Comparative genomics, temporal dynamics and degeneration of mating-type chromosomes in anther-smut fungi

From animals to plants and fungi, the temporal dynamics of degeneration in regions of suppressed recombination is an unresolved and fundamental question with relevance to further mutation accumulation, the emergence of sex-linked disorders, and impacts on individual fitness and adaptive potential. While multiple conceptual models are consistent with observed mutational decay, empirical tests are lacking due to the intractability of species with large genomes and the influences of multiple factors thought to drive the (sex) chromosome degeneration.

One of the anther-smut fungi we studied: Microbotryum violaceum-Silene virginica. The smut fungi infect the anthers of its host Silene virginica.

In the project, we are using the pathogenic fungi (Microbotryum, basidiomycetes) as the study system for degeneration in dimorphic mating-type chromosomes. We aim to reconstruct evolutionary histories for suppressed recombination, quantify the tempo of accumulated mutational load and gene loss, and determine the transitions from ancestral autosome to sex-chromosome-like structures. Below is the genome-level gene synteny between two Microbotryum fungi species.

Synteny between genomes of Microbotryum intermedium (in orange) and M. salviae (in purple). HD mating-type chromosome is denoted in in grey and PR mating type chromosome in green; yellow stripe denotes the centromere repeats region.

Evolutionary genomics of homomorphic sex chromosomes

1) in the common frog Rana temporaria

Unlike mammals, birds, and flies, sex chromosomes in >96% of frog species are not degenerated and homomorphic, partly because of frequent turnovers in sex chromosomes and sex reversals. In addition, sex-chromosome evolution is expected to lead to major changes in gene expression due to sex-specific patterns of selection and inheritance, resulting in X chromosomes often enriched in female-biased genes (feminization), and Z chromosomes in male-biased genes (masculinization). Such patterns have been documented in many species with highly degenerated sex chromosomes. However, we do not know how quickly sexualisation of gene expression and transcriptional degeneration evolve after sex-chromosome formation, and little is known about how sex-biased gene expression varies throughout development.

Project of developmental dynamics of sex-biased gene expression in the common frog, here pictures of rearing tadpoles of Rana temporaria.

The common frog, Rana temporaria, provides an ideal model to investigate these questions, as it possesses homomorphic sex chromosomes and thus represents an early stage of sex-chromosome evolution, distributed widely throughout Europe and has a variable sex-determination system ranging from genetic to non-genetic. In the projects, in combination of fieldwork, molecular, genetic, NGS sequencing and bioinformatic approaches, we use the common brown frogs to investigate various questions below:

  1. Evolution and dynamics of sex-biased gene expression in three populations with various Y-chromosome differentiation levels

Gene expression ratio of Log2(male/female) throughout development stages and adult tissues (Rana temporaria)

2. The sex determination mechanism of the common frog

3. Differentiation and signature of sexual antagonistic selection along X/Y chromosomes

4. Phytogeography and evolutionary origin of Y chromosomes in the common frog

5. Patterns of sex chromosome turnover in the true frog Ranidae 

2) in the annual plant Mercurialis annua

Polyploidy has played a major role in the diversification of land plants, likely because of the expansion in the ecological niche of polyploid populations, and because reproductive isolation is immediately established between a new polyploid population and its diploid progenitor species. It is now well established that most polyploid species are polyphyletic, with multiple independent origins, and that polyploid genomes may undergo rapid change after their duplication and hybridization associated with their origin.

Hexaploid monoecious female-like (a), male-like phenotype (b), and hexaploid male plants of Mercurialis annua. Photo credit @Xinji Li.

In the M. annua species complex, diploid populations are dioecious, but hexaploid populations are either monoecious or androdioecious. Diploid and polyploid males hold their flowers in erect ‘pedunculate’ inflorescences above the plant, whereas diploid females and hexaploid monoecious individuals (which are effectively modified pollen-producing females) typically hold both their male and female flowers in sub-sessile inflorescence in the leaf axils. However, we recently documented the existence in some populations of hexaploid monoecious individuals of M. annua that, like males, hold their male flowers on erect peduncles rather than in the sub-sessile axillary inflorescences that are more typical for hexaploid M. annua. One might expect such a superior strategy for pollen dispersal to quickly spread throughout the species range, particularly as it does not appear very costly in terms of other fitness components. Using the two broadly sympatric hexaploid lineages of the wind-pollinated annual plant Mercurialis annua, in combination with common garden experiments, ploidy assessment, reciprocal crosses and phylogenetic construction, and RADseq approaches, we aim to answer the following questions.

Sampling locations for both P– and P+ monoecious hexaploid populations of M. annua along the east coast of Iberian Peninsula.
  1. Reproductive isolation between divergent hexaploid populations of Mercurialis annuawith contrasting inflorescence architecture: the role of multiple origins of polyploidy for functional diversification
  2. Sex-linked markers across the annual plant Mercurialis annua species complex
  3. The evolutionary origin and population genetic differentiation of male-like inflorescence in M. annua

Evolutionary genetics of sex determination and Wolbachia induced asexuality in the parasitoid wasp Asobara (Thesis here)

During my PhD, I was interested in evolution and genetics of sex determination mechanisms in haplodiploid wasps. Hence the title of my PhD thesis below.

PhD thesis cover, illustrated by Loren Bes, designed by W-J Ma.

1) Using experimental crosses and simulation-modelling approaches, I tested for the so called Complementary Sex Determination (CSD) mechanisms in the four parasitoid Asobara wasp (PLoS ONE). We could excluded up to ten CSD loci and argued that it is unlikely they would evolve CSD system.

Simulation and empirical data of sex ratio on complementary sex determination loci in various Asobara wasp species.

2) For the asexual Asobara japonica, using introgression experiment and qPCR to detect Wolbachia density, I discovered a novel role of Wolbachia (bacteria) titre, involving in two separate steps of diploidisation and feminisation following fertilisation (BMC Evolutionary Biology).

Two step model of how Wolbachia induced female reproduction in Asobara japonica.

3) In order to understand the genetic architecture of the decayed sexual traits, we performed four generations of introgression experiments between sexual and asexual strains and tested various sexual traits. We revealed the genetic architecture of decayed female sexual traits are likely a few loci with major effects (Heredity).

4) Furthermore, I developed genome-wide SNP markers to construct a linkage map for a QTL study on decayed sexual traits.

5) I also wrote invited review articles regarding endosymbiont manipulation of host reproduction and sex determinations (Sexual Development, 2014; Journal of Evolutionary Biology, 2017).