Annual Review of Phytopathology - Volume 46, 2008

Starting with the influences of having a father who was an agricultural plant pathologist, I sketch my career through university and research institute from field epidemiology, basic virus characterization to molecular biology. I note what I consider to be the highlights of my scientific career and the events that shaped the development of my thinking. These include secondment to teach in a university in Uganda, a sabbatical year in the University of California, Davis, where I became aware of the emerging DNA technology, studying the molecular biology of Cauliflower mosaic virus, rice tungro viruses, and Banana streak virus with the aim of developing diagnostics and approaches to control of viruses. Bringing these experiences together, I am now involved in facilitating the uptake of the application of biotechnology to crop improvement in developing countries. I conclude with some thoughts on opportunities for young plant pathologists over the next years of rapid change. As I am one of the few British scientists who have had the honor of writing such an article, I also note some of the vagaries of the British system.

The oak wilt pathogen, Ceratocystis fagacearum, may be another example of a damaging, exotic species in forest ecosystems in the United States. Though C. fagacearum has received much research attention, the origin of the fungus is unknown. The pathogen may have been endemic at a low incidence until increased disturbances, changes in land use, and forest management created conditions favorable for disease epidemics. The host genus Quercus contains some relatively resistant species native to the United States, further supporting the hypothesis that the pathogen is native in origin. However, there are also many common, highly susceptible Quercus species—a characteristic typical of introduced pathogens. Most convincingly, studies have shown that the known populations of C. fagacearum have experienced a severe genetic bottleneck that can only be explained by a single introduction. The weight of evidence indicates that C. fagacearum is an introduced pathogen, with possible origins in Central or South America, or Mexico.

The past decade has seen fundamental changes in our understanding of powdery mildews (Erysiphales). Research on molecular phylogeny demonstrated that Erysiphales are Leotiomycetes (inoperculate discomycetes) rather than Pyrenomycetes or Plectomycetes. Life cycles are surprisingly variable, including both sexual and asexual states, or only sexual states, or only asexual states. At least one species produces dematiaceous conidia. Analyses of rDNA sequences indicate that major lineages are more closely correlated with anamorphic features such as conidial ontogeny and morphology than with teleomorph features. Development of molecular clock models is enabling researchers to reconstruct patterns of coevolution and host-jumping, as well as ancient migration patterns. Geographic distributions of some species appear to be increasing rapidly but little is known about species diversity in many large areas, including North America. Powdery mildews may already be responding to climate change, suggesting they may be useful models for studying effects of climate change on plant diseases.

Non-plant pathogenic endophytic bacteria can promote plant growth, improve nitrogen nutrition, and, in some cases, are human pathogens. Recent work in several laboratories has shown that enteric bacteria are common inhabitants of the interior of plants. These observations led to the experiments that showed the entry into plants of enteric human pathogens such as Salmonella and E. coli O157:H7. The extent of endophytic colonization by strains is regulated by plant defenses and several genetic determinants necessary for this interior colonization in endophytic bacteria have been identified. The genomes of four endophytic bacteria now available should promote discovery of other genes that contribute to this phenotype. Common virulence factors in plant and animal pathogens have also been described in bacteria that can infect both plant and animal models. Future directions in all of these areas are proposed.

Plant pathogens can emerge in agricultural ecosystems through several mechanisms, including host-tracking, host jumps, hybridization and horizontal gene transfer. High-throughput DNA sequencing coupled with new analytical approaches make it possible to differentiate among these mechanisms and to infer the time and place where pathogens first emerged. We present several examples to illustrate the different mechanisms and timescales associated with the origins of important plant pathogens. In some cases pathogens were domesticated along with their hosts during the invention of agriculture approximately 10,000 years ago. In other cases pathogens appear to have emerged very recently and almost instantaneously following horizontal gene transfer or hybridization. The predominant unifying feature in these examples is the environmental and genetic uniformity of the agricultural ecosystem in which the pathogens emerged. We conclude that agro-ecosystems will continue to select for new pathogens unless they are re-engineered to make them less conducive to pathogen emergence.

Pathogen entry into host tissue is a critical first step in causing infection. For foliar bacterial plant pathogens, natural surface openings, such as stomata, are important entry sites. Historically, these surface openings have been considered as passive portals of entry for plant pathogenic bacteria. However, recent studies have shown that stomata can play an active role in limiting bacterial invasion as part of the plant innate immune system. As a counter-defense, the plant pathogen Pseudomonas syringae pv. tomato DC3000 uses the virulence factor coronatine to actively open stomata. In nature, many foliar bacterial disease outbreaks require high humidity, rain, or storms, which could favor stomatal opening and/or bypass stomatal defense by creating wounds as alternative entry sites. Further studies on microbial and environmental regulation of stomatal closure and opening could fill gaps in our understanding of bacterial pathogenesis, disease epidemiology, and microbiology of the phyllosphere.

We describe two classes of models used for fungicide and antibiotic resistance dynamics. One class assumes that the density of the pathogen (or severity of the disease caused by the pathogen) has no feedback effects on the rate at which new infections arise. The second class does not make this assumption. A quantitative relationship between these two classes is derived. We then discuss the two sets of assumptions made in the literature about initial conditions: either both the fungicide-sensitive strain and the -resistant strain are initially at low density, or the sensitive strain is resident at nonlow density and the resistant strain is initially at low density. We show that models of fungicide resistance dynamics with and without density-dependent feedback give contrasting predictions on the effects of pathogen life-cycle parameters and the effects of the fungicide (dose, frequency, use of mixtures, spatial usage restrictions) on the evolution, invasion, and spread of fungicide resistance. We further show that the evaluation of a resistance management strategy requires a very precise definition of what constitutes a good strategy.

Maintaining the appropriate balance of iron between deficiency and toxicity requires fine-tuned control of systems for iron uptake and storage. Both among fungal species and within a single species, different systems for acquisition, storage, and regulation of iron are present. Here we discuss the most recent findings on the mechanisms involved in maintaining iron homeostasis with a focus on siderophores, low-molecular-mass iron chelators, employed for iron uptake and storage. Recently siderophores have been found to be crucial for pathogenicity of animal, as well as plant-pathogenic fungi and for maintenance of plant-fungal symbioses.

Adaptation to specialized environments allows microorganisms to inhabit an enormous variety of ecological niches. Growth inside plant tissues is a niche offering a constant nutrient supply, but to access this niche, plant defense mechanisms ranging from passive barriers to induced defense reactions have to be overcome. Pathogens have to break several, if not all, of these barriers. For this purpose, they secrete effector molecules into plant cells to interfere with individual defense responses. Plant defense is organized in multiple layers, and therefore the action of effectors likely follows this same order, leading to a hierarchy in effector orchestration. In this review we summarize the latest findings regarding the level at which effectors manipulate plant immunity. Particular attention is given to those effectors whose mechanism of action is known. Additionally, we compare methods to identify and characterize effector molecules.

The yeast Saccharomyces cerevisiae is invaluable for understanding fundamental cellular processes and disease states of relevance to higher eukaryotes. Plant viruses are intracellular parasites that take advantage of resources of the host cell, and a simple eukaryotic cell, such as yeast, can provide all or most of the functions for successful plant virus replication. Thus, yeast has been used as a model to unravel the interactions of plant viruses with their hosts. Indeed, genome-wide and proteomics studies using yeast as a model host with bromoviruses and tombusviruses have facilitated the identification of replication-associated factors that affect host-virus interactions, virus pathology, virus evolution, and host range. Many of the host genes that affect the replication of the two viruses, which belong to two dissimilar virus families, are distinct, suggesting that plant viruses have developed different ways to utilize the resources of host cells. In addition, a surprisingly large number of yeast genes have been shown to affect RNA-RNA recombination in tombusviruses; this opens an opportunity to study the role of the host in virus evolution. The knowledge gained about host-virus interactions likely will lead to the development of new antiviral methods and applications in biotechnology and nanotechnology, as well as new insights into cellular functions of individual genes and the basic biology of the host cell.

Diseases caused by Xylella fastidiosa have attained great importance worldwide as the pathogen and its insect vectors have been disseminated. Since this is the first plant pathogenic bacterium for which a complete genome sequence was determined, much progress has been made in understanding the process by which it spreads within the xylem vessels of susceptible plants as well as the traits that contribute to its acquisition and transmission by sharpshooter vectors. Athough this pathogen shares many similarities with Xanthomonas species, such as its use of a small fatty acid signal molecule to coordinate virulence gene expression, the traits that it utilizes to cause disease and the manner in which they are regulated differ substantially from those of related plant pathogens. Its complex lifestyle as both a plant and insect colonist involves traits that are in conflict with these stages, thus apparently necessitating the use of a gene regulatory scheme that allows cells expressing different traits to co-occur in the plant.

Peptides and small proteins exhibiting antimicrobial activity have been isolated from many organisms ranging from insects to humans, including plants. Their role in defense is established, and their use in agriculture was already being proposed shortly after their discovery. However, some natural peptides have undesirable properties that complicate their application. Advances in peptide synthesis and high-throughput activity screening have made possible the de novo and rational design of novel peptides with improved properties. This review summarizes findings in the identification and design of short antimicrobial peptides with activity against plant pathogens, and will discuss alternatives for their heterologous production suited to plant disease control. Recent studies suggest that peptide antimicrobial action is not due solely to microbe permeation as previously described, but that more subtle factors might account for the specificity and absence of toxicity of some peptides. The elucidation of the mode of action and interaction with microbes will assist the improvement of peptide design with a view to targeting specific problems in agriculture and providing new tools for plant protection.

Plant and animal viruses overcome host antiviral silencing by encoding diverse viral suppressors of RNA silencing (VSRs). Prior to the identification and characterization of their silencing suppression activities mostly in transgene silencing assays, plant VSRs were known to enhance virus accumulation in the inoculated protoplasts, promote cell-to-cell virus movement in the inoculated leaves, facilitate the phloem-dependent long-distance virus spread, and/or intensify disease symptoms in systemically infected tissues. Here we discuss how the various silencing suppression activities of VSRs may facilitate these distinct steps during plant infection and why VSRs may not play a direct role in eliciting disease symptoms by general impairments of host endogenous small RNA pathways. We also highlight many of the key questions still to be addressed on the role of viral suppression of antiviral silencing in plant infection.

The majority of described plant viruses are transmitted by insects of the Hemipteroid assemblage that includes aphids, whiteflies, leafhoppers, planthoppers, and thrips. In this review we highlight progress made in research on vector interactions of the more than 200 plant viruses that are transmitted by hemipteroid insects beginning a few hours or days after acquisition and for up to the life of the insect, i.e., in a persistent-circulative or persistent-propagative mode. These plant viruses move through the insect vector, from the gut lumen into the hemolymph or other tissues and finally into the salivary glands, from which these viruses are introduced back into the plant host during insect feeding. The movement and/or replication of the viruses in the insect vectors require specific interactions between virus and vector components. Recent investigations have resulted in a better understanding of the replication sites and tissue tropism of several plant viruses that propagate in insect vectors. Furthermore, virus and insect proteins involved in overcoming transmission barriers in the vector have been identified for some virus-vector combinations.

In recent years, plant virus capsids, the protein shells that form the surface of a typical plant virus particle, have emerged as useful biotemplates for material synthesis. All virus capsids are assembled from virus-coded protein subunits. Many plant viruses assemble capsids with precise 3D structures providing nanoscale architectures that are highly homogeneous and can be produced in large quantities. Capsids are amenable to both genetic and chemical modifications allowing new functions to be incorporated into their structure by design. The three capsid surfaces, the interior surface, the exterior surface, or the interface between coat protein subunits, can be independently functionalized to produce multifunctional biotemplates. In this review, we examine the recent advances in using plant virus capsids as biotemplates for nanomaterials and their potential for applications in nanotechnology, especially medicine.

Motivated by questions such as “Why do some diseases take off, while others die out?” and “How can we optimize the deployment of control methods,” we introduce simple epidemiological concepts for the invasion and persistence of plant pathogens. An overarching modeling framework is then presented that can be used to analyze disease invasion and persistence at a range of scales from the microscopic to the regional. Criteria for invasion and persistence are introduced, initially for simple models of epidemics, and then for models with greater biological realism. Some ways in which epidemiological models are used to identify optimal strategies for the control of disease are discussed. Particular attention is given to the spatial structure of host populations and to the role of chance events in determining invasion and persistence of plant pathogens. Finally, three brief case studies are used to illustrate the practical applications of epidemiological theory to understand invasion and persistence of plant pathogens. These comprise long-term predictions for the persistence and control of Dutch elm disease; identification of methods to manage the spread of rhizomania on sugar beet in the U.K. by matching the scale of control with the spatial and temporal scales of the disease; and analysis of evolutionary change in virus control to identify risks of inadvertent selection for damaging virus strains.