Annual Review of Phytopathology - Volume 47, 2009

In this article, I recount how I became a plant pathologist and used clues derived from light and electron microscopy to direct my research on the interactions between plants and biotrophic fungi. Examples of the value of microscopic examination are described for investigations of host compatibility, the hypersensitive response, nonhost resistance, and the evolution of host-parasite specificity.

Emerging, re-emerging and endemic plant pathogens continue to challege our ability to safeguard plant health worldwide. Further, globalization, climate change, increased human mobility, and pathogen and vector evolution have combined to increase the spread of invasive plant pathogens. Early and accurate diagnoses and pathogen surveillance on local, regional, and global scales are necessary to predict outbreaks and allow time for development and application of mitigation strategies. Plant disease diagnostic networks have developed worldwide to address the problems of efficient and effective disease diagnosis and pathogen detection, engendering cooperation of institutions and experts within countries and across national borders. Networking maximizes impact in the face of shrinking government investments in agriculture and diminishing human resource capacity in diagnostics and applied pathology. New technologies promise to improve the speed and accuracy of disease diagnostics and pathogen detection. Widespread adoption of standard operating procedures and diagnostic laboratory accreditation serve to build trust and confidence among institutions. Case studies of national, regional, and international diagnostic networks are presented.

The genus Verticillium encompasses phytopathogenic species that cause vascular wilts of plants. In this review, we focus on Verticillium dahliae, placing emphasis on the controversy surrounding the elevation of a long-spored variant as a new species, recent advances in the analysis of compatible and incompatible interactions, highlighted by the use of strains expressing fluorescent proteins, and the genetic diversity among Verticillium spp. A synthesis of the approaches to explore genetic diversity, gene flow, and the potential for cryptic recombination is provided. Control of Verticillium wilt has relied on a panoply of chemical and nonchemical strategies, but is beset with environmental or site-specific efficacy problems. Host resistance remains the most logical choice, but is unavailable in most crops. The genetic basis of resistance to Verticillium wilt is unknown in most crops, as are the subcellular signaling mechanisms associated with Ve-mediated, race-specific resistance. Increased understanding in each of these areas promises to facilitate management of Verticillium wilts across a broad range of crops.

A fundamental issue in biology is the question of how bacteria initiate and maintain pathogenic relationships with eukaryotic hosts. Despite billions of years of coexistence, far less is known about bacterial/fungal interactions than the equivalent associations formed by either of these types of microorganisms with higher eukaryotes. This review highlights recent research advances in the field of bacterial/fungal interactions, and provides examples of the various forms such interactions may assume, ranging from simple antagonism and parasitism to more intimate associations of pathogenesis and endosymbiosis. Information derived from the associations of bacteria and fungi in the context of natural and agronomic ecosystems is emphasized, including interactions observed from biological control systems, endosymbiotic relationships, diseases of cultivated mushrooms, and model systems that expand our understanding of human disease. The benefits of studying these systems at the molecular level are also emphasized.

Research on the pathogen components involved in Fusarium head blight (FHB) along with the effects of their interactions on disease development and mycotoxin accumulation is reviewed. The fungal components within the FHB complex differ significantly in different environments. Individual species may respond differently to, and be differentially influenced by, particular disease control measures. Almost all published co-inoculation studies on wheat spikes or grains show that competitive interactions among FHB pathogens are the rule when fungal/disease development is considered. However, the fungi with the competitive advantage do not usually gain any advantage from the presence of other weaker competing fungi. Total mycotoxin production in mixed inoculations may decrease, increase, or remain unchanged compared with single-isolate inoculations, depending on the fungal species concerned and environmental conditions. A few recent studies, where each individual fungal component was quantified using molecular methods, suggest that mycotoxin productivity in mixed inoculations generally increases.

Viroids are single-stranded, circular, and noncoding RNAs that infect plants. They replicate in the nucleus or chloroplast and then traffic cell-to-cell through plasmodesmata and long distance through the phloem to establish systemic infection. They also cause diseases in certain hosts. All functions are mediated directly by the viroid RNA genome or genome-derived RNAs. I summarize recent advances in the understanding of viroid structures and cellular factors enabling these functions, emphasizing conceptual developments, major knowledge gaps, and future directions. Newly emerging experimental systems and research tools are discussed that are expected to enable significant progress in a number of key areas. I highlight examples of groundbreaking contributions of viroid research to the development of new biological principles and offer perspectives on using viroid models to continue advancing some frontiers of life science.

Pantoea agglomerans, a widespread epiphyte and commensal bacterium, has evolved into an Hrp-dependent and host-specific tumorigenic pathogen by acquiring a plasmid containing a pathogenicity island (PAI). The PAI was evolved on an iteron plasmid of the IncN family, which is distributed among genetically diverse populations of P. agglomerans. The structure of the PAI supports the premise of a recently evolved pathogen. This review offers insight into a unique model for emergence of new bacterial pathogens. It illustrates how horizontal gene transfer was the major driving force in the creation of the PAI, although a pathoadaptive mechanism might also be involved. It describes the crucial function of plant-produced indole-3-acetic acid (IAA) and cytokinines (CK) in gall initiation as opposed to the significant but secondary role of pathogen-secreted phytohormones. It also unveils the role of type III effectors in determination of host specificity and evolution of the pathogen into pathovars. Finally, it describes how interactions between the quorum sensing system, hrp regulatory genes, and bacterially secreted IAA or CKs affect gall formation and epiphytic fitness.

Fatty acids (FAs) consist of long hydrophobic, often unbranched chains of hydrocarbons, with hydrophilic carboxylic acid groups at one end. They are an important source of reserve energy and essential components of membrane lipids in all living organisms. In plants, FA metabolic pathways play significant roles in pathogen defense. Historically, FAs were only assigned passive roles in plant defense such as biosynthetic precursors for cuticular components or the phytohormone jasmonic acid. However, recent discoveries demonstrate more direct roles for FAs and their breakdown products in inducing various modes of plant defenses. Both 16- and 18-carbon FAs participate in defense to modulate basal, effector-triggered, and systemic immunity in plants. Studies of FA metabolic mutants also reveal an active signaling role for the cuticle in plant defense. This review summarizes the current knowledge of the involvement of FAs, FA-derived oxylipins, and enzymes catalyzing FA metabolism in plant defense.

For more than 200 years, the plant hormone salicylic acid (SA) has been studied for its medicinal use in humans. However, its extensive signaling role in plants, particularly in defense against pathogens, has only become evident during the past 20 years. This review surveys how SA in plants regulates both local disease resistance mechanisms, including host cell death and defense gene expression, and systemic acquired resistance (SAR). Genetic studies reveal an increasingly complex network of proteins required for SA-mediated defense signaling, and this process is amplified by several regulatory feedback loops. The interaction between the SA signaling pathway and those regulated by other plant hormones and/or defense signals is also discussed.

Plant nematology is currently undergoing a revolution with the availability of the first genome sequences as well as comprehensive expressed sequence tag (EST) libraries from a range of nematode species. Several strategies are being used to exploit this wealth of information. Comparative genomics is being used to explore the acquisition of novel genes associated with parasitic lifestyles. Functional analyses of nematode genes are moving toward larger scale studies including global transcriptome profiling. RNA interference (RNAi) has been shown to reduce expression of a range of plant parasitic nematode genes and is a powerful tool for functional analysis of nematode genes. RNAi-mediated suppression of genes essential for nematode development, survival, or parasitism is revealing new targets for nematode control. Plant nematology in the genomics era is now facing the challenge to develop RNAi screens adequate for high-throughput functional analyses.

It is accepted that most fungal avirulence genes encode virulence factors that are called effectors. Most fungal effectors are secreted, cysteine-rich proteins, and a role in virulence has been shown for a few of them, including Avr2 and Avr4 of Cladosporium fulvum, which inhibit plant cysteine proteases and protect chitin in fungal cell walls against plant chitinases, respectively. In resistant plants, effectors are directly or indirectly recognized by cognate resistance proteins that reside either inside the plant cell or on plasma membranes. Several secreted effectors function inside the host cell, but the uptake mechanism is not yet known. Variation observed among fungal effectors shows two types of selection that appear to relate to whether they interact directly or indirectly with their cognate resistance proteins. Direct interactions seem to favor point mutations in effector genes, leading to amino acid substitutions, whereas indirect interactions seem to favor jettison of effector genes.

Both hypersensitive and quantitative forms of resistance to the bacterial spot pathogens (Xanthomonas spp.) occur in pepper and tomato. Five resistance genes involved in hypersensitivity in pepper and four in tomato have been identified so far. The corresponding pathogen avirulence genes have been cloned and characterized, and features, including a propensity for accumulating mutations and at times, loss of plasmid-borne avirulence genes, are known to occur. The frequency of these changes affects race composition among pathogen populations and determines the durability of the corresponding plant resistance. At least four different species of Xanthomonas are known to cause bacterial spot, and these can differ in specific avirulence gene content. Quantitative or multigenic resistance has also more recently been researched and appears to be more durable than the hypersensitive resistance. Two recessive genes have been identified that yield a nonhypersensitive form of resistance in pepper and together can provide strong resistance. More emphasis is being given to transfer of quantitative trait resistance to commercial cultivars of both tomato and pepper.

Seed pathology involves the study and management of diseases affecting seed production and utilization, as well as disease management practices applied to seeds. In this paper, three aspects of seed pathology are discussed: research innovations in detection of seedborne pathogens and elucidation of their epidemiology; advances in development and use of seed treatments; and progress toward standardization of phytosanitary regulations and seed health testing methods. The application of nucleic-acid based detection methods in seed health testing has been facilitated by integrating conventional or real-time PCR with other technologies (e.g., BIO-PCR, IMS-PCR, MCH-PCR). PCR-based methods and pathogen marker technologies are being applied to epidemiological research on seedborne pathogens, e.g., seed transmission mechanisms, the influence of external biotic and abiotic factors on seed transmission, and tracking progress of seed-transmitted pathogens. Seed treatment use is discussed in terms of the revolutionary expansion in seed-applied insecticide use, impacts of new fungicide active ingredients, and the effects of some seed treatments on crop physiology. International seed trade has been affected significantly by changing phytosanitary regulations, not always based on science. Efforts are underway to revise phytosanitary regulations to reflect pest risk analysis outcomes and to develop standards for seed health testing methods that facilitate safe and efficient international trade in seeds.

Species of migratory plant endoparasitic nematodes of three nematode families, Pratylenchidae, Anguinidae, and Aphelenchoididae, show marked variation in life cycles and fascinating contrasts in host-parasite interactions. The necessity for survival for periods in the absence of a host has resulted in some remarkable behavioral and physiological adaptations, especially in relation to anhydrobiotic survival. Many species are of major economic importance, and interactions with other pathogens enhance crop damage and yield loss. No single management strategy for endoparasitic nematodes is possible because control options have to be tailored to the nematode species, crop type, location, and economic returns. In this review, we focus on the contrast in life cycles and the wide spectrum of adaptations to obligate parasitism of most species of plant endoparasitic nematodes and examine how these aspects impinge on management options.

Plant-parasitic nematodes are the most destructive group of plant pathogens worldwide and are extremely challenging to control. The recent completion of two root-knot nematode genomes opens the way for a comparative genomics approach to elucidate the success of these parasites. Sequencing revealed that Meloidogyne hapla, a diploid that reproduces by facultative, meiotic parthenogenesis, encodes approximately 14,200 genes in a compact, 54 Mpb genome. Indeed, this is the smallest metazoan genome completed to date. By contrast, the 86 Mbp Meloidogyne incognita genome encodes approximately 19,200 genes. This species reproduces by obligate mitotic parthenogenesis and exhibits a complex pattern of aneuploidy. The genome includes triplicated regions and contains allelic pairs with exceptionally high degrees of sequence divergence, presumably reflecting adaptations to the strictly asexual reproductive mode. Both root-knot nematode genomes have compacted gene families compared with the free-living nematode Caenorhabditis elegans, and both encode large suites of enzymes that uniquely target the host plant. Acquisition of these genes, apparently via horizontal gene transfer, and their subsequent expansion and diversification point to the evolutionary history of these parasites. It also suggests new routes to their control.

Mycoviruses are widespread in all major groups of plant pathogenic fungi. They are transmitted intracellularly during cell division, sporogenesis, and cell fusion, but apparently lack an extracellular route for infection. Their natural host ranges are limited to individuals within the same or closely related vegetative compatibility groups. Recent advances, however, allowed the establishment of experimental host ranges for a few mycoviruses. Although the majority of known mycoviruses have dsRNA genomes that are packaged in isometric particles, an increasing number of usually unencapsidated mycoviruses with positive-strand RNA genomes have been reported. We discuss selected mycoviruses that cause debilitating diseases and/or reduce the virulence of their phytopathogenic fungal hosts. Such fungal-virus systems are valuable for the development of novel biocontol strategies and for gaining an insight into the molecular basis of fungal virulence. The availability of viral and host genome sequences and of transformation and transfection protocols for some plant pathogenic fungi will contribute to progress in fungal virology.

The last Hordeivirus review appearing in this series 20 years ago focused on the comparative biology, relationships, and genome organization of members of the genus (68). Prior to the 1989 review, useful findings about the origin, disease occurrence, host ranges, and general biological properties of Barley stripe mosaic virus (BSMV) were summarized in three comprehensive reviews (26, 67, 107). Several recent reviews emphasizing contemporary molecular genetic findings also may be of interest to various readers (15, 37, 42, 69, 70, 88, 113). In the current review, we briefly reiterate the biological properties of the four members of the Hordeivirus genus and describe advances in our understanding of organization and expression of the viral genomes. We also discuss the infection processes and pathogenesis of the most extensively characterized Hordeiviruses and frame these advances in the broader context of viruses in other families that have encoded triple gene block proteins. In addition, an overview of recent advances in the use of BSMV for virus-induced gene silencing is presented.

The Ustilago maydis–maize pathosystem has emerged as the current model for plant pathogenic basidiomycetes and as one of the few models for a true biotrophic interaction that persists throughout fungal development inside the host plant. This is based on the highly advanced genetic system for both the pathogen and its host, the ability to propagate U. maydis in axenic culture, and its unique capacity to induce prominent disease symptoms (tumors) on all aerial parts of maize within less than a week. The corn smut pathogen, though economically not threatening, will continue to serve as a model for related obligate biotrophic fungi such as the rusts, but also for closely related smut species that induce symptoms only in the flower organs of their hosts. In this review we describe the most prominent features of the U. maydis–maize pathosystem as well as genes and pathways most relevant to disease. We highlight recent developments that place this system at the forefront of understanding the function of secreted effectors in eukaryotic pathogens and describe the expected spin-offs for closely related species exploiting comparative genomics approaches.