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Publikationen - Molekulare Signalverarbeitung

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Publikation

Sreenivasulu, N.; Radchuk, V.; Alawady, A.; Borisjuk, L.; Weier, D.; Staroske, N.; Fuchs, J.; Miersch, O.; Strickert, M.; Usadel, B.; Wobus, U.; Grimm, B.; Weber, H.; Weschke, W.; De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8 Plant J. 64, 589-603, (2010) DOI: 10.1111/j.1365-313X.2010.04350.x

Grain development of the maternal effect shrunken endosperm mutant seg8 was analysed by comprehensive molecular, biochemical and histological methods. The most obvious finding was de‐regulation of ABA levels, which were lower compared to wild‐type during the pre‐storage phase but higher during the transition from cell division/differentiation to accumulation of storage products. Ploidy levels and ABA amounts were inversely correlated in the developing endosperms of both mutant and wild‐type, suggesting an influence of ABA on cell‐cycle regulation. The low ABA levels found in seg8 grains between anthesis and beginning endosperm cellularization may result from a gene dosage effect in the syncytial endosperm that causes impaired transfer of ABA synthesized in vegetative tissues into filial grain parts. Increased ABA levels during the transition phase are accompanied by higher chlorophyll and carotenoid/xanthophyll contents. The data suggest a disturbed ABA‐releasing biosynthetic pathway. This is indicated by up‐regulation of expression of the geranylgeranyl reductase (GGR) gene, which may be induced by ABA deficiency during the pre‐storage phase. Abnormal cellularization/differentiation of the developing seg8 endosperm and reduced accumulation of starch are phenotypic characteristics that reflect these disturbances. The present study did not reveal the primary gene defect causing the seg8 phenotype, but presents new insights into the maternal/filial relationships regulating barley endosperm development.
Publikation

Vandenborre, G.; Miersch, O.; Hause, B.; Smagghe, G.; Wasternack, C.; Van Damme, E. J.; Spodoptera littoralis-Induced Lectin Expression in Tobacco Plant Cell Physiol. 50, 1142-1155, (2009) DOI: 10.1093/pcp/pcp065

The induced defense response in plants towards herbivores is mainly regulated by jasmonates and leads to the accumulation of so-called jasmonate-induced proteins. Recently, a jasmonate (JA) inducible lectin called Nicotiana tabacum agglutinin or NICTABA was discovered in tobacco (N. tabacum cv Samsun) leaves. Tobacco plants also accumulate the lectin after insect attack by caterpillars. To study the functional role of NICTABA, the accumulation of the JA precursor 12-oxophytodienoic acid (OPDA), JA as well as different JA metabolites were analyzed in tobacco leaves after herbivory by larvae of the cotton leafworm (Spodoptera littoralis) and correlated with NICTABA accumulation. It was shown that OPDA, JA as well as its methyl ester can trigger NICTABA accumulation. However, hydroxylation of JA and its subsequent sulfation and glucosylation results in inactive compounds that have lost the capacity to induce NICTABA gene expression. The expression profile of NICTABA after caterpillar feeding was recorded in local as well as in systemic leaves, and compared to the expression of several genes encoding defense proteins, and genes encoding a tobacco systemin and the allene oxide cyclase, an enzyme in JA biosynthesis. Furthermore, the accumulation of NICTABA was quanti-fied after S. littoralis herbivory and immunofluorescence microscopy was used to study the localization of NICTABA in the tobacco leaf.
Publikation

Halim, V. A.; Altmann, S.; Ellinger, D.; Eschen-Lippold, L.; Miersch, O.; Scheel, D.; Rosahl, S.; PAMP-induced defense responses in potato require both salicylic acid and jasmonic acid Plant J. 57, 230-242, (2009) DOI: 10.1111/j.1365-313X.2008.03688.x

To elucidate the molecular mechanisms underlying pathogen‐associated molecular pattern (PAMP)‐induced defense responses in potato (Solanum tuberosum ), the role of the signaling compounds salicylic acid (SA) and jasmonic acid (JA) was analyzed. Pep‐13, a PAMP from Phytophthora , induces the accumulation of SA, JA and hydrogen peroxide, as well as the activation of defense genes and hypersensitive‐like cell death. We have previously shown that SA is required for Pep‐13‐induced defense responses. To assess the importance of JA, RNA interference constructs targeted at the JA biosynthetic genes, allene oxide cyclase and 12‐oxophytodienoic acid reductase, were expressed in transgenic potato plants. In addition, expression of the F‐box protein COI1 was reduced by RNA interference. Plants expressing the RNA interference constructs failed to accumulate the respective transcripts in response to wounding or Pep‐13 treatment, neither did they contain significant amounts of JA after elicitation. In response to infiltration of Pep‐13, the transgenic plants exhibited a highly reduced accumulation of reactive oxygen species as well as reduced hypersensitive cell death. The ability of the JA‐deficient plants to accumulate SA suggests that SA accumulation is independent or upstream of JA accumulation. These data show that PAMP responses in potato require both SA and JA and that, in contrast to Arabidopsis, these compounds act in the same signal transduction pathway. Despite their inability to fully respond to PAMP treatment, the transgenic RNA interference plants are not altered in their basal defense against Phytophthora infestans .
Publikation

Vigliocco, A.; Alemano, S.; Miersch, O.; Alvarez, D.; Abdala, G.; Endogenous jasmonates in dry and imbibed sunflower seeds from plants grown at different soil moisture contents Seed Sci. Res. 17, 91-98, (2007) DOI: 10.1017/S0960258507708371

In this study, we characterized two sunflower (Helianthus annuus L.) lines with differential sensitivity to drought, the sensitive line B59 and the tolerant line B71. Using both lines, we compared the content of endogenous jasmonates (JAs) in dry and imbibed seeds from plants grown under irrigation and drought. Jasmonic acid (JA), 12-oxo-phytodienoic acid (OPDA), 11-hydroxyjasmonate (11-OH-JA) and 12-hydroxyjasmonate (12-OH-JA) were detected in dry and imbibed sunflower seeds. Seeds from plants grown under drought had a lower content of total JAs and exhibited higher germination percentages than seeds from irrigated plants, demonstrating that environmental conditions have a strong influence on the progeny. OPDA and 12-OH-JA were the main compounds found in dry seeds of both lines. Imbibed seeds showed an enhanced amount of total JAs with respect to dry seeds produced by plants grown in both soil moisture conditions. Imbibition triggered a dramatic OPDA increase in the embryo, suggesting a role of this compound in germination. We conclude that JAs patterns vary during sunflower germination and that the environmental conditions experienced by the mother plant modify the hormonal content of the seed progeny.
Publikation

Lannoo, N.; Vandenborre, G.; Miersch, O.; Smagghe, G.; Wasternack, C.; Peumans, W. J.; Van Damme, E. J. M.; The Jasmonate-Induced Expression of the Nicotiana tabacum Leaf Lectin Plant Cell Physiol. 48, 1207-1218, (2007) DOI: 10.1093/pcp/pcm090

Previous experiments with tobacco (Nicotiana tabacum L. cv Samsun NN) plants revealed that jasmonic acid methyl ester (JAME) induces the expression of a cytoplasmic/nuclear lectin in leaf cells and provided the first evidence that jasmonates affect the expression of carbohydrate-binding proteins in plant cells. To corroborate the induced accumulation of relatively large amounts of a cytoplasmic/nuclear lectin, a detailed study was performed on the induction of the lectin in both intact tobacco plants and excised leaves. Experiments with different stress factors demonstrated that the lectin is exclusively induced by exogeneously applied jasmonic acid and JAME, and to a lesser extent by insect herbivory. The lectin concentration depends on leaf age and the position of the tissue in the leaf. JAME acts systemically in intact plants but very locally in excised leaves. Kinetic analyses indicated that the lectin is synthesized within 12 h exposure time to JAME, reaching a maximum after 60 h. After removal of JAME, the lectin progressively disappears from the leaf tissue. The JAME-induced accumulation of an abundant nuclear/cytoplasmic lectin is discussed in view of the possible role of this lectin in the plant.
Publikation

Sreenivasulu, N.; Radchuk, V.; Strickert, M.; Miersch, O.; Weschke, W.; Wobus, U.; Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA- regulated maturation in developing barley seeds Plant J. 47, 310-327, (2006) DOI: 10.1111/j.1365-313X.2006.02789.x

Gene expression patterns covering over 10 000 seed‐expressed sequences were analyzed by macroarray technology in maternal tissue (mainly pericarp) and filial endosperm and embryo during barley seed development from anthesis until late maturation. Defined sets of genes showing distinct expression patterns characterized both tissue type and major developmental phases. The analysis focused on regulatory networks involved in programmed cell death (PCD) and abscisic acid (ABA)‐mediated maturation. These processes were similar in the different tissues, but typically involved the expression of alternative members of a common gene family. The analysis of co‐expressed gene sets and the identification of cis regulatory elements in orthologous rice gene ‘promoter’ regions suggest that PCD in the pericarp is mediated by distinct classes of proteases and is under the hormonal control of both jasmonic acid (JA) and ethylene via ethylene‐responsive element binding protein (EREBP) transcription factors (TFs). On the other hand, PCD in endosperm apparently involves only the ethylene pathway, but employs distinct gene family members from those active in the pericarp, and a different set of proteases and TFs. JA biosynthetic genes are hardly activated. Accordingly, JA levels are high in the pericarp but low in the endosperm during middle and late developmental stages. Similarly, genes acting in the deduced ABA biosynthetic pathway and signaling network differ between endosperm and embryo. ABA in the endosperm appears to exert an influence over storage product synthesis via SNF1 kinase. In the embryo, ABA seems to influence the acquisition of desiccation tolerance via ABA response element binding factors, but the data also suggest the existence of an ABA‐independent but interactive pathway acting via the dehydration‐responsive element binding (DREB) 2A TF.
Publikation

Ziegler, J.; Voigtländer, S.; Schmidt, J.; Kramell, R.; Miersch, O.; Ammer, C.; Gesell, A.; Kutchan, T. M.; Comparative transcript and alkaloid profiling in Papaver species identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis Plant J. 48, 177-192, (2006) DOI: 10.1111/j.1365-313X.2006.02860.x

Plants of the order Ranunculales, especially members of the species Papaver , accumulate a large variety of benzylisoquinoline alkaloids with about 2500 structures, but only the opium poppy (Papaver somniferum ) and Papaver setigerum are able to produce the analgesic and narcotic morphine and the antitussive codeine. In this study, we investigated the molecular basis for this exceptional biosynthetic capability by comparison of alkaloid profiles with gene expression profiles between 16 different Papaver species. Out of 2000 expressed sequence tags obtained from P. somniferum , 69 show increased expression in morphinan alkaloid‐containing species. One of these cDNAs, exhibiting an expression pattern very similar to previously isolated cDNAs coding for enzymes in benzylisoquinoline biosynthesis, showed the highest amino acid identity to reductases in menthol biosynthesis. After overexpression, the protein encoded by this cDNA reduced the keto group of salutaridine yielding salutaridinol, an intermediate in morphine biosynthesis. The stereoisomer 7‐epi ‐salutaridinol was not formed. Based on its similarities to a previously purified protein from P. somniferum with respect to the high substrate specificity, molecular mass and kinetic data, the recombinant protein was identified as salutaridine reductase (SalR; EC 1.1.1.248). Unlike codeinone reductase, an enzyme acting later in the pathway that catalyses the reduction of a keto group and which belongs to the family of the aldo‐keto reductases, the cDNA identified in this study as SalR belongs to the family of short chain dehydrogenases/reductases and is related to reductases in monoterpene metabolism.
Publikation

Fortes, A. M.; Miersch, O.; Lange, P. R.; Malhó, R.; Testillano, P. S.; Risueño, M. d. C.; Wasternack, C.; Pais, M. S.; Expression of Allene Oxide Cyclase and Accumulation of Jasmonates during Organogenic Nodule Formation from Hop (Humulus lupulus var. Nugget) Internodes Plant Cell Physiol. 46, 1713-1723, (2005) DOI: 10.1093/pcp/pci187

A crucial step in the biosynthesis of jasmonic acid (JA) is the formation of its stereoisomeric precursor, cis-(+)-12-oxophytodienoic acid (OPDA), which is catalyzed by allene oxide cyclase (AOC, EC 5.3.99.6). A cDNA of AOC was isolated from Humulus lupulus var. Nugget. The ORF of 765 bp encodes a 255 amino acid protein, which carries a putative chloroplast targeting sequence. The recombinant protein without its putative chloroplast target sequence showed significant AOC activity. Previously we demonstrated that wounding induces organogenic nodule formation in hop. Here we show that the AOC transcript level increases in response to wounding of internodes, peaking between 2 and 4 h after wounding. In addition, Western blot analysis showed elevated levels of AOC peaking 24 h after internode inoculation. The AOC increase was accompanied by increased JA levels 24 h after wounding, whereas OPDA had already reached its highest level after 12 h. AOC is mostly present in the vascular bundles of inoculated internodes. During prenodule and nodule formation, AOC levels were still high. JA and OPDA levels decreased down to 10 and 118 pmol (g FW)–1, respectively, during nodule formation, but increased during plantlet regeneration. Double immunolocalization analysis of AOC and Rubisco in connection with lugol staining showed that AOC is present in amyloplasts of prenodular cells and in the chloroplasts of vacuolated nodular cells, whereas meristematic cells accumulated little AOC. These data suggest a role of AOC and jasmonates in organogenic nodule formation and plantlet regeneration from these nodules.
Publikation

Danon, A.; Miersch, O.; Felix, G.; op den Camp, R. G. L.; Apel, K.; Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana Plant J. 41, 68-80, (2005) DOI: 10.1111/j.1365-313X.2004.02276.x

Upon a dark/light shift the conditional flu mutant of Arabidopsis starts to generate singlet oxygen (1O2), a non‐radical reactive oxygen species that is restricted to the plastid compartment. Immediately after the shift, plants stop growing and develop necrotic lesions. We have established a protoplast system, which allows detection and characterization of the death response in flu induced by the release of 1O2. Vitamin B6 that quenches 1O2 in fungi was able to protect flu protoplasts from cell death. Blocking ethylene production was sufficient to partially inhibit the death reaction. Similarly, flu mutant seedlings expressing transgenic NahG were partially protected from the death provoked by the release of 1O2, indicating a requirement for salicylic acid (SA) in this process, whereas in cells depleted of both, ethylene and SA, the extent of cell death was reduced to the wild‐type level. The flu mutant was also crossed with the jasmonic acid (JA)‐depleted mutant opr3 , and with the JA, OPDA and dinor OPDA (dnOPDA)‐depleted dde2‐2 mutant. Analysis of the resulting double mutants revealed that in contrast to the JA‐induced suppression of H2O2/superoxide‐dependent cell death reported earlier, JA promotes singlet oxygen‐mediated cell death in flu , whereas other oxylipins such as OPDA and dnOPDA antagonize this death‐inducing activity of JA.
Publikation

Andrade, A.; Vigliocco, A.; Alemano, S.; Miersch, O.; Botella, M. A.; Abdala, G.; Endogenous jasmonates and octadecanoids in hypersensitive tomato mutants during germination and seedling development in response to abiotic stress Seed Sci. Res. 15, 309-318, (2005) DOI: 10.1079/SSR2005219

Although jasmonates (JAs) are involved in germination and seedling development, the regulatory mechanism of JAs, and their relation with endogenous level modifications in these processes, is not well understood. We report here the detection of 12-oxo-phytodienoic acid (OPDA), jasmonic acid (JA), 11-hydroxyjasmonate (11-OH-JA), 12-hydroxyjasmonate (12-OH-JA) and methyljasmonate (JAME) in unimbibed seeds and seedlings of tomato Lycopersicon esculentum Mill cv. Moneymaker (wild type) and tss1, tss2, tos1 mutants. The main compounds in wild-type and tss1, tss2, tos1 seeds were the hydroxylate-JAs; 12-OH-JA was the major component in dry seeds of the wild type and in tss2 and tos1. The amounts of these derivatives were higher in seeds than in seedlings. Changes in JAs during wild-type and tss1 imbibition were analysed in seeds and the imbibition water. In wild-type imbibed seeds, 11-OH-JA content was higher than in tss1. 12-OH-JA showed a different tendency with respect to 11-OH-JA, with high levels in the wild type at early imbibition. In tss1, levels of 12-OH-JA rose from 24 to 48 h of imbibition. At 72 h of imbibition, when radicles had emerged, the amounts of both hydroxylates in wild-type and tss1 seeds were minimal. An important release of the hydroxylate forms was observed in the imbibition water. 11-OH-JA decreased in the imbibition water of wild-type seeds at 48 h. On the contrary, a high and sustained liberation of this compound was observed in tss1 after 24 h. 12-OH-JA increased in wild-type as well in tss1 until 24 h. Thereafter, a substantial reduction in the content of this compound was registered. NaCl-treated wild-type seedlings increased their 12-OH-JA, but tss1 seedlings increased their JA in response to salt treatment. In tss2 seedlings, NaCl caused a slight decrease in 11-OH-JA and JAME, whereas tos1 seedlings showed a dramatic OPDA and 12-OH-JA decrease in response to salt treatment. Under salt stress the mutant seedlings showed different patterns of JAs according to their differential hypersensitivity to abiotic stress. The JA-hydroxylate forms found, and the differential accumulation of JAs during germination, imbibition and seedling development, as well as their response to NaCl stress, provide new evidence about the control of many developmental processes by JA.
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