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Publikationen - Stress- und Entwicklungsbiologie

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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.

Thum, A.; Mönchgesang, S.; Westphal, L.; Lübken, T.; Rosahl, S.; Neumann, S.; Posch, S. Supervised Penalized Canonical Correlation Analysis arXiv (2014)

The canonical correlation analysis (CCA) is commonly used to analyze data sets with paired data, e.g. measurements of gene expression and metabolomic intensities of the same experiments. This allows to find interesting relationships between the data sets, e.g. they can be assigned to biological processes. However, it can be difficult to interpret the processes and often the relationships observed are not related to the experimental design but to some unknown parameters.Here we present an extension of the penalized CCA, the supervised penalized approach (spCCA), where the experimental design is used as a third data set and the correlation of the biological data sets with the design data set is maximized to find interpretable and meaningful canonical variables. The spCCA was successfully tested on a data set of Arabidopsis thaliana with gene expression and metabolite intensity measurements and resulted in eight significant canonical variables and their interpretation. We provide an R-package under the GPL license.

Seybold, H.; Bortlik, J.; Conrads, B.; Hoehenwarter, W.; Romeis, T. Prioritization of abiotic and biotic stress responses by direct linkage of ABI1 phosphatase and CPK5 calcium-dependent protein kinase bioRxiv (2019) DOI: 10.1101/839662

In nature plants are constantly challenged by simultaneous abiotic and biotic stresses, and under conflicting stress scenarios prioritization of stress responses is required for plant survival. Calcium-dependent protein kinase CPK5 is a central hub in local and distal immune signaling, required upstream of hormone salicylic acid (SA)-dependent systemic acquired resistance (SAR). Here we show that CPK5 signaling-dependent immune responses are effectively blocked and pathogen resistance is reverted either upon treatment of plants with abscisic acid (ABA) or in genetic mutant backgrounds lacking PP2C phosphatase activities including abi1-2. Consistently, enhanced immune responses occur upon co-expression of CPK5 kinase with active variants of ABI1 phosphatase ABI1G180S and ABI1G181A. Biochemical studies and mass spectrometry-based phosphosite analysis reveal a direct ABI1 phosphatase-catalyzed de-phosphorylation of CPK5 at T98, a CPK5 auto-phosphorylation site. CPK5T98A, mimicking continuous de-phosphorylation through ABI1, correlates with an increase in kinase activity and CPK5 function in ROS production. CPK5T98D, mimicking a CPK5 auto-phosphorylated status under ABA-induced phosphatase inhibition, leads to inactivated CPK5 causative to an immediate stop of immune responses.Our work reveals an elegant mechanism for plant stress prioritization, where the ABA-dependent phosphatase ABI1, negative regulator of abiotic responses, functions as positive regulator of biotic stress responses, stabilizing CPK5-dependent immune responses in the absence of ABA. This mechanism allows continuous immune signaling during pathogen survey in environmentally non-challenging conditions. Under severe abiotic stress, immune signaling is discontinued via a direct biochemical intersection through a phosphatase/kinase pair recruiting two key regulatory enzymes of these antagonistic signaling pathways.

Jiang, X.; Hoehenwarter, W.; Scheel, D.; Lee, J. Phosphorylation of the CAMTA3 transcription factor triggers its destabilization and nuclear export bioRxiv (2019) DOI: 10.1101/825323

The calmodulin-binding transcription activator 3 (CAMTA3) is a repressor of immunity-related genes but an activator of cold-induced genes in plants. Post-transcriptional or -translational mechanisms have been proposed to control CAMTA3’s role in the crosstalk between immune and chilling responses. Here, we show that treatment with the bacterial flg22 elicitor, but not cold stress, induces a phospho-mobility shift of CAMTA3 proteins. Correspondingly, CAMTA3 is directly phosphorylated by two flg22-responsive mitogen-activated protein kinases (MAPKs), MPK3 and MPK6, which triggers CAMTA3 nuclear export and destabilization. SR1IP1, a substrate E3 ubiquitin ligase adaptor required for pathogen-induced CAMTA3 degradation, is shown here to be likely plasma-membrane-localized and therefore cannot physically interact with the nuclear CAMTA3. Despite the flg22-inducible re-localization of CAMTA3 to the cytoplasm, we failed to detect CAMTA3-SR1IP1 complexes. Hence, the role of SR1IP1 for CAMTA3 degradation needs to be re-evaluated. Surprisingly, flg22 elicitation can still induce nuclear export and phospho-mobility shift of a phospho-null CAMTA3 that cannot be phosphorylated by MAPKs, suggesting the participation of additional flg22-responsive kinase(s). A constitutively-active calcium-dependent protein kinase, CPK5, can stimulate a phospho-mobility shift in CAMTA3 similar to that induced by flg22. Although CPK5 can interact with CAMTA3, it did not directly phosphorylate CAMTA3, suggesting the requirement of a still unidentified downstream kinase or additional components. Overall, at least two flg22-responsive kinase pathways target CAMTA3 to induce degradation that presumably serves to remove CAMTA3 from target promoters and de-repress expression of defence genes.

Vainonen, J. P.; Shapiguzov, A.; Krasensky-Wrzaczek, J.; De Masi, R.; Gossens, R.; Danciu, I.; Battchikova, N.; Jonak, C.; Wirthmueller, L.; Wrzaczek, M.; Kangasjärvi, J. Arabidopsis Poly(ADP-ribose)-binding protein RCD1 interacts with Photoregulatory Protein Kinases in nuclear bodies bioRxiv (2020) DOI: 10.1101/2020.07.02.184937

Continuous reprograming of gene expression in response to environmental signals in plants is achieved through signaling hub proteins that integrate external stimuli and transcriptional responses. RADICAL-INDUCED CELL DEATH1 (RCD1) functions as a nuclear hub protein, which interacts with a variety of transcription factors with its C-terminal RST domain and thereby acts as a co-regulator of numerous plant stress reactions. Here a previously function for RCD1 as a novel plant PAR reader protein is shown; RCD1 functions as a scaffold protein, which recruits transcription factors to specific locations inside the nucleus in PAR-dependent manner. The N-terminal WWE- and PARP-like domains of RCD1 bind poly(ADP-ribose) (PAR) and determine its localization to nuclear bodies (NBs), which is prevented by chemical inhibition of PAR synthesis. RCD1 also binds and recruits Photoregulatory Protein Kinases (PPKs) to NBs. The PPKs, which have been associated with circadian clock, abscisic acid, and light signaling pathways, phosphorylate RCD1 at multiple sites in the intrinsically disordered region between the WWE- and PARP-like-domains, which affects the stability and function of RCD1 in the nucleus. Phosphorylation of RCD1 by PPKs provides a mechanism where turnover of a PAR-binding transcriptional co-regulator is controlled by nuclear phosphorylation signaling pathways.
Publikationen in Druck

Schulz, P.; Piepenburg, K.; Lintermann, R.; Herde, M.; Schöttler, M. A.; Schmidt, L. K.; Ruf, S.; Kudla, J.; Romeis, T.; Bock, R. Improving plant drought tolerance and growth under water limitation through combinatorial engineering of signaling networks Plant Biotechnol J (2020) DOI: 10.1111/pbi.13441

Agriculture is by far the biggest water consumer on our planet, accounting for 70 percent of all freshwater withdrawals. Climate change and a growing world population increase pressure on agriculture to use water more efficiently (‘more crop per drop’). Water‐use efficiency (WUE) and drought tolerance of crops are complex traits that are determined by many physiological processes whose interplay is not well understood. Here we describe a combinatorial engineering approach to optimize signaling networks involved in the control of stress tolerance. Screening a large population of combinatorially transformed plant lines, we identified a combination of calcium‐dependent protein kinase genes that confers enhanced drought stress tolerance and improved growth under water‐limiting conditions. Targeted introduction of this gene combination into plants increased plant survival under drought and enhanced growth under water‐limited conditions. Our work provides an efficient strategy for engineering complex signaling networks to improve plant performance under adverse environmental conditions, which does not depend on prior understanding of network function.
Publikationen in Druck

Trempel, F.; Eschen‐Lippold, L.; Bauer, N.; Ranf, S.; Westphal, L.; Scheel, D.; Lee, J. A mutation in Asparagine‐Linked Glycosylation 12 (ALG12) leads to receptor misglycosylation and attenuated responses to multiple microbial elicitors FEBS Lett (2020) DOI: 10.1002/1873-3468.13850

Changes in cellular calcium levels are one of the earliest signalling events in plants exposed to pathogens or other exogenous factors. In a genetic screen, we identified an Arabidopsis thaliana ‘changed calcium elevation 1 ’ (cce1 ) mutant with attenuated calcium response to the bacterial flagellin flg22 peptide and several other elicitors. Whole genome re‐sequencing revealed a mutation in ALG12 (Asparagine‐Linked Glycosylation 12 ) that encodes the mannosyltransferase responsible for adding the eighth mannose residue in an α‐1,6 linkage to the dolichol‐PP‐oligosaccharide N ‐glycosylation glycan tree precursors. While properly targeted to the plasma membrane, misglycosylation of several receptors in the cce1 background suggests that N ‐glycosylation is required for proper functioning of client proteins.
Publikationen in Druck

Wirthmueller, L.; Romeis, T. Sp(l)icing up PepR signalling Nat Plants (2020) DOI: 10.1038/s41477-020-0708-1

Alternative splicing provides a fundamental and ubiquitous mechanism of gene regulation. Stimuli-induced retention of introns introduces novel proteoforms with altered signalling output: full-length CPK28 blocks immune signalling, while a truncated variant, lacking calcium responsiveness, promotes it.

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.

Mönchgesang, S.; Strehmel, N.; Trutschel, D.; Westphal, L.; Neumann, S.; Scheel, D. Plant-to-plant variability in root metabolite profiles of 19 <i>Arabidopsis thaliana</i> accessions is substance-class-dependent Inter J Mol Sci 17, (2016) DOI: 10.3390/ijms17091565

Natural variation of secondary metabolism between different accessions of Arabidopsis thaliana (A. thaliana) has been studied extensively. In this study, we extended the natural variation approach by including biological variability (plant-to-plant variability) and analysed root metabolic patterns as well as their variability between plants and naturally occurring accessions. To screen 19 accessions of A. thaliana, comprehensive non-targeted metabolite profiling of single plant root extracts was performed using ultra performance liquid chromatography/electrospray ionization quadrupole time-of-flight mass spectrometry (UPLC/ESI-QTOF-MS) and gas chromatography/electron ionization quadrupole mass spectrometry (GC/EI-QMS). Linear mixed models were applied to dissect the total observed variance. All metabolic profiles pointed towards a larger plant-to-plant variability than natural variation between accessions and variance of experimental batches. Ratios of plant-to-plant to total variability were high and distinct for certain secondary metabolites. None of the investigated accessions displayed a specifically high or low biological variability for these substance classes. This study provides recommendations for future natural variation analyses of glucosinolates, flavonoids, and phenylpropanoids and also reference data for additional substance classes.
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