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

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    eLife Assessment

    This manuscript presents an in-depth analysis of gene expression across multiple brown algal species with differing life histories, providing convincing evidence for the conservation of life cycle-specific gene expression. While largely descriptive, the study is an important step forward in understanding the core cellular processes that differ between life cycle phases, and its findings will be of broad interest to developmental and evolutionary biologists.

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Abstract

Abstract

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.

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  1. eLife Assessment

    This manuscript presents an in-depth analysis of gene expression across multiple brown algal species with differing life histories, providing convincing evidence for the conservation of life cycle-specific gene expression. While largely descriptive, the study is an important step forward in understanding the core cellular processes that differ between life cycle phases, and its findings will be of broad interest to developmental and evolutionary biologists.

  2. Reviewer #1 (Public review):

    Summary:

    The authors have examined gene expression between life cycle stages in a range of brown macroalgae to examine whether there are conserved aspects of biological features.

    Strengths:

    The manuscript incorporates large gene expression datasets from 10 different species and therefore enables a comprehensive assessment of the degree of conservation of different aspects of gene expression and underlying biology.

    The findings represent an important step forward in our understanding of the core aspects of cell biology that differ between life cycle phases and provide a substantial resource for further detailed studies in this area. Convincing evidence is provided for the conservation of life-cycle-specific gene expression between species, particularly in core housekeeping gene modules.

    Weaknesses:

    I found a few weaknesses in the methodology and experimental design. I think the manuscript could have been clearer when linking the findings to the biology of the brown algae.

  3. Reviewer #2 (Public review):

    Summary:

    The manuscript by Ratchinski et al presents a comprehensive analysis of developmental and life history gene expression patterns in brown algal species. The manuscript shows that the degree of generation bias or generation-specific gene expression correlates with the degree of dimorphism. It also reports conservation of life cycle features within generations and marked changes in gene expression patterns in Ectocarpus in the transition between gamete and early sporophyte. The manuscript also reports considerable conservation of gene expression modules between two representative species, particularly in genes associated with conserved functional characteristics.

    Strengths:

    The manuscript represents a considerable "tour de force" dataset and analytical effort. While the data presented is largely descriptive, it is likely to provide a very useful resource for studies of brown algal development and for comparative studies with other developmental and life cycle systems.

    Weaknesses:

    Notwithstanding the well-known issues associated with inferring function from transcriptomics-only studies, no major weaknesses were identified by this reviewer.