Assessing the impact of plant mating system and ploidy on adaptation to parasitism in changing environments

Lead Research Organisation: University of Warwick
Department Name: Warwick HRI


Host-pathogen interactions are dynamic systems that are influenced by factors that act on both interacting partners, either separately, or in response to one another. For example, changes in temperature or habitats can alter distributions of hosts and pathogens and thus bring new combinations of organisms into contact but can also change the virulence of pathogens or the responses of hosts. Many studies have focused on how direct interactions are altered by respective changes in immune recognition and pathogen avoidance systems but fewer have focused on how factors indirectly related to the interaction might affect the abilities of hosts and pathogens to coexist. A wide range of economically important plants vary in either mating system (inbreeding or outcrossing) or in ploidy level (many crops are polyploids, with more than two sets of chromosomes) from wild relatives but it has not been well studied how such changes affect pathogen response systems. Recent research on the genetic control of host-pathogen interactions in the economically important Brassicacaceae (which includes broccoli, rapeseed, and turnips) has tended to focus on the highly selfing model plant, Arabidopsis thaliana. While much has been learned from this, the lack of naturally occurring variation in genetic diversity, heterozygosity, mating system and ploidy level limits the potential to explore the effects of variation in host factors. A close relative, Arabidopsis lyrata, has sufficient variation across its range to investigate the effects of mating system and ploidy variation within a single species with a broad geographic distribution. We propose to investigate variation in response of A. lyrata to an important pathogen of both wild and cultivated Brassicaceae, oomycete pathogens in the genus Albugo, which cause a disease known as white blister rust. We propose to use a combination of laboratory and polytunnel field experiments to investigate how populations of A. lyrata sampled from different geographic regions and that differ in mating system or ploidy level vary in their responses to experimental infection with Albugo. We also plan to screen wild populations for natural variation in infection with Albugo and investigate the genetic basis for differences in responses using the latest in genomic sequencing technologies. We hope to establish whether: 1) resistance to these pathogens is reduced with inbreeding (which reduces genetic diversity and heterozgyosity within populations and could limit variation in pathogen response systems) or whether local adaptation to particular pathogens might instead make outcrossing less desirable (because recombining genomes from unrelated individuals could disrupt combinations of genes that allow effective pathogen response); 2) the duplication of pathogen response systems that would be expected to accompany whole genome duplication (polyploidy) confers an advantage (in terms of the diversity of pathogens that can be recognized or increased production of products necessary to combat pathogens), or whether the normal balance in pathogen response systems present in the diploid state might be disrupted by genome duplication; 3) whether the strength of host response systems vary along a latitudinal gradient (where temperature variation, length of growing season, rainfall and habitat types are likely to vary). A. lyrata tends to grow in low competition environments so we will also question whether exposure to pathogens hosted by other species, such as A. thaliana, might be involved in limiting their distributions and whether this varies in relation to prior exposure to the Albugo pathogen. Finally, we hope to uncover the genes responsible for regulating interactions between A. lyrata and Albugo and establish whether the same resistance mechanisms operate in host populations sampled from widely separated geographic regions and whether responses are similar to different strains of the pathogen.
Description From the pathology work at the University of Warwick:
• A seedling test of A. lyrata diversity for resistance to Albugo indicated that North American (NA) populations of the host lack variation in major resistance to survive infection by the pathotype of Albugo candida pathotype from Capsella bursa-pastoris (which provides an abundant reservoir of inoculum from spring-autumn throughout the UK), whereas European populations appear to be uniformly resistant to the reproductive and dispersal phase (white rust) of this Albugo pathotype.
• In a polytunnel experiment in 2013, F1 hybrids between a NA selfing individual and several resistant European individuals were all susceptible to white rust when exposed to inoculum under epidemic conditions, suggesting no selective advantage of heterozygosity.
• Most interestingly, an attempt to establish disease-free nurseries from seed of a European A. lyrata diversity collection in Warwickshire (outside the current species range) was successful at one site, but failed at another when white rust erupted on floral stems of one plant and spread prolifically in floral tissue across all accessions. The inoculum source was from either latent seed-borne (endophytic) infection or by inoculum derived from a nearby Capsella population. Five Icelandic accessions became systemically diseased and the plants were unable to re-generate summer vegetative growth from rhizomes, whereas accessions from elsewhere (Scotland, Norway and Sweden) had vigorous re-growth without further disease spread. Thus, outbreaks of white rust can disrupt sexual reproduction of A. lyrata and is potentially a major factor limiting southward expansion of the species in the UK.

From the population genetics work at Glasgow University:
• Analysis of RAD sequences demonstrated genome-wide loss of heterozygosity and genetic diversity in selfing compared to outcrossing populations of NA A. lyrata. However, a common garden experiment to assess the relative ability of selfing and outcrossing populations from eastern North America to survive and reproduce in a novel environment did not reveal a cost to this lost diversity.
• Seedlings of both NA and European accessions were transplanted into an outdoor experimental garden in Scotland. The NA seedlings showed a remarkable ability to survive, attract pollinators and set seed. They showed similar flowering time as in their native habitat (irrespective of mating system), whereas European populations (which exhibited higher genetic diversity than NA) showed very low levels of survival and most survivors failed to set seed.

Together, these results question the dogma that loss of genetic diversity will hinder adaptation to novel environments. Follow up research is recommended, to explore whether hybridisation and/or polyploidy, which are both expected to increase levels of genetic diversity, provide an advantage in terms of adaptation to varying environments.
Exploitation Route We submitted an follow-up proposal (Glasgow-Warwick-Sterling) to NERC to investigate whether hybrid and/or polyploid status of a plant species influences adaptive potential in changing environments. This was unsuccessful.
Sectors Agriculture, Food and Drink,Education

Description One paper describing host molecular diversity of specific host R-genes was published in BMC Evolutionary Biol, and a second manuscript on pathogen-mediated selection using is pending review in BMC Genomics. The importance of floral infection for this host-parasite interaction has been instructive in re-thinking the life history and environmental reservoir of pathogen diversity, and in shaping a strategy for genetic improvement of white rust in oilseed mustard for small-holder farmers in India and China, and for English mustard farmers in the UK. White rust is a major disease in India, causing 30-60% annual losses of an important multi-use crop, whereas white rust is an emerging disease in the UK potentially related to climate change. The second paper (described above) applied an early version of genotype-by-sequencing (GBS) to investigate variation within and between natural populations of A. lyrata. Results from this study stimulated our thinking about how GBS could be used more practically to identify variation in useful genes (such as disease resistance) directly from public GeneBank resources. We decided to test this idea in the final year of a BBSRC funded project (BB/L011646/1) with research partners in India, using ten accessions of Brassica rapa (from the Warwick Vegetable GeneBank) to map loci for white rust resistance to the Albugo candida Race 2 that attacks Indian and English mustard (B. juncea). In this case, viable seed of brassica accessions is maintained in GeneBank collections as small, multi-parent, interbred populations (i.e., similar to natural populations of A. lyrata). Our Indian partners found previously that resistance to Ac Race 2 is rare in the original host and target crop (B. juncea). However, in a pilot experiment using GBS-mapping, we found white rust resistance is very common in the secondary genepool of B. rapa (1-3 loci mapped in each of the 10 accessions). Most of the loci contain candidate defence-related genes within 50kb of the genetic (SNP) marker.
First Year Of Impact 2016
Sector Agriculture, Food and Drink,Environment
Impact Types Economic