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Drost, H.-G.

Publications and source records attributed to Drost, H.-G..

12 recordsLinked to original sources

Comprehensive annotations of alternative splicing, lncRNAs, and circRNAs in seven species of flowering plants

The successful occupation of terrestrial habitats by early plants was catalyzed by the adaptive evolution of new organs able to supply water and compensate for the gravitational impact under changing land conditions. Because plants are sessile, it has been proposed that the capacity of plants to innovate specialized organs is driven by a complex interplay between developmental gene expression and regulatory RNAs such as lncRNAs and circRNAs, evolving through sequence polymorphisms, genomic rearrangements, and expression divergence. Despite the importance of alternative and noncoding transcripts for enabling plant life, their accurate quantification causes major challenges as many of them are expressed at low levels and tissue-specific. Here, we describe the re-annotation of seven land plant genomes based on deep, organ-specific, ribo-depleted developmental RNA-Seq data. Using this comparative resource, we uncover 5,000 new lncRNAs and 2,000 new circular RNAs that are promising candidates for further functional investigation. Our annotation will become a reference catalog for studies on plant organ evolution and for uncovering tissue-specific patterns of transcript emergence.

plant biology↗

Pangenomic context reveals the extent of intraspecific plant NLR evolution

Nucleotide-binding leucine-rich repeat (NLR) proteins are a major component of the plant immune system, which directly or indirectly detect molecular signals of pathogen invasion. Despite their critical role, the processes by which NLR genes diversify remain poorly characterised due to the extraordinary sequence, structural, and regulatory variability of NLRs, even among closely related individuals. To understand the evolution of NLR diversity in Arabidopsis thaliana, we leverage graph-based methods to define pangenomic NLR neighbourhoods in 17 genetically diverse genomes. We integrate full-length transcript and transposable element information to exhaustively annotate all intact and degraded NLRs, enabling exploration of the processes that underpin the birth, death and maintenance of NLR diversity within a species. Our main finding is that many uncorrelated mutational processes create NLR diversity, and that there is no single metric that captures on its own the true extent of NLR structural and sequence variation. This immense diversity in plant immune system diversification allows populations to survive the constant onslaught of pathogens, not unlike vertebrate adaptive immunity, where variation is also generated by a variety of complementary mechanisms, albeit at the level of individuals.

plant biology↗

Rapid evolution of gene expression patterns in flowering plants

Phenotypic differences between species are largely driven by changes in both protein-coding sequence and gene expression 1. The evolutionary history of angiosperms (flowering plants) is characterised by a highly accelerated rate of diversification, which Darwin referred to as an "abominable mystery" 2. Here we show, by analysing the transcriptomes from eight organs across seven species, that angiosperm protein-coding gene expression patterns evolve rapidly: within 45 million years, expression levels of orthologous genes diverged so strongly that they are more similar between different organs within a species than between what are considered homologous organs from different species. This finding differs from previous observations in mammals, which demonstrated that organ-dependent gene expression levels are largely conserved 3, 4, 5. Among the angiosperm organs, meristems and leaves show the highest degree of expression conservation, whereas stamen and pollen transcriptomes diverge rapidly. Examining changes in the expression level of functionally related genes, we found low rates for those involved in key cellular, metabolic and developmental processes. In contrast, particularly high rates were observed for genes that are involved in the response to endogenous and external stimuli, presumably reflecting an adaptive response of flowering plants to ever-changing environments. Our work reveals that the evolution of gene expression progresses at different rates in angiosperms and mammals, and provides a comprehensive resource to perform cross-kingdom comparative studies of transcriptome evolution.

plant biology↗

A Transcriptomic Hourglass In Brown Algae

Complex multicellularity has emerged independently across a few eukaryotic lineages and is often associated with the rise of elaborate, tightly coordinated developmental processes. How multicellularity and development are interconnected in evolution is a major question in biology. The hourglass model of embryonic evolution depicts how developmental processes are conserved during evolution, predicting morphological and molecular divergence in early and late embryo stages, bridged by a conserved mid-embryonic (phylotypic) period linked to the formation of the basic body plan. Initially found in animal embryos, molecular hourglass patterns have recently been proposed for land plants and fungi. However, whether the hourglass pattern is an intrinsic feature of all developmentally complex eukaryotic lineages remains elusive. Here, we tested the prevalence of a (molecular) hourglass in the brown algae, the third most developmentally complex lineage on earth that has evolved multicellularity independently from animals, fungi, and plants. By exploring the evolutionary transcriptome of brown algae with distinct morphological complexities, we uncovered an hourglass pattern during embryogenesis in developmentally complex species. Filamentous algae without a canonical embryogenesis display an evolutionary transcriptome that is most conserved in multicellular stages of the life cycle, whereas unicellular stages are more rapidly evolving. Our findings suggest that transcriptome conservation in brown algae is associated with cell differentiation stages, but not necessarily linked to embryogenesis. Together with previous work in animals, plants and fungi, we provide further evidence for the generality of a developmental hourglass pattern across complex multicellular eukaryotes.

evolutionary biology↗

Transposon dynamics in the emerging oilseed crop Thlaspi arvense

Genome evolution is partly driven by the mobility of transposable elements (TEs) which often leads to deleterious effects, but their activity can also facilitate genetic novelty and catalyze local adaptation. We explored how the intraspecific diversity of TE polymorphisms is shaping the broad geographic success and adaptation capacity of the emerging oil crop Thlaspi arvense. We achieved this by classifying the TE inventory of this species based on a high-quality genome assembly, age estimation of retrotransposon TE families and a comprehensive assessment of their mobilization potential. Our survey of TE insertion polymorphisms (TIPs) captured 280 accessions from 12 regions across the Northern hemisphere. We quantified over 90,000 TIPs, with their distribution mirroring genetic differentiation as measured by single nucleotide polymorphisms (SNPs). The number and types of mobile TE families vary substantially across populations, but there are also shared patterns common to all accessions. We found that Ty3/Athila elements are the main drivers of TE diversity in T. arvense populations, while a single Ty1/Alesia lineage might be particularly important for molding transcriptome divergence. We further observed that the number of retrotransposon TIPs is associated with variation at genes related to epigenetic regulation while DNA transposons are associated with variation at a Heat Shock Protein (HSP19). We propose that the high rate of mobilization activity can be harnessed for targeted gene expression diversification, which may ultimately present a toolbox for the potential use of transposition in breeding and domestication of T. arvense.

genomics↗

Sensitive clustering of protein sequences at tree-of-life scale using DIAMOND DeepClust

The biosphere genomics era is transforming life science research, but existing methods struggle to efficiently reduce the vast dimensionality of the protein universe. We present DIAMOND DeepClust, an ultra-fast cascaded clustering method optimized to cluster the 19 billion protein sequences currently defining the protein biosphere. As a result, we detect 1.7 billion clusters of which 32% hold more than one sequence. This means that 544 million clusters represent 94% of all known proteins, illustrating that clustering across the tree of life can significantly accelerate comparative studies in the Earth BioGenome era.

genomics↗

Sensitive inference of alignment-safe intervalsfrom biodiverse protein sequence clusters usingEMERALD

Sequence alignments are the foundation of life science research, but most innovation focused on optimal alignments, while ignoring information derived from suboptimal solutions. We argue that one optimal alignment per pairwise sequence comparison was a reasonable approximation when dealing with very similar sequences, but is insufficient when exploring the biodiversity of the protein universe at tree-of-life scale. To overcome this limitation, we introduce pairwise alignment-safety to uncover the amino acid positions robustly shared across all suboptimal solutions. We implemented this approach into EMERALD, a dedicated software solution for alignment-safety inference and apply it to 400k sequences from the SwissProt database.

bioinformatics↗

Canalization of genome-wide transcriptional activity in Arabidopsis thaliana accessions by MET1-dependent CG methylation

BACKGROUNDEukaryotes employ epigenetic marks such as DNA methylation at cytosines both for gene regulation and genome defense. In Arabidopsis thaliana, a central role is played by methylation in the CG context, with profound effects on gene expression and transposable element (TE) silencing. Nevertheless, despite its conserved role, genome-wide CG methylation differs substantially between wild A. thaliana accessions. RESULTSWe hypothesized that global reduction of CG methylation would reduce epigenomic, transcriptomic and phenotypic diversity in A. thaliana accessions. To test our hypothesis, we knocked out MET1, which is required for CG methylation, in 18 early-flowering A. thaliana accessions. Homozygous met1 mutants in all accessions suffered from a range of common developmental defects such as dwarfism and delayed flowering, in addition to accession-specific abnormalities in rosette leaf architecture, silique morphology and fertility. Integrated analysis of genome-wide methylation, chromatin accessibility and transcriptomes confirmed that inactivation of MET1 greatly reduces CG methylation and alters chromatin accessibility at thousands of loci. While the effects on TE activation were similarly drastic in all accessions, the quantitative effects on non-TE genes varied greatly. The expression profiles of accessions became considerably more divergent from each other after genome-wide removal of CG methylation, although the expression of genes with diverse expression profiles across wild-type accessions tended to become more similar in mutants. CONCLUSIONSOur systematic analysis of MET1 requirement for genome function in different A. thaliana accessions revealed a dual role for CG methylation: for many genes, CG methylation appears to canalize expression levels, with methylation masking regulatory divergence. However, for a smaller subset of genes, CG methylation increases expression diversity beyond genetically encoded differences.

plant biology↗

Uncovering gene-family founder events during major evolutionary transitions in animals, plants and fungi using GenEra

The emergence of new genes is an important driver of evolutionary novelty. Yet, we lack a conceptual and computational approach that accurately traces gene-family founder events and effectively associates them with trait innovation and major radiation events. Here, we present GenEra, a DIAMOND-fuelled gene-family founder inference framework that addresses previously raised limitations and biases of founder gene detection in genomic phylostratigraphy by accounting for homology detection failure (HDF). We demonstrate how GenEra can accelerate gene-family founder computations from several months to a few days for any query genome of interest. We analyzed 30 genomes to explore the emergence of new gene families during the major evolutionary transitions in plants, animals and fungi. The detection of highly conserved protein domains in these gene families indicates that neofunctionalization of preexisting protein domains is a richer source of gene-family founder events compared with de novo gene birth. We report vastly different patterns of gene-family founder events in animal and fungi before and after accounting for HDF. Only plants exhibit a consistent pattern of founder gene emergence after accounting for HDF, suggesting they are more likely to evolve novelty through the emergence of new genes compared to opisthokonts. Finally, we show that gene-family founder bursts are associated with the transition to multicellularity in streptophytes, the terrestrialization of land plants and the origin of angiosperms, as well as with the evolution of bilateral symmetry in animals.

evolutionary biology↗

Epigenetic bases of grafting-induced vigour in eggplant

In horticulture, grafting is a popular technique used to combine positive traits from two different plants. This is achieved by joining the plant top part (scion) onto a rootstock which contains the stem and roots. Despite its wide use, the biological mechanisms driving rootstock-induced alterations of the scion phenotype remain largely unknown. Given that epigenetics plays a crucial role during distance signalling in plants, we studied the genome-wide changes induced by DNA methylation in eggplant (Solanum melongena) plants grafted onto two interspecific rootstocks used to increase scion vigour. As a control, we compared any epigenetic effect found in such grafts to patterns detected in self-grafted plants. We found that vigour was associated with a specific change in scion gene expression and a genome-wide hypomethylation in CHH context. Interestingly, this hypomethylation correlated with the down-regulation of younger and potentially more active LTR retrotransposons (LTR-TEs), suggesting that graft-induced epigenetic modifications are associated to both physiological and molecular phenotypes in grafted plants. We propose that rootstocks can promote vigour by reducing DNA methylation in the scion genome, following similar principles found in some heterotic hybrids.

plant biology↗

Environmental and epigenetic regulation of Rider retrotransposons in tomato

Transposable elements in crop plants are the powerful drivers of phenotypic variation that has been selected during domestication and breeding programs. In tomato, transpositions of the LTR (long terminal repeat) retrotransposon family Rider have contributed to various phenotypes of agronomical interest, such as fruit shape and colour. However, the mechanisms regulating Rider activity are largely unknown. We have developed a bioinformatics pipeline for the functional annotation of retrotransposons containing LTRs and defined all full-length Rider elements in the tomato genome. Subsequently, we showed that accumulation of Rider transcripts and transposition intermediates in the form of extrachromosomal DNA is triggered by drought stress and relies on abscisic acid signalling. We provide evidence that residual activity of Rider is controlled by epigenetic mechanisms involving siRNAs and the RNA-dependent DNA methylation pathway. Finally, we demonstrate the broad distribution of Rider-like elements in other plant species, including crops. Thus our work identifies Rider as an environment-responsive element and a potential source of genetic and epigenetic variation in plants.

plant biology↗

Sensitive detection of pre-integration intermediates of LTR retrotransposons in crop plants

Retrotransposons have played an important role in the evolution of host genomes1,2. Their impact on host chromosomes is mainly deduced from the composition of DNA sequences, which have been fixed over evolutionary time. These studies provide important \"snapshots\" reflecting historical activities of transposons but do not predict current transposition potential. We previously reported Sequence-Independent Retrotransposon Trapping (SIRT) as a methodology that, by identification of extrachromosomal linear DNA (eclDNA), revealed the presence of active LTR retrotransposons in Arabidopsis9. Unfortunately, SIRT cannot be applied to large and transposon-rich genomes of crop plants. We have since developed an alternative approach named ALE-seq (amplification of LTR of eclDNAs followed by sequencing). ALE-seq reveals sequences of 5 LTRs of eclDNAs after two-step amplification: in vitro transcription and subsequent reverse transcription. Using ALE-seq in rice, we detected eclDNAs for a novel Copia family LTR retrotransposon, Go-on, which is activated by heat stress. Sequencing of rice accessions revealed that Go-on has preferentially accumulated in indica rice grown at higher temperatures. Furthermore, ALE-seq applied to tomato fruits identified a developmentally regulated Gypsy family of retrotransposons. Importantly, a bioinformatic pipeline adapted for ALE-seq data analyses allows the direct and reference-free annotation of new active retroelements. This pipeline allows assessment of LTR retrotransposon activities in organisms for which genomic sequences and/or reference genomes are unavailable or are of low quality.

plant biology↗