangiate and eusporangiate ferns (horsetails) and their distinct capacities to mediate gene expression dependent on JA-Ile or other oxylipins.
Oxylipin signaling in model systems: the ‘new’ kid on the block, Marchantia polymorpha, vs. the ‘old’ lady, Arabidopsis thaliana. (A) Conservation of the JA signaling pathway with a minimal set of components in the plant kingdom. Shown are gene counts for JA signaling components in A. thaliana, M. polymorpha and other plant model species (courtesy of Roberto Solano). (B) M. polymorpha gemmaling expressing a GFP-tagged MpJAZ protein. The inset shows the ligands of MpCOI1, which are two isomeric forms of the JA-Ile precursor dinor-OPDA, i.e. dinor-cis-OPDA (left) and dinor-iso-OPDA (right) (Monte et al. 2018). (C) Arabidopsis thaliana roots expressing a GFP-tagged AtJAZ1 protein. The inset shows the ligand of AtCOI1, which is (+)-7-iso-jasmonoyl-l-isoleucine (Fonseca et al. 2009).
Biochemistry and Structural Biology
In a series of invited and selected talks, Abraham Koo (University of Missouri, Columbia, SC, USA), Alexander Grechkin (Kazan Scientific Centre of Russian Academy of Sciences, Russia), Thierry Heitz (University of Strasbourg, France) and Lotte Caarls (Wageningen University, The Netherlands) presented their research on the numerous derivatives of JA and JA-Ile that plants can synthesize, particularly using A. thaliana as a model (e.g. Caarls et al. 2017). The enzymes involved in their biosynthesis and the potential role of these metabolites in different cellular processes, such as wound response and immunity, were discussed. Thierry Heitz also provided a good overview of this topic in his mini-review that features in this special issue, entitled ‘When JA-Ile levels do not dictate jasmonate signalling’ (see Heitz et al. 2019).
JA Signaling Mechanisms and Control of Growth, Defense and Metabolism
Inevitably, a session of the Regulatory Oxylipins 2019 meeting was devoted to signaling. Katayoon Dehesh (Institute for Integrative Genome Biology, USA) gave an inspiring talk about the interplay between oxylipin and retrograde signaling, which is also covered in the review by Savchenko et al. (2019; in this issue). Chuanyou Li (University of Chinese Academy of Sciences, Beijing, China), who has focused much work on transcriptional regulation (e.g. An et al. 2017), provided an impressive in-depth view on the transcriptional machineries involved in JA signaling in Arabidopsis and tomato (Solanum lycopersicum), comprising among others the well-studied MYC2, MED25 and COI1 proteins as well as some newly identified and less characterized transcription factors (TFs). Several of these factors have also been found to be involved in the touch response in Arabidopsis, as presented by Olivier Van Aken (Lund University, Sweden). Similarly, Andrej Pavlovič (Palacký University Olomouc, Czech Republic) showed that the touch response, as a mimic of prey capture, in the carnivorous Venus Flytrap (Dionaea muscipula) is also dependent on JA signaling (e.g. Pavlovič et al. 2017). Intriguingly, Andrej also demonstrated that the prey capture response could be abolished by anesthetic agents.
Signaling was also obviously addressed in the sessions on ‘control of growth and defense’ and ‘control of metabolism’ but then more particularly framed within the control of these cellular processes. Daoxin Xie (Tsinghua University, China) elaborated on the molecular basis of JA-regulated plant defense against insect attack, further elucidating the roles of COI1 and the JAZ8–JAV1–WRKY51 complexes (Yan et al. 2018). Debora Gasperini (Leibniz Institute of Plant Biochemistry, Halle, Germany) presented her work on how damage to cell walls triggers JA production, including a promising suppressor screen of the Arabidopsis korrigan cellulase mutant. This theme is further explored in the review by Mielke and Gasperini (2019; in this issue), in which they provide a detailed insight into cell wall-derived damage signals and discuss how they affect JA biosynthesis as well as future prospects in this fascinating area of research. Gregg Howe (Michigan State University, USA) presented his impressive work on the higher order jaz mutants to demonstrate that the JAZ proteins act at the nexus of growth, defense and metabolism (e.g. Guo et al. 2018). Karsten Melcher (Van Andel Research Institute, USA) showed how well-designed structural biology reveals astonishingly detailed molecular insights into the structural basis of JAZ-mediated gene repression in JA signaling, as evidenced by the crystal structures of (truncated) MYC, JAZ, TOPLESS and NINJA proteins. Knowledge gained by studies of JA perception and signaling in Arabidopsis allowed Minoru Ueda (Tohoku University, Japan) to rationally design JAZ subtype-selective agonists of the COI1-JAZ coreceptor, allowing him to uncouple the JA-modulated defense response from the growth arrest. In-depth RNA-Seq analysis of wild-type Arabidopsis plants exogenously treated with JA either in combination with or without salicylic or abscisic acid by Saskia Van der Wees (Utrecht University, The Netherlands) revealed the involvement of new TFs in hitherto undisclosed aspects of JA signaling. This was further supported by work from Ikram Blilou’s group (KAUST, Saudi Arabia) on RNA-Seq analyses of Arabidopsis mutants for the so-called BIRD proteins, which are plant-specific TFs with multiple roles in plant development and physiology.
Lastly, there were two plenary talks on the control of metabolism. The first talk, by Daniel Kliebenstein (UC Davis, USA), with the captivating title ‘Destroying the hierarchy; when the regulated are the regulators’, questioned the concept of ‘the master regulator TF’ by demonstrating that Arabidopsis glucosinolate metabolism is likely controlled by several hundred TFs. The second talk, by Xiao-Ya Chen (Shanghai Institutes for Biological Sciences, China), focused on the transcriptional regulation of gossypol biosynthesis in the trichomes of cotton (Gossypium hirsutum). In this issue, Chen et al. (2019) further discuss how JA signaling impacts on specialized metabolism in plants.
Ecology
JA signaling in a context that represents the complex environment more closely was addressed in the Ecology session. Ian Baldwin (Max Planck Institute for Chemical Ecology, Jena, Germany) gave a thrilling talk on JA signaling as ‘infochemicals’ and mediators of (insect) resistance in nature, in which he presented some of his field work with the native tobacco species Nicotiana attenuata in the Great Basin Desert of Utah and the creation of his pièce de résistance: the MAGIC collection. Corné Pieterse (Utrecht University, The Netherlands) focused on underground events, by elaborating on his research on induced systemic resistance triggered in Arabidopsis by beneficial microbes. Finally, Carlos Ballaré (University of Buenos Aires & San Martin National University, Argentina) talked about the light regulation of JA metabolism and signaling in Arabidopsis (e.g. Cerrudo et al. 2017), which occurs when plants detect and respond to the proximity of competitors using light signals perceived by photoreceptor proteins.
Reproduction
The last session of the meeting concentrated on reproduction. Bettina Hause (Leibniz Institute of Plant Biochemistry, Halle, Germany) talked about the role of JAs in tomato flower development (e.g. Schubert et al. 2019), whereas Ivan Acosta (Max Planck Institute for Plant Breeding Research, Cologne, Germany) discussed the spatiotemporal dynamics of JA signaling during stamen maturation in Arabidopsis. Finally, the meeting was closed by John Browse (Washington State University, USA), with a marvelously titled seminar of ‘Sex and the single hormone’, in which he gave a magnificent overview of his research on the role of JAs and the JA receptor COI1 in the regulation of male fertility in Arabidopsis and other plants (e.g. Jewell and Browse 2016). More information on this topic can also be found in this special issue, where Ivan Acosta discusses ‘Jasmonate signalling during Arabidopsis stamen maturation’ (Acosta and Przybyl 2019).
Funding
Organization of the Regulatory Oxylipins 2019 meeting was sponsored by the Facultaire Commissie voor Wetenschappelijk Onderzoek from Ghent University and the journals Plant and Cell Physiology, The Journal of Experimental Botany, The Plant Journal and The Plant Cell.
Acknowledgments
The organizers wish to thank all of their group members as well as all other staff for helping to deliver an exciting conference both socially and scientifically. We thank Roberto Solano for kindly providing images for Fig. 2.
Disclosures
The authors have no conflicts of interest to declare.
