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Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima.

ABSTRACT: In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.

SUBMITTER: Pearson GA

PROVIDER: S-EPMC6742357 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima.

Pearson Gareth A GA Martins Neusa N Madeira Pedro P Serrão Ester A EA Bartsch Inka I

PloS one 20190912 9

In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the ...[more]

PMID: 31513596

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Project description:BACKGROUND:Kelps (Laminariales, Phaeophyceae) are brown macroalgae of utmost ecological, and increasingly economic, importance on temperate to polar rocky shores. Omics approaches in brown algae are still scarce and knowledge of their acclimation mechanisms to the changing conditions experienced in coastal environments can benefit from the application of RNA-sequencing. Despite evidence of ecotypic differentiation, transcriptomic responses from distinct geographical locations have, to our knowledge, never been studied in the sugar kelp Saccharina latissima so far. RESULTS:In this study we investigated gene expression responses using RNA-sequencing of S. latissima from environments with contrasting temperature and salinity conditions - Roscoff, in temperate eastern Atlantic, and Spitsbergen in the Arctic. Juvenile sporophytes derived from uniparental stock cultures from both locations were pre-cultivated at 8 °C and SA 30. Sporophytes acclimated to 0 °C, 8 °C and 15 °C were exposed to a low salinity treatment (SA 20) for 24 h. Hyposalinity had a greater impact at the transcriptomic level than the temperature alone, and its effects were modulated by temperature. Namely, photosynthesis and pigment synthesis were extensively repressed by low salinity at low temperatures. Although some responses were shared among sporophytes from the different sites, marked differences were revealed by principal component analysis, differential expression and GO enrichment. The interaction between low temperature and low salinity drove the largest changes in gene expression in sporophytes from Roscoff while specimens from Spitsbergen required more metabolic adjustment at higher temperatures. Moreover, genes related to cell wall adjustment were differentially expressed between Spitsbergen and Roscoff control samples. CONCLUSIONS:Our study reveals interactive effects of temperature and salinity on transcriptomic profiles in S. latissima. Moreover, our data suggest that under identical culture conditions sporophytes from different locations diverge in their transcriptomic responses. This is probably connected to variations in temperature and salinity in their respective environment of origin. The current transcriptomic results support the plastic response pattern in sugar kelp which is a species with several reported ecotypes. Our data provide the baseline for a better understanding of the underlying processes of physiological plasticity and may help in the future to identify strains adapted to specific environments and its genetic control.

Dataset Information

Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima.

Publications

Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima.

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