Skip to main content

Resistance evolution in response to spatially variable pathogen communities

Periodic Reporting for period 3 - RESISTANCE (Resistance evolution in response to spatially variable pathogen communities)

Reporting period: 2019-01-01 to 2020-06-30

The European Research Council (ERC) Consolidator project RESISTANCE will study the development of disease resistance during the coming five years. The project focuses on plants, but the mechanisms of diseases and immunity are very similar in other species as well. The aim is to uncover how individuals and populations survive and develop their resistance under continuous attack by multiple pathogens.

Previous studies have focused on resistance mechanisms based on a model where a single host battles a single pathogen. In reality, the same host is often constantly bombarded by several pathogens, and symptoms may not reveal all of the diseases carried by the individual. The rapid development of sequencing methods has helped reveal the full diversity of the pathogen community infecting the same host.

The key aim in this project is determine how diseases and the immune systems of the hosts vary between populations. The work is carried out on the ribwort plantain across the 4,000 meadows which have been mapped and are annually surveyed in Åland Islands since the 1990s. The intention is to create projections of how the structure of disease communities can influence the growth and reproduction of individuals. At the same time, we will gain information on the factors that underlie the formation of disease communities. The follow-up key aims are to uncover how resitance functions when the same host is simultaneously or sequentially attacked by multiple different pathogen spcies, and how resitance evolves under the realistic scenario of multiple attack.

The results contribute knowledge that is urgently needed to develop alternative, non-pesticide reliant management strategies in the battle against plant diseases. Currently there is an over-reliance on pesticides with approximately 320,000 tonnes of active substance used annually in agriculture worldwide, and this is predicted to grow. This weighs heavily on our ecosystems and has generated a biased food production situation globally as developing countries lack the funds needed for effective pesticides. Host priming is one alternative method, in which broad spectrum resistance may be triggered by ‘priming' the host’s defences using a biotic (or abiotic) elicitor. Currently more data is needed on how priming functions under natural ecological conditions, and for this purpose results of Objective 3 will be most valuable.

A major challenge in resistance breeding in crops is fitness costs associated with resistance that reduce yield or resistance to other pathogens. A recent review highlighted that we can only begin to understand fitness costs in breeding by examining them under ecologically relevant conditions. Towards this end, the proposed research will yield novel information about how resistance evolution and efficacy may be constrained under attack by multiple pathogens – a relevant scenario in both natural and agricultural hosts.
Objective 1. How do pathogen communities and their key determinants vary across space and time?
In 2017 we carried out sampling of natural Plantago lanceolata populations, as well as survey of factors that may play a role in determining these communities (Post doc Susi). Following RNA extractions, the samples were sent to Fasteris, Switzerland for small RNA sequencing to reveal local virus communities. The resulting sequencing data quality is very high and we are currently analyzing these data using our bioinformatics pipeline (Susi) and developing community and spatial statistical modeling to reveal determinants of pathogen community structure (Pos docs Numminen, Mononen).

Objective 2. What is the role of host resistance in shaping its pathogen community?
As we had virus primers ready and had identified plant genotypes that differ in their resistance, contrary to the plan, we carried out the field trap plant experiment already in summer 2017 instead of in 2018 as was stated in the original plan. This work was carried out by PhD student Sallinen. The project also hosted MSc students Maarit Numminen and Vanja Milenkovic, who successfully completed her MSc thesis in May 2018. RNA and DNA has been extracted from most samples and those samples have been characterized for viruses using primers. Common garden experiment of Objective 2 was set up at Lammi Biological Station in summer 2018, and the multi-year experiment is intensively monitored and regularly sampled.

Objective 3. How do trade-offs and induced defences shape the functional resistance phenotype?
We have not yet started the multifactorial greenhouse experiment that was scheduled for 2018 to uncover the mechanisms underlying functional resistance phenotypes. We are currently refining qPCR protocols for testing titer for multiple viruses, and our recent chromosome-level assembly of Pl. lanceolata genome from Dovetail TM has helped in identifying further genes and pathways involved in resistance. Moreover, I want to wait until modeling in Objective 1 is completed to identify the key viruses to be included in this study. I expect to carry out this study in 2019-20.

Objective 4. What are the immediate and cross-generation fitness consequences of variable pathogen communities for the host?
Objective 4 has proceeded according to the plan, the multi-year experiment was established at the Lammi Biological Station in 2018 and is intensively monitored and regularly sampled.

Objective 5. How does pathogen community structure impact resistance evolution?
Objective 5 will be launched in 2019 according to plan.
The complexities arising from multispecies pathogen threats that operate at different scales ranging from individual hosts to populations and regional levels, are currently considered among the major challenges for human health and food security. The results of this study are expected to produce scientific breakthroughs towards this end: While individual hosts are known to support diverse pathogen communities, virtually nothing is known about how resistance evolves and functions given this diversity. The results of this study will unravel this both mechanistically and across scales that range from individual hosts to populations and landscapes. Jointly the objectives of this proposal will provide a unique synthesis of resistance evolution under realistic pathogen loads, leading to a conceptual shift in how resistance evolution should be studied, managed, and incorporated into the next generation of theory on the dynamics of pathogen resistance in nature. Moreover, these results will, for the first time, help us understand and predict how host resistance shapes pathogen communities, which will have broad basic and applied scientific impact. A major research opportunity that this study opens up is to compare the relative importance of intra- and inter-pathogen species diversity on how infection dynamics and host resistance function.
Proportion of individual virus-infected plants across the 12 Plantago lanceolata populations in the