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Publikation

Ried, M. K.; Banhara, A.; Hwu, F.-Y.; Binder, A.; Gust, A. A.; Höfle, C.; Hückelhoven, R.; Nürnberger, T.; Parniske, M. A set of Arabidopsis genes involved in the accommodation of the downy mildew pathogen Hyaloperonospora arabidopsidis PLOS Pathog 15, e1007747, (2019) DOI: 10.1371/journal.ppat.1007747

The intracellular accommodation structures formed by plant cells to host arbuscular mycorrhiza fungi and biotrophic hyphal pathogens are cytologically similar. Therefore we investigated whether these interactions build on an overlapping genetic framework. In legumes, the malectin-like domain leucine-rich repeat receptor kinase SYMRK, the cation channel POLLUX and members of the nuclear pore NUP107-160 subcomplex are essential for symbiotic signal transduction and arbuscular mycorrhiza development. We identified members of these three groups in Arabidopsis thaliana and explored their impact on the interaction with the oomycete downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). We report that mutations in the corresponding genes reduced the reproductive success of Hpa as determined by sporangiophore and spore counts. We discovered that a developmental transition of haustorial shape occurred significantly earlier and at higher frequency in the mutants. Analysis of the multiplication of extracellular bacterial pathogens, Hpa-induced cell death or callose accumulation, as well as Hpa- or flg22-induced defence marker gene expression, did not reveal any traces of constitutive or exacerbated defence responses. These findings point towards an overlap between the plant genetic toolboxes involved in the interaction with biotrophic intracellular hyphal symbionts and pathogens in terms of the gene families involved.
Publikation

Girardin, A.; Wang, T.; Ding, Y.; Keller, J.; Buendia, L.; Gaston, M.; Ribeyre, C.; Gasciolli, V.; Auriac, M.-C.; Vernié, T.; Bendahmane, A.; Ried, M. K.; Parniske, M.; Morel, P.; Vandenbussche, M.; Schorderet, M.; Reinhardt, D.; Delaux, P.-M.; Bono, J.-J.; Lefebvre, B. LCO Receptors Involved in Arbuscular Mycorrhiza Are Functional for Rhizobia Perception in Legumes Curr Biol 29, 4249-4259.e5, (2019) DOI: 10.1016/j.cub.2019.11.038

Bacterial lipo-chitooligosaccharides (LCOs) are key mediators of the nitrogen-fixing root nodule symbiosis (RNS) in legumes. The isolation of LCOs from arbuscular mycorrhizal fungi suggested that LCOs are also signaling molecules in arbuscular mycorrhiza (AM). However, the corresponding plant receptors have remained uncharacterized. Here we show that petunia and tomato mutants in the LysM receptor-like kinases LYK10 are impaired in AM formation. Petunia and tomato LYK10 proteins have a high affinity for LCOs (Kd in the nM range) comparable to that previously reported for a legume LCO receptor essential for the RNS. Interestingly, the tomato and petunia LYK10 promoters, when introduced into a legume, were active in nodules similarly to the promoter of the legume orthologous gene. Moreover, tomato and petunia LYK10 coding sequences restored nodulation in legumes mutated in their orthologs. This combination of genetic and biochemical data clearly pinpoints Solanaceous LYK10 as part of an ancestral LCO perception system involved in AM establishment, which has been directly recruited during evolution of the RNS in legumes.
Publikation

Drost, H.-G.; Bellstädt, J.; Ó'Maoiléidigh, D. S.; Silva, A. T.; Gabel, A.; Weinholdt, C.; Ryan, P. T.; Dekkers, B. J. W.; Bentsink, L.; Hilhorst, H. W. M.; Ligterink, W.; Wellmer, F.; Grosse, I.; Quint, M. Post-embryonic Hourglass Patterns Mark Ontogenetic Transitions in Plant Development Mol Biol Evol 33, 1158-1163, (2016) DOI: 10.1093/molbev/msw039

The historic developmental hourglass concept depicts the convergence of animal embryos to a common form during the phylotypic period. Recently, it has been shown that a transcriptomic hourglass is associated with this morphological pattern, consistent with the idea of underlying selective constraints due to intense molecular interactions during body plan establishment. Although plants do not exhibit a morphological hourglass during embryogenesis, a transcriptomic hourglass has nevertheless been identified in the model plant Arabidopsis thaliana. Here, we investigated whether plant hourglass patterns are also found postembryonically. We found that the two main phase changes during the life cycle of Arabidopsis, from embryonic to vegetative and from vegetative to reproductive development, are associated with transcriptomic hourglass patterns. In contrast, flower development, a process dominated by organ formation, is not. This suggests that plant hourglass patterns are decoupled from organogenesis and body plan establishment. Instead, they may reflect general transitions through organizational checkpoints. 
Bücher und Buchkapitel

Parniske, M.; Ried, M. Wahrnehmung und Interpretation symbiontischer Signale durch Pflanzen und ihre bakteriellen Partner (Deigele, C., ed.). 105-116, (2016) ISBN: 978-3-89937-214-4

Mutualistic symbioses between plant roots and microorganisms can reduce the demand for chemical fertilizers in agriculture. Most crops are able to establish arbuscular mycorrhiza (AM) symbiosis with fungi to take up phosphate more efficiently. A second symbiosis, nitrogen-fixing root nodule symbiosis, supersedes energy-intensive nitrogen fertilization: Legumes such as peas, clover and soybeans take up rhizobia – special bacteria that are capable of converting atmospheric nitrogen into ammonium – into their root cells. Plant root cells perceive rhizobia and AM fungi via very similar signaling molecules (N-acetylglucosamine tetra- or pentamers), even though the resultant developmental processes differ strongly. Interestingly, N-acetylglucosamine containing signals including fungal chitin- and bacterial peptidoglycan-fragments from their cell walls, also play a role in the recognition of pathogenic microorganisms.Despite the intrinsic sustainability potential of the nitrogen-fixing root nodule symbiosis, too much of a good thing, however, has led to global problems: The massive increase in global meat production is largely based on soybean. Large scale soybean monoculture destroyed ecosystems in South America. Large scale animal production results in excessive methane and nitrogen release into the environment, which causes climate change and death zones in marine ecosystems, respectively. This calls for a considerable reduction in meat consumption.
Publikation

Ryan,P. T.; Ó’Maoiléidigh, D. S.; Drost, H.-G.; Kwaśniewska, D.; Gabel, A.; Grosse, I.; Graciet, E.; Quint, M.; Wellmer, F. Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation BMC Genomics 16, 488 , (2015) DOI: 10.1186/s12864-015-1699-6

Background:The formation of flowers is one of the main model systems to elucidate the molecular mechanisms that control developmental processes in plants. Although several studies have explored gene expression during flower development in the model plant Arabidopsis thalianaon a genome-wide scale, a continuous series of expression data from the earliest floral stages until maturation has been lacking. Here, we used a floral induction system to closethis information gap and to generate a reference dataset for stage-specific gene expression during flower formation.Results:Using a floral induction system, we collected floral buds at 14 different stages from the time of initiation until maturation. Using whole-genome microarray analysis, we identified 7,405 genes that exhibit rapid expression changes during flower development. These genes comprise many known floral regulators and we found that the expression profiles for these regulators match their known expression patterns, thus validating the dataset. We analyzed groups ofco-expressed genes for over-represented cellular and developmental functions through Gene Ontology analysis and found that they could be assigned specific patterns of activities, which are in agreement with the progression of flower development. Furthermore, by mapping binding sites of floral organ identity factors onto our dataset, we were able to identify gene groups that are likely predominantly under control of these transcriptional regulators. We furtherfound that the distribution of paralogs among groups of co-expressed genes varies considerably, with genes expressed predominantly at early and intermediate stages of flower development showing the highest proportion of such genes.Conclusions:Our results highlight and describe the dynamic expression changes undergone by a large numberof genes during flower development. They further provide a comprehensive reference dataset for temporal gene expression during flower formation and we demonstrate that it can be used to integrate data from other genomics approaches such as genome-wide localization studies of transcription factor binding sites.
Publikation

Drost, H.-G.; Gabel, A.; Grosse, I.; Quint, M. Evidence for Active Maintenance of Phylotranscriptomic Hourglass Patterns in Animal and Plant Embryogenesis Mol Biol Evol 32, 1221-1231, (2015) DOI: 10.1093/molbev/msv012

The developmental hourglass model has been used to describe the morphological transitions of related species throughout embryogenesis. Recently, quantifiable approaches combining transcriptomic and evolutionary information provided novel evidence for the presence of a phylotranscriptomic hourglass pattern across kingdoms. As its biological function is unknown it remains speculative whether this pattern is functional or merely represents a nonfunctional evolutionary relic. The latter would seriously hamper future experimental approaches designed to test hypotheses regarding its function. Here, we address this question by generating transcriptome divergence index (TDI) profiles across embryogenesis of Danio rerio, Drosophila melanogaster, and Arabidopsis thaliana. To enable meaningful evaluation of the resulting patterns, we develop a statistical test that specifically assesses potential hourglass patterns. Based on this objective measure we find that two of these profiles follow a statistically significant hourglass pattern with the most conserved transcriptomes in the phylotypic periods. As the TDI considers only recent evolutionary signals, this indicates that the phylotranscriptomic hourglass pattern is not a rudiment but possibly actively maintained, implicating the existence of some linked biological function associated with embryogenesis in extant species.
Preprints

Drost, H.-G.; Bellstädt, J.; Ó'Maoiléidigh, D. S.; Silva, A. T.; Gabel, A.; Weinholdt, C.; Ryan, P. T.; Dekkers, B. J. W.; Bentsink, L.; Hilhorst, H. W. M.; Ligterink, W.; Wellmer, F.; Grosse, I.; Quint, M. Post-embryonic hourglass patterns mark ontogenetic transitions in plant development bioRxiv (2015) DOI: 10.1101/035527

The historic developmental hourglass concept depicts the convergence of animal embryos to a common form during the phylotypic period. Recently, it has been shown that a transcriptomic hourglass is associated with this morphological pattern, consistent with the idea of underlying selective constraints due to intense molecular interactions during body plan establishment. Although plants do not exhibit a morphological hourglass during embryogenesis, a transcriptomic hourglass has nevertheless been identified in the model plant Arabidopsis thaliana. Here, we investigated whether plant hourglass patterns are also found post-embryonically. We found that the two main phase changes during the life cycle of Arabidopsis, from embryonic to vegetative and from vegetative to reproductive development, are associated with transcriptomic hourglass patterns. In contrast, flower development, a process dominated by organ formation, is not. This suggests that plant hourglass patterns are decoupled from organogenesis and body plan establishment. Instead, they may reflect general transitions through organizational checkpoints.
Publikation

Ried, M. K.; Antolín-Llovera, M.; Parniske, M. Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases eLife 3, e03891, (2014) DOI: 10.7554/eLife.03891

Symbiosis Receptor-like Kinase (SYMRK) is indispensable for the development of phosphate-acquiring arbuscular mycorrhiza (AM) as well as nitrogen-fixing root nodule symbiosis, but the mechanisms that discriminate between the two distinct symbiotic developmental fates have been enigmatic. In this study, we show that upon ectopic expression, the receptor-like kinase genes Nod Factor Receptor 1 (NFR1), NFR5, and SYMRK initiate spontaneous nodule organogenesis and nodulation-related gene expression in the absence of rhizobia. Furthermore, overexpressed NFR1 or NFR5 associated with endogenous SYMRK in roots of the legume Lotus japonicus. Epistasis tests revealed that the dominant active SYMRK allele initiates signalling independently of either the NFR1 or NFR5 gene and upstream of a set of genes required for the generation or decoding of calcium-spiking in both symbioses. Only SYMRK but not NFR overexpression triggered the expression of AM-related genes, indicating that the receptors play a key role in the decision between AM- or root nodule symbiosis-development.
Publikation

Antolín-Llovera, M.; Ried, M. K.; Parniske, M. Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE Ectodomain Promotes Complex Formation with Nod Factor Receptor 5 Curr Biol 24, 422-427, (2014) DOI: 10.1016/j.cub.2013.12.053

Plants form root symbioses with fungi and bacteria to improve their nutrient supply. SYMBIOSIS RECEPTOR-LIKE KINASE (SYMRK) is required for phosphate-acquiring arbuscular mycorrhiza, as well as for the nitrogen-fixing root nodule symbiosis of legumes [1] and actinorhizal plants [2, 3], but its precise function was completely unclear. Here we show that the extracytoplasmic region of SYMRK, which comprises three leucine-rich repeats (LRRs) and a malectin-like domain (MLD) related to a carbohydrate-binding protein from Xenopus laevis [4], is cleaved to release the MLD in the absence of symbiotic stimulation. A conserved sequence motif—GDPC—that connects the MLD to the LRRs is required for MLD release. We discovered that Nod factor receptor 5 (NFR5) [5, 6, 7, 8] forms a complex with the SYMRK version that remains after MLD release (SYMRK-ΔMLD). SYMRK-ΔMLD outcompeted full-length SYMRK for NFR5 interaction, indicating that the MLD negatively interferes with complex formation. SYMRK-ΔMLD is present at lower amounts than MLD, suggesting rapid degradation after MLD release. A deletion of the entire extracytoplasmic region increased protein abundance, suggesting that the LRR region promotes degradation. Curiously, this deletion led to excessive infection thread formation, highlighting the importance of fine-tuned regulation of SYMRK by its ectodomain.
Publikation

Antolín-Llovera, M.; Petutsching, E. K.; Ried, M. K.; Lipka, V.; Nürnberger, T.; Robatzek, S.; Parniske, M. Knowing your friends and foes - plant receptor-like kinases as initiators of symbiosis or defence New Phytol 204, 791-802, (2014) DOI: 10.1111/nph.13117

The decision between defence and symbiosis signalling in plants involves alternative and modular plasma membrane‐localized receptor complexes. A critical step in their activation is ligand‐induced homo‐ or hetero‐oligomerization of leucine‐rich repeat (LRR)‐ and/or lysin motif (LysM) receptor‐like kinases (RLKs). In defence signalling, receptor complexes form upon binding of pathogen‐associated molecular patterns (PAMPs), including the bacterial flagellin‐derived peptide flg22, or chitin. Similar mechanisms are likely to operate during the perception of microbial symbiont‐derived (lipo)‐chitooligosaccharides. The structurally related chitin‐oligomer ligands chitooctaose and chitotetraose trigger defence and symbiosis signalling, respectively, and their discrimination involves closely related, if not identical, LysM‐RLKs. This illustrates the demand for and the challenges imposed on decision mechanisms that ensure appropriate signal initiation. Appropriate signalling critically depends on abundance and localization of RLKs at the cell surface. This is regulated by internalization, which also provides a mechanism for the removal of activated signalling RLKs. Abundance of the malectin‐like domain (MLD)‐LRR‐RLK Symbiosis Receptor‐like Kinase (SYMRK) is additionally controlled by cleavage of its modular ectodomain, which generates a truncated and rapidly degraded RLK fragment. This review explores LRR‐ and LysM‐mediated signalling, the involvement of MLD‐LRR‐RLKs in symbiosis and defence, and the role of endocytosis in RLK function.
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