Authors: Niklaus Zemp is a Post Doctoral Researcher and Alex Widmer is a Professor, both based at the Institute of Integrative Biology (IBZ), ETH Zurich, Zürich, Switzerland.
Competing interests: Niklaus Zemp and Alex Widmer are authors of the article discussed in this blog.
Host-pathogen interactions are of fundamental interest in evolutionary biology. While much is known about pathogen transmission dynamics and fitness effects on hosts, less is known about sex-specific responses to infection in those hosts that have separate sexes. A particularly intriguing situation occurs when pathogens induce sex reversals in their hosts, a phenomenon that can be associated with striking morphological changes in one or both host sexes. Pathogen-induced sex reversals may not only reveal whether the changes in gene expression following pathogen infection differ between males and females, but are also ideal systems to investigate the genetic basis of sexual dimorphism. Sexual dimorphism – defined as differences in morphology, behaviour and ecology between females and males – is found in most animal and plant species that have separate sexes, and genes that show sex-biased transcription may play an important role in the expression of that sexual dimorphism.
Parasite-induced sex reversals are relatively rare. However, a well-known example of a partial change from a female to a male flower involves the plant White Campion (Silene latifolia). This plant species has separate sexes (i.e. it is dioecious), chromosomal sex determination, and displays strong sexual dimorphism, most notably in reproductive traits such as flower size and number. Therefore S. latifolia has become a model system for studying the evolution of separate sexes and sex chromosomes. The anther smut fungus Microbotryum lychnidis-dioicae is a pathogen of White Campion and infection induces a partial sex reversal in female plants. Infected females produce male-specific reproductive structures which are essential for the successful transmission of fungal spores, because spores are produced in and released from the anthers (as shown in the issue image), where they may be picked up by pollinators. The S. latifolia – M. lychnidis-dioicae host-pathogen system is widely used in studies of host-pathogen co-evolution and disease transmission.
Sexual dimorphism and sex-biased gene expression
Our article, published in the October issue of PLOS Genetics, used RNA-seq to show that pathogen infection induced substantial and highly sex-specific changes across the transcriptome (the set of expressed genes). Surprisingly, these transcriptomic changes were not substantially stronger in infected females compared to males – even though most morphological changes underlying partial sex reversal are observed in female hosts. The observed sex-specific transcriptomic response was mainly caused by expression changes in genes with sex-biased and sex-specific expression and resulted in reduced sexual dimorphism of the host transcriptome. This reduced sexual dimorphism at the transcriptomic level was also associated with reduced sexual dimorphism in floral traits. This study therefore provides evidence for a direct link between sexual dimorphism and sex-biased gene expression.
Sex-specific responses to pathogen infection
Our study further revealed that host gender is of primary importance for the host’s response to pathogen infection – reminiscent of findings in animals and humans. Several high-value crop plants, including papaya, pistachio, persimmon, kiwifruit, and asparagus are dioecious, and the realization that these might also show sex-specific responses to pathogen infection may help improve future disease management when growing crops. More generally, our study suggests that ecological and evolutionary studies – as well as studies on human health – should explicitly consider separate sexes in their experimental design, because sex effects can be as strong – or even stronger – than the effects of experimental treatments.
Zemp N, Tavares R, Widmer A (2015) Fungal Infection Induces Sex-Specific Transcriptional Changes and Alters Sexual Dimorphism in the Dioecious Plant Silene latifolia. PLoS Genet 11(10): e1005536. doi:10.1371/journal.pgen.1005536