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Haas, F. B.

Publications and source records attributed to Haas, F. B..

18 recordsLinked to original sources

Haplotype tagging sheds light on speciation between two divergent cryptic species of the brown algae Ectocarpus

Understanding how genome-wide divergence translates to barriers to gene flow is a central question in speciation research, particularly in marine environments where interconnected habitats frequently accommodate cryptic diversity. Using linked-read whole-genome data from the brown alga Ectocarpus, we investigated genome-wide reproductive isolation between two cryptic brown algal species E. siliculosus and E. crouaniorum across replicated hybrid zones in Europe and Chile. We first uncover deep genetic structure within E. crouaniorum, revealing a more intricate species complex than previously recognized. Despite this complexity, we found parallel patterns of asymmetric introgression that emerged independently in Europe and Chile, where we detected both, F1 and low-level introgressed individuals. However, the specific lineage pairs involved in hybridization depended on local demographic history. Demographic modeling further indicated that reproductive isolation strengthens gradually with divergence time and differs markedly between geographic regions, with ongoing asymmetric gene flow even between lineage pairs where hybrids were not detected in the field. In all cases, the genomic landscape of hybridization is consistent with a polygenic, genome-wide barrier to gene flow rather than a few large-effect regions. Our results show that cryptic speciation in brown algae is driven by repeatable, regionally parallel architectures of genome-wide reproductive isolation which is shaped by ecological and demographic context.

evolutionary biology↗

Regulatory innovation and transcriptome turnover drive the evolution of multicellularity in brown algae

How complex multicellularity evolved repeatedly across eukaryotes remains a central unresolved question in biology. Whether principles inferred largely from animals and plants reflect universal features of multicellular evolution or lineage-specific outcomes is unknown. Here, using a stage- and tissue-resolved transcriptomic atlas spanning the full life cycles of 15 species across the brown algal radiation, comprising 639 RNA-seq libraries, we uncover general principles governing the evolution of developmental programs in an independently evolved multicellular lineage. Despite broad conservation of genome architecture and synteny, developmental and morphological diversification is accompanied by pervasive rewiring of gene expression and rapid turnover of co-expression networks, identifying regulatory evolution as a major driver of multicellular innovation. We show that evolutionarily young genes, including genes of giant viral origin, are repeatedly recruited into developmental programs, particularly in motile unicellular stages, revealing a broader role for these stages as hotspots of evolutionary novelty. We further identify lineage-specific cis-regulatory innovation linked to active chromatin and large-scale transcriptional rewiring, providing a mechanistic basis for transcriptome turnover. Together, these findings show that brown algae reinvented complex multicellularity through distinct molecular routes shaped by rapid regulatory innovation, while revealing organizational principles conserved across independent multicellular lineages.

evolutionary biology↗

Fast zygotic genome activation in brown algae

The maternal-to-zygotic transition (MZT), during which developmental control shifts from maternal products to the zygotic genome, is a fundamental feature of embryogenesis. The prevailing model, established from animal systems, holds that maternal provisioning and nuclear-to-cytoplasmic (N/C) ratio determine the timing of zygotic genome activation (ZGA). Whether this developmental logic is conserved across multicellular eukaryotes remains unknown. Using brown algae, an independently evolved multicellular lineage spanning broad natural variation in maternal provisioning, we generated comparative embryonic transcriptomes across three species and resolved parental contributions through reciprocal crosses and allele-specific expression. Contrary to canonical animal models, all species activated their zygotic genomes immediately after fertilisation, including highly provisioned species with low N/C ratios, and showed no evidence of stable parental imprinting. These findings reveal that timing and regulation of MZT during embryogenesis is evolutionarily flexible and independently shaped across the tree of life.

developmental biology↗

Ribosome profiling reveals widespread translational control across developmental stages in the brown alga Ectocarpus

Translation represents a central regulatory layer of gene expression, enabling rapid and dynamic modulation of protein output. While its importance in development is well established, it remains poorly characterized outside animals and land plants. Brown algae, and in particular Ectocarpus, offer a compelling system to investigate translational regulation in development, having evolved multicellularity independently of other major eukaryotic lineages and exhibiting a complex life cycle with distinct haploid and diploid developmental programs. Although transcriptional regulation contributes to Ectocarpus development, the striking similarity of transcriptomes across life cycle stages indicates that transcription alone is insufficient to explain their distinct developmental identities, pointing to a major role for post-transcriptional regulation. Here, we establish ribosome profiling in Ectocarpus and define its translatome across key developmental stages. We uncover widespread stage- and sex-specific translational regulation, with post-transcriptional buffering emerging as the predominant mode of control. Genes subject to translational regulation exhibit optimized codon usage, broader transcriptional profiles and shorter 3' UTRs. These genomic features are associated with variation in translation efficiency. Collectively, these results provide the first comprehensive characterization of the Ectocarpus translatome and highlight a major role for translational regulation in developmental gene expression in an independently evolved multicellular lineage.

developmental biology↗

Lineage-wide evolution of 3D genome organisation and centromeres in brown algae

Although 3D genome architecture has been described for an increasing number of plant and algal species, comparative analyses across closely related lineages remain scarce. Consequently, fundamental questions persist about how chromatin organization is maintained or reshaped over deep evolutionary time, and how such changes relate to life-history traits, genome size, and linear genome features. Here, we present a comprehensive analysis of 3D chromatin architecture across six brown algae species and one outgroup, spanning the phylogenetic breadth and biological complexity of this key photosynthetic lineage. We show that compact genomes lack chromatin domains whereas larger, transposable element-rich genomes of morphologically complex taxa tend to exhibit structured organization including TAD-like domains. We investigate chromatin folding patterns and gene expression over evolutionary time and uncover 3D chromatin features associated with transitions in sexual systems. Moreover, we reconstruct the ancestral brown algal karyotype, revealing deeply conserved macrosynteny and providing a new framework for interpreting chromosome-scale genome dynamics. Finally, we uncover an ancient and highly conserved association between centromeres and chromodomain-encoding retrotransposons, revealing a remarkable example of convergence in centromere-transposon co-evolution between brown algae and angio-sperms, and one of the most stable examples of centromere-linked transposable elements known in eukaryotes. Together, our findings elucidate the evolutionary history of 3D chromatin and linear genome architectures across an entire eukaryotic lineage and highlight extreme centromere stability in brown algae, providing a powerful point of comparison with land plants and deepening our understanding of genome evolution in independent multicellular lineages. One sentence summaryWe present a lineage-wide evolutionary analysis of 3D genome architecture and organization across brown algae, revealing conserved chromosomal features, lineage-specific rearrangements, and long-term co-evolution of centromeres and retrotransposons that together illuminate how nuclear architecture evolves over hundreds of millions of years.

genomics↗

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↗

Latent endogenous viral elements drive active infection and inheritance in a multicellular host

Endogenous viral elements (EVEs) inserted in host genomes are often regarded as inert relics of past infections. Whether they can retain infective potential and contribute to active viral cycles has remained unresolved. Here, we demonstrate that EVEs in the brown alga Ectocarpus can reactivate and drive productive viral infections. Using long-read sequencing and transcriptomics, we identify full-length, transcriptionally active giant viruses integrated within the host genome. Reactivation of these elements is specific to reproductive cells, transforming gametangia into virus-producing structures, and viral symptoms strictly correlate to the presence of active EVEs. Genetic analyses show that these elements are stably inherited, while their activation is precisely regulated by developmental and environmental cues. By resolving the genomic integration sites, we propose a mechanism for Phaeovirus integration and replication. This work provides the first direct evidence that giant EVEs can reactivate, replicate, and transmit both horizontally and vertically in a multicellular eukaryote, establishing a new model to explore latency, inheritance and the evolutionary impact of large dsDNA viruses.

genetics↗

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↗

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↗

Developmental pathways underlying sexual differentiation in a U/V sex chromosome system

In many multicellular organisms, sexual development is not determined by XX/XY or ZW/ZZ systems but by U/V sex chromosomes. In U/V systems, sex determination occurs in the haploid phase, with U chromosomes in females and V chromosomes in males. Here, we explore several male, female and partially sex-reversed male lines of giant kelp to decipher how U/V sex chromosomes and autosomes initiate male versus female development. We identify a key set of genes on the sex chromosomes involved in triggering sexual development, and characterise autosomal effector genes underlying sexual differentiation. We show that male, but not female, development involves large-scale transcriptome reorganisation with pervasive enrichment in regulatory genes, faster evolutionary rates, and high species specificity of male-biased genes. Our observations imply that a female-like phenotype is the "ground state", which is complemented by the presence of a U-chromosome, but overridden by a dominant male developmental program in the presence of a V-chromosome.

developmental biology↗

Origin and evolutionary trajectories of brown algal sex chromosomes

Sex chromosomes fall into three classes: XX/XY, ZW/ZZ and U/V systems. The rise, evolution and demise of U/V systems has remained an evolutionary enigma. Here, we analyse genomes spanning the entire brown algal phylogeny to decipher their sex-determination evolutionary history. U/V sex chromosomes emerged between 450 and 224 million years ago, when a region containing the pivotal male-determinant MIN located in a discrete region in proto-U and proto-V chromosomes ceased recombining. Over time, nested inversions led to step-wise expansions of the sex locus, accompanying increasing morphological complexity and sexual differentiation of brown seaweeds. Unlike XX/XY and ZW/ZZ, brown algal U/V evolve mainly by gene gain, showing minimal degeneration. They are structurally dynamic and act as genomic cradles fostering the birth of new genes, potentially from ancestrally non coding sequences. Our analyses demonstrate that hermaphroditism arose from ancestral males that acquired U-specific genes by ectopic recombination, and that in the transition from a U/V to an XX/XY system, V-specific genes moved down the genetic hierarchy of sex determination. Both events lead to the demise of U and V and erosion of their specific genomic characteristics. Taken together, our findings offer a comprehensive model of U/V sex chromosome evolution.

evolutionary biology↗

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↗

PARALLEL LOSS OF SEX IN FIELD POPULATIONS OF A BROWN ALGA SHEDS LIGHT ON THE MECHANISMS UNDERLYING THE EMERGENCE OF ASEXUALITY

AO_SCPLOWBSTRACTC_SCPLOWSexual reproduction is widespread among eukaryotes, but asexual lineages have repeatedly arisen from sexual ancestors across a wide range of taxa. Despite extensive research on the evolution of asexuality from sexual ancestors, the molecular changes underpinning the switch to asexual reproduction remain elusive, particularly in organisms with haploid sexual systems such as bryophytes, and red and brown algae in which males and females are haploid and multicellular. Here, we investigate independent events in which asexuality has emerged from sexual ancestor lineages in species of the brown algal Scytosiphon, we examine the proximate and evolutionary mechanisms involved, and test the importance of sexual conflict on gene expression changes following loss of sex. We find that individuals from asexual, female-only ( Amazon) populations lose their ability to produce and sex pheromone and, consequently, are unable to attract and fuse with male gametes, whereas they gain the ability to trigger parthenogenic (asexual) development from large, unfertilized eggs. This independent and convergent decline in pheromone production and optimization of asexual traits is accompanied by convergent changes in gene expression, including de-feminization and masculinization of the Amazon gamete transcriptomes. These data are consistent with the idea that decay of female functions, rather than relaxation of sexual antagonism, is the dominant force at play during the emergence of asexuality in haploid sexual systems. Moreover, we identify a locus on an autosomal protein-coding gene that is associated with the switch to asexuality. We propose that the sex chromosome, together with this autosomal locus, may underlie the switch to obligate asexuality in the Amazon populations.

evolutionary biology↗

Evolutionary conserved and divergent responses to copper zinc superoxide dismutase inhibition in plants

Life evolved in the presence of reactive oxygen species (ROS) and was further challenged by two consecutive great oxidation events. Therefore, ROS are deeply intertwined into the physological, morphological and transcriptional responses of organisms. Copper zinc superoxide dismutases (CuZnSODs) evolved around the first great oxidation event and have next to their classical role in ROS detoxification also important roles in signaling and transcriptional regulation. Here we addressed the role of CuZnSODs in early land plant evolution. We show, that pharmaceutical inhibition of CuZnSODs with Lung Cancer Screen 1 (LCS-1) in different plant species, including Marchantia polymorpha and Physcomitrium patens, representing the evolutionary early stages of land plants, and Arabidopsis thaliana as a modern vascular plant, lead to impairment of development and growth. Interestingly, Marchantia only possesses the cytosolic CuZnSOD isoform, whereas Physcomitrium additionally contains a plastidial isoform and Arabidopsis contains next to that a third peroxisomal isoform. An RNA-seq analysis revealed that the inhibition of CuZnSODs provoked a similar core response in all plant species analyzed, while those that contain more isoforms showed an extended response. In addition, an untargeted metabolomics approach revealed a specific metabolic signature for each plant species. Through the above approach the oxidative stress provoked by LCS-1 in plants can be specified and we argue that CuZnSOD functions are evolutionary conserved and might be important for plant terrestrialization.

plant biology↗

Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution

The filamentous and unicellular algae of the class Zygnematophyceae are the closest algal relatives of land plants. Inferring the properties of the last common ancestor shared by these algae and land plants allows us to identify decisive traits that enabled the conquest of land by plants. We sequenced four genomes of filamentous Zygnematophyceae (three strains of Zygnema circumcarinatum and one strain of Z. cylindricum) and generated chromosome-scale assemblies for all strains of the emerging model system Z. circumcarinatum. Comparative genomic analyses reveal expanded genes for signaling cascades, environmental response, and intracellular trafficking that we associate with multicellularity. Gene family analyses suggest that Zygnematophyceae share all the major enzymes with land plants for cell wall polysaccharide synthesis, degradation, and modifications; most of the enzymes for cell wall innovations, especially for polysaccharide backbone synthesis, were gained more than 700 million years ago. In Zygnematophyceae, these enzyme families expanded, forming co-expressed modules. Transcriptomic profiling of over 19 growth conditions combined with co-expression network analyses uncover cohorts of genes that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution. HIGHLIGHTSO_LIGenomes of four filamentous algae (Zygnema) sisters to land plants C_LIO_LIZygnema are rich in genes for multicellular growth and environmental acclimation: signaling, lipid modification, and transport C_LIO_LICell wall innovations: diversification of hexameric rosette cellulose synthase in Zygnematophyceae C_LIO_LICo-expression networks reveal conserved modules for balancing growth and acclimation C_LI

evolutionary biology↗

JGI Plant Gene Atlas: An updateable transcriptome resource to improve structural annotations and functional gene descriptions across the plant kingdom

Gene functional descriptions, which are typically derived from sequence similarity to experimentally validated genes in a handful of model species, offer a crucial line of evidence when searching for candidate genes that underlie trait variation. Plant responses to environmental cues, including gene expression regulatory variation, represent important resources for understanding gene function and crucial targets for plant improvement through gene editing and other biotechnologies. However, even after years of effort and numerous large-scale functional characterization studies, biological roles of large proportions of protein coding genes across the plant phylogeny are poorly annotated. Here we describe the Joint Genome Institute (JGI) Plant Gene Atlas, a public and updateable data resource consisting of transcript abundance assays from 2,090 samples derived from 604 tissues or conditions across 18 diverse species. We integrated across these diverse conditions and genotypes by analyzing expression profiles, building gene clusters that exhibited tissue/condition specific expression, and testing for transcriptional modulation in response to environmental queues. For example, we discovered extensive phylogenetically constrained and condition-specific expression profiles across many gene families and genes without any functional annotation. Such conserved expression patterns and other tightly co-expressed gene clusters let us assign expression derived functional descriptions to 64,620 genes with otherwise unknown functions. The ever-expanding Gene Atlas resource is available at JGI Plant Gene Atlas (https://plantgeneatlas.jgi.doe.gov) and Phytozome (https://phytozome-next.jgi.doe.gov), providing bulk access to data and user-specified queries of gene sets. Combined, these web interfaces let users access differentially expressed genes, track orthologs across the Gene Atlas plants, graphically represent co-expressed genes, and visualize gene ontology and pathway enrichments.

plant biology↗

Neanderthals did not likely consume Physcomitrium patens - a model moss species

This manuscript is discussing the method of Weyrich et al., 2017, "Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus". When studying the dietary profile of a Neanderthal specimen from El Sidron cave (Spain) by sequencing ancient DNA present in calcified dental plaque (calculus) the authors identified a wide-range of potential food sources, including woolly rhinoceros, mushrooms, pine nuts, and moss - namely the less-than-abundant model species Physcomitrium patens. We doubted that Neanderthals were actually eating P. patens. By analyzing the ancient DNA reads using different mapping methods, we show likely a misinterpretation based on the previously used methods. The probability of Neanderthals eating P. patens is the same as eating rice or tomato. However, neither crop was grown in Europe at the time Neanderthals thrived.

evolutionary biology↗

Characterization of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model

Defects in flagella/cilia are often associated with infertility and disease. Motile male gametes (sperm cells) with flagella are an ancestral eukaryotic trait that has been lost in several lineages, for example in flowering plants. Here, we made use of a phenotypic male fertility difference between two moss (Physcomitrella patens) strains to explore spermatozoid function. We compare genetic and epigenetic variation as well as expression profiles between the Gransden and Reute strain to identify a set of genes associated with moss male infertility. Defects in mammal and algal homologs of these genes coincide with a loss of fertility, demonstrating the evolutionary conservation of flagellar function related to male fertility across kingdoms. As a proof of principle, we generated a loss-of-function mutant of a coiled-coil domain containing 39 (ccdc39) gene that is part of the flagellar hydin network. Indeed, the Ppccdc39 mutant resembles the male infertile Gransden strain phenotype. Potentially, several somatic (epi-)mutations occurred during prolonged vegetative propagation of P. patens Gransden, causing regulatory differences of e.g. the homeodomain transcription factor BELL1. Probably these somatic changes are causative for the observed male fertility. We propose that P. patens spermatozoids might be employed as an easily accessible system to study male infertility of human and animals.

plant biology↗