Benign infections or damaging epidemics: the influence of biology, the environment and agricultural practice on vector-borne phytobacteria

Factors that contribute to some pests and diseases being serious problems in one location and not another are largely unknown. Identifying these factors is fundamental to better understand risks associated with introductions of pests and diseases into new environments via globalised trade of plants and plant products. The bacterium Candidatus Liberibacter solanacearum (Lso) is an emerging threat to a range of crops including potato, tomato, carrot and celery and is under statutory control in the EU. In potato Lso induces zebra chip, a damaging disease manifest by brown stripes in the tubers, which cause large losses in fresh and processing markets. The disease has spread quickly through the Americas and more recently into New Zealand. A genetically different sub-group (haplotype) of the bacteria causes a damaging disease of carrots in Scandinavia, Northern France and the Mediterranean basin. Whereas this haplotype can infect potato, disease in this crop is not evident in Europe. The disease is transmitted by psyllids, which are sap-feeding insects. The psyllid Bactericera cockerelli spreads Lso in the Americas and New Zealand, whilst two native species (Trioza apicalis and Bactericera trigonica) and possibly a third species (B. nigricornis) spreads the bacteria in Europe. In the UK the pathogen has been detected in carrots, weeds and in psyllids caught in insect traps. Despite the presence of the pathogen and competent vector species, the bacteria is not currently causing widespread crop damage in either potato or carrots.
The focus of this project is to better understand the factors that may contribute to Lso becoming a more important pathogen in the UK. Factors may include differences between Lso haplotypes, the geographical distributions and genetics variations of Lso haplotypes and psyllid vectors, landscape designs (such as weeds that surround crop fields), and agricultural practice/policy.
The overall aim of the work is to investigate the complex network of Lso haplotypes, hosts and vectors in the UK landscape, focussing on carrots, related crops and apiaceous weeds. Working within this system our objectives are to: (i) Generate genome sequence information for Lso haplotypes and psyllids to understand genetic variations of the pathogens and vectors present in the UK, and use this information to develop rapid diagnostics tests; (ii) Study the spatial and temporal distributions of Lso and psyllid vectors in crops and the surrounding environments; (iii) Improve our understanding of vector host plant preferences and ability to transmit the bacteria; (iv) Use ecological network analysis to build a comprehensive picture of the pathosytem; and (v) Use ecological and trade models to examine how future policy options (changes in the UKs tariff structure with trading partners and how UK habitats are managed) might alter this transmission risk. Ultimately the modelling will consider the systems readiness to withstand changes in risk and provide information on the drivers (biological, ecological and man made) that influence the potential of a pathogen to become a damaging disease-causing agent.
The outcomes will be of interest to government stakeholders working in Plant Health, where the research will provide insights into prioritising responses to Lso and other complex pests and diseases. The overall approach should improve our ability to predict risk and prioritise surveillance activity on the most damaging threats. For agri-food-environment, information on the impact of changes in land and crop management and approaches to assess this will help us to better understand the complex networks that exist and the impact of future environmental and trade policies. For industry, better understanding of emerging pathogens will help them to proactively manage this and future problems. Finally the interdisciplinary consortium will deliver innovative science of interest to academics in a number of fields.

A summary of planned work under each objective.
1. Sequence the genomes of Lso haplotypes and psyllid vectors found in the UK and develop rapid tests based on haplotype/species specific markers

Produce genome sequences of Lso haplotypes E, F, G, U, S, S2 and Y and vector species Trioza apicalis and Trioza anthrisci. Use comparative genomic tools to identify haplotype/species specific markers and design/validate qPCR tests to use in objective 2 and 3

2. Understand the incidence of Lso in carrots and plants in the environment surrounding the crops in major carrot growing regions of the UK

We will carry out surveys on farms and plants from the surrounding environment in the four main carrot growing areas of the UK over three seasons to identify which Lso haplotypes are present in which plant species.

3. Determine UK-wide diversity and potential distribution of Lso vector species

Using trapped insects at both a landscape and field scale, we will identify which psyllid vectors carry which haplotypes of Lso. We will use generate data to understand the population structure of the main vector species.

4. Assess the potential for newly discovered Lso haplotypes to be transmitted to carrot and other economically important crops by psyllids and other vectors

Biological studies will conclude which putative vectors identified in WP3 are competent vectors of Lso

5. Consider the impact on pathway risks of economic policy changes with respect to tariffs

6. Consider the impact on transmission risk of environmental land management policy
We will assess likely policy scenarios to inform the trade and ecological modelling that will evaluate changes in transmission risk. Modelling how future trading and the Environmental Land Management Scheme change the pathways of introduction, distribution and abundance of wild hosts will be tested. Using data from WP2-4 ecological network modelling will indicate the relative importance of transmission and host species

Globally there are increasing threats to plant and tree health from bacterial phytopathogens caused by a combination of increased movement in traded plants and plant materials, changes in climate and growing practices. The CALIBER consortium (CAndidatus LIBeribacter solanacearum Epidemiology Research) seeks to better understand the pathosystem dynamics of Liberibacters in farmed and natural environments. Ca. L. solancearum is listed in the UK Plant Health Risk Register as a high-risk plant pest due to its impact on potato. However, significant gaps in our understanding of the interactions between the pathogen, vector, hosts and environment make assessment of risk difficult, causing uncertainty for government and industry. Preliminary work by SASA showed that Ca. L solancearum is present in Scotland in both vectors and wild hosts that were not previously associated with the pathogen. Multilocus sequence typing (MLST) suggests there are previously undescribed haplotypes present in the UK. This situation of an inoculum source and presence of pathogen-carrying vectors suggests a significant risk to crops, which is either not being realised or may be under reported. Using Apiaceae and Ca. L. solanacearum as a model pathosystem, the proposed work will help to better understand the drivers that distinguish organisms which are benign pathogens and those with significant potential to cause harm.
Managing this type of emerging threat needs a system approach to consider both agricultural production methods and the interrelationship with the natural environment (which itself is being increasingly "managed"). The project will engage and benefit key stakeholders who reflect the trade-offs inherent in the system through the use of a consultative panel made up from representatives of growers, academics, the environmental/ecological, and regulatory sectors as well as plant health bodies. This panel will help refine and shape the research in response to ongoing outputs throughout the life of the project. We will seek to engage with the farming sector to take the outcomes from the research work to support changes to production practice that will help farmers mitigate the impact of plant diseases. The consortium is already connected to the British Carrot Growers Association (see letter of support from BCGA) and the potato industry throughout the UK. These industry connections are necessary to identify relevant field sites for sampling, but more critically to better understand current practices and constraints and what the impact of changing agricultural practice would have on the industry. Additionally, these connections allow a route for knowledge exchange directly to a broad range of stakeholders. The consortium will undertake engagement with Government, its agencies and key delivery bodies (in the UK SASA, Fera and APHA, and overseas through engagement with EPPO and IPPC respectively) responsible for plant health issues. We are also engaged with key stakeholders involved in the proposed Environmental Land Management Scheme (ELMS), including Defra, Natural England and the Rural Payments Agency, through our projects in the area and will provide links to the appropriate personnel. ELMS will be evolving as CALIBER progresses but our strong links will enable us to account for changes in the scheme (as they affect the range and scale of potential hosts within field margins) as it is developed and implemented.
Throughout the project we aim to generate direct impact by having an open access policy around release of new genomic data. We will engage directly with delivery bodies (NPPOs in the UK and EU) to accelerate the uptake of the rapid identification tools developed in the project which will enable the organisations to identify key organisms more quickly, develop work programmes more accurately and thus initiate timely and effective interventions.