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Publikationen - Molekulare Signalverarbeitung

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Preprints

Brunoni, F.; Široká, J.; Mik, V.; Pospíšil, T.; Kralová, M.; Ament, A.; Pernisová, M.; Karady, M.; Htitich, M.; Ueda, M.; Floková, K.; Wasternack, C.; Strnad, M.; Novák, O.; Conjugation ofcis-OPDA with amino acids is a conserved pathway affectingcis-OPDA homeostasis upon stress responses (2023) DOI: 10.1101/2023.07.18.549545

Jasmonates (JAs) are a family of oxylipin phytohormones regulating plant development and growth and mediating ‘defense versus growth’ responses. The upstream JA biosynthetic precursor cis-(+)-12-oxo-phytodienoic acid (cis-OPDA) has been reported to act independently of the COI1-mediated JA signaling in several stress-induced and developmental processes. However, its means of perception and metabolism are only partially understood. Furthermore, cis-OPDA, but not JA, occurs in non-vascular plant species, such as bryophytes, exhibiting specific functions in defense and development. A few years ago, a low abundant isoleucine analog of the biologically active JA-Ile, OPDA-Ile, was detected in wounded leaves of flowering plants, opening up to the possibility that conjugation of cis-OPDA to amino acids might be a relevant mechanism for cis-OPDA regulation. Here, we extended the analysis of amino acid conjugates of cis-OPDA and identified naturally occurring OPDA-Val, OPDA-Phe, OPDA-Ala, OPDA-Glu, and OPDA-Asp in response to biotic and abiotic stress in Arabidopsis. The newly identified OPDA-amino acid conjugates show cis-OPDA-related plant responses in a JAR1-dependent manner. We also discovered that the synthesis and hydrolysis of cis-OPDA amino acid conjugates are regulated by members of the amidosynthetase GH3 and the amidohydrolase ILR1/ILL families. Finally, we found that the cis-OPDA conjugative pathway already functions in non-vascular plants and gymnosperms. Thus, one level of regulation by which plants modulate cis-OPDA homeostasis is the synthesis and hydrolysis of OPDA-amino acid conjugates, which temporarily store cis-OPDA in stress responses.
Bücher und Buchkapitel

Wasternack, C.; Jasmonates: Synthesis, Metabolism, Signal Transduction and Action (2016) DOI: 10.1002/9780470015902.a0020138.pub2

Jasmonic acid and other fatty‐acid‐derived compounds called oxylipins are signals in stress responses and development of plants. The receptor complex, signal transduction components as well as repressors and activators in jasmonate‐induced gene expression have been elucidated. Different regulatory levels and cross‐talk with other hormones are responsible for the multiplicity of plant responses to environmental and developmental cues.
Publikation

Bosch, M.; Wright, L. P.; Gershenzon, J.; Wasternack, C.; Hause, B.; Schaller, A.; Stintzi, A.; Jasmonic Acid and Its Precursor 12-Oxophytodienoic Acid Control Different Aspects of Constitutive and Induced Herbivore Defenses in Tomato Plant Physiol. 166, 396-410, (2014) DOI: 10.1104/pp.114.237388

The jasmonate family of growth regulators includes the isoleucine (Ile) conjugate of jasmonic acid (JA-Ile) and its biosynthetic precursor 12-oxophytodienoic acid (OPDA) as signaling molecules. To assess the relative contribution of JA/JA-Ile and OPDA to insect resistance in tomato (Solanum lycopersicum), we silenced the expression of OPDA reductase3 (OPR3) by RNA interference (RNAi). Consistent with a block in the biosynthetic pathway downstream of OPDA, OPR3-RNAi plants contained wild-type levels of OPDA but failed to accumulate JA or JA-Ile after wounding. JA/JA-Ile deficiency in OPR3-RNAi plants resulted in reduced trichome formation and impaired monoterpene and sesquiterpene production. The loss of these JA/JA-Ile -dependent defense traits rendered them more attractive to the specialist herbivore Manduca sexta with respect to feeding and oviposition. Oviposition preference resulted from reduced levels of repellant monoterpenes and sesquiterpenes. Feeding preference, on the other hand, was caused by increased production of cis-3-hexenal acting as a feeding stimulant for M. sexta larvae in OPR3-RNAi plants. Despite impaired constitutive defenses and increased palatability of OPR3-RNAi leaves, larval development was indistinguishable on OPR3-RNAi and wild-type plants, and was much delayed compared with development on the jasmonic acid-insensitive1 (jai1) mutant. Apparently, signaling through JAI1, the tomato ortholog of the ubiquitin ligase CORONATINE INSENSITIVE1 in Arabidopsis (Arabidopsis thaliana), is required for defense, whereas the conversion of OPDA to JA/JA-Ile is not. Comparing the signaling activities of OPDA and JA/JA-Ile, we found that OPDA can substitute for JA/JA-Ile in the local induction of defense gene expression, but the production of JA/JA-Ile is required for a systemic response.
Bücher und Buchkapitel

Wasternack, C.; Jasmonates in Plant Growth and Stress Responses (Tran, L.-S. P. & Pal, S., eds.). 221-263, (2014) ISBN: 978-1-4939-0491-4 DOI: 10.1007/978-1-4939-0491-4_8

Jasmonates are lipid-derived compounds which are signals in plant stress responses and development. They are synthesized in chloroplasts and peroxisomes. An endogenous rise occurs upon environmental stimuli or in distinct stages of development such as that of anthers and trichomes or in root growth. Hydroxylation, carboxylation, glucosylation, sulfation, methylation, or conjugation of jasmonic acid (JA) leads to numerous metabolites. Many of them are at least partially biologically inactive. The most bioactive JA is the (+)-7-iso-JA–isoleucine conjugate. Its perception takes place by the SCFCOI1-JAZ-co-receptor complex. At elevated levels of JAs, negative regulators such as JAZ, or JAV are subjected to proteasomal degradation, thereby allowing positively acting transcription factors of the MYC or MYB family to switch on JA-induced gene expression. In case of JAM negative regulation takes place by anatagonism to MYC2. JA and COI1 are dominant signals in gene expression after wounding or in response to necrotrophic pathogens. Cross-talk to salicylic acid, ethylene, auxin, and other hormones occurs. Growth is inhibited by JA, thereby counteracting the growth stimulation by gibberellic acid. Senescence, trichome formation, arbuscular mycorrhiza, and formation of many secondary metabolites are induced by jasmonates. Effects in cold acclimation; in intercropping; during response to herbivores, nematodes, or necrotrophic pathogens; in pre- and post-harvest; in crop quality control; and in biosynthesis of secondary compounds led to biotechnological and agricultural applications.
Publikation

Goetz, S.; Hellwege, A.; Stenzel, I.; Kutter, C.; Hauptmann, V.; Forner, S.; McCaig, B.; Hause, G.; Miersch, O.; Wasternack, C.; Hause, B.; Role of cis-12-Oxo-Phytodienoic Acid in Tomato Embryo Development Plant Physiol. 158, 1715-1727, (2012) DOI: 10.1104/pp.111.192658

Oxylipins including jasmonates are signaling compounds in plant growth, development, and responses to biotic and abiotic stresses. In Arabidopsis (Arabidopsis thaliana) most mutants affected in jasmonic acid (JA) biosynthesis and signaling are male sterile, whereas the JA-insensitive tomato (Solanum lycopersicum) mutant jai1 is female sterile. The diminished seed formation in jai1 together with the ovule-specific accumulation of the JA biosynthesis enzyme allene oxide cyclase (AOC), which correlates with elevated levels of JAs, suggest a role of oxylipins in tomato flower/seed development. Here, we show that 35S::SlAOC-RNAi lines with strongly reduced AOC in ovules exhibited reduced seed set similarly to the jai1 plants. Investigation of embryo development of wild-type tomato plants showed preferential occurrence of AOC promoter activity and AOC protein accumulation in the developing seed coat and the embryo, whereas 12-oxo-phytodienoic acid (OPDA) was the dominant oxylipin occurring nearly exclusively in the seed coat tissues. The OPDA- and JA-deficient mutant spr2 was delayed in embryo development and showed an increased programmed cell death in the developing seed coat and endosperm. In contrast, the mutant acx1a, which accumulates preferentially OPDA and residual amount of JA, developed embryos similar to the wild type, suggesting a role of OPDA in embryo development. Activity of the residual amount of JA in the acx1a mutant is highly improbable since the known reproductive phenotype of the JA-insensitive mutant jai1 could be rescued by wound-induced formation of OPDA. These data suggest a role of OPDA or an OPDA-related compound for proper embryo development possibly by regulating carbohydrate supply and detoxification.
Bücher und Buchkapitel

Wasternack, C.; Jasmonates in Stress, Growth, and Development 91-118, (2010) ISBN: 9783527628964 DOI: 10.1002/9783527628964.ch5

This chapter contains sections titled:IntroductionJA BiosynthesisJA MetabolismBound OPDA – ArabidopsidesMutants of JA Biosynthesis and SignalingCOI1–JAZ–JA‐Ile‐Mediated JA SignalingTranscription Factors Involved in JA SignalingJasmonates and Oxylipins in DevelopmentConclusionsAcknowledgmentsReferences
Publikation

Weigelt, K.; Küster, H.; Rutten, T.; Fait, A.; Fernie, A. R.; Miersch, O.; Wasternack, C.; Emery, R. J. N.; Desel, C.; Hosein, F.; Müller, M.; Saalbach, I.; Weber, H.; ADP-Glucose Pyrophosphorylase-Deficient Pea Embryos Reveal Specific Transcriptional and Metabolic Changes of Carbon-Nitrogen Metabolism and Stress Responses Plant Physiol. 149, 395-411, (2009) DOI: 10.1104/pp.108.129940

We present a comprehensive analysis of ADP-glucose pyrophosphorylase (AGP)-repressed pea (Pisum sativum) seeds using transcript and metabolite profiling to monitor the effects that reduced carbon flow into starch has on carbon-nitrogen metabolism and related pathways. Changed patterns of transcripts and metabolites suggest that AGP repression causes sugar accumulation and stimulates carbohydrate oxidation via glycolysis, tricarboxylic acid cycle, and mitochondrial respiration. Enhanced provision of precursors such as acetyl-coenzyme A and organic acids apparently support other pathways and activate amino acid and storage protein biosynthesis as well as pathways fed by cytosolic acetyl-coenzyme A, such as cysteine biosynthesis and fatty acid elongation/metabolism. As a consequence, the resulting higher nitrogen (N) demand depletes transient N storage pools, specifically asparagine and arginine, and leads to N limitation. Moreover, increased sugar accumulation appears to stimulate cytokinin-mediated cell proliferation pathways. In addition, the deregulation of starch biosynthesis resulted in indirect changes, such as increased mitochondrial metabolism and osmotic stress. The combined effect of these changes is an enhanced generation of reactive oxygen species coupled with an up-regulation of energy-dissipating, reactive oxygen species protection, and defense genes. Transcriptional activation of mitogen-activated protein kinase pathways and oxylipin synthesis indicates an additional activation of stress signaling pathways. AGP-repressed embryos contain higher levels of jasmonate derivatives; however, this increase is preferentially in nonactive forms. The results suggest that, although metabolic/osmotic alterations in iAGP pea seeds result in multiple stress responses, pea seeds have effective mechanisms to circumvent stress signaling under conditions in which excessive stress responses and/or cellular damage could prematurely initiate senescence or apoptosis.
Bücher und Buchkapitel

Dorka, R.; Miersch, O.; Hause, B.; Weik, P.; Wasternack, C.; Chronobiologische Phänomene und Jasmonatgehalt bei Viscum album L. 49-66, (2009)

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Bücher und Buchkapitel

Wasternack, C.; Hause, B.; Stenzel, I.; Goetz, S.; Feussner, I.; Miersch, O.; Jasmonate signaling in tomato – The input of tissue-specific occurrence of allene oxide cyclase and JA metabolites (Benning C., Ollrogge, J.). 107-111, (2007)

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Publikation

Mur, L. A.; Kenton, P.; Atzorn, R.; Miersch, O.; Wasternack, C.; The Outcomes of Concentration-Specific Interactions between Salicylate and Jasmonate Signaling Include Synergy, Antagonism, and Oxidative Stress Leading to Cell Death Plant Physiol. 140, 249-262, (2006) DOI: 10.1104/pp.105.072348

Salicylic acid (SA) has been proposed to antagonize jasmonic acid (JA) biosynthesis and signaling. We report, however, that in salicylate hydroxylase-expressing tobacco (Nicotiana tabacum) plants, where SA levels were reduced, JA levels were not elevated during a hypersensitive response elicited by Pseudomonas syringae pv phaseolicola. The effects of cotreatment with various concentrations of SA and JA were assessed in tobacco and Arabidopsis (Arabidopsis thaliana). These suggested that there was a transient synergistic enhancement in the expression of genes associated with either JA (PDF1.2 [defensin] and Thi1.2 [thionin]) or SA (PR1 [PR1a-β-glucuronidase in tobacco]) signaling when both signals were applied at low (typically 10–100 μm) concentrations. Antagonism was observed at more prolonged treatment times or at higher concentrations. Similar results were also observed when adding the JA precursor, α-linolenic acid with SA. Synergic effects on gene expression and plant stress were NPR1- and COI1-dependent, SA- and JA-signaling components, respectively. Electrolyte leakage and Evans blue staining indicated that application of higher concentrations of SA + JA induced plant stress or death and elicited the generation of apoplastic reactive oxygen species. This was indicated by enhancement of hydrogen peroxide-responsive AoPR10-β-glucuronidase expression, suppression of plant stress/death using catalase, and direct hydrogen peroxide measurements. Our data suggests that the outcomes of JA-SA interactions could be tailored to pathogen/pest attack by the relative concentration of each hormone.
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