Abstract

BackgroundSexual life cycles in eukaryotes involve a cyclic alternation between haploid and diploid phases. While most animals possess a diploid life cycle, many 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 during each of the life cycle generations. Here, we analyze 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.ResultsWe show that the proportion of the transcriptome that is generation-specific is broadly 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 of a role for newly emerged, lineage-specific gene expression patterns 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 tend to exhibit changes in their patterns of expression.ConclusionOur analysis uncovers the characteristics, expression patterns, and evolution of generation-biased genes and underlines the selective forces that shape this previously underappreciated source of phenotypic diversity.

Highlights

  • Sexual life cycles in eukaryotes involve a cyclic alternation between haploid and diploid phases

  • And annotation of reference genomes for four brown algae The identification and analysis of generation-biased genes carried out in this study was based on an analysis of assembled genome sequences for four brown algae, including two high-quality, published genomes for Ectocarpus sp. and S. japonica [21, 25] and two draft genome sequences for S. lomentaria and M. pyrifera

  • Considering that the reference genomes recover 95.0% (Ectocarpus sp.) and 91.1% (S. japonica) of this BUSCO gene set, the BUSCO scores for S. lomentaria and M. pyrifera assemblies indicate that these draft genomes are of good quality

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Summary

Introduction

Sexual life cycles in eukaryotes involve a cyclic alternation between haploid and diploid phases. While most animals possess a diploid life cycle, many plants and algae alternate between multicellular haploid (gametophyte) and diploid (sporophyte) generations. As a consequence of sexual reproduction, the vast majority of eukaryotes have life cycles involving an alternation between haploid and diploid phases [1, 2]. Haploid mitosis may lead to asexual (clonal) reproduction, as in Chlamydomonas for example, or involve somatic growth and cellular differentiation as in Volvox. In these organisms, the zygote undergoes meiosis immediately after syngamy without undergoing any mitotic divisions. In diplontic life cycles, mitosis only occurs during the diploid phase, Lipinska et al Genome Biology (2019) 20:35 programs that are coordinated with, but not absolutely linked to, life cycle progression

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