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Lipinska, A. P.

Publications and source records attributed to Lipinska, A. P..

12 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↗

Structural and evolutionary features of red algal UV sex chromosomes

BackgroundSex chromosomes in red algae have remained relatively understudied, despite their fundamental role in understanding the evolution of sex determination across eukaryotes. In this study, we investigate the structure, gene composition, and evolutionary history of the U and V sex chromosomes in four Gracilaria species, which diverged approximately 100 million years ago (MYA). ResultsOur findings reveal that UV sex chromosomes, previously identified in green and brown algae as well as bryophytes, have also evolved in red algae, contributing to the diversity of sex determination systems across eukaryotes. The shared orthology of conserved sex-determining region (SDR) genes between Gracilaria and distantly related red algae suggests that this system may have originated approximately 390 MYA, making it one of the oldest known sex chromosome systems. The SDR in Gracilaria is relatively small but contains conserved gametologs and V-specific genes involved in transcriptional regulation and signaling, suggesting their essential role in sexual differentiation. Unlike the conserved V-specific genes, U-specific genes appear absent, pointing to a dominant role of the V chromosome in sex determination. The evolution of Gracilaria sex chromosomes involved recombination suppression, gene relocations, duplications, and potential gene loss. Despite their ancient origin, the sex chromosomes show low levels of degeneration, likely due to haploid purifying selection during the gametophytic phase of the life cycle. ConclusionThis study provides the first detailed characterization of the U and V sex chromosomes in red algae, preparing the ground for future studies on reproductive life cycles and speciation in this understudied group of eukaryotes.

evolutionary biology↗

Evolutionary history of the main extracellular matrix polysaccharides in brown algae

Brown algae belong to the Stramenopiles phylum and are phylogenetically distant from plants and other multicellular organisms. This independent evolutionary history has shaped brown algae with numerous metabolic characteristics specific to this group, including the synthesis of peculiar polysaccharides contained in their extracellular matrix (ECM). Alginates and fucose-containing sulphated polysaccharides (FCSP), the latter including fucans, are the main components of ECMs. However, the metabolic pathways of these polysaccharides remain poorly described due to a lack of genomic data. An extensive genomic dataset has been recently released for brown algae and their close sister species. We performed an expert annotation of key genes involved in ECM-carbohydrate metabolisms, combined with comparative genomics, phylogenetics analyses, and protein modelling. Our analysis indicates that the gene families involved in both the synthesis and degradation of alginate were acquired by the common ancestor of brown algae and their closest sister species Schizocladia ischiensis, and subsequently expanded in brown algae. The pathway for the biosynthesis of fucans still remains biochemically unresolved and we identify the most likely fucosyltransferase genes that may harbour a fucan synthase activity in brown algae. Our analysis questions the possible occurrence of FCSPs outside brown algae, notably within their closest sister taxon.

evolutionary 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↗

THE RHODOEXPLORER PLATFORM FOR RED ALGAL GENOMICS AND WHOLE GENOME ASSEMBLIES FOR SEVERAL GRACILARIA SPECIES

Macroalgal (seaweed) genomic resources are generally lacking as compared to other eukaryotic taxa, and this is particularly true in the red algae (Rhodophyta). Understanding red algal genomes is critical to understanding eukaryotic evolution given that red algal genes are spread across eukaryotic lineages from secondary endosymbiosis and red algae diverged early in the Archaeplastids. The Gracilariales are highly diverse and widely distributed order whose species can serve as ecosystem engineers in intertidal habitats, including several notorious introduced species. The genus Gracilaria is cultivated worldwide, in part for its production of agar and other bioactive compounds with downstream pharmaceutical and industrial applications. This genus is also emerging as a model for algal evolutionary ecology. Here, we report new whole genome assemblies for two species (G. chilensis and G. gracilis), a draft genome assembly of G. caudata, and genome annotation of the previously published G. vermiculophylla genome. To facilitate accessibility and comparative analysis, we integrated these data in a newly created web-based portal dedicated to red algal genomics (https://rhodoexplorer.sb-roscoff.fr). These genomes will provide a resource for understanding algal biology and, more broadly, eukaryotic evolution.

genomics↗

Low spontaneous mutation rate in a complex multicellular eukaryote with a haploid-diploid life cycle

The spontaneous mutation rate {micro} is a crucial parameter driving evolution and biodiversity. Mutation rates are highly variable across species, suggesting that {micro} is susceptible to selection and drift and that species life cycle and life history may impact its evolution. In particular, asexual reproduction and haploid selection are expected to affect mutation rate, but very little empirical data is available to test this expectation. Here, we sequence 30 genomes of a parent-offspring pedigree in the brown algae Ectocarpus to test the impact of its life cycle on mutation rate. Ectocarpus alternates between a haploid and a diploid stage, both multicellular and free living, and utilizes both sexual and asexual reproduction. Ectocarpus is therefore a unique model to empirically test expectations of the effect of asexual reproduction and haploid selection on mutation rate evolution. We estimate that Ectocarpus has a nucleotide mutation rate of {micro}bs=4.07x10-10 per site per generation, a surprisingly low number for a multicellular complex eukaryote. Effective population size (Ne) and genome size could not explain this low mutation rate. We propose that the haploid-diploid life cycle, combined with extensive asexual reproduction may be key drivers of mutation rate.

evolutionary biology↗

Evolutionary dynamics of sex-biased gene expression in a young XY system: Insights from the brown algae

The sex-dependent regulation of gene expression is considered to be an underlying cause of often extensive, sexually dimorphic traits between males and females. Although the nature and degree of sex-biased gene expression has been well-documented in several animal and plant systems, far less is known about the commonality, conservation, recruitment mechanisms and evolution of sex-biased genes in more distant eukaryotic groups. Brown algae are of particular interest for empirical studies on the evolution of sex-biased gene expression, as they have been evolving independently from animals and plants for over one billion years. Here we focus on two brown algal dioecious species, Fucus serratus and Fucus vesiculosus, where male heterogamety (XX/XY) has recently emerged. Using RNA-seq, we study sex-biased gene expression and discuss different evolutionary forces responsible for the evolution of sex-biased genes. We find that both species evolved masculinized transcriptomes, with sex-biased genes allocated mainly to male reproductive tissue, but virtually absent in vegetative tissues. Conserved male-biased genes were enriched in functions related to gamete production, along with sperm competition and include two flagellar proteins under positive selection. In contrast to female-biased genes, which show high turnover rates, male-biased genes reveal remarkable conservation of bias and expression levels between the two species. As observed in other XY systems, male-biased genes also display accelerated rates of coding sequence evolution compared to female-biased or unbiased genes. Our results imply that evolutionary forces affect male and female sex-biased genes differently on structural and regulatory levels. Similar to evolutionarily distant plant and animal lineages, sex-biased gene expression in Fucus evolved during the transition to dioecy to resolve intra-locus sexual conflict arising from anisogamy.

evolutionary biology↗

SELECTION DRIVES THE EVOLUTION OF CONVERGENT GENE EXPRESSION CHANGES DURING TRANSITIONS TO CO-SEXUALITY IN HAPLOID SEXUAL SYSTEMS

AO_SCPLOWBSTRACTC_SCPLOWCo-sexuality has evolved repeatedly from ancestors with separate sexes across a wide range of taxa. The switch to co-sexuality is expected to involve major molecular readjustments at the level of gene expression patterns, as modified males or females will express the opposite sexual function for which their phenotypes have been optimized. However, the molecular changes underpinning this important transition remain unknown, particularly in organisms with haploid sexual systems such as bryophytes, red and brown algae. Here, we explore four independent events of emergence of co-sexuality from uni-sexual (dioicous) ancestors in brown algal clades in order to examine the nature, evolution and degree of convergence of gene expression changes that accompany the breakdown of dioicy. The amount of male versus female phenotypic differences in dioicous species were not correlated with the extent of sex-biased gene expression, in strike contrast to what is observed in animals. Although sex-biased genes exhibited a high turnover rate during brown alga diversification, their predicted functions were remarkably conserved. Transition to co-sexuality consistently involved adaptive gene expression shifts and rapid sequence evolution, particularly of male-biased genes. The gene expression profiles of co-sexual species were more similar to those of females than to males of related dioicous species, suggesting that the former may have arisen from ancestral females. Finally, we identified extensive convergent gene expression changes associated with the transition to co-sexuality, and these changes appear to be driven by selection. Together, our observations provide novel insights on how co-sexual systems arise from ancestral, haploid UV sexual systems.

evolutionary biology↗

Chromatin dynamics associated with sexual differentiation in a UV sex determination system

In many eukaryotes, such as dioicous mosses and many algae, sex is determined by UV sex chromosomes and is expressed during the haploid phase of the life cycle. In these species, the male and female developmental programs are initiated by the presence of the U- or V-specific regions of the sex chromosomes but, as in XY and ZW systems, phenotypic differentiation is largely driven by autosomal sex-biased gene expression. The mechanisms underlying sex-biased transcription in XY, ZW or UV sexual systems currently remain elusive. Here, we set out to understand the extent and nature of epigenomic changes associated with sexual differentiation in the brown alga Ectocarpus, which has a well described UV system. Five histone modifications, H3K4me3, H3K27Ac, H3K9Ac, H3K36me3, H4K20me3, were quantified in near-isogenic male and female lines, leading to the identification of 13 different chromatin states across the Ectocarpus genome that showed different patterns of enrichment at transcribed, silent, housekeeping or narrowly-expressed genes. Chromatin states were strongly correlated with levels of gene expression indicating a relationship between the assayed marks and gene transcription. The relative proportion of each chromatin state across the genome remained stable in males and females, but a subset of genes exhibited different chromatin states in the two sexes. In particular, males and females displayed distinct patterns of histone modifications at sex-biased genes, indicating that chromatin state transitions occur preferentially at genes involved in sex-specific pathways. Finally, our results reveal a unique chromatin landscape of the U and V sex chromosomes compared to autosomes. Taken together, our observations reveal a role for histone modifications in sex determination and sexual differentiation in a UV sexual system, and suggest that the mechanisms of epigenetic regulation of genes on the UV sex chromosomes may differ from those operating on autosomal genes.

evolutionary biology↗

Convergent recruitment of life cycle regulators to direct sporophyte development in two eukaryotic supergroups

Three amino acid loop extension homeodomain transcription factors (TALE HD TFs) act as life cycle regulators in green algae and land plants. In mosses these regulators are required for the deployment of the sporophyte developmental program. We demonstrate that mutations in either of two TALE HD TF genes, OUROBOROS or SAMSARA, in the brown alga Ectocarpus result in conversion of the sporophyte generation into a gametophyte. The OUROBOROS and SAMSARA proteins heterodimerise in a similar manner to TALE HD TF life cycle regulators in the green lineage. These observations demonstrate that TALE-HD-TF-based life cycle regulation systems have an extremely ancient origin, and that these systems have been independently recruited to regulate sporophyte developmental programs in at least two different complex multicellular eukaryotic supergroups, Archaeplastida and Chromalveolata.

plant biology↗

The genome of Ectocarpus subulatus highlights unique mechanisms for stress tolerance in brown algae

Brown algae are multicellular photosynthetic stramenopiles that colonize marine rocky shores worldwide. Ectocarpus sp. Ec32 has been established as a genomic model for brown algae. Here we present the genome and metabolic network of the closely related species, Ectocarpus subulatus Kutzing, which is characterized by high abiotic stress tolerance. Since their separation, both strains show new traces of viral sequences and the activity of large retrotransposons, which may also be related to the expansion of a family of chlorophyll-binding proteins. Further features suspected to contribute to stress tolerance include an expanded family of heat shock proteins, the reduction of genes involved in the production of halogenated defence compounds, and the presence of fewer cell wall polysaccharide-modifying enzymes. Overall, E. subulatus has mainly lost members of gene families down-regulated in low salinities, and conserved those that were up-regulated in the same condition. However, 96% of genes that differed between the two examined Ectocarpus species, as well as all genes under positive selection, were found to encode proteins of unknown function. This underlines the uniqueness of brown algal stress tolerance mechanisms as well as the significance of establishing E. subulatus as a comparative model for future functional studies.

genomics↗

Rapid turnover of life-cycle-related genes in the brown algae

BackgroundSexual life cycles in eukaryotes involve a cyclic alternation between haploid and diploid phases. While most animals possess a diploid life cycle, plants and algae alternate between multicellular haploid (gametophyte) and diploid (sporophyte) generations. In many algae, gametophytes and sporophytes are independent and free living, and may present dramatic phenotypic differences. The same shared genome can therefore be subject to different, even conflicting, selection pressures in each of the life cycle generations. Here, we have analysed the nature and extent of genome-wide generation-biased gene expression in four species of brown algae with contrasting levels of dimorphism between life cycle generations, in order to assess the potential role of generation-specific selection in shaping patterns of gene expression and divergence.\n\nResultsWe show that the proportion of the transcriptome that is generation-biased is associated with the level of phenotypic dimorphism between the life cycle stages. Importantly, our data reveals a remarkably high turnover rate for life-cycle-related gene sets across the brown algae and highlights the importance not only of co-option of regulatory programs from one generation to the other but also a key role for newly emerged, lineage-specific genes in the evolution of the gametophyte and sporophyte developmental programs in this major eukaryotic group. Moreover, we show that generation-biased genes display distinct evolutionary modes, with gametophyte-biased genes evolving rapidly at the coding sequence level whereas sporophyte-biased genes exhibit changes in their patterns of expression.\n\nConclusionOur analysis uncovers the characteristics, expression patterns and evolution of generation-biased genes and underline the selective forces that shape this previously underappreciated source of phenotypic diversity.

evolutionary biology↗