Evolutionary consequences of facultative plant parasitism

Parasitism is a widespread phenomenon in the natural world, with dramatic consequences for hosts, parasites, and their communities. There are over 3,000 described parasitic plant species, including mistletoes, the important grassland plant Rhinanthus, and the agricultural pest Striga. A particularly interesting, yet poorly studied group, are the facultative hemiparasites-which can grow and reproduce independent of a host, but grow more vigorously after host attachment. Facultative hemiparasitism represents a remarkably flexible growing strategy, which has largely been overlooked in preference of studies of obligate parasites-organisms which require a host to complete their lifecycle. This project investigates a case study of facultative hemiparasitism, from an evolutionary genetic perspective.

The genus Euphrasia contains approximately 300 species, all of which are facultative hemiparasites. This proposal will make progress towards using this genus as a study system for investigating the evolutionary consequences of facultative hemiparasitism, on two fronts. Firstly, it will provide the funds to test emerging genomic approaches, develop new protocols, and produce preliminary data, required for ongoing research in Euphrasia. This will include testing a new chloroplast genome enrichment approach, applying a tissue-specific RNA sequencing method, and the development of a draft whole genome sequence. These resources will be essential for future work identifying loci involved in the evolution of facultative hemiparasites, and testing whether plant parasites are a vector for adaptive horizontal gene transfer. Secondly, this proposal will develop an international collaboration between a UK researcher in plant evolutionary genomics, the world expert in plant parasitism, a leader in plant genomics, and an international expert in the biology of Euphrasia. Such an international collaboration draws on the long history of research of parasitic plants in the USA, as well as the knowledge of Euphrasia biology centred in mainland Europe, to tackle questions about hemiparasitism in an integrated fashion.

An increased understanding of plant parasitism will greatly benefit many areas of research, including evolutionary biology, plant biology, parasitology, and genome biology. In particular, understanding genomic changes associated with parasitism will be informative for researchers interested in the genetic basis of major life history transitions, while an understanding of transcriptional changes during host attachment will demonstrate a dramatic example of gene expression changes in the life of an organism. More generally, the identification of common loci underlying parasitic growth across diverse plant parasites, will facilitate the development of genetic tools to tackle parasitic plants that grow as agricultural pests.

The results generated by this research may lead to important future developments for the control of parasitic plants on agricultural crops. Five parasitic plant genera are considered serious agricultural pests: Aeginetia, Alectra, Cuscuta, Orobanche, and Striga. Striga (witchweed) alone causes $12 billion worth of damage to sub-Saharan rice crops per year. This damage is particularly problematic as the region is highly reliant on rice as its major food crop. The results from this project, and future work, will contribute to a general understanding of the conserved genetic loci involved in plant parasitism. This may enable future generations of plant scientists to find genetic solutions to reduce the growth of parasitic plants attached to agricultural plants, e.g. by engineering knock-out mutants for core parasitism genes. It seems particularly appropriate that this research is performed by an international collaborative team, given that the concern of parasitic plants in agriculture is a global issue.

This research will also raise the public profile of parasitic plants. While the general public are aware of human parasites, such as malaria, few know about parasitic plants, and their important role in ecosystems. AT is currently developing an Evolution Garden at the Royal Botanic Garden Edinburgh (RBGE), as a means to inform the general public of basic principles of evolution. If this project is successfully funded, we will present our research findings on notice boards adjacent to Euphrasia plants, from 2017. It is then hoped that individuals will both be more aware of the importance of parasitic plants, as well as be willing to try and grow them in their own gardens. This engagement activity also benefits the RBGE-a publicly funded scientific institution-as they are looking for ways to integrate scientific research with public engagement.

This work will also lead to an improved understanding of parasitic plants in horticulture. There is real demand to cultivate certain parasitic plants, with many seed companies reporting good sales of parasitic plants for meadows (e.g. Rhinanthus, www.wildseed.co.uk), or simply for general interest (e.g. mistletoes). While there is interest in introducing Euphrasia into cultivation, most seed companies do not currently stock Euphrasia, as they are perceived as being difficult to germinate and grow. This funding will pump-prime research on the parasitic biology of Euphrasia, with future grants to include workshops on growing parasitic plants (in collaboration with the RBGE), as well as germination and growth research on parasitic plants, in collaboration with industrial partners Scotia Seeds.

Evolutionary biologists will greatly benefit from this research. This work will be a major advance in our understanding of the evolution of plant parasites, with this information being of value to the broad community studying parasite biology. Moreover, the genomic resources, which include transcriptome sequences, chloroplast genomes, and a draft nuclear genome, will be of value to other researchers in parasite biology, plant biology, and students of genome evolution. This information will contribute to the growing resources available through our Euphrasia website (Euphrasia.bio.ed.ac.uk).

The lead PI, Alex Twyford, will benefit greatly from the transferable skills learnt during this project. As an early career PI, he has already organised an international conference, and networked in the US, and this project will further his skills in developing international collaborations. He will also benefit from specific training in laser dissection microscopy and transcriptome sequencing (with Claude dePamphilis), de novo genome assembly (with Rob Ness), and Euphrasia identification (with Galina Gusarova).