Biology subjects

Borg, M.

Publications and source records attributed to Borg, M..

10 recordsLinked to original sources

bioRxiv2025

Rewiring of chromatin regulation underlies the evolution of brown algal multicellularity

Chromatin structure plays a central role in regulating transcription, genome stability, and epigenetic inheritance in eukaryotes. Much of our understanding of chromatin architecture and histone post-translational modifications (hPTMs) comes from a narrow set of animal and plant models, but emerging data from non-model lineages are challenging canonical views of how chromatin functions across the tree of life. Brown algae are complex multicellular eukaryotes that provide a unique perspective on chromatin evolution given their independent origin of complex multicellularity. Here, we compile the chromatin toolkit of brown algae and show that canonical silencing systems involving DNA cytosine methylation and PRC2-mediated H3K27 methylation were lost early in their evolution. By generating hPTM profiles from diverse brown algal clades, we resolve the nature and regulatory roles of chromatin states in this lineage and show how H3K79 methylation emerged and diversified as a repressive system. We further uncover sex-specific reconfigurations in species with varying degrees of sexual dimorphism and reconstruct the ancestral regulatory landscape that likely preceded the emergence of brown algae. Together, our findings illuminate the dynamic evolution of chromatin regulation in a distinct multicellular lineage and challenge assumptions about the universality of chromatin-based mechanisms across eukaryotes.

evolutionary biology↗

bioRxiv2025

The expanded Bostrychia moritziana genome unveils evolution in the most diverse and complex order of red algae

Red seaweeds form part of an ancient lineage of eukaryotes that were one of the first to evolve multicellularity. Although they share a common evolutionary origin with modern-day plants and display complex multicellular development, we still lack comprehensive genome data from the most highly-evolved groups of red algae. Here, we present a chromosome-level genome assembly of Bostrychia moritziana, a species that is classified into the Rhodomelaceae family of the Ceramiales order, both of which constitute the largest and most diverse family and order of red algae, respectively. Contrary to the commonly held view that red algae generally have small genomes, we report significant genome size expansion in Bostrychia and other Ceramiales species, which we posit as one of at least three independent genome expansion events that occurred during red algal evolution. Our analyses suggest that these expansions do not involve polyploidy or ancient whole genome duplications, but in the case of Bostrychia appear to be largely driven by the dramatic proliferation of a single lineage of giant Plavaka DNA transposons. Consistent with increased genome size, we identify a substantial increase in gene content in Bostrychia that was shaped both by de novo gene emergence and by the amplification of gene families in common with other Ceramiales seaweeds, providing key insight into the genetic adaptations underpinning the evolutionary success of this species-rich order. Finally, our sex-specific assemblies enabled us to resolve the UV sex chromosomes in Bostrychia, which feature expanded gene-rich sex-linked regions. Notably, these sex-linked regions each harbour a distinct TALE-HD transcription factor orthologous to ancient regulators of haploid-diploid transitions in other multicellular lineages. Together, our findings offer a unique perspective of the genomic adaptations driving red algal diversity and demonstrate how this highly successful group of red seaweeds can provide insight into the evolutionary origins and universal principles of complex multicellular plant life.

genomics↗

bioRxiv2024

The expansion and diversification of epigenetic regulatory networks underpins major transitions in the evolution of land plants

Epigenetic silencing is essential for regulating gene expression and cellular diversity in eukaryotes. While DNA and H3K9 methylation silence transposable elements (TEs), H3K27me3 marks deposited by the Polycomb repressive complex 2 (PRC2) silence varying proportions of TEs and genes across different lineages. Despite the major development role epigenetic silencing plays in multicellular eukaryotes, little is known about how epigenetic regulatory networks were shaped over evolutionary time. Here, we analyse epigenomes from diverse species across the green lineage to infer the chronological epigenetic recruitment of genes during land plant evolution. We first reveal the nature of plant heterochromatin in the unicellular chlorophyte microalga Chlorella sorokiniana and identify several genes marked with H3K27me3, highlighting the deep origin of PRC2-regulated genes in the green lineage. By incorporating genomic phylostratigraphy, we show how genes of differing evolutionary age occupy distinct epigenetic states in plants. While young genes tend to be silenced by H3K9 methylation, genes that emerged in land plants are preferentially marked with H3K27me3, some of which form part of a common network of PRC2-repressed genes across distantly-related species. Finally, we analyse the potential recruitment of PRC2 to plant H3K27me3 domains and identify conserved DNA-binding sites of ancient transcription factor (TF) families known to interact with PRC2. Our findings shed light on the conservation and potential origin of epigenetic regulatory networks in the green lineage, while also providing insight into the evolutionary dynamics and molecular triggers that underlie the adaptation and elaboration of epigenetic regulation, laying the groundwork for its future consideration in other eukaryotic lineages.

evolutionary biology↗

bioRxiv2024

3D chromatin maps of a brown alga reveal U/V sex chromosome spatial organisation

Sex chromosomes are unique genomic regions displaying structural and evolutionary features that distinguish them markedly from autosomes. Although nuclear three dimensional (3D) folding of chromatin structure is im-portant for gene expression regulation and correct developmental programs, very little is known about the 3D architecture of sex chromosomes within the nucleus, and how that impacts their function in sex determination. Here, we determine the sex-specific 3D organization of the model brown alga Ectocarpus chromosomes at 2 kb resolution, by comprehensively mapping long-range chromosomal interactions using Hi-C coupled with Oxford Nanopore long reads. We report that Ectocarpus interphase chromatin exhibits a non-Rabl conformation, with strong contacts among telomeres and among centromeres, which feature centromere-specific LTR retrotranspos-ons. The Ectocarpus chromosomes do not contain large local interactive domains that resemble TADs described in animals, but their 3D genome organization is largely shaped by post-translational modifications of histone pro-teins that regulate chromatin compaction and mediate transcriptional regulation. We describe the spatial confor-mation and sub-nuclear positioning of the sex determining region (SDR) within the U and V chromosomes and show that these regions are very insulated and span the centromeres. Moreover, we link sex-specific chromatin dynamics and gene expression levels to the 3D chromatin structure of U and V chromosomes. Finally, we uncover the unique conformation of a large genomic region on chromosome 6 harboring an endogenous viral element (EVE), providing insights regarding the functional significance of the chromatin organisation of latent giant dsDNA virus.

genomics↗

bioRxiv2024

Discovery and heterologous expression of functional 4-O-dimethylallyl-L-tyrosine synthases from lichen-forming fungi.

Fungal DMATS-type aromatic prenyltransferases are a family of biosynthetic enzymes that catalyze the prenylation of a range of aromatic substrates during the biosynthesis of bioactive indole alkaloids, diketopiperazines, and meroterpenoids. Together with their broad substrate scope and soluble nature, this makes DMATS-type prenyltransferases particularly adept for applications in biocatalysis, for example to derivatize aromatic drug leads and improve their bioactivity. Here, we investigated four putative DMATS-type prenyltransferases from lichen-forming fungi, an underexplored group of organisms that produce more than 1,000 unique metabolites. We were able to successfully express two functional lichen prenyltransferases in the heterologous host A. oryzae, which allowed us to identify them as 4-O-dimethylallyltyrosine synthases. Our extensive bioinformatic analysis shows that related lichen prenyltransferases are likely not active on indoles but rather on aromatic polyketides and phenylpropanoids, common metabolites in these organisms. Overall, our work not only provides new insights into fungal DMATS-type prenyltransferases at the family level, but it also enables future efforts aimed at identifying new candidates for biocatalytic transformations of aromatic compounds.

microbiology↗

bioRxiv2023

Sex chromosome dominance in a UV sexual system

The alternation between multicellular haploid gametophytes and diploid sporophytes is a defining feature of most plant and algal life cycles. In such organisms, male and female sexes are determined in the haploid gametophyte with a female (U) or male (V) sex chromosome. Once the U and V chromosomes unite at fertilisation, sex determination no longer occurs, raising key questions about the fate of UV sex chromosomes in the diploid sporophyte stage of the life cycle. Here, we unravel the genetic and molecular interactions between the U and V chromosomes by assessing transcriptional and chromatin states across the life cycle of the brown alga Ectocarpus alongside ouroboros mutants that decouple life cycle stage from ploidy. We reveal how sex chromosome genes are developmentally regulated across the life cycle, with genes involved in female sex determination in particular undergoing strong down-regulation in the sporophyte. Diploid ouroboros mutants containing both a U and V sex chromosome behave as functional male gametophytes yet still exhibit feminized transcription, suggesting that presence of the V chromosome alone is insufficient to fully suppress female developmental program. Although the silencing of sex chromosome genes in the diploid sporophyte does not appear to correlate with localised changes in chromatin state, small RNAs may play a role in the repression of a female sex-linked gene. Finally, we show how histone H3K79me2 is globally re-configured in the diploid phase of the life cycle, including the sex determining region of the UV sex chromosomes. Contrary to its pattern in the haploid gametophyte, H3K79me2 no longer associates with repressed genes in the diploid sporophyte, suggesting that the function of this histone mark in Ectocarpus may be more complex than previously appreciated.

evolutionary biology↗

bioRxiv2023

Inhibition of mammalian mtDNA transcription paradoxically activates liver fatty acid oxidation to reverse diet-induced hepatosteatosis and obesity

The oxidative phosphorylation (OXPHOS) system in mammalian mitochondria plays a key role in harvesting energy from ingested nutrients1, 2. Mitochondrial metabolism is very dynamic and can be reprogrammed to support both catabolic and anabolic reactions, depending on physiological demands or disease states3, 4. Rewiring of mitochondrial metabolism is intricately linked to metabolic diseases5, 6 and is also necessary to promote tumour growth7-11. Here, we demonstrate that per oral treatment with an inhibitor of mitochondrial transcription (IMT)11 shifts whole animal metabolism towards fatty acid oxidation, which, in turn, leads to rapid normalization of body weight, reversal of hepatosteatosis and restoration of glucose tolerance in mice on high-fat diet. Paradoxically, the IMT treatment causes a severe reduction of OXPHOS capacity concomitant with a marked upregulation of fatty acid oxidation in the liver, as determined by proteomics and non-targeted metabolomics analyses. The IMT treatment leads to a marked reduction of complex I, the main dehydrogenase that feeds electrons into the ubiquinone (Q) pool, whereas the levels of electron transfer flavoprotein dehydrogenase (ETF-DH) and other dehydrogenases connected to the Q pool are increased. This rewiring of metabolism caused by reduced mtDNA expression in the liver provides a novel principle for drug treatment of obesity and obesity-related pathology.

physiology↗

bioRxiv2023

Cell-cycle status of male and female gametes during Arabidopsis reproduction

Fertilization in Arabidopsis thaliana is a highly coordinated process that begins with a pollen tube delivering the two sperm cells into the embryo sac. Each sperm cell can then fertilize either the egg or the central cell to initiate embryo or endosperm development, respectively. The success of this double fertilization process requires a tight cell cycle synchrony between the male and female gametes to allow karyogamy (nuclei fusion). However, the cell cycle status of the male and female gametes during fertilization still remains elusive as DNA quantification and DNA replication assays have given conflicting results1-4. Here, to reconcile these results, we quantified the DNA replication state by DNA sequencing and performed microscopic analyses of fluorescent markers covering all the phases of the cell cycle. We show that male and female gametes in Arabidopsis are both arrested prior to DNA replication at maturity and initiate their DNA replication only during fertilization.

plant biology↗

bioRxiv2020

Comparative transcriptomic analysis reveals conserved transcriptional programs underpinning organogenesis and reproduction in land plants

The evolution of plant organs, including leaves, stems, roots, and flowers, mediated the explosive radiation of land plants, which shaped the biosphere and allowed the establishment of terrestrial animal life. Furthermore, the fertilization products of angiosperms, seeds serve as the basis for most of our food. The evolution of organs and immobile gametes required the coordinated acquisition of novel gene functions, the co-option of existing genes, and the development of novel regulatory programs. However, our knowledge of these events is limited, as no large-scale analyses of genomic and transcriptomic data have been performed for land plants. To remedy this, we have generated gene expression atlases for various organs and gametes of 10 plant species comprising bryophytes, vascular plants, gymnosperms, and flowering plants. Comparative analysis of the atlases identified hundreds of organ- and gamete-specific gene families and revealed that most of the specific transcriptomes are significantly conserved. Interestingly, the appearance of organ-specific gene families does not coincide with the corresponding organs appearance, suggesting that co-option of existing genes is the main mechanism for evolving new organs. In contrast to female gametes, male gametes showed a high number and conservation of specific genes, suggesting that male reproduction is highly specialized. The expression atlas capturing pollen development revealed numerous transcription factors and kinases essential for pollen biogenesis and function. To provide easy access to the expression atlases and these comparative analyses, we provide an online database, www.evorepro.plant.tools, that allows the exploration of expression profiles, organ-specific genes, phylogenetic trees, co-expression networks, and others.

evolutionary biology↗

bioRxiv2019

Fungal effector Jsi1 hijacks plant JA/ET signaling through Topless

Ustilago maydis (U. maydis) is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins which suppress immune responses and redirect the host-metabolism in favor of the pathogen. Here we describe a novel strategy by which U. maydis induces plant jasmonate/ethylene (JA/ET) hormone signaling and thereby biotrophic susceptibility. The U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1) possesses an ethylene-responsive element binding factor-associated amphiphilic repression (EAR) motif, DLNxxP, which interacts with the second WD40 domain of the conserved plant co-repressor family Topless/Topless related (TPL/TPR). Jsi1 interaction with TPL/TPRs leads to derepression of the ethylene response factor (ERF) branch of the JA/ET signaling pathway, supporting biotrophic susceptibility. Jsi1 likely activates the ERF branch by interfering with the binding of endogenous DLNxxP motif-containing ERF transcription factors to TPL/TPR proteins. The identification of effector proteins possessing a DLNxxP motif in different fungal species with biotrophic and hemibiotrophic lifestyles together with the validation of the interaction between such effectors from Magnaporthe oryzae (M. oryzae), Sporisorium scitamineum (S. scitamineum), and S. reilianum with TPL proteins indicates the convergent evolution of effectors for modulating the TPL/TPR co-repressor hub.

plant biology↗