Genetic mapping to mine the genome of the plant Silene latifolia for pseudoautosomal genes, and for future QTL analysis

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

Abstract

There is good evidence for trade-offs between male and female functions, and evolutionary biologists are interested in situations like this, when genes that survival or fertility in one circumstance have a cost in a different environment. Examples include adaptation of plants or animals to their local environment in a subdivided population (which often involves trade-offs, because it is not possible simultaneously to be highly adapted to many different environments), or adaptations of pathogens to their plant or animal hosts (leading to the evolution of restricted host ranges that a given pathogen can infect). These situations are thought to be important in maintaining genetic differences between individuals of the same species.

Sex differences (with one version of a gene conferring increased males survival or fertility, relative to a variant copy of the gene, and the opposite in females) are one interesting sub-set of these situations. In the shorthand of evolutionary biology, the term "fitness" is used to mean survival or fertility, and these sexual conflict situations are called "sexual antagonism". These differences have some properties in common with subdivided populations (it turns out to be helpful to regard the two sexes as different populations), so it is again likely that genetic differences may sometimes be maintained between the two sexes of the same species. Our project aims to test for such genetic differences.

Theoretical studies have modelled such situations have found that such sex differences in fitness, can indeed lead to situations where a gene ends up having two different variant types in a population of species, one type commonest in males, and the other in females. However, this is unlikely unless the gene is on the sex chromosome pair, and the male-beneficial is associated with the male-determining gene of the Y chromosome (while the other variant of the gene is associated with the X chromosome). In this kind of situation, models studied by theoreticians have shown that natural selection promotes a reduced rate of genetic recombination between the gene with the sexually antagonistic variants and the sex-determining gene. This is very interesting, because the loss of genetic recombination on Y chromosomes is a major topic of interest among biologists working to understand the evolution of sex chromosomes.
A favorable situation for detecting genes that behave in this way is therefore to study an organism whose sex chromosomes are in the process of evolving, but which still have a large region containing genes that undergo genetic recombination with the sex-determining region. Only one example of such genes is known: in some fish, genes on the sex chromosomes have a variant that makes males have bright coloration. This increases conspicuousness to predators and is therefore disadvantageous to females, but bright males are more attractive to females, and thus have higher fitness. However, this is just a special case, and it is necessary to discover whether this kind of genetic variation occurs more widely.

This project will take an important step towards studying the genetics underlying sexual antagonism in a plant, Silene latifolia, which is a good choice because it has been shown to be in the process of evolving a sex chromosome system. The study builds on previous studies in this species, and genetic and genomic resources that we and other labs have accumulated. We have a family suitable for genetic mapping, and have collected samples from a natural population, and the project will genetically map a large number of genes we have sequenced from the family, in order to find those that are in the recombining regions of the sex chromosomes. This genetic fine map will allow us to employ methods developed for crop plant and domesticated animal genetics that can identify individual sexually antagonistic genetic factors.

Planned Impact

The research develops a novel approach to genetic mapping in a species without a complete genome sequence, using the output of RNA-Seq sequencing. As such, it has the potential to interest plant breeding companies and research institutes, as well as academic researchers.
The general question within which the project is a part is the evolution of sex chromosomes, and specifically the evolution of loss of recombination between sex chromosome pairs. Although this is of interest to academic researchers, it is again also of interest to plant breeders whose crop plant has separate sexes (including papaya, strawberries, dates, grapes, and others). My genetic and evolutionary expertise has been useful to people working on all these crops, on several different occasions, and I am regularly asked for advice on mapping and understanding mapping results for sex chromosomes.

The evolutionary reasons for the existence of two sexes (and not more than 2) and the reasons why the sexes are sometimes, but not always, controlled by sex chromosomes, and the reasons why sex chromosomes evolve their well-known strange properties, are all interesting questions, not only to the academic and research community, but mush more widely. This has given me opportunities to give talks about plants to non-scientific audiences, and I have found that it is easy to raise interest in plants through such topics. I plan to continue to give talks that help to interest people in plant biology.

Publications

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Description We have genetically mapped many genes. The results have been used in a submitted manuscript that tests whether genes have been lost from the Y chromosome of the plant we study.

They have also been used to help a research group in the Czech Replublic, who are trying to identify the sex chromosomes of a related plant species.
Exploitation Route We can use the data for several other analyses. These are in progress.
Sectors Environment

 
Title Genetic map of Silene latifolia 
Description Large set of sequence variants useful as genetic markers for mapping 
Type Of Material Biological samples 
Year Produced 2013 
Provided To Others? Yes  
Impact Determination of the sex chromosome of other Silene species, and evidence that it differs from that of S. latifolia 
 
Title Sequences of Silene latifolia genes in GenBank 
Description Transcriptome sequences 
Type Of Material Database/Collection of data 
Year Produced 2008 
Provided To Others? Yes  
Impact Combined with transcriptome sequences obtained in other labs to estimate gene losses from the Y chromosome of Silene latifolia 
 
Description Evolution of sex-biased gene expression in a dioecious plant 
Organisation ETH Zurich
Country Switzerland 
Sector Academic/University 
PI Contribution Discussion to understand expectations and compare with results, including discussing analyses, writing much of the paper
Collaborator Contribution RNA sequencing and analyses of results, discussions, outline of paper, including preparing tables and figures
Impact Published paper: Zemp N, Tavares R, Muyle A, Charlesworth D, Marais G et al. (2016) Evolution of sex-biased gene expression in a dioecious plant. Nature Plants 2: 16168. doi: 10.1038/nplants.2016.168
Start Year 2013
 
Description Genetic mapping of sex-linked genes in a set of related plant species 
Organisation Academy of Sciences of the Czech Republic
Country Czech Republic 
Sector Learned Society 
PI Contribution Providing sequences for use as genetic markers, and their map location in one species, hosting a research student for training in genetic mapping using the markers in related species, and in genetic mapping. A paper has been submitted for publication.
Collaborator Contribution Sending a research student for training, generating families in related plants, PCR amplifications and genetic mapping. Co-authoring a paper, involving lengthy discussions via email, to understand the results.
Impact Evidence that the SEX locus is on a different chromosome in the 3 species so far studied
Start Year 2011