The Pseudoautosomal Regions of the U/V Sex Chromosomes of the Brown Alga Ectocarpus Exhibit Unusual Features

International audienceThe recombining regions of sex chromosomes (pseudoautosomal regions, PARs) are predicted to exhibit unusual features due to their being genetically linked to the nonrecombining, sex-determining region. This phenomenon is expected to occur in both diploid (XY, ZW) and haploid (UV) sexual systems, with slightly different consequences for UV sexual systems because of the absence of masking during the haploid phase (when sex is expressed) and because there is no homozygous sex in these systems. Despite a considerable amount of theoretical work on PAR genetics and evolution, these genomic regions have remained poorly characterized empirically. We show here that although the PARs of the U/V sex chromosomes of the brown alga Ectocarpus recombine at a similar rate to autosomal regions of the genome, they exhibit many genomic features typical of nonrecombining regions. The PARs were enriched in clusters of genes that are preferentially, and often exclusively, expressed during the sporophyte generation of the life cycle, and many of these genes appear to have evolved since the Ectocarpales diverged from other brown algal lineages. A modeling-based approach was used to investigate possible evolutionary mechanisms underlying this enrichment in sporophyte-biased genes. Our results are consistent with the evolution of the PAR in haploid systems being influenced by differential selection pressures in males and females acting on alleles that are advantageous during the sporophyte generation of the life cycle

Repeated co-option of HMG-box genes for sex determination in brown algae and animals

In many eukaryotes, genetic sex determination is not governed by XX/XY or ZW/ZZ systems but by a specialized region on the poorly studied U (female) or V (male) sex chromosomes. Previous studies have hinted at the existence of a dominant male-sex factor on the V chromosome in brown algae, a group of multicellular eukaryotes distantly related to animals and plants. The nature of this factor has remained elusive. Here, we demonstrate that an HMG-box gene acts as the male-determining factor in brown algae, mirroring the role HMG-box genes play in sex determination in animals. Over a billion-year evolutionary timeline, these lineages have independently co-opted the HMG box for male determination, representing a paradigm for evolution’s ability to recurrently use the same genetic “toolkit” to accomplish similar tasks.</p

Uncovering the genetic basis for early isogamete differentiation: a case study of Ectocarpus siliculosus

Background: The phenomenon of sexual reproduction characterizes nearly all eukaryotes, with anisogamy being the most prevalent form of gamete discrimination. Since dimorphic gametes most likely descend from equal-sized specialized germ cells, identifying the genetic bases of the early functional diversification in isogametes can provide better understanding of the evolution of sexual dimorphism. However, despite the potential importance to the evolutionary biology field, no comprehensive survey of the transcriptome profiling in isomorphic gametes has been reported hitherto. Results: Gamete differentiation on the genomic level was investigated using Ectocarpus siliculosus, a model organism for brown algal lineage which displays an isogamous sexual reproduction cycle. Transcriptome libraries of male and female gametes were generated using Next Generation Sequencing technology (SOLiD) and analyzed to identify differentially regulated genes and pathways with potential roles in fertilization and gamete specialization. Gamete transcriptomes showed a high level of complexity with a large portion of gender specific gene expression. Our results indicate that over 4,000 of expressed genes are differentially regulated between male and female, including sequences related to cell movement, carbohydrate and lipid metabolism, signaling, transport and RNA processing. Conclusions: This first comprehensive transcriptomic study of protist isogametes describes considerable adaptation to distinct sexual roles, suggesting that functional anisogamy precedes morphological differentiation. Several sex-biased genes and pathways with a putative role in reproduction were identified, providing the basis for more detailed investigations of the mechanisms underlying evolution of mating types and sexual dimorphism

Genetic and cellular characterization of parthenogenesis in the brown alga Ectocarpus

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Development of PCR-Based Markers to Determine the Sex of Kelps.

Sex discriminating genetic markers are commonly used to facilitate breeding programs in economically and ecologically important animal and plant species. However, despite their considerable economic and ecological value, the development of sex markers for kelp species has been very limited. In this study, we used the recently described sequence of the sex determining region (SDR) of the brown algal model Ectocarpus to develop novel DNA-based sex-markers for three commercially relevant kelps: Laminaria digitata, Undaria pinnatifida and Macrocystis pyrifera. Markers were designed within nine protein coding genes of Ectocarpus male and female (U/V) sex chromosomes and tested on gametophytes of the three kelp species. Seven primer pairs corresponding to three loci in the Ectocarpus SDR amplified sex-specific bands in the three kelp species, yielding at least one male and one female marker for each species. Our work has generated the first male sex-specific markers for L. digitata and U. pinnatifida, as well as the first sex markers developed for the genus Macrocystis. The markers and methodology presented here will not only facilitate seaweed breeding programs but also represent useful tools for population and demography studies and provide a means to investigate the evolution of sex determination across this largely understudied eukaryotic group

Rapid Evolution of microRNA Loci in the Brown Algae

International audienceStringent searches for microRNAs (miRNAs) have so far only identified these molecules in animals, land plants, chlorophyte green algae, slime molds and brown algae. The identification of miRNAs in brown algae was based on the analysis of a single species, the filamentous brown alga Ectocarpus sp. Here, we have used deep sequencing of small RNAs and a recently published genome sequence to identify miRNAs in a second brown alga, the kelp Saccharina japonica. S. japonica possesses a large number of miRNAs (117) and these miRNAs are highly diverse, falling into 98 different families. Surprisingly, none of the S. japonica miRNAs share significant sequence similarity with the Ectocarpus sp. miRNAs. However, the miRNA repertoires of the two species share a number of structural and genomic features indicating that they were generated by similar evolutionary processes and therefore probably evolved within the context of a common, ancestral miRNA system. This lack of sequence similarity suggests that miRNAs evolve rapidly in the brown algae (the two species are separated by ~95 Myr of evolution). The sets of predicted targets of miRNAs in the two species were also very different suggesting that the divergence of the miRNAs may have had significant consequences for miRNA function

A) Electrophoresis pattern of sex marker products amplified in six diploid sporophytes of <i>L</i>. <i>digitata</i>. M: male marker (M_68_16_1); F: female marker (M_68_58_3). B) Electrophoresis pattern of sex marker products amplified in a diploid sporophyte and female partheno-sporophyte of <i>Undaria pinnatifida</i>. M: male marker (M_68_16_2), F: female marker (M_285_20_2), PAR gene (M_285_26_1); SP: sporophyte, pSP: partheno-sporophyte.

<p>A) Electrophoresis pattern of sex marker products amplified in six diploid sporophytes of <i>L</i>. <i>digitata</i>. M: male marker (M_68_16_1); F: female marker (M_68_58_3). B) Electrophoresis pattern of sex marker products amplified in a diploid sporophyte and female partheno-sporophyte of <i>Undaria pinnatifida</i>. M: male marker (M_68_16_2), F: female marker (M_285_20_2), PAR gene (M_285_26_1); SP: sporophyte, pSP: partheno-sporophyte.</p