Michael Jeger

Factors Influencing Begomovirus Evolution and Their Increasing Global Significance: Implications for Sustainable Control

Begomoviruses (Family Geminiviridae, Genus Begomovirus) have become the most destructive group of plant viruses in tropical and subtropical regions of the world. The recent emergence of begomoviruses is notable, as these viruses have been co-evolving with their dicotyledonous plant hosts for millennia. Agricultural intensification has been proposed as one of the main causes, together with increases in populations of their vector Bemisia tabaci, partly due to the worldwide spread of the more fecund B-biotype. Reports of new diseases and associated epidemics are frequent. Many such reports describe the evolution of more aggressive virus variants through recombination. Little is known about the selection pressures that seem to operate and drive begomovirus evolution towards increased virulence and an extended host range. It is apparent, however, that the genomes of begomoviruses show extreme plasticity leading to an ability to evolve very rapidly in response to changing cropping systems. Genetic diversity is created not only by recombination between genomic components, but also by exchange (pseudorecombination) of their genomic components, and even by acquiring DNA sequences from viruses of other genera. Recently, associations with some satellite molecules, termed DNA-β and DNA1, have also been shown to be widespread in the Old World. Functional DNA-β molecules encode pathogenicity determinants and are often critical for disease symptom development. They appear to act by suppressing host plant defense mechanism(s), such as post-transcriptional gene silencing (PTGS), enabling a diverse range of begomoviruses to infect particular hosts. In this review, suppression of PTGS is one of the driving forces discussed as a likely and important influence on the evolution of begomoviruses. The known sources of genetic variation in begomoviruses are also considered together with the factors driving evolutionary change, the potential for limiting the extent and rate of adverse change, and therefore the potential for achieving more sustainable control of crop disease epidemics. Referee: Professor J.O. Strandberg, Mid-Florida Research and Education Center, University of Florida/IFAS, 2725 Binion Road, Apopka, FL 32704 USA

Impacts of climate change on plant diseases—opinions and trends

There has been a remarkable scientific output on the topic of how climate change is likely to affect plant diseases. This overview addresses the need for review of this burgeoning literature by summarizing opinions of previous reviews and trends in recent studies on the impacts of climate change on plant health. Sudden Oak Death is used as an introductory case study: Californian forests could become even more susceptible to this emerging plant disease, if spring precipitations will be accompanied by warmer temperatures, although climate shifts may also affect the current synchronicity between host cambium activity and pathogen colonization rate. A summary of observed and predicted climate changes, as well as of direct effects of climate change on pathosystems, is provided. Prediction and management of climate change effects on plant health are complicated by indirect effects and the interactions with global change drivers. Uncertainty in models of plant disease development under climate change calls for a diversity of management strategies, from more participatory approaches to interdisciplinary science. Involvement of stakeholders and scientists from outside plant pathology shows the importance of trade-offs, for example in the land-sharing vs. sparing debate. Further research is needed on climate change and plant health in mountain, boreal, Mediterranean and tropical regions, with multiple climate change factors and scenarios (including our responses to it, e.g. the assisted migration of plants), in relation to endophytes, viruses and mycorrhiza, using long-term and large-scale datasets and considering various plant disease control methods.

Epidemiology of insect-transmitted plant viruses: modelling disease dynamics and control interventions

Abstract.  Plant viruses are an important constraint to crop production world‐wide. Rarely have plant virologists, vector entomologists and crop specialists worked together in search of sustainable management practices for viral diseases. Historically, modelling approaches have been vector‐based dealing with empirical forecasting systems or simulation of vector population dynamics. More recently, epidemiological models, such as those used in human/animal epidemiology, have been introduced in an attempt to characterize and analyse the population ecology of viral diseases. The theoretical bases for these models and their use in evaluating control strategies in terms of the interactions between host, virus and vector are considered here. Vector activity and behaviour, especially in relation to virus transmission, are important determinants of the rate and extent of epidemic development. The applicability and flexibility of these models are illustrated by reference to specific case studies, including the increasing importance of whitefly‐transmitted viruses. Some outstanding research and methodological issues are considered.

Plant health and global change – some implications for landscape management

Global change (climate change together with other worldwide anthropogenic processes such as increasing trade, air pollution and urbanization) will affect plant health at the genetic, individual, population and landscape level. Direct effects include ecosystem stress due to natural resources shortage or imbalance. Indirect effects include (i) an increased frequency of natural detrimental phenomena, (ii) an increased pressure due to already present pests and diseases, (iii) the introduction of new invasive species either as a result of an improved suitability of the climatic conditions or as a result of increased trade, and (iv) the human response to global change. In this review, we provide an overview of recent studies on terrestrial plant health in the presence of global change factors. We summarize the links between climate change and some key issues in plant health, including tree mortality, changes in wildfire regimes, biological invasions and the role of genetic diversity for ecosystem resilience. Prediction and management of global change effects are complicated by interactions between globalization, climate and invasive plants and/or pathogens. We summarize practical guidelines for landscape management and draw general conclusions from an expanding body of literature.

Evolution of the international regulation of plant pests and challenges for future plant health

Plant pathogens and invertebrates harmful to plants, collectively referred to as plant pests, continue to threaten food security. International cooperation and regulatory systems to inhibit the spread of plant pests began formally in 1878. Initially seven countries worked together and agreed phytosanitary measures against grape phylloxera, Phylloxera vastatrix (=Daktulosphaira vitifoliae). There are now 172 countries that are contracting parties to the International Plant Protection Convention, a treaty that aims to prevent the introduction and spread of pests of plants and plant products, and to promote appropriate measures for their control. Apparently contradictory interests between international trade, which has facilitated the spread of plant pests, and the protection of plants are mutually recognised in global trade and phytosanitary agreements. The principle that risk management measures should provide an appropriate level of protection without undue interference in trade was established within the plant protection agreements at the beginning of the 20th Century and is still fundamental to risk management policy today. Globally ten Regional Plant Protection Organizations facilitate more local cooperation and recommend the regulation of over 1,000 named quarantine plant pests. Member States of the European Union work together and regulate imported plant material on the grounds of plant health with each Member State taking into account the plant health concerns of every other Member State. However, decision making can be slow and border inspections poorly targeted. Close relationships between regulatory scientists and policy makers, focussed on agricultural and horticultural production, are changing to take a broader stakeholder community into consideration as decisions regarding the environment seek to draw upon a wider knowledge base. Challenges that impede the success of limiting international pest movement include increased international trade and climate change. International guidelines designed to prevent pest spread present challenges of their own if they remain difficult to implement.

An analytical model of plant virus disease dynamics with roguing and replanting.

The dynamics of a virus disease in a perennial plant population are modelled. The population is divided into healthy, latently infected, infectious and post-infectious plants and linked differential equations describe the dynamics of each category. Qualitative analysis of this model shows stable dynamics and threshold conditions for disease persistence. Stable equilibria are reached after several years. The dynamics of the model are highly sensitive to changes in contact rate and infectious period. Disease management by roguing (removal) of infected plants and replanting with healthy ones is investigated. Roguing only in the post-infectious category confers no advantage. At low contact rates, roguing only when plants become infectious is sufficient to eradicate the disease (...)

Networks in plant epidemiology: from genes to landscapes, countries, and continents

There is increasing use of networks in ecology and epidemiology, but still relatively little application in phytopathology. Networks are sets of elements (nodes) connected in various ways by links (edges). Network analysis aims to understand system dynamics and outcomes in relation to network characteristics. Many existing natural, social, and technological networks have been shown to have small-world (local connectivity with short-cuts) and scale-free (presence of super-connected nodes) properties. In this review, we discuss how network concepts can be applied in plant pathology from the molecular to the landscape and global level. Wherever disease spread occurs not just because of passive/natural dispersion but also due to artificial movements, it makes sense to superimpose realistic models of the trade in plants on spatially explicit models of epidemic development. We provide an example of an emerging pathosystem (Phytophthora ramorum) where a theoretical network approach has proven particularly fruitful in analyzing the spread of disease in the UK plant trade. These studies can help in assessing the future threat posed by similar emerging pathogens. Networks have much potential in plant epidemiology and should become part of the standard curriculum.

Disease spread in small-size directed networks: epidemic threshold, correlation between links to and from nodes, and clustering.

Network epidemiology has mainly focused on large-scale complex networks. It is unclear whether findings of these investigations also apply to networks of small size. This knowledge gap is of relevance for many biological applications, including meta-communities, plant-pollinator interactions and the spread of the oomycete pathogen Phytophthora ramorum in networks of plant nurseries. Moreover, many small-size biological networks are inherently asymmetrical and thus cannot be realistically modelled with undirected networks. We modelled disease spread and establishment in directed networks of 100 and 500 nodes at four levels of connectance in six network structures (local, small-world, random, one-way, uncorrelated, and two-way scale-free networks). The model was based on the probability of infection persistence in a node and of infection transmission between connected nodes. Regardless of the size of the network, the epidemic threshold did not depend on the starting node of infection but was negatively related to the correlation coefficient between in- and out-degree for all structures, unless networks were sparsely connected. In this case clustering played a significant role. For small-size scale-free directed networks to have a lower epidemic threshold than other network structures, there needs to be a positive correlation between number of links to and from nodes. When this correlation is negative (one-way scale-free networks), the epidemic threshold for small-size networks can be higher than in non-scale-free networks. Clustering does not necessarily have an influence on the epidemic threshold if connectance is kept constant. Analyses of the influence of the clustering on the epidemic threshold in directed networks can also be spurious if they do not consider simultaneously the effect of the correlation coefficient between in- and out-degree.

Integrating natural and social science perspectives on plant disease risk, management and policy formulation

Plant diseases threaten both food security and the botanical diversity of natural ecosystems. Substantial research effort is focused on pathogen detection and control, with detailed risk management available for many plant diseases. Risk can be assessed using analytical techniques that account for disease pressure both spatially and temporally. We suggest that such technical assessments of disease risk may not provide an adequate guide to the strategies undertaken by growers and government to manage plant disease. Instead, risk-management strategies need to account more fully for intuitive and normative responses that act to balance conflicting interests between stakeholder organizations concerned with plant diseases within the managed and natural environments. Modes of effective engagement between policy makers and stakeholders are explored in the paper, together with an assessment of such engagement in two case studies of contemporary non-indigenous diseases in one food and in one non-food sector. Finally, a model is proposed for greater integration of stakeholders in policy decisions.

Infectious diseases of animals and plants : an interdisciplinary approach

Animal and plant diseases pose a serious and continuing threat to food security, food safety, national economies, biodiversity and the rural environment. New challenges, including climate change, regulatory developments, changes in the geographical concentration and size of livestock holdings, and increasing trade make this an appropriate time to assess the state of knowledge about the impact that diseases have and the ways in which they are managed and controlled. In this paper, the case is explored for an interdisciplinary approach to studying the management of infectious animal and plant diseases. Reframing the key issues through incorporating both social and natural science research can provide a holistic understanding of disease and increase the policy relevance and impact of research. Finally, in setting out the papers in this Theme Issue, a picture of current and future animal and plant disease threats is presented.