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de Vries, J.

Publications and source records attributed to de Vries, J..

At least 19 recordsLinked to original sources

Signatures for conserved phenolic-based acclimation responses to UV in a unicellular algal sister of land plants

Ultraviolet (UV) light is a major stressor that particularly comes to bear in the terrestrial habitat. As such it is among the major challenges that the earliest land plants had to overcome. The closest algal relatives of land plants, the zygnematophytes, are single celled and filamentous algae that - in the context of their terrestrial and freshwater habitats - have diverse adaptations to UV irradiance. As such, contextualized with data on land plants, zygnematophyte algae harbor important information for inferring how the earliest land plants have acclimated to UV. Here we exposed the unicellular zygnematophyte model Mesotaenium to daily UV irradiance and assessed its response through microscopy, untargeted metabolomics, and global gene expression profiling using transcriptomics. Our data reveal cell biological acclimation by formation of lipid droplets. Further, we find that the cells accumulated chemodiverse coumarin-like derivatives. Altogether, our data suggest that acclimation to long-term UV exposure is composed of building blocks of a molecular chassis conserved with that of land plants, underpinned by phenolics and genes that are tied to their biosynthesis. From this chassis, divergent evolutionary trajectories have assembled them into a divergent conformation - one of which ushering in the emergence of the phenylpropanoid pathway.

evolutionary biology↗

Chemically-induced Jamming and 3D printing of Granular Hydrogels: Microgels as Reservoirs of Volume

Granular hydrogels, made of jammed soft microparticles, are of great interest for 3D (bio)printing, as they combine ideal rheological properties and extensive modularity, yielding favorable microstructures for tissue engineering. Typically, the yield-stress properties of these materials, which facilitate printability, are defined by the preparation state and the initial particle content of the hydrogel. Here, we propose a granular hydrogel whose yield-stress and, consequently, printability and printed scaffolds shape retention can be controlled not only by the initial weight fraction of particles but also by their stimuli-responsive swelling. The responsive microgels are prepared from poly(N-isopropylacrylamide) crosslinked by dynamic covalent disulfide bonds. The particles swelling is triggered by reduction-induced cleavage of the disulfide bonds into two pendant thiol groups, enabling printing of multilayer scaffolds with high shape fidelity. Without chemically induced swelling, the same formulation requires higher particle concentrations to be printable. Importantly, the printed structures can be annealed by oxidizing the thiol units back into disulfide inter-particle bonds. The printed scaffolds are compatible with human dermal fibroblasts (HDF) and support cell-material interactions. This system offers a unique opportunity for on-demand modulation of both printability and scaffold microstructure, enabling unique control over local stiffness, packing density, and porosity in granular scaffolds.

bioengineering↗

Imaging guided single-cell multiomics unveils shared autoreactive CD4+ T-cell responses in blood, locoregional lymph node and affected tissues of patients with systemic autoimmunity

Systemic autoimmune connective tissue diseases (CTDs) are characterized by anti-nuclear antibodies, shared HLA-associated genetic risk, and frequent disease overlap, suggesting a central role for CD4+ T cells in pathogenesis. However, defining disease-driving CD4+ T-cell responses remains challenging due to their localization within lymphoid and affected tissues and the lack of approaches linking these responses to circulating counterparts. We combined [18F]-labeled thymidine PET/CT-guided tissue sampling, ex vivo antigen stimulation, and single-cell multiomics to characterize CD4+ T-cell responses in blood, PET-avid locoregional lymph nodes (LNs), and disease-affected tissues from patients with the immunologically distinct CTDs systemic sclerosis and Sjogren's disease. PET-avid LNs from both diseases exhibited enhanced adaptive immune activity and contained an expanded population of interferon-stimulated gene (ISG)-expressing TRAIL+ CD4+ T cells. In Sjogren's disease, active LNs and affected tissues harbored diverse effector CD4+ T-cell populations, including follicular and peripheral helper T cells and Th2/Th17 cells. In contrast, systemic sclerosis tissues lacked effector CD4+ T cells, while active LNs were enriched for naive, regulatory, and TRAIL+ ISG CD4+ T cells. Antigen stimulation of peripheral blood mononuclear cells enriched for expanded effector CD4+ T-cell populations that shared activation profiles and clonal relationships with cells in LNs and affected tissues, many representing autoreactive antigen-specific T cells. TRAIL+ CD4+ T cells suppressed effector T-cell differentiation, autoreactive plasma cell generation, and autoantibody production in vitro, identifying a previously unrecognized immunoregulatory population. Together, this workflow enables comprehensive characterization of pathogenic and regulatory CD4+ T-cell responses across CTDs.

immunology↗

Prediction of plant organismal complexity based on transcription factor annotation: an AI approach

How morphological complexity evolves is still enigmatic. While there is evidence in algae and plants as well as animals that diversification of the repertoire of transcription factors (TF) is causative for evolution of organismal complexity, there are many examples from lineages that follow their own way of complexity evolution, for example by expansion of particular families. For land plants, correlation of the size of the TF complement with number of cell types (as a proxy for morphological complexity) has been shown, and several families were identified as candidates to drive complexity evolution. Here, we expand a previously available dataset of cell type numbers from 12 to 82 proteomes and introduce a four class body plan scheme. We find that the total TF complement correlates with the number of cell types of Archaeplastida (primary plastid bearing plants and algae). We used TabPFN (Tabular Prior-data Fitted Network) for binary (uni- vs. multicellularity) as well as for four class Bauplan classification. TabPFN is able to predict the morphological complexity with high accuracy. This approach allows to determine organismal complexity based on the gene space of an organism. Based on our results, we can confirm that plant morphological evolution is driven by gain and expansion of TF families.

evolutionary biology↗

The Conserved N-Terminal Extension of AtKEA1 Is Largely Dispensable for Plastid Function but Contributes to Potassium Homeostasis

Members of the K efflux antiporter (KEA) family fulfill key roles in plastids and the endomembrane system. Plants and green algae possess at least one KEA mediating K/H exchange across the plastid inner envelope (IE) membrane. Recently, IE KEAs were shown to be essential for plastid gene expression (PGE), chloroplast development, and photosynthesis. Plants lacking these antiporters exhibit reduced stromal protein synthesis and accumulation of unprocessed rRNA precursors. KEA proteins comprise a conserved monovalent cation/proton antiporter 2 (CPA2) domain and a regulatory K transport and NAD-binding (KTN) domain. IE KEAs are distinguished by an additional [~]500-amino-acid N-terminal extension containing a coiled-coil (CC) domain embedded within a largely intrinsically disordered region (IDR). Intrigued by this unusual architecture, we performed phylogenetic analyses, revealing that this N-terminal fusion arose early and has been conserved throughout the green lineage. We then investigated the oligomeric state, native distribution, and function of the N-terminal domain. Using Arabidopsis thaliana, we found that IE KEAs localize to discrete clusters within the inner envelope membrane and assemble into complexes of approximately 600 kDa. Finally, complementary approaches using a functional KEA1 variant lacking the core N-terminal domains (KEA1{Delta}N) indicate that this extension plays a regulatory rather than an essential role. Our findings uncover an evolutionarily ancient regulatory module that shapes the molecular organization and function of IE KEAs, advancing our understanding of plastid ion and pH homeostasis and plastid ribosome integrity. One-sentence summaryPlastid KEA1/2 proteins feature a unique N-terminal extension that modulates potassium transport activity in a yet unknown manner but is not essential for normal plant growth under ambient conditions.

plant biology↗

Old Yellow Enzyme from Brevibacillus nitrificans functions as 12-oxo-phytodienoic acid reductase in planta

Old Yellow Enzymes (OYEs) are a widely distributed family of ene-reductases that were first described in a Saccharomyces cerevisiae ferment. In plants, cis-12-oxo-phytodienoic acid (cis-OPDA) reductase (OPR) is the best studied OYE. In Arabidopsis thaliana, the peroxisomal AtOPR3 was characterized as the major OPDA reductase, which generates 3-oxo-2-(2-pentenyl)-cyclopentane-1-octanoic acid in the jasmonic acid (JA) biosynthesis. In Atopr3 lines, only small amounts of JA are detectable after wounding. Here, we describe an OPR-like enzyme (named BnOPR) from the gram-positive Brevibacillus nitrificans. The sequence was identified in an early version of the Physcomitrium patens genome and is assumed to be a contamination by a bacterium growing in association with P. patens. In complementation experiments with an Atopr3 line, we demonstrate that expression of BnOPR, fused with a peroxisomal targeting signal, rescues the male infertile phenotype and increases JA and JA-Ile levels. The catalytic parameters of BnOPR were determined for a set of substrates, including cis-OPDA and prednisone. Interestingly, B. nitrificans, B. brevis, and Paenibacillus physcomitrellae were shown to have a positive effect on P. patens growth. HighlightThe bacterial enzyme BnOPR rescues the male infertile phenotype of Atopr3 plants.

biochemistry↗

Homologous ABA-independent kinase tracks coalesced into osmotic stress circuits during plant terrestrialization

Land plants possess a unique system for responding to environmental stressors. How this system evolved during plant terrestrialization remains one of the major questions in plant evolutionary biology. To retrace this process, it is essential to study both land plants and their closest algal relatives, the zygnematophytes. Using the single-celled zygnematophyte Mesotaenium, we integrated physiological stress experiments with phosphoproteomics, genome-wide transcription factor binding analyses, and protein-protein interaction studies to investigate the architecture of a key stress response pathway: the signaling cascade homologous to the plant abscisic acid (ABA)-mediated pathway. Our results highlight the roles of histidine kinases (HKs) and calcium-dependent protein kinases (CDPKs) in osmotic stress signaling. Focusing on SnRK2 and ABF, key components at the downstream end of the canonical ABA signaling pathway, we provide evidence that ABF plays a central role in osmotic stress responses even in the absence of ABA. Together, our data reveal the coordinated action of parallel functional modules that were likely integrated into the ABA response cascade during plant terrestrialization.

evolutionary biology↗

A deep genetic structure phylogenomically frames the closest algal relatives of land plants

To discern the nature of the closest streptophyte algal relatives of land plants (embryophytes) is a major question in the field of plant evolutionary biology; discerning that nature is essential for our ability to infer the last common ancestor of embryophytes and algae, allowing to retrace the adaptations that ushered in the conquest of land by plants. Albeit initially coming as a surprise, all major phylogenomic efforts have concluded that the Zygnematophyceae are the algal sisters to land plants1-6. The Zygnematophyceae are the streptophyte algal class with the greatest species richness7 and while we now have ample genome information on a few select members of zygnematophytes8-13, our understanding of the genetic and genomic divergence as well as potential is limited by a lack of phylodiverse data that accounts for this diversity and integrates it into a phylogenomic framework. We here sequenced 43 new transcriptome datasets for the Zygnematophyceae and built a phylogenomic tree based on a total of 104 zygnematophyceaen transcriptomes and 2243 loci. We recover a deep genetic structure for the Zygnematophyceae, revealing that this algal class is ancient. Despite the deep split between Spirogyrales and their unicellular sister group Desmidiales, most Spirogyrales emerged after pronounced genetic divergence, accommodating the attainment of multicellularity and divergent traits such as unique cell and plastid division13. Overall, our data capture signatures of massive ancient radiations. Zygnematophyceae are characterized by deep genetic divergences that necessitated a phylodiverse sampling to be revealed, together with their vast evolutionary history, and to illuminate the nature of the algal progenitors of land plants.

evolutionary biology↗

Chemodiverse cell systems responses to UV in an algal sister of land plants

Plant terrestrialization necessitated that a barrage of stressors had to be overcome1. Land plants use an integrated response network in adjusting their molecular physiology to terrestrial stressors2--one of the foremost being UV irradiance. The zygnematophytes are the closest streptophyte algal relatives of land plants3-5, are renowned for their resilience to UV stress6-8, and thus allow to glean key information for inferring the UV response toolkit of the earliest land plants9,10. Throughout streptophyte evolution, specialised metabolism radiated into creating diverse compounds used for responses to environmental challenges, such as sun-shielding compounds and antioxidants11-14. This includes UV-shielding compounds like flavonoids and coumarins but also the land plant specific polymer lignin, giving structural support in vascular plants15; homologs of the underpinning core pathway occur in streptophyte algae16. Here, we exposed the zygnematophyte Mesotaenium to UV-B irradiation and profiled its physiology, morphology, transcriptomics as well as metabolomic features. After UV-B exposure, cells showed rapid photophysiological responses and progressively growing terminal vacuoles. Our transcriptome data capture dynamic changes in gene expression of (i) core downstream responses such as genes homologous to phenol metabolic enzymes, photophysiological homeostats, and DNA repair factors; but also (ii) upstream components featuring key homologs of kinase-mediated signalling cascades, as well as light quality and abscisic acid-mediated signalling components. To scrutinize the acclimatory chassis, we created a metabolite feature database specifically for the Mesotaenium metabolome. Upon UV-B exposure, the metabolome displayed pronounced temporal shifts, with several phenolic features that accumulate along the stress-acclimation kinetics. Overall, we capture a chemodiverse response including various phenolics such as purpurogallin-like, methoxypsoralen-like derivatives and coumarins. Our data establish an integrated model for UV responses in the closest algal relatives of land plants, shedding light on the toolkit that allowed the progenitors of land plants to move out of a protective water column.

evolutionary biology↗

Conserved and Lineage-Specific Roles of KEA-Mediated Ion Homeostasis in Chlamydomonas

In Arabidopsis thaliana, seamless plastid gene expression and development depend on finely balanced ion homeostasis across the inner envelope (IE) membrane, maintained by the K/H antiporters AtKEA1/2. To assess whether these functions are retained across mono- and polyplastidic representatives of the green lineage, we studied CrKEA1, the sole IE KEA homolog in the unicellular alga Chlamydomonas reinhardtii. Using CRISPR/Cas9, we generated a Cr-kea1 knockout mutant that exhibits impaired photoautotrophic growth, chloroplast deformation, and photoinhibition. Transcriptomics revealed strong induction of ribosome biogenesis genes and reduced abundance of transcripts associated with cell and plastid division. Further RNA analyses confirmed defects in stromal rRNA maturation of Cr-kea1, paralleling observations from Arabidopsis kea1kea2 mutants. Expression of CrKEA1 in Arabidopsis rescued growth and rRNA maturation in At-kea1kea2, demonstrating functional continuity after the ancient divergence between the two lineages. Cross-species transcriptomic comparisons further revealed that IE KEA loss elicits both shared and species-specific transcriptional responses: PhANG repression was conserved between algae and plants, whereas activation of the chloroplast unfolded protein response (cpUPR) and reduced expression of genes tied to cell-cycle and plastid fission occurred only in Chlamydomonas. Single-cell time-lapse imaging confirmed that Cr-kea1 exhibits an increased frequency of aberrant cytokinesis, unequal division, and division failure. Our findings demonstrate that while IE KEA transporters fulfill conserved roles in maintaining the conditions for plastid gene expression, their integration into broader cellular networks has diverged between unicellular chlorophytes and embryophytes (land plants). This underscores a lineage-dependent tuning of plastid-nucleus communication shaped by organismal complexity and plastid number. One-sentence summaryDisruption of KEA-mediated chloroplast ion homeostasis in Chlamydomonas reinhardtii reveals conserved and lineage-specific control of plastid rRNA processing and cell cycle progression.

plant biology↗

Rooting the deep divergence of land plants

Unravelling the deep phylogenetic structure of embryophytes is essential for understanding their evolutionary success on land. However, pronounced phylogenetic dispute remains: while recent phylogenomic studies have recurrently recovered the bryophyte monophyly in the presence of algal outgroups, absence of such outgroup representatives yields paraphyletic bryophytes. Here, we assembled a large-scale genome dataset encompassing 243 embryophyte species and 12 representative algal species to test the hypothesis of bryophyte monophyly. Across different substitution models and species tree inference methods, we recover strong support for bryophyte monophyly in the presence of algal outgroups; by varying the algal outgroup sampling, we revealed a salient outgroup effect that can significantly alter the embryophyte deep divergence relationship. We show that (1) bryophyte monophyly is consistently supported across three distinct outgroup-free rooting methods; and (2) incomplete lineage sorting, substitution saturation, heterogeneous site and branch profiles through deep time underpin prevalent phylogenomic discordance across genes and sites. Our data explain decades of difficulty in resolving the deep dichotomy of land plants. Bryophyte monophyly is not an artefact by outgroups but underpinned by genuine phylogenetic signal.

evolutionary biology↗

The Spirogyra genome: signatures of shared and divergent division and differentiation

Zygnematophytes emerged as the unexpected closest algal relatives of land plants despite their simple body plans, raising questions about the morphogenetic toolkit present in the last common ancestor of land plants and algae. Genomic analyses have revealed that zygnematophytes are cellular giants, sharing homologous frameworks for several phytohormones, secondary metabolites, and key morphogenetic and transcriptional regulatory processes. Zygnematophytes fall into five orders, each of which has charted its own evolutionary path. Here, we have sequenced a contiguous genome of Spirogyra pratensis, the eponymous representative of Spirogyrales and a classical model system for evolutionary cell biology in the green lineage. Building on this genome, we transcriptionally profiled the tractable life cycle of Spirogyra and its responses to a bifactorial gradient of light and temperature. Our data highlight the activation of quiescence and homeostatic programs. Yet what stands out most in Spirogyra is its spiral chloroplast--undulating intracellularly and abscising during mixed phragmoplast formation and furrowing. Leveraging the genome in tandem with co-expression network analyses, we describe the molecular underpinnings of the unique cytokinetic processes that govern both cell and plastid division. We find that Spirogyra deploys a molecular program characteristic of Phragmoplastophyta, yet lacks the deeply conserved plastid division machinery found in other archaeplastid plastids.

plant biology↗

A diverse community constitutes global coccolithophore calcium carbonate stocks

Coccolithophores are diverse calcifying plankton, yet most research has focused on a single species, Gephyrocapsa huxleyi, with the global contributions of other species hitherto unexplored. Since coccolithophores account for the majority of marine calcium carbonate (CaCO3) production, this narrow focus risks biasing our understanding of CaCO3 cycling, as other species differ in their distributions, CaCO3 production and response to climate change. Using a global, species-resolved machine-learning approach, we show that G. huxleyi contributes only about 7% of estimated coccolithophore CaCO3 stock, while a morphologically and functionally diverse assemblage dominates. Since stock contributions are a good proxy for contribution to production, our findings challenge the view that G. huxleyi underpins CaCO3 cycling and show that lab and in situ datasets centred on this species capture only a small fraction of coccolithophore calcification. Our work identifies key species and regions to guide future laboratory, in situ, and modelling efforts, laying the groundwork for more realistic representations of CaCO3 cycling under climate change.

ecology↗

Systems acclimation to osmotic stress in zygnematophyte cells

Zygnematophytes are the closest algal relatives of land plants. They hold key information to infer how the earliest land plants overcame the barrage of terrestrial stressors, prime of which is osmotic stress. Here, we applied two osmotic stressors on a unicellular and a multicellular representative of zygnematophytes and studied their response over a 25-hour time course generating 130, 60, and 30 of transcriptomic, proteomic, and metabolomic samples combined with photophysiology, sugar analysis, immunocytochemical glycoprotein analysis, and microscopy. Our data highlight a shared protein chassis that shows divergent responses with the same outcome: successful acclimation to osmotic challenges. We establish a model of how the algal sisters of land plants can overcome a prime stressor in the terrestrial habitat and highlight components of the plant terrestrialization toolkit.

evolutionary biology↗

A single pathogen-secreted protein reprograms plants for drought resilience

Climate change-enforced drought stress conditions and diseases caused by pathogens often co-occur and represent one of the greatest challenges in plant science1-3. Wilt pathogens that colonize water-conducting plant tissues can aggravate the problem and affect a wide range of agricultural crops4,5. However, whilst fungal infections with the vascular pathogen Verticillium dahliae are typically associated with wilt symptoms due to occlusion of xylem tissues, the related V. longisporum induces de novo formation of tracheary elements6,7. This promotes not only its virulence but also enables elevated water storage capacity of the infected host plant and resilience against drought stress conditions6,7. Here, we identified a secreted Verticillium protein, TRANSDIFFERENTIATION EFFECTOR (TRADE), which triggers cell identity switches of bundle sheath cells into tracheary elements. We show that TRADE interacts with the intracellular plant protein VARICOSE (VCS), a conserved component of the mRNA turnover machinery and ortholog of the metazoan protein ENHANCER OF DECAPPING 4 (EDC4/HEDLS/Ge-1)8. The TRADE-VCS interaction induces SUCROSE NON-FERMENTING 1 (SNF1)-related protein kinase (SRK)-dependent phosphorylation and thus dysfunction of VCS. This affects the abundance of mRNAs encoding master regulators of xylem differentiation and demonstrates how a single pathogen effector protein triggers complex tissue-specific developmental reprogramming and thus promotes abiotic stress resilience.

plant biology↗

Comparative transcriptomics in ferns reveals key innovations and divergent evolution of secondary cell wall

Despite ferns being crucial to understanding plant evolution, their large and complex genomes has kept their genetic landscape largely uncharted, with only a handful of genomes sequenced and sparse transcriptomic data. Addressing this gap, we generated extensive RNA-sequencing data for multiple organs across 22 representative species over the fern phylogeny, assembling high-quality transcriptomes. These data facilitated the construction of a time-calibrated fern phylogeny covering all major clades, revealing numerous whole-genome duplications and highlighting the uniqueness of fern genetics, with half of the uncovered gene families being fern-specific. Our investigation into fern cell walls through biochemical and immunological analyses identified occurrences of the lignin syringyl unit and its independent evolution in ferns. Moreover, the discovery of an unusual sugar in fern cell walls hints at a divergent evolutionary path in cell wall biochemistry, potentially driven by gene duplication and sub-functionalization. We provide an online database preloaded with genomic and transcriptomic data for ferns and other land plants, which we used to identify an independent evolution of lignocellulosic gene modules in ferns. Our data provide a framework for the unique evolutionary path that ferns have navigated since they split from the last common ancestor of euphyllophytes more than 360 million years ago.

plant biology↗

Enhanced sensitivity of TAPscan v4 enables comprehensive analysis of streptophyte transcription factor evolution

Transcription associated proteins (TAPs) fulfill multiple functions in regulatory and developmental processes and display lineage-specific evolution. TAPscan is a comprehensive and highly reliable tool for genome-wide TAP annotation via domain profiles. Here, we present TAPscan v4, including an updated web interface (https://tapscan.plantcode.cup.uni-freiburg.de/), which enables an in-depth representation of the distribution of 138 TAP families across 678 species from diverse groups of organisms, with a focus on Archaeplastida (plants in the wide sense). With this release, we also make the underlying "Genome Zoo" available, a curated protein data set with scripts and metadata. 18 new TAP (sub)families were added as part of the update. Nine of those were gained in the most recent common ancestor of the Streptophyta (comprising streptophyte algae and land plants), or within the streptophyte algae. More than one-third of all detected TAP family gains were identified during the evolution of streptophyte algae, before the emergence of land plants, and are thus likely to have been significant for plant terrestrialization. The TAP complement of the Zygnematophyceae was identified to be the most similar to that of land plants, consistent with the finding that this lineage is sister to land plants. Overall, our data retrace the evolution of streptophyte TAPs, allowing us to pinpoint the regulatory repertoire of the earliest land plants.

bioinformatics↗

Time-resolved oxidative signal convergence across the algae-embryophyte divide

The earliest land plants faced a significant challenge in adapting to environmental stressors. Stress on land is unique in its dynamics, entailing swift and drastic changes in light and temperature. While we know that land plants share with their closest streptophyte algal relatives key components of the genetic makeup for dynamic stress responses, their concerted action is little understood. Here, we combined time-course stress profiling using photophysiology, transcriptomics on 2.7 Tbp of data, and metabolite profiling analyses on more than 270 distinct samples, to study stress kinetics across three 600-million-year-divergent streptophytes. Through co-expression analysis and Granger causal inference we predict a gene regulatory network that retraces a web of ancient signal convergence at ethylene signaling components, osmosensors, and chains of major kinases. These kinase hubs already integrated diverse environmental inputs since before the dawn of plants on land.

evolutionary biology↗