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Cock, J. M.

Publications and source records attributed to Cock, J. M..

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Comparison of the performance of sporophytes derived from narrow and wide genetic crosses between strains of the cultivated kelp Saccharina latissima

Seaweed mariculture allows sustainable production of large quantities of biomass for multiple downstream applications but the genotypes cultivated by this industry need to be improved to increase efficiency and cost-effectiveness. It is important that the genetic improvement of cultivated strains does not lead to the introduction of foreign genetic material into wild seaweed populations, which are already under threat from global heating. To circumvent this problem, efforts are being made to develop breeding approaches based on the use of locally-resourced genetic material. The aim of this study was to evaluate the potential effectiveness of this 'local' breeding strategy compared to a classical breeding approach based on wide genetic crosses. Analyses of growth rates and cell wall composition of F1 hybrids derived from either intra- or inter-population crosses between Saccharina latissima strains from two localities, southern Brittany, France and the Faroe Islands, did not identify any clear advantage of inter- compared to intra-population crosses. Breeding based on locally-resourced strains would therefore appear to be a valid approach for current strain selection programs. The study also established a large collection of gametophyte strains from multiple sites for future breeding programs and showed that these strains retained the capacity to become fertile after more than ten years in culture.

genetics↗

Life-cycle-related gene expression patterns in the brown algae

Brown algae are important primary constituents of marine coastal ecosystems, characterised by complex life cycles and various levels of complex multicellular development. However, the molecular processes that underlie development and life cycle progression in the brown algae remain poorly understood. In this study, pairwise comparisons of gametophyte and sporophyte transcriptomes across ten diverse brown algal species showed that the total number of genes exhibiting generation-biased or generation-specific expression in each species was correlated with the degree of dimorphism between life cycle generations. However, analysis of gene ontology terms assigned to the generation-biased/generation-specific genes indicated that each generation (i.e. the sporophyte and the gametophyte) also has characteristic broad life-cycle-related features that have been conserved during evolution. A more detailed analysis of Ectocarpus species 7, identified progressive transcriptome changes over its entire life cycle with a particularly marked change in transcriptome composition during the first day of sporophyte development, characterised by downregulation of flagellar and transcription factor genes and upregulation of a subset of translation genes. Comparison with a similar transcriptomic time series for the evolutionarily-distant (about 250 My) brown alga Dictyota dichotoma indicated considerable conservation of co-expressed gene modules between the two species, particularly for modules that were enriched in genes assigned to evolutionarily-conserved functional categories. This study therefore identified broad life-cycle- and development-related patterns of gene expression that are conserved across the brown algae.

developmental biology↗

Wild and farmed Saccharina latissima in Europe: genetic insights for sustainable cultivation, traceability and environmental challenges

Kelp cultivation is expanding rapidly worldwide, although the aquaculture of Saccharina latissima (sugar kelp) in Europe remains in its early stages. However, major concerns have emerged about the potential impact of selected cultivars of the species on native populations of S. latissima which are already vulnerable to stressors including climate change. To address these concerns and support sustainable cultivation, it is essential to characterise genetic diversity and structure of wild kelp populations to monitor potential farm-to-wild gene flow. In this study we used 21 microsatellite loci to characterise the genetic structure of 24 natural and 3 farmed populations of S. latissima along European coasts. Results confirmed strong genetic differentiation between the northern and southern coasts, refining the boundaries between these two clusters compared to previous studies. Within each cluster, a clear genetic substructure was detected, with population differentiation being far more pronounced in the southern cluster. Cultivated sporophytes exhibited pedigrees that were all traced back to the local parent populations. Bayesian model-based structure analysis, discriminant analysis of principal components and assignment tests revealed no significant genetic differentiation between the farms and their wild populations. This indicates that farmed populations and neighbouring populations share the same gene pool, reflecting current cultivation practices. These findings contribute to understanding risks of gene flow between wild and farmed populations and demonstrate that strain traceability is feasible. Additionally, the study highlights the challenge European seaweed farmers face in securing reliable seedling stock, especially in the context of global change.

genetics↗

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↗

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↗

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↗

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↗

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↗

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↗

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↗

Evolution of life cycles and reproductive traits: insights from 1 the brown algae

Brown algae are characterized by a remarkable diversity of life cycles, sexual systems, and reproductive modes, and these traits seem to be very labile across the whole group. This diversity makes them ideal models to test existing theories on the evolution of alternation between generations, and to examine correlations between life cycle and reproductive life history traits. In this study, we investigate the dynamics of trait evolution for four life-history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assign states to up to 70 species in a multi-gene phylogeny of brown algae, and use maximum likelihood and Bayesian analyses of correlated evolution, taking phylogeny into account, to test for correlations between life history traits and sexual systems, and to investigate the sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth may evolve because it allows the complementation of deleterious mutations, and that haploid sex determination is ancestral in relation to diploid sex determination. However, the idea that increased zygotic and diploid growth is associated with increased sexual dimorphism is not supported by our analysis. Finally, it appears that in the brown algae isogamous species evolved from anisogamous ancestors.

evolutionary biology↗

A key role for UV sex chromosomes in the regulation of parthenogenesis in the brown alga Ectocarpus

AO_SCPLOWBSTRACTC_SCPLOWAlthough evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of these shifts remain largely elusive. Here, we used classic quantitative trait analysis, combined with genomic and transcriptomic information to dissect the genetic basis of asexual, parthenogenetic reproduction in the brown alga Ectocarpus. We found that parthenogenesis is controlled by the sex locus, together with two additional autosomal loci, highlight the key role of the sex chromosome as a major regulator of asexual reproduction. Importantly, we identify several negative effects of parthenogenesis on male fitness, but also different fitness effects between parthenogenesis and life cycle generations, supporting the idea that parthenogenesis may be under both sexual selection and generation/ploidally-antagonistic selection. Overall, our data provide the first empirical illustration, to our knowledge, of a trade-off between the haploid and diploid stages of the life cycle, where distinct parthenogenesis alleles have opposing effects on sexual and asexual reproduction and may contribute to the maintenance of genetic variation. These types of fitness trade-offs have profound evolutionary implications in natural populations and may structure life history evolution in organisms with haploid-diploid life cycles.

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↗

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↗