Biology subjects

Coelho, S. M.

Publications and source records attributed to Coelho, S. M..

32 records · Page 2Linked to original sources

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

Role of transcription and translation during the early development of the brown alga Ectocarpus

Background and aimsParthenogenesis, the embryonal development of an unfused gamete, is a widespread trait within the brown algae (Phaeophyceae). We hypothesized that the parthenogenetic development of male gametes of the model brown alga Ectocarpus species 7 would rapidly be dependent on de novo transcription and translation because of the small size of the gamete cell. MethodsWe followed the development of male Ectocarpus gametes to parthenosporophytes in the presence of either the transcription inhibitor thiolutin or the translation inhibitor emetine. Responses in morphology and growth were compared to development in inhibitor-free control conditions at three time points over 12 days. Potentially persistent inhibitor effects were then investigated by growing parthenosporophytes in an inhibitor-free post-culture for 14 days. Key resultsThiolutin did not affect gamete germination, but growth of parthenosporophytes was significantly delayed. While almost all control parthenosporophytes had grown larger than 10 cells over 12 days, thiolutin inhibited growth beyond a size of 5-10 cells. The effects of thiolutin were reversible in the post-culture. Consequences of the emetine treatment were more severe, germination was already strongly inhibited by day 5, and on average only 27.5% of emetine-treated gametes had completed the first cell division on day 12. Emetine fully inhibited development beyond the 5-cell stage during the treatment, and induced morphological abnormalities (i.e., round cell shape and abnormal cell division planes) which persisted throughout the post-culture. ConclusionsThese results imply that Ectocarpus gametes contain sufficient proteins to germinate, and that the first cell cycles of parthenogenetic gamete development presumably utilize mRNA already present in the gametes. We discuss that storing mRNA and proteins in the developing gametes before release may be an adaptive trait in Ectocarpus to ensure quick development after fertilization, or alternatively the vegetative completion of the life cycle in the absence of mates.

developmental biology↗

bioRxiv2023

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↗

bioRxiv2022

The baseless mutant links protein phosphatase 2A with basal cell identity in the brown alga Ectocarpus

The first mitotic division of the initial cell is a key event in all multicellular organisms and is usually concomitant with the establishment of major developmental axes and cell fates. The brown alga Ectocarpus has a haploid-diploid life cycle that involves the development of two multicellular and independent generations, the sporophyte and the gametophyte. Each generation deploys a distinct developmental program autonomously from an initial cell, whose first cell division sets up the future body pattern. Here, we show that mutations in the BASELESS (BAS) gene result in multiple cellular defects during the first division of the initial cell and subsequently failure to produce basal structures (rhizoids and prostrate filaments) during both generations of the life cycle. Cloning-by-sequencing revealed that BAS encodes a type B" regulatory subunit of protein phosphatase 2A, and transcriptomic analysis of early developmental stages uncovered potential effector genes involved in setting up basal cell fate in this organism. The bas mutant phenotype is very similar to that observed in the distag (dis) mutants, which lack a functional TBCCd1 protein, at both the cellular and morphological levels. The high level of similarity of the dis and bas mutant phenotypes indicate that TBCCd1 and PP2A are two critical components of the cellular machinery that regulates the division of the initial cell and mediates the establishment of basal cell fate in the developing thallus.

developmental biology↗

bioRxiv2022

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

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

evolutionary biology↗

bioRxiv2022

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↗

bioRxiv2022

Evolution and diversity of the TopoVI and TopoVI-like subunits with extensive divergence of the TOPOVIBL subunit

Type II DNA topoisomerases regulate topology by double-stranded DNA cleavage and ligation. The TopoVI family of DNA topoisomerase, first identified and biochemically characterized in Archaea, represents, with TopoVIII and mini-A, the type IIB family. TopoVI has several intriguing features in terms of function and evolution. TopoVI has been identified in some eucaryotes, and a global view is lacking to understand its evolutionary pattern. In addition, in eucaryotes, the two TopoVI subunits (TopoVIA and TopoVIB) have duplicated and evolved to give rise to Spo11 and TopoVIBL, forming TopoVI-like (TopoVIL), a complex essential for generating DNA breaks that initiation homologous recombination during meiosis. TopoVIL is essential for sexual reproduction. How the TopoVI subunits have evolved to ensure this meiotic function is unclear. Here, we investigated the phylogenetic conservation of TopoVI and TopoVIL. We demonstrate that BIN4 and RHL1, potentially interacting with TopoVIB, have co-evolved with TopoVI. Based on model structures, this observation supports the hypothesis for a role of TopoVI in decatenation of replicated chromatids and predicts that in eucaryotes the TopoVI catalytic complex includes BIN4 and RHL1. For TopoVIL, the phylogenetic analysis of Spo11, which is highly conserved among Eukarya, highlighted a eukaryal-specific N-terminal domain that may be important for its regulation. Conversely, TopoVIBL was poorly conserved and rapidly evolving, giving rise to ATP hydrolysis-mutated or -truncated protein variants, or was undetected in some species. This remarkable plasticity of TopoVIBL provides important information for the activity and function of TopoVIL during meiosis.

evolutionary biology↗

bioRxiv2021

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↗

bioRxiv2021

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↗

bioRxiv2021

A partially sex-reversed giant kelp sheds light into the mechanisms of sexual differentiation in a UV sexual system

In UV sexual systems, sex is determined during the haploid phase of the life cycle and males have a V chromosome whereas females have a U chromosome. Previous work in the brown algal model Ectocarpus revealed that the V chromosome has a dominant role in male sex determination and suggested that the female developmental program may occur by default, triggered in the absence of the male master sex determination gene(s). Here, we describe the identification of a genetically male giant kelp strain presenting phenotypic features typical of a female, despite lacking the U-specific region. The conversion to the female developmental program is however incomplete, because gametes of this feminised male are unable to produce the sperm-attracting pheromone lamoxirene. We identify the transcriptomic patterns underlying the male and female specific developmental programs, and reveal the faster evolutionary rates of male-biased genes compared to female-biased and unbiased genes. Moreover, we show that the phenotypic feminisation of the variant strain is associated with both feminisation and de-masculinisation of gene expression patterns. Importantly, the feminisation phenotype was associated with the dramatic downregulation of two V-specific genes including a candidate sex-determining gene on the V-specific region. Our results reveal the transcriptional changes associated with sexual differentiation in a UV system with marked sexual dimorphism, and contribute to disentangling the role of sex-linked genes and autosomal gene expression in the initiation of the male and female developmental programs. Overall, the data presented here imply that the U-specific region in the giant kelp is not required to initiate the female developmental program, but is critical to produce fully functional eggs, arguing against the idea that female is the default sex in this species.

evolutionary biology↗

bioRxiv2020

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↗

bioRxiv2020

Histone modifications during the life cycle of the brown alga Ectocarpus

BackgroundBrown algae evolved complex multicellularity independently of the animal and land plant lineages and are the third most developmentally complex phylogenetic group on the planet. An understanding of developmental processes in this group is expected to provide important insights into the evolutionary events necessary for the emergence of complex multicellularity. Here we have focused on mechanisms of epigenetic regulation involving post-translational modifications (PTMs) of histone proteins. ResultsA total of 47 histone PTMs were identified, including a novel mark H2AZR38me1, but Ectocarpus lacks both H3K27me3 and the major polycomb complexes. ChIP-seq identified PTMs associated with transcription start sites (TSSs) and gene bodies of active genes, and with transposons. H3K79me2 exhibited an unusual pattern, often marking large genomic regions spanning several genes. TSSs of closely spaced divergently transcribed gene pairs shared a common nucleosome depleted region and exhibited shared histone PTM peaks. Overall, patterns of histone PTMs were stable through the life cycle. Analysis of histone PTMs at generation-biased genes identified a correlation between the presence of specific chromatin marks and the level of gene expression. ConclusionsThe overview of histone PTMs in the brown algae presented here will provide a foundation for future studies aimed at understanding the role of chromatin modifications in the regulation of brown algal genomes.

genomics↗

bioRxiv2018

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↗

bioRxiv2018

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↗