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Publications

Ziegler, J.; Stenzel, I.; Hause, B.; Maucher, H.; Miersch, O.; Hamberg, M.; Grimm, M.; Ganal, M.; Wasternack, C. Molecular cloning of allene oxide cyclase: The enzyme establishing the stereochemistry of octadecanoids and jasmonates J. Biol. Chem. 275, 19132-19138, (2000) DOI: 10.1074/jbc.M002133200

Allene oxide cyclase (AOC) catalyses the stereospecific cyclisation of an unstable allene oxide to 9(S),13(S)-12-oxo-10,15(Z)-phytodienoic acid, the ultimate precursor of jasmonic acid. This enzyme has previously been purified, and two identical N-terminal peptides were found suggesting AOC to be a homodimeric protein. Furthermore, the native protein was N-terminal processed. Using degenerate primers, a PCR fragment could be generated from tomato, which was further used to isolate a full length cDNA clone of 1kb coding for a protein with 245 amino acids with a molecular mass of 26 kDa. Whereas expression of the whole coding region failed to detect AOC activity, a 5-'truncated protein showed high activity, suggesting that additional amino acids impair the enzymatic function. Steric analysis of the 12-oxo-phytodienoic acid formed by the recombinant AOC revealed exclusive (>99%) formation of the 9(S),13(S) enantiomer. Exclusive formation of this enantiomer was also found in wounded tomato leaves. Southern analysis and genetic mapping revealed the existence of a single gene for AOC located on chromosome 2 of tomato. Inspection of the N-terminus revealed the presence of a chloroplastic transit peptide, and the location of AOC protein in that compartment could be shown by immunohistochemical methods. Concomitant with the jasmonate levels, the accumulation of AOC mRNA was transiently induced after wounding of tomato leaves.
Publications

Hause, B.; Stenzel, I.; Miersch, O.; Maucher, H.; Kramell, R.; Ziegler, J.; Wasternack, C. Tissue-specific oxylipin signature of tomato flower - The allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles Plant J. 24, 113-126, (2000) DOI: 10.1046/j.1365-313x.2000.00861.x

A crucial step in the biosynthesis of jasmonic acid (JA) is the formation of its correct stereoisomeric precursor, cis(+)12-oxophytodienoic acid (OPDA). This step is catalyzed by allene oxide cyclase (AOC) which has been recently cloned from tomato (Ziegler et al., 2000). In stems, young leaves and young flowers AOC mRNA accumulates weakly, contrasting with a strong accumulation in flower buds, flower stalks and roots. The high levels of AOC mRNA and AOC protein in distinct flower organs correlate with high AOC activity, and with elevated levels of JA, OPDA and JA isoleucine conjugate. These compounds accumulate in flowers to levels of about 20 nmoles g-1 f.w., which is two orders of magnitude higher than in leaves. In pistils OPDA is much higher than JA, whereas in flower stalks JA exceeds the level of OPDA. Also in other flower tissues the ratios among JA, OPDA and JA isoleucine conjugate differ remarkably suggesting a tissue-specific oxylipin signature. Immunocytochemical analysis revealed the specific occurrence of the AOC protein in ovules, the transmission tissue of the style and in vascular bundles of receptacles, flower stalks, stems, petioles and roots. Based on the tissue-specific AOC expression and formation of JA, OPDA and JA amino acid conjugates, a possible role for these compounds in flower development is discussed in terms of their effect on sink-source relationships and plant defense reactions. Furthermore, the AOC expression in vascular bundles might have a role in the systemin-mediated wound response of tomato.
Books and chapters

Stumpe, M.; Stenzel, I.; Weichert, H.; Hause, B.; Feussner, I. The lipoxygenase pathway in mycorrhizal roots of <span>Medicago truncatula</span> (Murata, N., Yamada, M., Nishida, I., Okuyama, H., Sekijar, J., Hajme, W.). Kluwer Academic Publishers, Dordrecht 287-290, (2003)

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Books and chapters

Stenzel, I.; Hause, B.; Feussner, I.; Wasternack, C. Transcriptional activation of jasmonate biosynthesis enzymes is not reflected at protein level (Murata, N., Yamada, M., Nishida, I., Okuyama, H., Sekijar, J., Hajme, W.). Kluwer Academic Publishers 267-270, (2003)

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Publications

Stenzel, I.; Hause, B.; Maucher, H.; Pitzschke, A.; Miersch, O.; Ziegler, J.; Ryan, C.; Wasternack, C. Allene oxide cyclase dependence of the wound response and vascular bundle specific generation of jasmonates in tomato - amplification in wound-signalling Plant J. 33, 577-589, (2003) DOI: 10.1046/j.1365-313X.2003.01647.x

The allene oxide cyclase (AOC) catalyzed step in jasmonate (JA) biosynthesis is important in the wound response of tomato. As shown by treatments with systemin and its inactive analog, by analysis of 35S::prosysteminsense and 35S::prosysteminantisense plants, the AOC expression and JA formation is systemin-dependent. Data are presented on amplification of the local wound response by activation of the constitutively occurring AOC and generation of JA, both in vascular bundles, whereas a lipoxygenase and allene oxide synthase are equally distributed in all leaf tissues. The tissue-specific occurrence of AOC protein and generation of JA is kept upon wounding or other stresses, but is compromised in 35S::AOCsense plants, whereas 35S::AOCantisense plants exhibited residual AOC expression, less than 10 % rise in JA and no detectable expression of wound response genes. The systemin-dependency of AOC expression, the activation of JA biosynthesis occurring only upon substrate generation, and the tissue-specific occurrence of AOC including tissue-specific generation of JA suggest a pre-activated state of tomato leaves which allows local and rapid defense responses.
Publications

Hause, B.; Stenzel, I.; Miersch, O.; Wasternack, C. Occurrence of the allene oxide cyclase in different organs and tissues of <em>Arabidopsis thaliana</em> Phytochemistry 64, 971-980, (2003) DOI: 10.1016/S0031-9422(03)00447-3

Occurrence of an essential enzyme in jasmonate (JA) biosynthesis, the allene oxide cyclase, (AOC) was analyzed in different developmental stages and various organs of Arabidopsis thaliana plants by immuno blot analysis and immunocytological approaches. Levels of AOC and of the two preceding enzymes in JA biosynthesis increased during seedling development accompanied by increased levels of JA and 12-oxophytodienoic acid levels after 4 and 8 weeks. Most tissues including all vascular bundles and that of flower buds contain AOC protein. Flowers shortly before opening, however, contain AOC protein preferentially in ovules, stigma cells and vascular bundles, whereas in anthers and pollen AOC could not be detected. The putative roles of AOC and JA in development are discussed.
Publications

Stenzel, I.; Hause, B.; Miersch, O.; Kurz, T.; Maucher, H.; Weichert, H.; Ziegler, J.; Feussner, I.; Wasternack, C. Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana Plant Mol. Biol. 51, 895-911, (2003) DOI: 10.1023/A:1023049319723

In biosynthesis of octadecanoids and jasmonate (JA), the naturally occurring enantiomer is established in a step catalysed by the gene cloned recently from tomato as a single-copy gene (Ziegler et al., 2000). Based on sequence homology, four full-length cDNAs were isolated from Arabidopsis thaliana ecotype Columbia coding for proteins with AOC activity. The expression of AOC genes was transiently and differentially up-regulated upon wounding both locally and systemically and was induced by JA treatment. In contrast, AOC protein appeared at constitutively high basal levels and was slightly increased by the treatments. Immunohistochemical analyses revealed abundant occurrence of AOC protein as well as of the preceding enzymes in octadecanoid biosynthesis, lipoxygenase (LOX) and allene oxide synthase (AOS), in fully developed tissues, but much less so in 7-day old leaf tissues. Metabolic profiling data of free and esterified polyunsaturated fatty acids and lipid peroxidation products including JA and octadecanoids in wild-type leaves and the jasmonate-deficient mutant OPDA reductase 3 (opr3) revealed preferential activity of the AOS branch within the LOX pathway. 13-LOX products occurred predominantly as esterified derivatives, and all 13-hydroperoxy derivatives were below the detection limits. There was a constitutive high level of free 12-oxo-phytodienoic acid (OPDA) in untreated wild-type and opr3 leaves, but an undetectable expression of AOC. Upon wounding opr3 leaves exhibited only low expression of AOC, wounded wild-type leaves, however, accumulated JA and AOC mRNA. These and further data suggest regulation of JA biosynthesis by OPDA compartmentalization and a positive feedback by JA during leaf development.
Publications

Stenzel, I.; Ziehte, K.; Schurath, J.; Hertel, S.C.; Bosse, D.; Köck, M. Differential expression of PSI14, a phosphatase gene family, in response to phosphate availability, plant infection and pathogen infection Physiol. Plant 118, 138-146, (2003)

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Publications

Schüler, G.; Mithöfer, A.; Baldwin, I.T.; Berger, S.; Ebel, S.; Santos, J.G.; Herrmann, G.; Hölscher, D.; Kramell, R.; Kutchan, T.M.; Maucher, H.; Schneider, B.; Stenzel, I.; Wasternack, C.; Boland, W. Coronalon: a powerful tool in plant stress physiology FEBS Lett. 563, 17-22, (2004) DOI: 10.1016/S0014-5793(04)00239-X

Coronalon, a synthetic 6-ethyl indanoyl isoleucine conjugate, has been designed as a highly active mimic of octadecanoid phytohormones that are involved in insect and disease resistance. The spectrum of biological activities that is affected by coronalon was investigated in nine different plant systems specifically responding to jasmonates and/or 12-oxo-phytodienoic acid. In all bioassays analyzed, coronalon demonstrated a general strong activity at low micromolar concentrations. The results obtained showed the induction of (i) defense-related secondary metabolite accumulation in both cell cultures and plant tissues, (ii) specific abiotic and biotic stress-related gene expression, and (iii) root growth retardation. The general activity of coronalon in the induction of plant stress responses together with its simple and efficient synthesis suggests that this compound might serve as a valuable tool in the examination of various aspects in plant stress physiology. Moreover, coronalon might become employed in agriculture to elicit plant resistance against various aggressors.
Publications

Miersch, O.; Weichert, H.; Stenzel, I.; Hause, B.; Maucher, H.; Feussner, I.; Wasternack, C. Constitutive overexpression of allene oxide cyclase in tomato (<em>Lycopersicon esculentum</em> cv. Lukullus) elevates levels of some jasmonates and octadecanoids in flower organs but not in leaves Phytochemistry 65, 847-856, (2004) DOI: 10.1016/j.phytochem.2004.01.016

The allene oxide cyclase (AOC), an enzyme in jasmonate biosynthesis, occurs in vascular bundles and ovules of tomato flowers which exhibit a tissue-specific oxylipin signature (Plant J. 24, 113-126, 2000). Constitutive overexpression of the AOC did not led to altered levels of jasmonates in leaves, but these levels increased upon wounding or other stresses suggesting regulation of jasmonate biosynthesis by substrate availability (Plant J. 33, 577-589, 2003). Here, we show dramatic changes in levels of jasmonic acid (JA), of 12-oxo-phytodienoic acid (OPDA), their methyl esters (JAME, OPDAME), and of dinor-OPDA in most flower organs upon constitutive overexpression of AOC. Beside a dominant occurrence of OPDAME and JA in most flower organs, the ratio among the various compounds was altered differentially in the organs of transgenic flowers, e.g. OPDAME increased up to 53-fold in stamen, and JA increased about 51-fold in buds and 7.5-fold in sepals. The increase in jasmonates and octadecanoids was accompanied by decreased levels of free lipid hydro(per)oxy compounds. Except for 16:2, the AOC overexpression led to a significant increase in free but not esterified polyunsaturated fatty acids in all flower organs. The data suggest different regulation of JA biosynthesis in leaves and flowers of tomato.Constitutive overexpression of the AOC increases in all flower organs levels of some jasmonates and octadecanoids, alters the ratios among the compounds, decreases levels of free lipid hydro(per)oxy compounds and increases levels of free but not of esterified polyunsaturated fatty acids.
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