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Vandepoele, K.

Publications and source records attributed to Vandepoele, K..

At least 37 records · Page 2Linked to original sources

Identification of new leaf intrinsic yield genes using cross-species network analysis in plants

With the need to increase plant productivity, one of the challenges plant scientists are facing is to identify genes playing a role in beneficial plant traits. Moreover, even when such genes are found, it is generally not trivial to transfer this knowledge about gene function across species to identify functional orthologs. Here, we focused on the leaf to study plant growth. First, we built leaf growth transcriptional networks in Arabidopsis thaliana, maize (Zea mays), and aspen (Populus tremula). Next, known growth regulators, here defined as genes that when mutated or ectopically expressed alter plant growth, together with cross-species conserved networks, were used as guides to predict novel Arabidopsis growth regulators. Using an in-depth literature screening, 34 out of 100 top predicted growth regulators were confirmed to affect leaf phenotype when mutated or overexpressed and thus represent novel potential growth regulators. Globally, these new growth regulators were involved in cell cycle, plant defense responses, gibberellin, auxin, and brassinosteroid signaling. Phenotypic characterization of loss-of-function lines confirmed two newly predicted growth regulators to be involved in leaf growth (NPF6.4 and LATE MERISTEM IDENTITY2). In conclusion, the presented network approach offers an integrative cross-species strategy to identify new genes involved in plant growth and development. One-sentence summaryCross-species network analysis results in the identification and validation of new growth regulators in Arabidopsis.

plant biology↗

Multi-omics network-based functional annotation of unknown Arabidopsis genes

Unraveling gene functions is pivotal to understand the signaling cascades controlling plant development and stress responses. Given that experimental profiling is costly and labor intensive, the need for high-confidence computational annotations is evident. In contrast to detailed gene-specific functional information, transcriptomics data is widely available in both model and crop species. Here, we developed a novel automated function prediction (AFP) algorithm, leveraging complementary information present in multiple expression datasets through the analysis of study-specific gene co-expression networks. Benchmarking the prediction performance on recently characterized Arabidopsis thaliana genes, we showed that our method outperforms state-of-the-art expression-based approaches. Next, we predicted biological process annotations for known (n=15,790) and unknown (n=11,865) genes in A. thaliana and validated our predictions using experimental protein-DNA and protein-protein interaction data (covering >220 thousand interactions in total), obtaining a set of high-confidence functional annotations. 5,054 (42.6%) unknown genes were assigned at least one validated annotation, and 3,408 (53.0%) genes with only computational annotations gained at least one novel validated function. These omics-supported functional annotations shed light on a variety of developmental processes and molecular responses, such as flower and root development, defense responses to fungi and bacteria, and phytohormone signaling, and help alleviate the knowledge gap of biological process annotations in Arabidopsis. An in-depth analysis of two context-specific networks, modeling seed development and response to water deprivation, shows how previously uncharacterized genes function within the respective networks. Moreover, our AFP approach can be applied in future studies to facilitate gene discovery for crop improvement. Significance statementFor the majority of plant genes, it is unknown in which processes they are involved. Using a multi-omics approach, leveraging transcriptome, protein-DNA and protein-protein interaction data, we functionally annotated 42.6% of unknown Arabidopsis thaliana genes, providing insight into a variety of developmental processes and molecular responses, as well as a resource of annotations which can be explored by the community to facilitate future research.

plant biology↗

Diurnal transcript profiling of the diatom Seminavisrobusta reveals adaptations to a benthic lifestyle

1Coastal regions contribute an estimated 20% of annual gross primary production in the oceans, despite occupying only 0.03% of their surface area. Diatoms frequently dominate coastal sediments, where they experience large variations in light regime resulting from the interplay of diurnal and tidal cycles. Here, we report on an extensive diurnal transcript profiling experiment of the motile benthic diatom Seminavis robusta. Nearly 90% (23,328) of expressed protein-coding genes and 66.9% (1124) of expressed long intergenic non-coding RNAs (lincRNAs) showed significant expression oscillations and are predominantly phasing at night with a periodicity of 24h. Phylostratigraphic analysis found that rhythmic genes are enriched in deeply conserved genes, while diatom-specific genes are predominantly associated with midnight expression. Integration of genetic and physiological cell cycle markers with silica depletion data revealed potential new silica cell wall associated gene families specific to diatoms. Additionally, we observed 1752 genes with a remarkable semidiurnal (12-h) periodicity, while the expansion of putative circadian transcription factors may reflect adaptations to cope with highly unpredictable external conditions. Taken together, our results provide new insights into the adaptations of diatoms to the benthic environment and serve as a valuable resource for diurnal regulation in photosynthetic eukaryotes. O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

systems biology↗

Mitotic interhomolog recombination drives genomic diversity in diatoms

Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific variability in natural populations. However, the process generating such diversity is unknown. Here we estimated the variability within a natural diatom population and subsequently mapped the genomic changes arising within cultures clonally propagated from single diatom cells. We demonstrate that genome rearrangements and mitotic recombination between homologous chromosomes underlie clonal variability, resulting in haplotype diversity accompanied by the appearance of novel protein variants and loss of heterozygosity resulting in the fixation of alleles. The frequency of interhomolog mitotic recombination exceeds 4 out of 100 cell divisions and increases under environmental stress. We propose that this plastic response in the interhomolog mitotic recombination rate increases the evolutionary potential of diatoms, contributing to their ecological success. One Sentence SummaryRecombination between homologous chromosomes in diatom vegetative cells leads to extensive genomic diversity in clonal populations.

genomics↗

TRAPID 2.0: a web application for taxonomic and functional analysis of de novo transcriptomes

Advances in high-throughput sequencing have resulted in a massive increase of RNA-Seq transcriptome data. However, the promise of rapid gene expression profiling in a specific tissue, condition, unicellular organism, or microbial community comes with new computational challenges. Owing to the limited availability of well-resolved reference genomes, de novo assembled (meta)transcriptomes have emerged as popular tools for investigating the gene repertoire of previously uncharacterized organisms. Yet, despite their potential, these datasets often contain fragmented or contaminant sequences, and their analysis remains difficult. To alleviate some of these challenges, we developed TRAPID 2.0, a web application for the fast and efficient processing of assembled transcriptome data. The initial processing phase performs a global characterization of the input data, providing each transcript with several layers of annotation, comprising structural, functional, and taxonomic information. The exploratory phase enables downstream analyses from the web application. Available analyses include the assessment of gene space completeness, the functional analysis and comparison of transcript subsets, and the study of transcripts in an evolutionary context. A comparison with similar tools highlights TRAPIDs unique features. Finally, analyses performed within TRAPID 2.0 are complemented by interactive data visualizations, facilitating the extraction of new biological insights, as demonstrated with diatom community metatranscriptomes.

bioinformatics↗

Chromatin accessibility landscapes activated by cell surface and intracellular immune receptors

Activation of cell Surface and Intracellular Receptor-Mediated Immunity (SRMI and IRMI) results in rapid transcriptional reprogramming that underpins disease resistance. However, the mechanisms by which SRMI and IRMI lead to transcriptional changes are not clear. Here, we combine RNA-seq and ATAC-seq to define changes in gene expression and chromatin accessibility; both SRMI and IRMI increase chromatin accessibility at induced defense genes. Analysis of ATAC-seq and RNA-seq data combined with publicly available information on transcription factor DNA-binding motifs enabled comparison of individual gene regulatory networks activated by SRMI and IRMI, and by both. These results and analyses reveal overlapping and conserved transcriptional regulatory mechanism between the two immune systems.

plant biology↗

A modular system regulates specialized metabolite pathway branch choice in the medicinal plant Catharanthus roseus

Catharanthus roseus produces a diverse range of specialized metabolites of the monoterpenoid indole alkaloid (MIA) class in a heavily branched pathway. Recent great progress in identification of MIA biosynthesis genes revealed that the different pathway branch genes are expressed in a highly cell type- and organ-specific and stress-dependent manner. This implies a complex control by specific transcription factors (TFs), only partly revealed today. We generated and mined a comprehensive compendium of publicly available C. roseus transcriptome data for MIA pathway branch-specific TFs. Functional analysis was performed through extensive comparative gene expression analysis and profiling of over 40 MIA metabolites in the C. roseus flower petal expression system. We identified additional members of the known BIS and ORCA regulators. Further detailed study of the ORCA TFs suggests subfunctionalization of ORCA paralogs in terms of target gene-specific regulation and synergistic activity with the central jasmonate response regulator MYC2. Moreover, we identified specific amino acid residues within the ORCA DNA-binding domains that contribute to the differential regulation of some MIA pathway branches. Our results advance our understanding of TF paralog specificity for which, despite the common occurrence of closely related paralogs in many species, comparative studies are scarce. SIGNIFICANCE STATEMENTA gene discovery program for regulators of monoterpenoid indole alkaloid biosynthesis in Catharanthus roseus advances our understanding of paralog specificity and subfunctionalization of the renowned class of ORCA transcription factors, particularly in terms of target gene-specificity and synergistic activity with other jasmonate-responsive transcription factors.

plant biology↗

Traceback of Core Transcription Factors for Soybean Root Growth Maintenance under Water Deficit

Some crops inhibit shoot growth but maintain root growth under water-deficit conditions. Unraveling the molecular mechanisms of root plasticity under water deficit conditions in plants remains a major challenge. We developed an efficient platform for identifying core transcription factors (TFs) that collectively regulate each other and/or themselves in response to water stress, and exploring their interconnected regulatory circuitry involved in root growth maintenance under water deficit in soybean. We performed multi-species phylogenetic footprinting combined with spatial-temporal transcriptome analysis of soybean (Glycine max) roots under water deficit to identify conserved motifs that function in the water-stress response. Using these functional conserved cis-motifs, we applied a new approach to trace back motifs-associated core TFs ingroup as signal mediators, which mediate signaling between abiotic and endogenous stimuli. We integrated a co-functional TF-TF network and conserved motif-centered TF-DNA networks to construct a core TF network defined by mutual cross-regulation among core TFs. We found that core TF ARG (Abscisic acid response element binding factor-like Root Growth regulator) represses BRG (Brassinosteroid enhanced expression-like Root Growth regulator) expression through binding to its promoter at a conserved binding site. ARG and BRG antagonistically regulate Phytochrome-interacting factor-like Root Growth regulator (PRG) and combinatorially regulate some other core TFs. These core TFs form complex regulatory circuits to integrate light and multiple hormone signaling pathways and maintain root growth in response to varying degrees of water stress. Our study provides valuable information to unravel the complicated mechanisms of molecular networks involved in the regulation of root growth under water deficit.

plant biology↗

Mating type specific transcriptomic response to sex inducing pheromone in the pennate diatom Seminavis robusta

Sexual reproduction is a fundamental phase in the life cycle of most diatoms. Despite its role as a source of genetic variation, it is rarely reported in nature and its molecular foundations remain largely unknown. Here, we integrate independent transcriptomic datasets, in order to prioritize genes responding to sex inducing pheromones (SIPs) in the pennate diatom Seminavis robusta. We observe marked gene expression changes associated with SIP treatment in both mating types, including an inhibition of S-phase progression, chloroplast division, mitosis and cell wall formation. Meanwhile, meiotic genes are upregulated in response to SIP, including a sexually induced diatom specific cyclin (dsCyc). Our data further suggest an important role for reactive oxygen species, energy metabolism and cGMP signaling during the early stages of sexual reproduction. In addition, we identify several genes with a mating type specific response to SIP, and link their expression pattern with physiological responses such as the production of the attraction pheromone diproline and mate-searching behaviour in MT+. Combined, our results provide a model for early sexual reproduction in pennate diatoms and significantly expand the suite of target genes to detect sexual reproduction events in natural diatom populations.

molecular biology↗

The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms

Benthic diatoms are the main primary producers in shallow freshwater and coastal environments, fulfilling important ecological functions such as nutrient cycling and sediment stabilization. However, little is known about their evolutionary adaptations to these highly structured but heterogeneous environments. Here, we report a reference genome for the marine biofilm-forming diatom Seminavis robusta, showing that gene family expansions are responsible for a quarter of all 36,254 protein-coding genes. Tandem duplications play a key role in extending the repertoire of specific gene functions, including light and oxygen sensing, which are probably central for its adaptation to benthic habitats. Genes differentially expressed during interactions with bacteria are strongly conserved in other benthic diatoms while many species-specific genes are strongly upregulated during sexual reproduction. Combined with re-sequencing data from 48 strains, our results offer new insights on the genetic diversity and gene functions in benthic diatoms.

bioinformatics↗

Systematic and functional analysis of horizontal gene transfer events in diatoms.

1.Diatoms are a diverse group of mainly photosynthetic algae, responsible for 20% of worldwide oxygen production, which can rapidly respond to favourable conditions and often outcompete other phytoplankton. We investigated the contribution of horizontal gene transfer (HGT) to its ecological success. A systematic phylogeny-based bacterial HGT detection procedure across nine sequenced diatoms showed that 3-5% of their proteome has a horizontal origin and a large influx occurred at the ancestor of diatoms. More than 90% of HGT genes are expressed, and species-specific HGT genes in Phaeodactylum tricornutum undergo strong purifying selection. They are implicated in several processes including environmental sensing, and expand the metabolic toolbox. Cobalamin (vitamin B12) is an essential cofactor for roughly half of the diatoms and is only produced by bacteria. Genes involved in its final synthesis were detected as HGT, including five consecutive enzymes in Fragilariopsis cylindrus. This might give diatoms originating from the Southern Ocean, a region typically depleted in cobalamin, a competitive advantage. Overall, we show that HGT is a prevalent mechanism that is actively used in diatoms to expand its adaptive capabilities.

evolutionary biology↗

Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds

The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focusses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations, with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that the unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified following recolonization of benthic environments that became increasingly available as sea ice retreated. An increased supply of nutrients and biotic interactions such as grazing pressure has likely triggered the independent evolution of macroscopic growth via different strategies, including both true multicellularity, and multiple types of giant celled forms.\n\nSignificance StatementGreen seaweeds are important primary producers along coastlines worldwide, and likely played a key role in the evolution of animals. To understand their origin and diversification, we resolve key relationships among extant green algae using a phylotranscriptomic approach. We calibrate our tree using available fossil data, to reconstruct important evolutionary events such as transitions to benthic environments, and evolution of macroscopic growth. We estimate green seaweeds to have originated in the late Tonian/Cryogenian Period, followed by a marked Ordovician diversification of macroscopic forms. This ancient proliferation of green seaweeds likely modified shallow marine ecosystems, which set off an evolutionary arms race between ever larger seaweeds and grazers.

evolutionary biology↗

Evolution of vascular plants through redeployment of ancient developmental regulators

Vascular plants provide most of the biomass, food and feed on earth; yet the molecular innovations that led to the evolution of their conductive tissues are unknown. Here, we reveal the evolutionary trajectory for the heterodimeric TMO5/LHW transcription factor complex, which is rate-limiting for vascular cell proliferation in Arabidopsis thaliana. Both regulators have origins predating vascular tissue emergence, and even terrestrialization. We further show that TMO5 evolved its modern function, including dimerization with LHW, at the origin of land plants. A second innovation in LHW, coinciding with vascular plant emergence, conditioned obligate heterodimerization and generated the critical function in vascular development. In summary, our results suggest that division potential of vascular cells may have been a major driver in the evolution of vascular plants.

plant biology↗

Enhanced TF binding site maps improve regulatory networks learned from accessible chromatin data

Determining where transcription factors (TF) bind in genomes provides insights into which transcriptional programs are active across organs, tissue types, and environmental conditions. Recent advances in high-throughput profiling of regulatory DNA have yielded large amounts of information about chromatin accessibility. Interpreting the functional significance of these datasets requires knowledge of which regulators are likely to bind these regions. This can be achieved by using information about TF binding preferences, or motifs, to identify TF binding events that are likely to be functional. Although different approaches exist to map motifs to DNA sequences, a systematic evaluation of these tools in plants is missing. Here we compare four motif mapping tools widely used in the Arabidopsis research community and evaluate their performance using chromatin immunoprecipitation datasets for 40 TFs. Downstream gene regulatory network (GRN) reconstruction was found to be sensitive to the motif mapper used. We further show that the low recall of FIMO, one of the most frequently used motif mapping tools, can be overcome by using an Ensemble approach, which combines results from different mapping tools. Several examples are provided demonstrating how the Ensemble approach extends our view on transcriptional control for TFs active in different biological processes. Finally, a new protocol is presented to efficiently derive more complete cell type-specific GRNs through the integrative analysis of open chromatin regions, known binding site information, and expression datasets.

bioinformatics↗

Virus-host coexistence in phytoplankton through the genomic lens

Phytoplankton-virus interactions are major determinants of geochemical cycles in the oceans. Viruses are responsible for the redirection of carbon and nutrients away from larger organisms back towards microorganisms via the lysis of microalgae in a process coined the viral shunt. Virus-host interactions are generally expected to follow boom and bust dynamics, whereby a numerically dominant strain is lysed and replaced by a virus resistant strain. Here, we isolated a microalga and its infective nucleo-cytoplasmic large DNA virus (NCLDV) concomitantly from the environment in the surface NW Mediterranean Sea, Ostreococcus mediterraneus, and show continuous growth in culture of both the microalga and the virus. Evolution experiments through single cell bottlenecks demonstrate that, in the absence of the virus, susceptible cells evolve from one ancestral resistant single cell, and vice-versa; that is that resistant cells evolve from one ancestral susceptible cell. This provides evidence that the observed sustained viral production is the consequence of a minority of virus-susceptible cells. The emergence of these cells is explained by low-level phase switching between virus-resistant and virus-susceptible phenotypes, akin to a bet hedging strategy. Whole genome sequencing and analysis of the ~14 Mb microalga and the ~200 kb virus points towards ancient speciation of the microalga within the Ostreococcus species complex and frequent gene exchanges between prasinoviruses infecting Ostreococcus species. Re-sequencing of one susceptible strain demonstrated that the phase switch involved a large 60 Kb deletion of one chromosome. This chromosome is an outlier chromosome compared to the streamlined, gene dense, GC-rich standard chromosomes, as it contains many repeats and few orthologous genes. While this chromosome has been described in three different genera, its size increments have been previously associated to antiviral immunity and resistance in another species from the same genus. Mathematical modelling of this mechanism predicts microalga-virus population dynamics consistent with the observation of continuous growth of both virus and microalga. Altogether, our results suggest a previously overlooked strategy in phytoplankton-virus interactions.

evolutionary biology↗

EnsembleNet: ensemble gene function predictions for Arabidopsis thaliana

Despite increasing availability of sequenced genomes, accurate characterization of gene functions is needed to close the genotype-phenotype gap. Recent advances in gene function prediction rely on ensemble approaches that integrate the results from multiple inference methods to produce superior predictions. Yet, these developments remain largely unexplored in plants. We present Neighbor Counting Ensemble, a gene function prediction method which integrates eleven gene co-function networks for Arabidopsis thaliana, and produces more accurate gene function predictions for a larger fraction of genes with unknown function. We used these predictions to identify genes involved in mitochondrial complex I formation, and for five of them we confirmed the predictions experimentally. The ensemble predictions are provided as a user-friendly online database, EnsembleNet, available at http://www.gene2function.de/ensemblenet.html.

bioinformatics↗

TF2Network: predicting transcription factor regulators and gene regulatory networks in Arabidopsis using publicly available binding site information

A gene regulatory network (GRN) is a collection of regulatory interactions between transcription factors (TFs) and their target genes. GRNs control different biological processes and have been instrumental to understand the organization and complexity of gene regulation. Although various experimental methods have been used to map GRNs in Arabidopsis thaliana, their limited throughput combined with the large number of TFs makes that for many genes our knowledge about regulating TFs is incomplete. We introduce TF2Network, a tool that exploits the vast amount of TF binding site information and enables the delineation of GRNs by detecting potential regulators for a set of co-expressed or functionally related genes. Validation using two experimental benchmarks reveals that TF2Network predicts the correct regulator in 75-92% of the test sets. Furthermore, our tool is robust to noise in the input gene sets, has a low false discovery rate, and shows a better performance to recover correct regulators compared to other plant tools. TF2Network is accessible through a web interface where GRNs are interactively visualized and annotated with various types of experimental functional information. TF2Network was used to perform systematic functional and regulatory gene annotations, identifying new TFs involved in circadian rhythm and stress response.

bioinformatics↗

The Plastid Genome In Cladophorales Green Algae Is Encoded By Hairpin Plasmids

Virtually all plastid (chloroplast) genomes are circular double-stranded DNA molecules, typically between 100-200 kb in size and encoding circa 80-250 genes. Exceptions to this universal plastid genome architecture are very few and include the dinoflagellates where genes are located on DNA minicircles. Here we report on the highly deviant chloroplast genome of Cladophorales green algae, which is entirely fragmented into hairpin plasmids. Short and long read high-throughput sequencing of DNA and RNA demonstrated that the chloroplast genes of Boodlea composita are encoded on 1-7 kb DNA contigs with an exceptionally high GC-content, each containing a long inverted repeat with one or two protein-coding genes and conserved non-coding regions putatively involved in replication and/or expression. We propose that these contigs correspond to linear single-stranded DNA molecules that fold onto themselves to form hairpin plasmids. The Boodlea chloroplast genes are highly divergent from their corresponding orthologs. The origin of this highly deviant chloroplast genome likely occurred before the emergence of the Cladophorales, and coincided with an elevated transfer of chloroplast genes to the nucleus. A chloroplast genome that is composed only of linear DNA molecules is unprecedented among eukaryotes and highlights unexpected variation in the plastid genome architecture.

genomics↗