Sex-biased gene expression in the brown alga Fucus vesiculosus

The fucoid brown algae (Heterokontophyta, Phaeophyceae) are increasingly the focus of ecological genetics, biodiversity, biogeography and speciation research. The molecular genetics underlying mating system variation, where repeated dioecious - hermaphrodite switches during evolution are recognized, and the molecular evolution of sex-related genes are key questions currently hampered by a lack of genomic information. We therefore undertook a comparative analysis of male and female reproductive tissue transcriptomes against a vegetative background during natural reproductive cycles in Fucus vesiculosus.

Over 300 k reads were assembled and annotated against public protein databases including a brown alga. Compared with the vegetative tissue, photosynthetic and carbohydrate metabolism pathways were under-expressed, particularly in male tissue, while several pathways involved in genetic information processing and replication were over-expressed. Estimates of sex-biased gene (SBG) expression were higher for male (14% of annotated orthologues) than female tissue (9%) relative to the vegetative background. Mean expression levels and variance were also greater in male- than female-biased genes. Major female-biased genes were carbohydrate-modifying enzymes with likely roles in zygote cell wall biogenesis and/or modification. Male-biased genes reflected distinct sperm development and function, and orthologues for signal perception (a phototropin), transduction (several kinases), and putatively flagella-localized proteins (including candidate gamete-recognition proteins) were uniquely expressed in males. Overall, the results suggest constraint on female-biased genes (possible pleiotropy), and less constrained male-biased genes, mostly associated with sperm-specific functions.

Our results support the growing contention that males possess a large array of genes regulating male fitness, broadly supporting findings in evolutionarily distant heterogametic animal models. This work identifies an annotated set of F. vesiculosus gene products that potentially regulate sexual reproduction and may contribute to prezygotic isolation, one essential step towards developing tools for a functional understanding of species isolation and differentiation.