Genome evolution following transition to separate sexes

Lead Research Organisation: University of Oxford
Department Name: Plant Sciences

Abstract

Males and females of the same species are often quite different from each other (i.e. exhibit sexual dimorphism). In fact, in some species the differences between genders can be stronger than between individuals of different species or even genera. In humans these differences (e.g. in behaviour) are partly cultural, but to a large extent they are determined by genes. This is more surprising than it may seem as the two sexes share almost identical sets of genes and separate regulatory pathways have to evolve in order to build different male and female phenotypes from a shared pool of genes. How long does it take to develop sexual dimorphism when a species switches from a hermaphroditic state to separate sexes (dioecy)? What happens at the genome level when such transition occurs? These questions will be addressed in this project using a plant species that evolved dioecy and sex chromosomes only a few million years ago.
Unlike most plants, Silene latifolia has separate males and females and whether an individual develops as a male or a female depends on the presence or absence of the Y chromosome, not dissimilar to the situation in many animal species (e.g. in humans). However, unlike humans, where sex chromosomes are quite ancient (~200 million years), S. latifolia evolved sex chromosomes relatively recently, within the last ~10 million years, which provides an opportunity to study evolutionary processes at the most interesting early stages of their evolution. This project will use high-throughput DNA sequencing to 'read' the genome of S. latifolia and compare it to the genome of a closely related species Silene vulgaris that does not have separate sexes nor sex chromosomes. Comparing the two genomes it will be possible to study how the genome of S. latifolia evolved following transition to separate sexes in this species.

Technical Summary

Separate sexes (dioecy) and sex chromosomes evolved relatively recently (~10 million years ago) in a few species of mainly non-dioecious plant genus Silene. To study genome evolution following transition to dioecy we propose to sequence the genome of the dioecious Silene latifolia and compare it to the genome of the closely related Silene vulgaris (genome is being sequenced by the project partner in the USA) that is not dioecious and does not have sex chromosomes. Such a comparison between a species that recently evolved dioecy and sex chromosomes and its close relative without sex chromosomes has never been conducted before and will be very informative about the processes and events that shape the genome and sex chromosomes following transition to dioecy. Furthermore, we will study evolution of sexually dimorphic gene expression using RNAseq data from male and female S. latifolia plants. This will allow us to answer the following long-standing questions central to our understanding of genome evolution in general and sex chromosomes in particular:
1) Have sex chromosomes originated from a single pair of autosomes, or were they assembled from fragments of several different autosomes?
2) How quickly does lack of recombination on the newly formed Y-chromosome lead to genetic degeneration and whether degeneration occurs primarily via reduction of expression, amino acid replacements or a combination of both?
3) Has dosage compensation already started to evolve on young S. latifolia sex chromosomes?
4) What proportion of genes show sexually dimorphic expression?
5) Has sexually dimorphic gene regulation evolved primarily due to cis- or trans-acting mutations?
6) What is the contribution of sex chromosomes to sexually dimorphic gene regulation?
7) How has evolution of dioecy and sex chromosomes affected genome-wide recombination rates?

Planned Impact

Understanding the forces driving genome evolution is the prime goal in Evolutionary Genetics field and the effects of reproductive strategy of a species on its evolutionary trajectory is one of the hottest topics in Evolutionary Biology. This project combines both of these topics in a study of genome evolution following a dramatic shift in its reproductive strategy - a transition from a co-sexual state to separate sexes. Our project is the first to study genome-wide evolutionary trends following such a transition. Thus, our results are likely to have fairly wide-reaching implications in Evolutionary Biology and its impact will be ensured by publication of the results in the top scientific journals and magazines. Beyond biology, this project will also help to attract more attention to science and promote popularisation of biology. All sorts of questions related to sexual reproduction prove particularly attractive for the general public and they often enjoy extensive media coverage (e.g. 'Dr Tatiana' TV series). It will be relatively easy to explain the essence and interest of our work to the public in an accessible form as the question of why males and females are so different from each other is intuitively appealing and is of intrinsic interest to a non-specialist. We will take benefit of this with our outreach activities.

Publications

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Description Sex chromosomes have repeatedly evolved in animals and plants, but the evolutionary forces driving this process are not entirely understood. In this project we created a much needed and long overdue integrated high density genetic map and genome sequence for Silene latifolia, a species that is a de facto model system for plant sex chromosome evolution research. The analysis of this genome revealed significant genetic degeneration of a recently evolved plant Y-chromosome. Surprisingly, we find that Y-degeneration is already accommodated for by highly variable dosage compensation, despite these sex chromosomes originated only few million years ago. The results were recently published in PNAS (Papadopulos et al 2015 doi: 10.1073/pnas.1508454112). Furthermore, in collaboration with colleagues in Edinburgh and Tokyo we published a deletion map of the Silene latifolia Y-chromosome (Kazama et al 2016 doi: 10.1038/srep18917) that will greatly facilitate isolation of sex-determining genes in this species. Our results significantly advance our unerstanding of sex chromosome evolution in plants.
Exploitation Route We published the Silene latifolia genome sequence integrated with high density genetic map. Furthermore, we published a deletion map for Y-chromosome of this species. These genomic resources will be instrumental for the further research in this field.
Sectors Other

 
Description Evolution of dosage compensation on recently evolved sex chromosomes
Amount £363,625 (GBP)
Funding ID BB/P009808/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 06/2017 
End 06/2021
 
Description Deletion mapping of the Y-chromosome in Silene 
Organisation RIKEN
Department RIKEN-Nishina Center for Accelerator-Based Science
Country Japan 
Sector Public 
PI Contribution We conducted genomic sequencing of male and female individuals of Silene latifolia, identified Y-linked sequences and helped to designed a chip for analyses of Y-deletion mutants.
Collaborator Contribution They generated Y-deletion mutants and identified the approximate location of the deletions.
Impact Kazama Y, Ishii K, Aonuma W, Ikeda T, Kawamoto H, Koizumi A, Filatov DA, Chibalina M, Bergero R, Charlesworth D, Abe T, Kawano S. (2016) A new physical mapping approach refines the sex-determining gene positions on the Silene latifolia Y-chromosome. Sci Rep. 6:18917. doi: 10.1038/srep18917.
Start Year 2015