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

PLoS One. 2019 Sep 12;14(9):e0219723. doi: 10.1371/journal.pone.0219723. eCollection 2019.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Computational Biology / methods
  • Gametogenesis / genetics*
  • Gene Expression Profiling*
  • Haploidy*
  • High-Throughput Nucleotide Sequencing
  • Molecular Sequence Annotation
  • Phaeophyceae / cytology
  • Phaeophyceae / genetics*
  • Phaeophyceae / metabolism
  • Sugars / metabolism
  • Transcriptome*

Substances

  • Sugars

Grants and funding

This work was supported by the Portuguese Science Foundation (FCT; https://www.fct.pt/index.phtml.pt) programs UID/Multi/04326/2019, GENEKELP-PTDC/MAR-EST/6053/2014 and MARFOR-Biodiversa/0004/2015 (https://www.biodiversa.org/1019) to ES and GAP. The BiodivERsA project MARFOR includes the funding agencies Formas, Naturvardsverket, ANR, FCT, MEC, FRCT, DFG. Author NM is supported by a grant from FCT (SFRH/BPD/122567/2016) and ES by a Pew Marine Fellowship (https://www.pewtrusts.org/en/projects/marine-fellows). This work was additionally supported by a STSM Grant from the COST Action “Phycomorph” FA1406 (https://www.phycomorph.org) to NM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.