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Publications - Stress and Develop Biology

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Printed publications

Teh, O.-K., Lee, C.-W., Ditengou, F. A., Klecker, T., Furlan, G., Zietz, M., Hause, G., Eschen-Lippold, L., Hoehenwarter, W., Lee, J., Ott, T. & Trujillo, M. Phosphorylation of the exocyst subunit Exo70B2 contributes to the regulation of its function BioRxiv (2018) DOI: 10.1101/266171

The exocyst is a conserved hetero-octameric complex mediating early tethering during exocytosis. Its Exo70 subunit plays a critical role as a spatiotemporal regulator by mediating numerous protein and lipid interactions. However, a molecular understanding of the exocyst function remains challenging. We show that Exo70B2 locates to dynamic foci at the plasma membrane and transits through a BFA-sensitive compartment, reflecting its canonical function in secretion. However, treatment with the salicylic acid (SA) defence hormone analogue Benzothiadiazole (BTH), or the immunogenic peptide flg22, induced Exo70B2 transport into the vacuole. We uncovered two ATG8-interacting motifs (AIMs) located in the C-terminal domain (C-domain) of Exo70B2 that mediate its recruitment into the vacuole. Moreover, we also show that Exo70B2 is phosphorylated near the AIMs and mimicking phosphorylation enhanced ATG8 interaction. Finally, Exo70B2 phosphonull lines were hypersensitive to BTH and more resistant to avirulent bacteria which induce SA production. Our results suggests a molecular mechanism in which phosphorylation of Exo70B2 by MPK3 functions in a feed-back system linking cellular signalling to the secretory pathway.
Printed publications

Peters, K., Gorzolka, K., Bruelheide, H. & Neumann, S. Seasonal variation of secondary metabolites in nine different bryophytes Ecol Evol (2018) DOI: 10.1002/ece3.4361

Bryophytes occur in almost all land ecosystems and contribute to global biogeochemical cycles, ecosystem functioning, and influence vegetation dynamics. As growth and biochemistry of bryophytes are strongly dependent on the season, we analyzed metabolic variation across seasons with regard to ecological characteristics and phylogeny. Using bioinformatics methods, we present an integrative and reproducible approach to connect ecology with biochemistry. Nine different bryophyte species were collected in three composite samples in four seasons. Untargeted liquid chromatography coupled with mass spectrometry (LC/MS) was performed to obtain metabolite profiles. Redundancy analysis, Pearson's correlation, Shannon diversity, and hierarchical clustering were used to determine relationships among species, seasons, ecological characteristics, and hierarchical clustering. Metabolite profiles of Marchantia polymorpha and Fissidens taxifolius which are species with ruderal life strategy (R‐selected) showed low seasonal variability, while the profiles of the pleurocarpous mosses and Grimmia pulvinata which have characteristics of a competitive strategy (C‐selected) were more variable. Polytrichum strictum and Plagiomnium undulatum had intermediary life strategies. Our study revealed strong species‐specific differences in metabolite profiles between the seasons. Life strategies, growth forms, and indicator values for light and soil were among the most important ecological predictors. We demonstrate that untargeted Eco‐Metabolomics provide useful biochemical insight that improves our understanding of fundamental ecological strategies.
Printed publications

Khoonsari, P. E., Moreno, P., Bergmann, S., Burman, J., Capuccini, M., Carone, M., Cascante, M., de Atauri, P., Foguet, C., Gonzalez-Beltran, A., Hankemeier, T., Haug, K., He, S., Herman, S., Johnson, D., Kale, N., Larsson, A., Neumann, S., Peters, K., Pireddu, L., Rocca-Serra, P., Roger, P., Rueedi, R., Ruttkies, C., Sadawi, N., Salek, R. M., Sansone, S.-A., Schober, D., Selivanov, V., Thévenot, E. A., van Vliet, M., Zanetti, G., Steinbeck, C., Kultima, K. & Spjuth, O. Interoperable and scalable data analysis with microservices: Applications in Metabolomics BioRxiv (2018) DOI: 10.1101/213603

Developing a robust and performant data analysis workflow that integrates all necessary components whilst still being able to scale over multiple compute nodes is a challenging task. We introduce a generic method based on the microservice architecture, where software tools are encapsulated as Docker containers that can be connected into scientific workflows and executed in parallel using the Kubernetes container orchestrator. The access point is a virtual research environment which can be launched on-demand on cloud resources and desktop computers. IT-expertise requirements on the user side are kept to a minimum, and established workflows can be re-used effortlessly by any novice user. We validate our method in the field of metabolomics on two mass spectrometry studies, one nuclear magnetic resonance spectroscopy study and one fluxomics study, showing that the method scales dynamically with increasing availability of computational resources. We achieved a complete integration of the major software suites resulting in the first turn-key workflow encompassing all steps for mass-spectrometry-based metabolomics including preprocessing, multivariate statistics, and metabolite identification. Microservices is a generic methodology that can serve any scientific discipline and opens up for new types of large-scale integrative science.

Zembek, P., Danilecka, A., Hoser, R., Eschen-Lippold, L., Benicka, M., Grech-Baran, M., Rymaszewski, W., Barymow-Filoniuk, I., Morgiewicz, K., Kwiatkowski, J., Piechocki, M., Poznanski, J., Lee, J., Hennig, J. & Krzymowska, M. Two Strategies of Pseudomonas syringae to Avoid Recognition of the HopQ1 Effector in Nicotiana Species Front Plant Sci 9, 978, (2018) DOI: 10.3389/fpls.2018.00978

Pseudomonas syringae employs a battery of type three secretion effectors to subvert plant immune responses. In turn, plants have developed receptors that recognize some of the bacterial effectors. Two strain-specific HopQ1 effector variants (for Hrp outer protein Q) from the pathovars phaseolicola 1448A (Pph) and tomato DC3000 (Pto) showed considerable differences in their ability to evoke disease symptoms in Nicotiana benthamiana. Surprisingly, the variants differ by only six amino acids located mostly in the N-terminal disordered region of HopQ1. We found that the presence of serine 87 and leucine 91 renders PtoHopQ1 susceptible to N-terminal processing by plant proteases. Substitutions at these two positions did not strongly affect PtoHopQ1 virulence properties in a susceptible host but they reduced bacterial growth and accelerated onset of cell death in a resistant host, suggesting that N-terminal mutations rendered PtoHopQ1 susceptible to processing in planta and, thus, represent a mechanism of recognition avoidance. Furthermore, we found that co-expression of HopR1, another effector encoded within the same gene cluster masks HopQ1 recognition in a strain-dependent manner. Together, these data suggest that HopQ1 is under high host-pathogen co-evolutionary selection pressure and P. syringae may have evolved differential effector processing or masking as two independent strategies to evade HopQ1 recognition, thus revealing another level of complexity in plant – microbe interactions.

Schober, D., Jacob, D., Wilson, M., Cruz, J. A., Marcu, A., Grant, J. R., Moing, A., Deborde, C., de Figueiredo, L. F., Haug, K., Rocca-Serra, P., Easton, J., Ebbels, T. M. D., Hao, J., Ludwig, C., Günther, U. L., Rosato, A., Klein, M. S., Lewis, I. A., Luchinat, C., Jones, A. R., Grauslys, A., Larralde, M., Yokochi, M., Kobayashi, N., Porzel, A., Griffin, J. L., Viant, M. R., Wishart, D. S., Steinbeck, C., Salek, R. M. & Neumann, S. nmrML: A Community Supported Open Data Standard for the Description, Storage, and Exchange of NMR Data Anal Chem 90, 649–656, (2018) DOI: 10.1021/acs.analchem.7b02795

NMR is a widely used analytical technique with a growing number of repositories available. As a result, demands for a vendor-agnostic, open data format for long-term archiving of NMR data have emerged with the aim to ease and encourage sharing, comparison, and reuse of NMR data. Here we present nmrML, an open XML-based exchange and storage format for NMR spectral data. The nmrML format is intended to be fully compatible with existing NMR data for chemical, biochemical, and metabolomics experiments. nmrML can capture raw NMR data, spectral data acquisition parameters, and where available spectral metadata, such as chemical structures associated with spectral assignments. The nmrML format is compatible with pure-compound NMR data for reference spectral libraries as well as NMR data from complex biomixtures, i.e., metabolomics experiments. To facilitate format conversions, we provide nmrML converters for Bruker, JEOL and Agilent/Varian vendor formats. In addition, easy-to-use Web-based spectral viewing, processing, and spectral assignment tools that read and write nmrML have been developed. Software libraries and Web services for data validation are available for tool developers and end-users. The nmrML format has already been adopted for capturing and disseminating NMR data for small molecules by several open source data processing tools and metabolomics reference spectral libraries, e.g., serving as storage format for the MetaboLights data repository. The nmrML open access data standard has been endorsed by the Metabolomics Standards Initiative (MSI), and we here encourage user participation and feedback to increase usability and make it a successful standard.

Peters, K., Worrich, A., Weinhold, A., Alka, O., Balcke, G., Birkemeyer, C., Bruelheide, H., Calf, O. W., Dietz, S., Dührkop, K., Gaquerel, E., Heinig, U., Kücklich, M., Macel, M., Müller, C., Poeschl, Y., Pohnert, G., Ristok, C., Rodríguez, V. M., Ruttkies, C., Schuman, M., Schweiger, R., Shahaf, N., Steinbeck, C., Tortosa, M., Treutler, H., Ueberschaar, N., Velasco, P., Weiß, B. M., Widdig, A., Neumann, S. & van Dam, N. M. Current Challenges in Plant Eco-Metabolomics Int J Mol Sci 19, 1385, (2018) DOI: 10.3390/ijms19051385

The relatively new research discipline of Eco-Metabolomics is the application of metabolomics techniques to ecology with the aim to characterise biochemical interactions of organisms across different spatial and temporal scales. Metabolomics is an untargeted biochemical approach to measure many thousands of metabolites in different species, including plants and animals. Changes in metabolite concentrations can provide mechanistic evidence for biochemical processes that are relevant at ecological scales. These include physiological, phenotypic and morphological responses of plants and communities to environmental changes and also interactions with other organisms. Traditionally, research in biochemistry and ecology comes from two different directions and is performed at distinct spatiotemporal scales. Biochemical studies most often focus on intrinsic processes in individuals at physiological and cellular scales. Generally, they take a bottom-up approach scaling up cellular processes from spatiotemporally fine to coarser scales. Ecological studies usually focus on extrinsic processes acting upon organisms at population and community scales and typically study top-down and bottom-up processes in combination. Eco-Metabolomics is a transdisciplinary research discipline that links biochemistry and ecology and connects the distinct spatiotemporal scales. In this review, we focus on approaches to study chemical and biochemical interactions of plants at various ecological levels, mainly plant–organismal interactions, and discuss related examples from other domains. We present recent developments and highlight advancements in Eco-Metabolomics over the last decade from various angles. We further address the five key challenges: (1) complex experimental designs and large variation of metabolite profiles; (2) feature extraction; (3) metabolite identification; (4) statistical analyses; and (5) bioinformatics software tools and workflows. The presented solutions to these challenges will advance connecting the distinct spatiotemporal scales and bridging biochemistry and ecology

Döll, S., Kuhlmann, M., Rutten, T., Mette, M. F., Scharfenberg, S., Petridis, A., Berreth, D.-C. & Mock, H.-P. Accumulation of the coumarin scopolin under abiotic stress conditions is mediated by the Arabidopsis thaliana THO/TREX complex Plant J 93, 431-444, (2018) DOI: 10.1111/tpj.13797

Secondary metabolites are involved in the plant stress response. Among these are scopolin and its active form scopoletin, which are coumarin derivatives associated with reactive oxygen species scavenging and pathogen defence. Here we show that scopolin accumulation can be induced in the root by osmotic stress and in the leaf by low‐temperature stress in Arabidopsis thaliana. A genetic screen for altered scopolin levels in A. thaliana revealed a mutant compromised in scopolin accumulation in response to stress; the lesion was present in a homologue of THO1 coding for a subunit of the THO/TREX complex. The THO/TREX complex contributes to RNA silencing, supposedly by trafficking precursors of small RNAs. Mutants defective in THO, AGO1, SDS3 and RDR6 were impaired with respect to scopolin accumulation in response to stress, suggesting a mechanism based on RNA silencing such as the trans‐acting small interfering RNA pathway, which requires THO/TREX function.

Sopeña‐Torres, S., Jordá, L., Sánchez‐Rodríguez, C., Miedes, E., Escudero, V., Swami, S., López, G., Piślewska‐Bednarek, M., Lassowskat, I., Lee, J., Gu, Y., Haigis, S., Alexander, D., Pattathil, S., Muñoz‐Barrios, A., Bednarek, P., Somerville, S., Schulze‐Lefert, P., Hahn, M. G., Scheel, D. & Molina, A. YODA MAP3K kinase regulates plant immune responses conferring broad‐spectrum disease resistance New Phytol 218, 661-680, (2018) DOI: 10.1111/nph.15007


Furlan, G., Nakagami, H., Eschen-Lippold, L., Jiang, X., Majovsky, P., Kowarschik, K., Hoehenwarter, W., Lee, J. & Trujillo, M. Changes in PUB22 Ubiquitination Modes Triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 Dampen the Immune Response Plant Cell 29, 726-745, (2017) DOI: 10.1105/tpc.16.00654

Crosstalk between post-translational modifications such as ubiquitination and phosphorylation play key roles in controlling the duration and intensity of signalling events to ensure cellular homeostasis. However, the molecular mechanisms underlying the regulation of negative feedback loops remain poorly understood. Here we uncover a pathway in Arabidopsis thaliana by which a negative feedback loop involving the E3 ubiquitin ligase PUB22 that dampens the immune response is triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3), best known for its function in the activation of signalling. PUB22's stability is controlled by MPK3-mediated phosphorylation of residues localized in and adjacent to the E2 docking domain. We show that phosphorylation is critical for stabilization by inhibiting PUB22 oligomerization and thus autoubiquitination. The activity switch allows PUB22 to dampen the immune response. This regulatory mechanism also suggests that autoubiquitination, which is inherent to most single unit E3s in vitro, can function as a self-regulatory mechanism in vivo. 

Herz, K., Dietz, S., Haider, S., Jandt, U., Scheel, D. & Bruelheide, H. Predicting individual plant performance in grasslands. Ecol Evol 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.
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