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Publikation

Witzel, K., Strehmel, N., Baldermann, S., Neugart, S., Becker, Y., Becker, M., Berger, B., Scheel, D., Grosch, R., Schreiner, M. & Ruppel, S. Arabidopsis thaliana root and root exudate metabolism is altered by the growth-promoting bacterium Kosakonia radicincitans DSM 16656T.  Plant Soil 419 , 557-573, (2017) DOI: 10.1007/s11104-017-3371-1

Aims
Plant growth-promoting bacteria (PGPB) affect host physiological processes in various ways. This study aims at elucidating the dependence of bacterial-induced growth promotion on the plant genotype and characterizing plant metabolic adaptations to PGPB.

Methods
Eighteen Arabidopsis thaliana accessions were inoculated with the PGPB strain Kosakonia radicincitans DSM 16656T. Colonisation pattern was assessed by enhanced green fluorescent protein (eGFP)-tagged K. radicincitans in three A. thaliana accessions differing in their growth response. Metabolic impact of bacterial colonisation was determined for the best responding accession by profiling distinct classes of plant secondary metabolites and root exudates.

Results
Inoculation of 18 A. thaliana accessions resulted in a wide range of growth responses, from repression to enhancement. Testing the bacterial colonisation of three accessions did not reveal a differential pattern. Profiling of plant secondary metabolites showed a differential accumulation of glucosinolates, phenylpropanoids and carotenoids in roots. Analysis of root exudates demonstrated that primary and secondary metabolites were predominantly differentially depleted by bacterial inoculation.

Conclusions
The plant genotype controls the bacterial growth promoting traits. Levels of lutein and β-carotene were elevated in inoculated roots. Supplementing a bacterial suspension with β-carotene increased bacterial growth, while this was not the case when lutein was applied, indicating that β-carotene could be a positive regulator of plant growth promotion.
Publikation

Herz, K., Dietz, S., Haider, S., Jandt, U., Scheel, D. & Bruelheide, H. Predicting individual plant performance in grasslands. Ecology and Evolution 7, 8958-8965, (2017) DOI: 10.1002/ece3.3393


Plant functional traits are widely used to predict community productivity. However, they are rarely used to predict individual plant performance in grasslands. To assess the relative importance of traits compared to environment, we planted seedlings of 20 common grassland species as phytometers into existing grassland communities varying in land-use intensity. After 1 year, we dug out the plants and assessed root, leaf, and aboveground biomass, to measure plant performance. Furthermore, we determined the functional traits of the phytometers and of all plants growing in their local neighborhood. Neighborhood impacts were analyzed by calculating community-weighted means (CWM) and functional diversity (FD) of every measured trait. We used model selection to identify the most important predictors of individual plant performance, which included phytometer traits, environmental conditions (climate, soil conditions, and land-use intensity), as well as CWM and FD of the local neighborhood. Using variance partitioning, we found that most variation in individual plant performance was explained by the traits of the individual phytometer plant, ranging between 19.30% and 44.73% for leaf and aboveground dry mass, respectively. Similarly, in a linear mixed effects model across all species, performance was best predicted by phytometer traits. Among all environmental variables, only including land-use intensity improved model quality. The models were also improved by functional characteristics of the local neighborhood, such as CWM of leaf dry matter content, root calcium concentration, and root mass per volume as well as FD of leaf potassium and root magnesium concentration and shoot dry matter content. However, their relative effect sizes were much lower than those of the phytometer traits. Our study clearly showed that under realistic field conditions, the performance of an individual plant can be predicted satisfyingly by its functional traits, presumably because traits also capture most of environmental and neighborhood conditions.
Publikationen in Druck

Herz, K., Dietz, S., Haider, S., Jandt, U., Scheel, D. & Bruelheide, H.  Drivers of intraspecific trait variation of grass and forb species in German meadows and pastures J. Vegetation Sci. 28, 705–716, (2017) DOI: 10.1111/jvs.12534

Questions
To what extent is trait variation in grasses and forbs driven by land-use intensity, climate, soil conditions and plant diversity of the local neighbourhood? Do grass and forb species differ in the degree of intraspecific trait variation?

Location
Managed grasslands in three regions of Germany.

Methods
Using a phytometer approach, we raised 20 common European grassland species (ten forbs and ten grasses) and planted them into 54 plots of different land-use types (pasture, meadow, mown pasture). After 1 yr in the field, we measured above- and below-ground plant functional traits. Linear mixed effects models (LMEM) were used to identify the most powerful predictors for every trait. Variation partitioning was applied to assess the amount of inter- and intraspecific trait variation in grasses and forbs explained by environmental conditions (land-use intensity, climate and soil conditions) and plant species diversity of the local neighbourhood.

Results
For 12 out of the 14 traits studied, either land-use intensity or local neighbourhood diversity were predictors in the best LMEM. Land-use intensity had considerably stronger effects than neighbourhood diversity. Root dry matter content and root phosphorus concentration of forbs were more affected by land-use intensity than those of grasses. For almost all traits, intraspecific trait variation of grasses was much higher than that of forbs, while traits of forbs varied more among species. Overall, inter- and intraspecific variation was of the same magnitude.

Conclusion
The similar magnitude of intra- and interspecific trait variation suggests that both sources should be considered in grassland studies at a scale similar to that of our study. The high amount of intraspecific trait variation that was explained by environmental factors and local neighbourhood diversity clearly demonstrates the high potential of species to adjust to local conditions, which would be ignored when only considering species mean trait values.

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Publikation

Cotrim, C. A., Weidner, A., Strehmel, N., Bisol, T. B., Meyer, D., Brandt, W., Wessjohann, L. A. & Stubbs, M. T. A distinct aromatic prenyltransferase associated with the futalosine pathway. ChemistrySelect 2, 9319-9325, (2017) DOI: 10.1002/slct.201702151

Menaquinone (MK) is an electron carrier molecule essential for respiration in most Gram positive bacteria. A crucial step in MK biosynthesis involves the prenylation of an aromatic molecule, catalyzed by integral membrane prenyltransferases of the UbiA (4-hydroxybenzoate oligoprenyltransferase) superfamily. In the classical MK biosynthetic pathway, the prenyltransferase responsible is MenA (1,4-dihydroxy-2-naphthoate octaprenyltransferase). Recently, an alternative pathway for formation of MK, the so-called futalosine pathway, has been described in certain micro-organisms. Until now, five soluble enzymes (MqnA-MqnE) have been identified in the first steps. In this study, the genes annotated as ubiA from T. thermophilus and S. lividans were cloned, expressed and investigated for prenylation activity. The integral membrane proteins possess neither UbiA nor MenA activity and represent a distinct class of prenyltransferases associated with the futalosine pathway that we term MqnP. We identify a critical residue within a highly conserved Asp-rich motif that serves to distinguish between members of the UbiA superfamily.
Publikation

Nakano, R. T., Piślewska-Bednarek, M., Yamada, K., Edger, P. P., Miyahara, M., Kondo, M., Böttcher, C., Mori, M., Nishimura, M., Schulze-Lefert, P., Hara-Nishimura, I. & Bednarek, P. PYK10 myrosinase reveals a functional coordination between endoplasmic reticulum bodies and glucosinolates in Arabidopsis thaliana Plant J. 89, 204-220, (2017) DOI: 10.1111/tpj.13377

The endoplasmic reticulum body (ER body) is an organelle derived from the ER that occurs in only three families of the order Brassicales and is suggested to be involved in plant defense. ER bodies in Arabidopsis thaliana contain large amounts of β-glucosidases, but the physiological functions of ER bodies and these enzymes remain largely unclear. Here we show that PYK10, the most abundant β-glucosidase in A. thaliana root ER bodies, hydrolyzes indole glucosinolates (IGs) in addition to the previously reported in vitro substrate scopolin. We found a striking co-expression between ER body-related genes (including PYK10), glucosinolate biosynthetic genes and the genes for so-called specifier proteins affecting the terminal products of myrosinase-mediated glucosinolate metabolism, indicating that these systems have been integrated into a common transcriptional network. Consistent with this, comparative metabolite profiling utilizing a number of A. thaliana relatives within Brassicaceae identified a clear phylogenetic co-occurrence between ER bodies and IGs, but not between ER bodies and scopolin. Collectively, our findings suggest a functional link between ER bodies and glucosinolate metabolism in planta. In addition, in silico three-dimensional modeling, combined with phylogenomic analysis, suggests that PYK10 represents a clade of 16 myrosinases that arose independently from the other well-documented class of six thioglucoside glucohydrolases. These findings provide deeper insights into how glucosinolates are metabolized in cruciferous plants and reveal variation of the myrosinase–glucosinolate system within individual plants.
Publikation

Ziegler, J., Schmidt, S., Chutia, R., Müller, J., Böttcher, C., Strehmel, N., Scheel, D. & Abel, S. Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J. Exp. Bot. 67, 1421-1432, (2016) DOI: 10.1093/jxb/erv539

Plants have evolved two major strategies to cope with phosphate (Pi) limitation. The systemic response, mainly comprising increased Pi uptake and metabolic adjustments for more efficient Pi use, and the local response, enabling plants to explore Pi-rich soil patches by reorganization of the root system architecture. Unlike previous reports, this study focused on root exudation controlled by the local response to Pi deficiency. To approach this, a hydroponic system separating the local and systemic responses was developed. Arabidopsis thaliana genotypes exhibiting distinct sensitivities to Pi deficiency could be clearly distinguished by their root exudate composition as determined by non-targeted reversed-phase ultraperformance liquid chromatography electrospray ionization quadrupole-time-of-flight mass spectrometry metabolite profiling. Compared with wild-type plants or insensitive low phosphate root 1 and 2 (lpr1 lpr2) double mutant plants, the hypersensitive phosphate deficiency response 2 (pdr2) mutant exhibited a reduced number of differential features in root exudates after Pi starvation, suggesting the involvement of PDR2-encoded P5-type ATPase in root exudation. Identification and analysis of coumarins revealed common and antagonistic regulatory pathways between Pi and Fe deficiency-induced coumarin secretion. The accumulation of oligolignols in root exudates after Pi deficiency was inversely correlated with Pi starvation-induced lignification at the root tips. The strongest oligolignol accumulation in root exudates was observed for the insensitive lpr1 lpr2 double mutant, which was accompanied by the absence of Pi deficiency-induced lignin deposition, suggesting a role of LPR ferroxidases in lignin polymerization during Pi starvation. 

Publikation

Brömme, T., Schmitz,C., Moszner, N., Burtscher, P., Strehmel, N. & Strehmel, B. Photochemical Oxidation of NIR Photosensitizers in the Presence of Radical Initiators and Their Prospective Use in Dental Applications ChemistrySelect 1, 524–532, (2016) DOI: 10.1002/slct.201600048

Photochemical oxidation of near infrared (NIR) photosensitizers in the presence of diaryl iodonium salts bearing either bis(trifluoromethylsulfonyl)imide or hexafluorophosphate was investigated by exposure with NIR LEDs emitting either at 790 nm, 830 nm, 850 nm or 870 nm. Four different cyanines with barbituryl group at the meso position exhibit similar absorption in the NIR. These photosensitizers initiate in combination with diaryliodonium salts radical photopolymerization of dental composites with the focus to cure large thicknesses. Furthermore, the mixture comprising the cyanine and the iodonium salt was used to generate brown color in dental composites on demand. This required to understand the mechanism of dye decomposition in more detail applying exposure kinetics and a coupling of Ultra Performance Liquid Chromatography (UPLC) with mass spectrometry (MS) to analyze the photoproducts formed. Data showed cleavage of the polymethine chain at typical positions in case of the oxidized species. These were formed as result of electron transfer between the excited state of the photosensitizer and the iodonium salt. UPLC-MS experiments additionally indicated a certain sensitivity of the system upon adding of acids and radicals generated by thermal treatment of azobisisobutyronitrile (AIBN). Thus, treatment of the photoinitiator composition led almost to the same products no matter the system was either exposed with NIR light or treated with acids or radicals generated by thermal decomposition of AIBN. These findings helped to understand the large curing depth of 14 mm upon NIR exposure at 850 nm and the brown color formed.

Publikation

Strehmel, N., Mönchgesang,S., Herklotz, S., Krüger, S., Ziegler, J. & Scheel, D. Piriformospora indica Stimulates Root Metabolism of Arabidopsis thaliana. Int. J. Mol. Sci. 17, 1091, (2016) DOI: 10.3390/ijms17071091

Piriformospora indica is a root-colonizing fungus, which interacts with a variety of plants including Arabidopsis thaliana. This interaction has been considered as mutualistic leading to growth promotion of the host. So far, only indolic glucosinolates and phytohormones have been identified as key players. In a comprehensive non-targeted metabolite profiling study, we analyzed Arabidopsis thaliana’s roots, root exudates, and leaves of inoculated and non-inoculated plants by ultra performance liquid chromatography/electrospray ionization quadrupole-time-of-flight mass spectrometry (UPLC/(ESI)-QTOFMS) and gas chromatography/electron ionization quadrupole mass spectrometry (GC/EI-QMS), and identified further biomarkers. Among them, the concentration of nucleosides, dipeptides, oligolignols, and glucosinolate degradation products was affected in the exudates. In the root profiles, nearly all metabolite levels increased upon co-cultivation, like carbohydrates, organic acids, amino acids, glucosinolates, oligolignols, and flavonoids. In the leaf profiles, we detected by far less significant changes. We only observed an increased concentration of organic acids, carbohydrates, ascorbate, glucosinolates and hydroxycinnamic acids, and a decreased concentration of nitrogen-rich amino acids in inoculated plants. These findings contribute to the understanding of symbiotic interactions between plant roots and fungi of the order of Sebacinales and are a valid source for follow-up mechanistic studies, because these symbioses are particular and clearly different from interactions of roots with mycorrhizal fungi or dark septate endophytes 

Bücher und Buchkapitel

Mönchgesang, S., Strehmel, N., Schmidt, S., Westphal, L., Taruttis, F., Müller, E., Herklotz, S., Neumann, S. & Scheel, D. Natural variation of roots exudates in Arabidopsis thaliana - linking metabolomic and genomic data. Sci Rep 6, 29033 , (2016) DOI: 10.1038/srep29033

Many metabolomics studies focus on aboveground parts of the plant, while metabolism within roots and the chemical composition of the rhizosphere, as influenced by exudation, are not deeply investigated. In this study, we analysed exudate metabolic patterns of Arabidopsis thaliana and their variation in genetically diverse accessions. For this project, we used the 19 parental accessions of the Arabidopsis MAGIC collection. Plants were grown in a hydroponic system, their exudates were harvested before bolting and subjected to UPLC/ESI-QTOF-MS analysis. Metabolite profiles were analysed together with the genome sequence information. Our study uncovered distinct metabolite profiles for root exudates of the 19 accessions. Hierarchical clustering revealed similarities in the exudate metabolite profiles, which were partly reflected by the genetic distances. An association of metabolite absence with nonsense mutations was detected for the biosynthetic pathways of an indolic glucosinolate hydrolysis product, a hydroxycinnamic acid amine and a flavonoid triglycoside. Consequently, a direct link between metabolic phenotype and genotype was detected without using segregating populations. Moreover, genomics can help to identify biosynthetic enzymes in metabolomics experiments. Our study elucidates the chemical composition of the rhizosphere and its natural variation in A. thaliana, which is important for the attraction and shaping of microbial communities.

Publikation

Hettwer, K., Böttcher, C., Frolov, A., Mittasch, J., Albert, A., von Roepenack-Lahayeb, E., Strack, D. & Milkowski, C. Dynamic metabolic changes in seeds and seedlings of Brassica napus (oilseed rape) suppressing UGT84A9 reveal plasticity and molecular regulation of the phenylpropanoid pathway 124, 46–57, (2016) DOI: 10.1016/j.phytochem.2016.01.014

In Brassica napus, suppression of the key biosynthetic enzyme UDP-glucose:sinapic acid glucosyltransferase (UGT84A9) inhibits the biosynthesis of sinapine (sinapoylcholine), the major phenolic component of seeds. Based on the accumulation kinetics of a total of 158 compounds (110 secondary and 48 primary metabolites), we investigated how suppression of the major sink pathway of sinapic acid impacts the metabolome of developing seeds and seedlings. In UGT84A9-suppressing (UGT84A9i) lines massive alterations became evident in late stages of seed development affecting the accumulation levels of 58 secondary and 7 primary metabolites. UGT84A9i seeds were characterized by decreased amounts of various hydroxycinnamic acid (HCA) esters, and increased formation of sinapic and syringic acid glycosides. This indicates glycosylation and β-oxidation as metabolic detoxification strategies to bypass intracellular accumulation of sinapic acid. In addition, a net loss of sinapic acid upon UGT84A9 suppression may point to a feedback regulation of HCA biosynthesis. Surprisingly, suppression of UGT84A9 under control of the seed-specific NAPINC promoter was maintained in cotyledons during the first two weeks of seedling development and associated with a reduced and delayed transformation of sinapine into sinapoylmalate. The lack of sinapoylmalate did not interfere with plant fitness under UV-B stress. Increased UV-B radiation triggered the accumulation of quercetin conjugates whereas the sinapoylmalate level was not affected.

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