Does a functional interaction between X chromosome and autosome exist in vivo to regulate male fertility? If yes, how?

Some related species may look similar but belong to different species due mainly to their inability to exchange genetic materials, a phenomenon known as hybrid incompatibility. One common hybrid incompatibility is caused by genetic or genomic conflicts between parental alleles after fusion of their gametes, which is referred to as postzygotic hybrid incompatibility (PHI). Although PHI is the central question of evolutionary biology, the mechanistic understanding of PHI is rather limited. Isolation of PHI loci or genes is crucial for understanding its mechanism.

The recent discovery of the nematode, C. nigoni, as a sister species of C. briggsae, had opened the possibility of genetic and molecular characterization of PHI for the first time using nematode species. To facilitate the identification of PHI loci, we previously generated nearly 100 green fluorescent protein (GFP) markers that were randomly inserted into different C. briggsae chromosomes. By backcrossing the individual GFP markers with C. nigoni, we produced around 110 introgression lines that each carried a GFP-linked C. briggsae genomic fragments in an otherwise C. nigoni background, which manifests various PHI phenotypes. One of the most common PHIs is hybrid male sterility.

Our functional genomic studies of hybrid sterile males suggest a long-range functional interaction between the sex chromosome X and autosome, which is essential for hybrid male fertility. However, the solid evidence of such an interaction is still lacking. If such an interaction is indeed present, how many are there and how do they regulate hybrid male sterility? The identification of such interacting loci and determination of their molecular identities is crucial for answering these questions. However, identification of these interacting loci/genes would be technically challenging.

We have recently found that in contrast to the hybrid male sterility between wild-type C. briggsae male and C. nigoni female, the hybrid males are fertile when their X chromosomes are partially derived from a combination of C. briggsae and C. nigoni X chromosomes. This provides a good opportunity for identifying the interacting loci between the X and autosome by backcrossing the fertile males with wild-type C. nigoni females. Our preliminary backcrossing effort supported the presence of such interacting loci between the X chromosome and autosome.

This proposal aims to take advantage of the rescued hybrid F1 male sterility to systematically identify X-autosome interaction loci/genes that are responsible for the hybrid male fertility. The proposed study would provide important insights into whether and how the X and autosome interaction is required for the male’s fertility.