Abstract

Sexual dimorphism, including differences in morphology, behavior and physiology between females and males, is widespread in animals and plants and is shaped by gene expression differences between the sexes. Such expression differences may also underlie sex-specific responses of hosts to pathogen infections, most notably when pathogens induce partial sex reversal in infected hosts. The genetic changes associated with sex-specific responses to pathogen infections on the one hand, and sexual dimorphism on the other hand, remain poorly understood. The dioecious White Campion (Silene latifolia) displays sexual dimorphism in floral traits and infection with the smut fungus Micobrotryum lychnidis-dioicae induces a partial sex reversal in females. We find strong sex-specific responses to pathogen infection and reduced sexual dimorphism in infected S. latifolia. This provides a direct link between pathogen-mediated changes in sex-biased gene expression and altered sexual dimorphism in the host. Expression changes following infection affected mainly genes with male-biased expression in healthy plants. In females, these genes were up-regulated, leading to a masculinization of the transcriptome. In contrast, infection in males was associated with down-regulation of these genes, leading to a demasculinization of the transcriptome. To a lesser extent, genes with female-biased expression in healthy plants were also affected in opposite directions in the two sexes. These genes were overall down-regulated in females and up-regulated in males, causing, respectively, a defeminization in infected females and a feminization of the transcriptome in infected males. Our results reveal strong sex-specific responses to pathogen infection in a dioecious plant and provide a link between pathogen-induced changes in sex-biased gene expression and sexual dimorphism.

Highlights

  • Sexual dimorphism is widespread in animal and plant species with separate sexes females and males are often genetically very similar

  • Our study reveals that infection with the anther smut fungus alters the extent of sex-biased gene expression in S. latifolia in a sex-specific manner and highlights how transcriptomic changes in females and males shape sexual dimorphism

  • Our analysis revealed that gene expression changes upon infection of female and male S. latifolia with M. lychnidis-dioicae are dependent on infection per se and on host sex

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Summary

Introduction

Sexual dimorphism is widespread in animal and plant species with separate sexes females and males are often genetically very similar. Genes with sex-biased expression often accumulate on sex chromosomes and contribute importantly to the expression of sexually dimorphic traits [1,3], as for instance in Drosophila melanogaster [4] or mice [5]. Host responses to parasite and pathogen infections may be sex-specific and lead to different effects on female and male hosts [7,8]. Sex-specific transcriptional changes upon pathogen infection, remain poorly understood [9,10] and have not been reported to date in plants

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