Hajk-Georg Drost

A transcriptomic hourglass in plant embryogenesis

Animal and plant development starts with a constituting phase called embryogenesis, which evolved independently in both lineages. Comparative anatomy of vertebrate development—based on the Meckel-Serrès law and von Baer’s laws of embryology from the early nineteenth century—shows 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 ‘hourglass’, and its bottleneck of high conservation in mid-embryogenesis is referred to as the phylotypic stage. 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 genes and global gene expression profiles were reported to be most conserved. 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.

Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination

Gene expression profiling in two seed compartments uncovers two transcriptional phases during seed germination that are separated by testa rupture. 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) seeds with both temporal and spatial detail and provide Web-accessible visualizations of the data reported (vseed.nottingham.ac.uk). We show the potential of this high-resolution data set for the construction of meaningful 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.

Evidence for active maintenance of phylotranscriptomic hourglass patterns in animal and plant embryogenesis

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.

Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation

BackgroundThe 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.ResultsUsing 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.ConclusionsOur results highlight and describe the dynamic expression changes undergone by a large number of 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.

Post-embryonic Hourglass Patterns Mark Ontogenetic Transitions in Plant Development

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.

Biomartr: genomic data retrieval with R.

Motivation: Retrieval and reproducible functional annotation of genomic data are crucial in biology. However, the current poor usability and transparency of retrieval methods hinders reproducibility. Here we present an open source R package, biomartr, which provides a comprehensive easy‐to‐use framework for automating data retrieval and functional annotation for meta‐genomic approaches. The functions of biomartr achieve a high degree of clarity, transparency and reproducibility of analyses. Results: The biomartr package implements straightforward functions for bulk retrieval of all genomic data or data for selected genomes, proteomes, coding sequences and annotation files present in databases hosted by the National Center for Biotechnology Information (NCBI) and European Bioinformatics Institute (EMBL‐EBI). In addition, biomartr communicates with the BioMart database for functional annotation of retrieved sequences. Comprehensive documentation of biomartr functions and five tutorial vignettes provide step‐by‐step instructions on how to use the package in a reproducible manner. Availability and Implementation: The open source biomartr package is available at https://github.com/HajkD/biomartr and https://cran.r‐project.org/web/packages/biomartr/index.html. Contact: hgd23@cam.ac.uk Supplementary information: Supplementary data are available at Bioinformatics online.

myTAI: evolutionary transcriptomics with R

Abstract Motivation Next Generation Sequencing (NGS) technologies generate a large amount of high quality transcriptome datasets enabling the investigation of molecular processes on a genomic and metagenomic scale. These transcriptomics studies aim to quantify and compare the molecular phenotypes of the biological processes at hand. Despite the vast increase of available transcriptome datasets, little is known about the evolutionary conservation of those characterized transcriptomes. Results The myTAI package implements exploratory analysis functions to infer transcriptome conservation patterns in any transcriptome dataset. Comprehensive documentation of myTAI functions and tutorial vignettes provide step-by-step instructions on how to use the package in an exploratory and computationally reproducible manner. Availability and implementation The open source myTAI package is available at https://github.com/HajkD/myTAI and https://cran.r-project.org/web/packages/myTAI/index.html. Supplementary information Supplementary data are available at Bioinformatics online.

Cross-kingdom comparison of the developmental hourglass

The developmental hourglass model has its foundations in classic anatomical studies by von Baer and Haeckel. In this context, even the conservation of animal body plans has been explained by evolutionary constraints acting on mid-embryogenic development. Recent studies have shown that developmental hourglass patterns also exist on the transcriptomic level, mirroring the corresponding morphological patterns. The identification of similar patterns in embryonic, post-embryonic, and life cycle spanning transcriptomes in plant and fungus development, however, contradict the notion of a direct coupling between morphological and molecular patterns. To explain the existence of hourglass patterns across kingdoms and developmental processes, we propose the organizational checkpoint model that integrates the developmental hourglass model into a framework of transcriptome switches.

Capturing Evolutionary Signatures in Transcriptomes with myTAI

Combining transcriptome data of biological processes or response to stimuli with evolutionary information such as the phylogenetic conservation of genes or their sequence divergence rates enables the investigation of evolutionary constraints on these processes or responses. Such phylotranscriptomic analyses recently unraveled that mid-developmental transcriptomes of fly, fish, and cress were dominated by evolutionarily conserved genes and genes under negative selection and thus recapitulated the developmental hourglass on the transcriptomic level. Here, we present a protocol for performing phylotranscriptomic analyses on any biological process of interest. When applying this protocol, users are capable of detecting different evolutionary constraints acting on different stages of the biological process of interest in any species. For each step of the protocol, modular and easy-to-use open-source software tools are provided, which enable a broad range of scientists to apply phylotranscriptomic analyses to a wide spectrum of biological questions.

High-frequency recombination between members of an LTR retrotransposon family during transposition bursts.

Retrotransposons containing long terminal repeats (LTRs) form a substantial fraction of eukaryotic genomes. The timing of past transposition can be estimated by quantifying the accumulation of mutations in initially identical LTRs. This way, retrotransposons are divided into young, potentially mobile elements, and old that moved thousands or even millions of years ago. Both types are found within a single retrotransposon family and it is assumed that the old members will remain immobile and degenerate further. Here, we provide evidence in Arabidopsis that old members enter into replication/transposition cycles through high rates of intra-family recombination. The recombination occurs pairwise, resembling the formation of recombinant retroviruses. Thus, each transposition burst generates a novel progeny population of chromosomally integrated LTR retrotransposons consisting of pairwise recombination products produced in a process comparable the sexual exchange of genetic information. Our observations provide an explanation for the reported high rates of sequence diversification in retrotransposons.Retrotransposons are abundant in eukaryotic genomes. Here, Sanchez et al. show evidence of high-frequency recombination between members of an LTR retrotransposon family during transposition bursts in Arabidopsis.