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Publications - Cell and Metabolic Biology

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Hazman, M., Hause, B., Eiche, E., Nick, P., Riemann & M. Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J. Exp. Bot. 66, 3339-3352, (2015) DOI: 10.1093/jxb/erv142

Salinity stress represents a global constraint for rice, the most important staple food worldwide. Therefore the role of the central stress signal jasmonate for the salt response was analysed in rice comparing the responses to salt stress for two jasmonic acid (JA) biosynthesis rice mutants (cpm2 and hebiba) impaired in the function of ALLENE OXIDE CYCLASE (AOC) and their wild type. The aoc mutants were less sensitive to salt stress. Interestingly, both mutants accumulated smaller amounts of Na+ ions in their leaves, and showed better scavenging of reactive oxygen species (ROS) under salt stress. Leaves of the wild type and JA mutants accumulated similar levels of abscisic acid (ABA) under stress conditions, and the levels of JA and its amino acid conjugate, JA–isoleucine (JA-Ile), showed only subtle alterations in the wild type. In contrast, the wild type responded to salt stress by strong induction of the JA precursor 12-oxophytodienoic acid (OPDA), which was not observed in the mutants. Transcript levels of representative salinity-induced genes were induced less in the JA mutants. The absence of 12-OPDA in the mutants correlated not only with a generally increased ROS-scavenging activity, but also with the higher activity of specific enzymes in the antioxidative pathway, such as glutathione S-transferase, and fewer symptoms of damage as, for example, indicated by lower levels of malondialdehyde. The data are interpreted in a model where the absence of OPDA enhanced the antioxidative power in mutant leaves.


Dobritzsch, S., Weyhe, M., Schubert, R., Dindas, J., Hause, G., Kopka, J. & Hause, B. Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses. BMC Biology 13:28, 28, (2015) DOI: 10.1186/s12915-015-0135-3


Jasmonates are well known plant signaling components required for stress responses and development. A prominent feature of jasmonate biosynthesis or signaling mutants is the loss of fertility. In contrast to the male sterile phenotype of Arabidopsis mutants, the tomato mutant jai1-1 exhibits female sterility with additional severe effects on stamen and pollen development. Its senescence phenotype suggests a function of jasmonates in regulation of processes known to be mediated by ethylene. To test the hypothesis that ethylene involved in tomato stamen development is regulated by jasmonates, a temporal profiling of hormone content, transcriptome and metabolome of tomato stamens was performed using wild type and jai1-1.


Wild type stamens showed a transient increase of jasmonates that is absent in jai1-1. Comparative transcriptome analyses revealed a diminished expression of genes involved in pollen nutrition at early developmental stages of jai1-1 stamens, but an enhanced expression of ethylene-related genes at late developmental stages. This finding coincides with an early increase of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in jai1-1 and a premature pollen release from stamens, a phenotype similarly visible in an ethylene overproducing mutant. Application of jasmonates to flowers of transgenic plants affected in jasmonate biosynthesis diminished expression of ethylene-related genes, whereas the double mutant jai1-1 NeverRipe (ethylene insensitive) showed a complementation of jai1-1 phenotype in terms of dehiscence and pollen release.

ConclusionsOur data suggest an essential role of jasmonates in the temporal inhibition of ethylene production to prevent premature desiccation of stamens and to ensure proper timing in flower development.


Brandt, W., Manke, K. & Vogt, T. A catalytic triad – Lys-Asn-Asp – Is essential for the catalysis of the methyl transfer in plant cation-dependent O-methyltransferases Phytochemistry 113, 130-139, (2015) DOI: 10.1016/j.phytochem.2014.12.018

Crystal structure data of cation-dependent catechol O-methyltransferases (COMTs) from mammals and related caffeoyl coenzyme A OMTs (CCoAOMTs) from plants have suggested operative molecular mechanisms. These include bivalent cations that facilitate deprotonation of vicinal aromatic dihydroxy systems and illustrate a conserved arrangement of hydroxyl and carboxyl ligands consistent with the requirements of a metal-activated catalytic mechanism. The general concept of metal-dependent deprotonation via a complexed aspartate is only one part of a more pronounced proton relay, as shown by semiempirical and DFT quantum mechanical calculations and experimental validations. A previously undetected catalytic triad, consisting of Lys157-Asn181-Asp228 residues is required for complete methyl transfer in case of a cation-dependent phenylpropanoid and flavonoid OMT, as described in this report. This triad appears essential for efficient methyl transfer to catechol-like hydroxyl group in phenolics. The observation is consistent with a catalytic lysine in the case of mammalian COMTs, but jettisons existing assumptions on the initial abstraction of the meta-hydroxyl proton to the metal stabilizing Asp154 (PFOMT) or comparable Asp-carboxyl groups in type of cation-dependent enzymes in plants. The triad is conserved among all characterized plant CCoAOMT-like enzymes, which are required not only for methylation of soluble phenylpropanoids like coumarins or monolignol monomers, but is also present in the similar microbial and mammalian cation-dependent enzymes which methylate a comparable set of substrates.


Matschi, S., Hake, K., Herde, M., Hause, B. & Romeis, T. The Calcium-dependent protein kinase CPK28 regulates development by inducing growth phase-specific, spatiallyrestricted alterations in Jasmonic acid levels independent of defense responses in Arabidopsis Plant Cell 27, 591–60, (2015) DOI: 10.1105/tpc.15.00024

Phytohormones play an important role in development and stress adaptations in plants, and several interacting hormonal pathways have been suggested to accomplish fine-tuning of stress responses at the expense of growth. This work describes the role played by the CALCIUM-DEPENDENT PROTEIN KINASE CPK28 in balancing phytohormone-mediated development in Arabidopsis thaliana, specifically during generative growth. cpk28 mutants exhibit growth reduction solely as adult plants, coinciding with altered balance of the phytohormones jasmonic acid (JA) and gibberellic acid (GA). JA-dependent gene expression and the levels of several JA metabolites were elevated in a growth phase-dependent manner in cpk28, and accumulation of JA metabolites was confined locally to the central rosette tissue. No elevated resistance toward herbivores or necrotrophic pathogens was detected for cpk28 plants, either on the whole-plant level or specifically within the tissue displaying elevated JA levels. Abolishment of JA biosynthesis or JA signaling led to a full reversion of the cpk28 growth phenotype, while modification of GA signaling did not. Our data identify CPK28 as a growth phase-dependent key negative regulator of distinct processes: While in seedlings, CPK28 regulates reactive oxygen species-mediated defense signaling; in adult plants, CPK28 confers developmental processes by the tissue-specific balance of JA and GA without affecting JA-mediated defense responses. 


Staniek, A., Bouwmeester, H., Fraser, P. D., Kayser, O., Martens, S., Tissier, A., van der Krol, S., Wessjohann, L. & Warzecha, H. Natural products – learning chemistry from plants. Biotechnol. J. 9, 326-336, (2014) DOI: 10.1002/biot.201300059

Plant natural products (PNPs) are unique in that they represent a vast array of different structural features, ranging from relatively simple molecules to very complex ones. Given the fact that many plant secondary metabolites exhibit profound biological activity, they are frequently used as fragrances and flavors, medicines, as well as industrial chemicals. As the intricate structures of PNPs often cannot be mimicked by chemical synthesis, the original plant providers constitute the sole source for their industrial, large-scale production. However, sufficient supply is not guaranteed for all molecules of interest, making the development of alternative production systems a priority. Modern techniques, such as genome mining and thorough biochemical analysis, have helped us gain preliminary understanding of the enzymatic formation of the valuable ingredients in planta. Herein, we review recent advances in the application of biocatalytical processes, facilitating generation of complex PNPs through utilization of plant-derived specific enzymes and combinatorial biochemistry. We further evaluate the options of employing heterologous organisms harboring PNP biosynthetic pathways for the production of secondary metabolites of interest.


Wasternack, C. & Hause, B. Jasmonsäure – ein universelles Pflanzenhormon: Blütenduft, Abwehr, Entwicklung Biologie in unserer Zeit 44, 164 - 171, (2014) DOI: 10.1002/biuz.201410535

Jasmonsäure (JA) und ihre Metaboliten kommen in allen niederen und höheren Pflanzen vor. Sie sind universell wirksame, aus Lipiden gebildete Signalstoffe bei der Abwehr von biotischem und abiotischem Stress sowie in der pflanzlichen Entwicklung. Rezeptor und Komponenten von JA–Signalketten wurden identifiziert. In der Entwicklung von Blüten, Früchten, Samen, Trichomen oder in der Abwehr von Insekten und Pathogenen treten ähnliche JA-vermittelte Signalproteine auf, die eine Feinregulation der Prozesse erlauben und eine Verbindung (cross-talk) zu anderenPflanzenhormonen aufweisen.

Books and chapters

Tissier, A., Ziegler, J. & Vogt T. Specialized plant metabolites: Diversity and biosynthesis . In: Ecological Biochemistry: environmental and Interspecies Interactions (Krauß, G. J.; Nies, D. H.). 14-37, (2014) ISBN: 978-3-527-31650-2 DOI: 10.1002/9783527686063.ch2

Plant secondary metabolites, also termed specialized plant metabolites, currently comprise more than 200 000 natural products that are all based on a few biosynthetic pathways and key primary metabolites. Some pathways like flavonoid and terpenoid biosynthesis are universally distributed in the plant kingdom, whereas others like alkaloid or cyanogenic glycoside biosynthesis are restricted to a limited set of taxa. Diversification is achieved by an array of mechanisms at the genetic and enzymatic level including gene duplications, substrate promiscuity of enzymes, cell-specific regulatory systems, together with modularity and combinatorial aspects. Specialized metabolites reflect adaptations to a specific environment. The observed diversity illustrates the heterogeneity and multitude of ecological habitats and niches that plants have colonized so far and constitutes a reservoir of potential new metabolites that may provide adaptive advantage in the face of environmental changes. The code that connects the observed chemical diversity to this ecological diversity is largely unknown. One way to apprehend this diversity is to realize its tremendous plasticity and evolutionary potential. This chapter presents an overview of the most widespread and popular secondary metabolites, which provide a definite advantage to adapt to or to colonize a particular environment, making the boundary between the “primary” and the “secondary” old fashioned and blurry.
Books and chapters

Thieme, F., Marillonnet, S. Quick and clean cloning. In: DNA Cloning and Assembly Methods.  (Valla, S.; R. Lale, R). Meth Mol Biol 1116, 37-48, (2014) ISBN: 978-1-62703-763-1 DOI: 10.1007/978-1-62703-764-8_3

Identification of unknown sequences that flank known sequences of interest requires PCR amplification of DNA fragments that contain the junction between the known and unknown flanking sequences. Since amplified products often contain a mixture of specific and nonspecific products, the quick and clean (QC) cloning procedure was developed to clone specific products only. QC cloning is a ligation-independent cloning procedure that relies on the exonuclease activity of T4 DNA polymerase to generate single-stranded extensions at the ends of the vector and insert. A specific feature of QC cloning is the use of vectors that contain a sequence called catching sequence that allows cloning specific products only. QC cloning is performed by a one-pot incubation of insert and vector in the presence of T4 DNA polymerase at room temperature for 10 min followed by direct transformation of the incubation mix in chemo-competent Escherichia coli cells.
Books and chapters

Balcke, G. U., Bennewitz, S., Zabel, S. & Tissier, A. Isoprenoid and metabolite profiling of plant trichomes. In: Methods in Molecular Biology 1153, 189-202, (2014) ISBN: 978-1-4939-0606-2 DOI: 10.1007/978-1-4939-0606-2_13

Plant glandular trichomes are specialized secretory structures located on the surface of the aerial parts of plants with large biosynthetic capacity, often with terpenoids as output molecules. The collection of plant trichomes requires a method to separate trichomes from leaf epidermal tissues. For metabolite profiling, trichome tissue needs to be rapidly quenched in order to maintain the indigenous state of intracellular intermediates. Appropriate extraction and chromatographic separation methods must be available, which address the wide-ranging polarity of metabolites. In this chapter, a protocol for trichome harvest using a frozen paint brush is presented. A work flow for broad-range metabolite profiling using LC-MS2 analysis is described, which is applicable to assess very hydrophilic isoprenoid precursors as well as more hydrophobic metabolites from trichomes and other plant tissues.

Hilou, A., Zhang, H., Franken, P. & Hause, B. Do jasmonates play a role in arbuscular mycorrhiza-induced local bioprotection of Medicago truncatula against root rot disease caused by Aphanomyces euteiches? Mycorrhiza 24, 45-54, (2014) DOI: 10.1007/s00572-013-0513-z

Bioprotective effects of mycorrhization with two different arbuscular mycorrhizal (AM) fungi, Funneliformis mosseae and Rhizophagus irregularis, against Aphanomyces euteiches, the causal agent of root rot in legumes, were studied in Medicago truncatula using phenotypic and molecular markers. Previous inoculation with an AM-fungus reduced disease symptoms as well as the amount of pathogen within roots, as determined by the levels of A. euteiches rRNA or transcripts of the gene sterol C24 reductase. Inoculation with R. irregularis was as efficient as that with F. mosseae. To study whether jasmonates play a regulatory role in bioprotection of M. truncatula by the AM fungi, composite plants harboring transgenic roots were used to modulate the expression level of the gene encoding M. truncatula allene oxide cyclase 1, a key enzyme in jasmonic acid biosynthesis. Neither an increase nor a reduction in allene oxide cyclase levels resulted in altered bioprotection by the AM fungi against root infection by A. euteiches. These data suggest that jasmonates do not play a major role in the local bioprotective effect of AM fungi against the pathogen A. euteiches in M. truncatula roots.

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