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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. 

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.

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 thaliana

on 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 close

this 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 of

co-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 further

found 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

Dekkers, B.J.W., Pearce, S., van Bolderen-Veldkamp, R.P., Marshall, A., Widera, P., Gilbert, J., Drost, H.-G., Basseli, G.W., Müller, K., King, J.R., Wood, A.T.A., Grosse, I., Quint, M., Krasnogor, N., Leubner-Metzger, G. & Holdsworth, M.J. & Bentsink, L. Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination Plant Physiol 163, 205-215, (2013)

Seed germination is a critical stage in the plant life cycle and the first step toward successful plant establishment. Therefore, understanding

germination is of important ecological and agronomical relevance. Previous research revealed that different seed compartments (testa,

endosperm, and embryo) control germination, but little is known about the underlying spatial and temporal transcriptome changes that

lead to seed germination. We analyzed genome-wide expression in germinating Arabidopsis (Arabidopsis thaliana) seedswith both temporal

and spatial detail and provide Web-accessible visualizations of the data reported (vseed.nottingham.ac.uk). We show the potential of this highresolution

data set for the construction ofmeaningful coexpression networks, which provide insight into the genetic control of germination.

The data set reveals two transcriptional phases during germination that are separated by testa rupture. The first phase is marked by large

transcriptome changes as the seed switches from a dry, quiescent state to a hydrated and active state. At the end of this first transcriptional

phase, the number of differentially expressed genes between consecutive time points drops. This increases again at testa rupture, the start of

the second transcriptional phase. Transcriptome data indicate a role for mechano-induced signaling at this stage and subsequently highlight

the fates of the endosperm and radicle: senescence and growth, respectively. Finally, using a phylotranscriptomic approach, we show that

expression levels of evolutionarily young genes drop during the first transcriptional phase and increase during the second phase.Evolutionarily old genes show an opposite pattern, suggesting a more conserved transcriptome prior to the completion of germination.

Publikation

Quint, M., Drost, H-G., Gabel, A., Ullrich, K., Bönner, M. & Grosse, I. A transcriptomic hourglass in plant embryogenesis Nature 490, 98-101, (2012)

Animal and plant development starts with a constituting phase called embryogenesis, which evolved independently in both lineages1. Comparative anatomy of vertebrate developmentbased on the Meckel-Serrès law2 and von Baers laws of embryology3 from the early nineteenth centuryshows that embryos from various taxa appear different in early stages, converge to a similar form during mid-embryogenesis, and again diverge in later stages. This morphogenetic series is known as the embryonic hourglass4, 5, and its bottleneck of high conservation in mid-embryogenesis is referred to as the phylotypic stage6. Recent analyses in zebrafish and Drosophila embryos provided convincing molecular support for the hourglass model, because during the phylotypic stage the transcriptome was dominated by ancient genes7 and global gene expression profiles were reported to be most conserved8. Although extensively explored in animals, an embryonic hourglass has not been reported in plants, which represent the second major kingdom in the tree of life that evolved embryogenesis. Here we provide phylotranscriptomic evidence for a molecular embryonic hourglass in Arabidopsis thaliana, using two complementary approaches. This is particularly significant because the possible absence of an hourglass based on morphological features in plants suggests that morphological and molecular patterns might be uncoupled. Together with the reported developmental hourglass patterns in animals, these findings indicate convergent evolution of the molecular hourglass and a conserved logic of embryogenesis across kingdoms.

Publikation

Delker, C., Pöschl, Y., Raschke, A., Ullrich, K., Ettingshausen, S., Hauptmann, V., Grosse, I. & Quint, M. Natural variation of transcriptional auxin response networks in Arabidopsis thaliana Plant Cell 22, 2184-2200, (2010)

Natural variation has been observed for various traits in Arabidopsis thaliana. Here, we investigated natural variation in the context of physiological and transcriptional responses to the phytohormone auxin, a key regulator of plant development. A survey of the general extent of natural variation to auxin stimuli revealed significant physiological variation among 20 genetically diverse natural accessions. Moreover, we observed dramatic variation on the global transcriptome level after induction of auxin responses in seven accessions. Although we detect isolated cases of major-effect polymorphisms, sequencing of signaling genes revealed sequence conservation, making selective pressures that favor functionally different protein variants among accessions unlikely. However, coexpression analyses of a priori defined auxin signaling networks identified variations in the transcriptional equilibrium of signaling components. In agreement with this, cluster analyses of genome-wide expression profiles followed by analyses of a posteriori defined gene networks revealed accession-specific auxin responses. We hypothesize that quantitative distortions in the ratios of interacting signaling components contribute to the detected transcriptional variation, resulting in physiological variation of auxin responses among accessions.

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