Genetic and epigenetic mechanisms involved in allopolyploid speciation in Senecio
Lead Research Organisation:
University of Bristol
Department Name: Biological Sciences
Abstract
Hybrid speciation is one of the most important mechanisms of speciation in plants. Evolution is generally considered to be a slow process, but in plants, hybridization and changes in chromosome number (polyploidy) can generate new species (reproductively isolated from their parental species) in just a few generations. Genetic studies indicate that hybridization between two related species can lead to large-scale alterations in the hybrid genome, a phenomenon described as 'genome shock'. Such changes include rearrangement of chromosomes and alterations in levels of gene expression. We have been studying changes in the expression of flower genes arising as a consequence of hybrid speciation in the genus Senecio (ragworts). Senecio squalidus, commonly known as Oxford ragwort, because it was introduced into the UK (roughly 300 years ago) via the Oxford Botanic Garden, is a hybrid of two Senecio species native to Sicily, S. aethnensis and S. chrysanthemifolius, and since its escape from the Oxford Botanic Garden about 150 years ago, it has hybridized extensively with native groundsel, S. vulgaris, to produce three new hybrid species. One of these newly formed species, S. cambrensis (Welsh ragwort) formed from a sterile intermediate hybrid S. x baxteri by a doubling up of its chromosomes. S. x baxteri is sterile because it contains an odd number of chromosomes that cannot pair up properly during cell division. However a chance doubling up of these chromosomes in S. x baxteri during a faulty cell division led to the emergence of the fertile polyploid species S. cambrensis, which has become successfully established in Wales. Interestingly, these new hybrid Senecio species have all formed within the last 70 years. Our previous research has shown that following hybridization there is a dramatic change in the pattern of gene expression between the initial hybrid, S. baxteri, and its parents, S. vulgaris and S. squalidus, as well as between S. x baxteri and the fertile polyploid hybrid S. cambrensis (from which it differs only in chromosome number). Further experiments suggest that this change in gene expression can occur in a single generation. This suggests a dramatic 'shock' to the parental genomes, as a result of them coming together within a new hybrid, a phenomenon described as 'genome shock' by the geneticist Barbara McClintock. We are therefore interested in finding out how the different copies of these genes inherited from the parents are behaving in the hybrids and what factors may be causing the differences we observe. To do this we have selected small groups of genes with interesting patterns of expression and possible roles in flower development. These are: 1. genes affected by hybridisation, 2. genes affected by change in chromosome number (polyploidy), 3. genes that may regulate changes in flower structure and physiology between hybrids and parents, and 3. genes that appear to be inherited just from the mother plant, S. vulgaris (maternally inherited genes). To study the regulation of these subsets of genes we will use a technique that allows us to determine which parental gene copies are active within the hybrids. In theory, one parental gene copy will be switched off (gene silencing) allowing preferential expression of the other. This has been shown in studies of other polyploid hybrids, but has not yet been investigated in intermediate hybrids such as S. x baxteri. Secondly, we will use a variety of techniques to determine the mechanisms by which gene expression is altered in the hybrids, primarily studying DNA methylation, which has long been known to be part of the gene silencing process. Finally, we will look at the site of expression of genes we have identified as potentially involved in changes to flower form and physiology associated with the hybrid speciation process.
Publications
Abbott R
(2008)
Recent hybrid origin and invasion of the British Isles by a self-incompatible species, Oxford ragwort (Senecio squalidus L., Asteraceae)
in Biological Invasions
Allen AM
(2010)
Characterisation of sunflower-21 (SF21) genes expressed in pollen and pistil of Senecio squalidus (Asteraceae) and their relationship with other members of the SF21 gene family.
in Sexual plant reproduction
Brennan AC
(2010)
Expression and inheritance of sporophytic self-incompatibility in synthetic allohexaploid Senecio cambrensis (Asteraceae).
in The New phytologist
Hegarty M
(2007)
Polyploidy: doubling up for evolutionary success.
in Current biology : CB
Hegarty M
(2013)
Lessons from natural and artificial polyploids in higher plants.
in Cytogenetic and genome research
Hegarty MJ
(2008)
Genomic clues to the evolutionary success of polyploid plants.
in Current biology : CB
Hegarty MJ
(2009)
The complex nature of allopolyploid plant genomes.
in Heredity
Hegarty MJ
(2011)
Nonadditive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae).
in Molecular ecology
Hegarty MJ
(2008)
Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Hegarty MJ
(2009)
Extreme changes to gene expression associated with homoploid hybrid speciation.
in Molecular ecology
Description | Hybrid speciation is one of the most important mechanisms of speciation in plants. Evolution is generally considered to be a slow process, but in plants, hybridization and changes in chromosome number (polyploidy) can generate new species in just a few generations. Genetic studies indicate that hybridization between two related species can lead to large-scale alterations in the hybrid genome, a phenomenon described as 'genome shock'. Such changes include rearrangement of chromosomes and alterations in levels of gene expression. We have been studying changes in the expression of flower genes arising as a consequence of hybrid speciation in the genus Senecio (ragworts). Senecio squalidus is a hybrid of two Senecio species native to Sicily, S. aethnensis and S. chrysanthemifolius, since its escape from the Oxford Botanic Garden about 150 years ago, it has hybridized extensively with native S. vulgaris, to produce three new hybrid species. One of these, S. cambrensis (Welsh ragwort) formed from a sterile intermediate hybrid S. x baxteri by a doubling up of its chromosomes. S. x baxteri is sterile because it contains an odd number of chromosomes. However a chance doubling up of these chromosomes in S. x baxteri during a faulty cell division led to the emergence of the fertile polyploid species S. cambrensis, which has become successfully established in Wales. Interestingly, these new hybrid Senecio species have all formed within the last 70 years. Our previous research has shown that following hybridization there is a dramatic change in the pattern of gene expression between the initial hybrid, S. baxteri, and its parents, S. vulgaris and S. squalidus, as well as between S. x baxteri and the fertile polyploid hybrid S. cambrensis (from which it differs only in chromosome number). Further experiments suggest that this change in gene expression can occur in a single generation. This suggests a dramatic 'shock' to the parental genomes, as a result of them coming together within a new hybrid, a phenomenon described as 'genome shock' by Barbara McClintock. We were therefore interested in finding out how the different copies of these genes inherited from the parents are behaving in the hybrids and what factors may be causing these differences. To do this we selected small groups of genes with interesting patterns of expression and possible roles in flower development. These are: 1. genes affected by hybridisation, 2. genes affected by change in chromosome number (polyploidy), and 3. genes that may regulate changes in flower structure and physiology between hybrids and parents. To study the regulation of these subsets of genes we developed an SSCP technique to identify silencing of parental specific alleles, as well as patterns of inheritance and mutation during hybridisation and genome doubling. This is the first time parental specific allele silencing has been investigated in intermediate hybrids such as S. x baxteri. Secondly, we used MSAP to study global patterns of DNA methylation, which has long been known to be part of the gene silencing process. This revealed small but significant levels of nonadditive methylation patterns both triploid and allohexaploid hybrids, at levels comparable to the nonadditive expression observed in our microarray experiments, while genome duplication appears to reduce the level of nonadditivity in the allohexaploids. Global changes in transposon activity were also investigated using a combination of southern blots and RT-PCR, and showed that nonadditive changes in genome size during hybridisation are largely due to changes in retrotransposon copy number. Finally, we looked at the site of expression of genes we previously identified as potentially involved in changes to flower form and physiology associated with the hybrid speciation process using in situ hybridisation. Particularly interesting patterns of expression were observed for 3 genes with putative roles in SI. |
Exploitation Route | The story of Oxford ragwort's invasion of the UK via railway lines during the industrial revolution and its subsequent hybridization with native groundsel to generate three new Senecio taxa in the UK is of pernnial interest to naturalists and anyone with an interest in the British flora. SJH has been invited to talk about the broad aspects of this research many times by local naturalist trusts and groups, e.g. Bristol Naturalists Trust, Avon and Somerset Wildlife Trust, Friends of the University of Bristol Botanic Garden. This work is primarily of interest to other academics, particularly those working on genetics of the Asteraceae, genetics of hybridisation and genome evolution. |
Sectors | Environment |
URL | http://openwetware.org/wiki/Senecio_Research_Network |
Description | Impact has been purely scientific. |
First Year Of Impact | 2008 |
Sector | Environment |
Description | Use of NBAF Sheffield genotyping facility |
Amount | £8,000 (GBP) |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start |
Description | Epigenetic basis of speciation in African lake cichlid fishes |
Organisation | University of Bristol |
Department | School of Biological Sciences |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | I am co-I on this EU Marie Currie Fellowship Award |
Collaborator Contribution | My collaborators are Dr Martin Genner (PI) and Tom Batstone (Bioinformatician). Both discuss and advise on my Senecio work and Tom continues to contribute to bioinformatic analyses of the Senecio genome |
Impact | Too early for outcomes |
Start Year | 2015 |