Trends in plant virus epidemiology: Opportunities from new or improved technologies

Plant virus epidemiology provides powerful tools to investigate key factors that contribute to virus epidemics in agricultural crops. When successful, epidemiological approaches help to guide decisions regarding plant protection strategies. A recent example is epidemiological research on Potato virus Y (PVY) in Finnish seed potato production; this study led to the identification of the main PVY vector species and helped to determine the timing of virus transmission. However, pathosystems rarely allow research to produce such clear-cut results. In fact, the notorious complexity of plant virus pathosystems, with multiple interactions between virus, vector, plant and environment, makes them often impenetrable even for advanced epidemiological models. This dynamic complexity questions the universal validity of employing epidemiological models that attempt to single out key factors in plant virus epidemics. Therefore, a complementary approach is needed that acknowledges the partly indeterministic nature of complex and evolving pathosystems. Such an approach is the use of diversity, employing functionally complementary elements that can jointly buffer against environmental changes. I argue that for a wider range of plant production problems, the strategy of combining mechanistic and diversity-based approaches will provide potent and sustainable solutions. In addition, to translate insights from plant virus epidemiology into practice, improvements need to be made in knowledge transfer, both within the scientific community and between researchers and practitioners. Finally, moving towards more appropriate virus control strategies is only possible if economic interests of stakeholders are in line with changing current practices.

Plant diseases caused by viruses share many common features with those caused by other pathogen taxa in terms of the host-pathogen interaction, but there are also distinctive features in epidemiology, most apparent where transmission is by vectors. Consequently, the host-virus-vector-environment interaction presents a continuing challenge in attempts to understand and predict the course of plant virus epidemics. Theoretical concepts, based on the underlying biology, can be expressed in mathematical models, and tested through quantitative assessments of epidemics in the field; this remains a goal in understanding why plant virus epidemics occur and how they can be controlled. To this end, this review identifies recent emerging themes and approaches to fill in knowledge gaps in plant virus epidemiology. We review quantitative work on impact of climatic fluctuations and change on plants, virus and vectors under different scenarios where impacts on the individual components of the plant-virus-vector interaction may vary disproportionately; the continuing sometimes discordant debate on host resistance and tolerance as plant defense mechanisms, including aspects of farmer behavior and attitudes to disease management that may affect deployment in crops; disentangling host-virus-vector-environment interactions as these contribute to temporal and spatial disease progress in field populations, computational techniques for estimating epidemiological parameters from field observations, and the use of optimal control analysis to assess disease control options. We end by proposing new challenges and questions in plant virus epidemiology.

The basic reproduction number of vector-borne plant virus epidemics

Ecologists require spatially explicit data to relate structure to function. To date, heavy reliance has been placed on obtaining such data from remote‐sensing instruments mounted on spacecraft or manned aircraft, although the spatial and temporal resolutions of the data are often not suited to local‐scale ecological investigations. Recent technological innovations have led to an upsurge in the availability of unmanned aerial vehicles (UAVs) – aircraft remotely operated from the ground – and there are now many lightweight UAVs on offer at reasonable costs. Flying low and slow, UAVs offer ecologists new opportunities for scale‐appropriate measurements of ecological phenomena. Equipped with capable sensors, UAVs can deliver fine spatial resolution data at temporal resolutions defined by the end user. Recent innovations in UAV platform design have been accompanied by improvements in navigation and the miniaturization of measurement technologies, allowing the study of individual organisms and their spatiotemporal dynamics at close range.

In recent years, mathematical modeling has increasingly been used to complement experimental and observational studies of biological phenomena across different levels of organization. In this article, we consider the contribution of mathematical models developed using a wide range of techniques and uses to the study of plant virus disease epidemics. Our emphasis is on the extent to which models have contributed to answering biological questions and indeed raised questions related to the epidemiology and ecology of plant viruses and the diseases caused. In some cases, models have led to direct applications in disease control, but arguably their impact is better judged through their influence in guiding research direction and improving understanding across the characteristic spatiotemporal scales of plant virus epidemics. We restrict this article to plant virus diseases for reasons of length and to maintain focus even though we recognize that modeling has played a major and perhaps greater part in the epidemiology of other plant pathogen taxa, including vector-borne bacteria and phytoplasmas.

After clarifying the relationship between the closely related concepts of ecology and epidemiology as they are used in plant virology, this article provides a historical perspective on the subject before discussing recent progress and future prospects. Ecology focuses on virus populations interacting with host populations within a variable environment, while epidemiology focuses on the complex association between virus and host plant, and factors that influence spread. The evolution and growth of plant virus ecology and epidemiology since its inception to the present day, and the major milestones in its development, are illustrated by examples from influential historical reviews published in the Annals of Applied Biology over the last 100 years. Original research papers published in the journal are used to illustrate important ecological and epidemiological principles and new developments in both fields. Both areas are multifaceted with many factors influencing host plants, and virus and vector behaviour. The highly diverse scenarios that arise from this process influence the virus population and the spatiotemporal dynamics of virus distribution and spread. The review then describes exciting progress in research in the areas of molecular epidemiology and ecology, and understanding virus–vector interactions. Application of new molecular techniques has greatly accelerated the rate of progress in understanding virus populations and the way changes in these populations influence epidemics. Viruses cause direct and plant‐mediated indirect effects on insect vectors by modifying their life cycles, fitness and behaviour, and one of the most fascinating recent fields of research concerns plant‐mediated indirect virus manipulation of insect vector behaviour that encourages virus spread. Next, the review describes the current state of knowledge about spread of plant viruses at the critical agro‐ecological interface between managed and natural vegetation. There is an urgent need to understand how viruses move in both directions between the two and be able to anticipate these kinds of events. To obtain an understanding of, and ability to foresee, such events will require a major research effort into the future. The review finishes by discussing the implications of climate change and rapid technological innovation for the types of research needed to avoid virus threats to future world food supplies and plant biodiversity. There has been lamentably little focus on research to determine the magnitude of the threat from diseases caused in diverse plant virus pathosystems under different climate change scenarios. Increasing technological innovation offers many opportunities to help ensure this situation is addressed, and provide plant virus ecology and epidemiology with a very exciting future.

Interactions between vector insects, plant viruses and host plants are complex and diverse. Although much work has been done to study the tripartite relationships, their roles in biological invasions have been rarely explored. The limited case studies available indicate that the interactions may be mediated by the host plant susceptibility to viruses, the suitability of host plants to vector insects, and the insects’ capacity to utilize host plants. When a host plant is highly susceptible to the virus but shows a low level of suitability to the insect, and the insect has a strong capacity to use different host plants, an indirect mutualistic relationship is likely to occur between vector insect and plant virus via their shared host plants. This kind of mutualism can contribute to the widespread invasion of vector insects as well as the epidemics of plant viruses. In view of the significance of the tripartite interactions in biological invasions, future effort should be made to investigate comparatively many more combinations of different species, and various technologies can be used to reveal the physiological and molecular mechanisms of the interactions.

Plant viruses are a threat to a sustainable economy because they cause economic losses in yields. The epidemiology of plant viruses is of particular interest because of their dynamic spread by insect vectors and their transmission by seeds. The speed and direction of viral evolution are determined by the selective environment in which they are found. Knowledge of the ecology of plant viruses is critical to the transmission of many plant viruses. Accurate and timely detection of plant viruses is an essential part of their control. Rapid climate change and the globalization of trade through free trade agreements encourage the transmission of vectors and viruses from country to country. Another factor affecting the emergence of viruses is the cultivation of monocultures with low genetic diversity a nd high plant density. Trade in plant material (germplasm and living plants) also cause the emergence of new viruses. Viruses have a fast adaptation and development in a new environment. Aphids are the most widespread and important vectors of plant viruses. Myzus persicae transmits more than 100 different plant viruses. In nature plant viruses are transmitted also by nematodes, fungi, mites, leafhoppers, whiteflies, beetles, and planthoppers. The symptoms of viral diseases are very diverse and are often confused with symptoms of abiotic stress. Control of viral diseases is based on two strategies: i) immunization (genetic resistance acquired by plant transformation, breeding, or cross-protection), ii) prophylaxis to limit viruses (removal of infected plants and control of their vectors). For management, we rely on quick and accurate identification of the disease.

Climate change refers to a change in the state of the climate that can be identified (e.g. using statistical tests) by changes in the mean and/or the variability of its properties and that persists for an extended period, typically decades or longer. Atmospheric CO2 levels are currently about 410 ppm and elevated CO2 (eCO2) levels are forecasted to rise up to 650 ppm by the year 2100. The global surface temperature increases by the end of the twenty-first century and is likely to exceed 1.5 °C. Climate change is likely to modify many critical virus epidemic components in different ways often resulting in epidemic, but sometimes may have the opposite effect, depending on the pathosystem and circumstances. Increasing global temperatures and elevated atmospheric CO2 levels and the occurrence of water stress episodes driven by climate change have a dramatic effect on plant viral diseases, which alters the plant biochemistry and plant defence responses. It has a major impact on the diverse type of vector biology, feeding behaviour and fecundity, ultimately results in the transmission of plant virus diseases and the ease by which previously unknown viruses can emerge and leads to severe yield losses in many cultivated crops. Climate change is likely to diminish the effectiveness of some control measures of plant viral diseases. Fortunately, rapid advancing technological innovations currently underway in the world have the potential to provide many opportunities to improve the effectiveness of virus and vector control and they help to mitigate the impact of climate change on plant virus epidemics.

CHAPTER 17 - PLANT VIRUS EPIDEMIOLOGY AND COMPUTER SIMULATION OF APHID POPULATIONS

Climate change and plant virus epidemiology

Most plant viruses in nature are transmitted from one plant to another by hemipteran insects. A high population density of the vector insects that are highly efficient at virus transmission plays a key role in virus epidemics in fields. Studying virus-insect vector interactions can advance our understanding of virus transmission and epidemics with the aim of designing novel strategies to control plant viruses and their vector insects. Immunofluorescence labeling has been widely used to analyze interactions between pathogens and hosts and is used here in the white-backed planthopper (WBPH, Sogatella furcifera), which efficiently transmits the southern rice black streaked dwarf virus (SRBSDV, genus Fijivirus, family Reoviridae), to locate the virions and insect proteins in the midgut epithelial cells. Using laser scanning confocal microscopy, we studied the morphological characteristics of midgut epithelial cells, cellular localization of insect proteins, and the colocalization of virions and an insect protein. This protocol can be used to study virus activities in insects, functions of insect proteins, and interactions between virus and vector insect.

Ecology and control of plant viruses should be stressed together, for it is through understanding the ecology and epidemiology of plant viruses and their vectors that we have been able to control successfully a number of important plant virus diseases. It will be seen that some of the ground covered here has been detailed from a different viewpoint in Chapter 7. However, we feel that some overlap is inevitable in putting control measures and their ecological basis in context.

Many archeological sites have been destroyed totally or partially around the globe due to earth quakes, floods and/or fire. It is the need of time to digitally preserve the historical sites before they get destroyed. It is difficult to obtain data using conventional methods due to difficulty in accessing the historical sites because of their location and neighborhood. Recent innovations in Unmanned Aerial Systems (UASs) have enabled to remote sense and acquire data using aerial imagery. In this research photogrammetry is used to develop highly accurate photo realistic 3D models. This method contributes in terms of quality, time and investment to acquire data compared to other methods which demand more time and investment. The automated flight stability and altitude control of the UAS and the fully stabilized and calibrated RGB sensor helps deliver high quality data to provide reliable results. Using aerial data acquired from a low cost and light weight Unmanned Aerial Vehicles (UAV) equipped with high resolution RGB sensor and image processing using photogrammetry tools highly accurate 3D model is formed. The main goals of this study were to conduct survey of a historical site in Pakistan utilizing advanced robotics and photogrammetry stitching techniques to investigate the potential of UAV in producing geo-referenced 3D reconstruction. The study is carried out to achieve an accuracy of within 5cm/pixel of the 3D model. The digitally preserved 3D models will help to maintain and reconstruct and historical site in case of any damage. The 3D model produced can be quickly produced for inventory, architectural and facility management system.

Predicting epidemics of plant virus disease constitutes a challenging undertaking due to the complexity of the three-cornered pathosystems (virus, vector, and host) involved and their interactions with the environment. A complicated nomenclature is used to describe virus epidemiological models. This review explains how the nomenclature evolved and provides a historical account of the development of such models. The process and steps involved in devising models that incorporate weather variables and data retrieval and are able to forecast plant virus epidemics effectively are explained. Their application to provide user-friendly, Internet-based decision support systems (DSSs) that determine when and where control measures are needed is described. Finally, case studies are provided of eight pathosystems representing different scenarios in which modeling approaches have been used with varying degrees of effectiveness to forecast virus epidemics in parts of the world with temperate, Mediterranean, subtropical, and tropical climates.