Annual Review of Phytopathology - Volume 39, 2001

E.M. Freeman's role in early cereal disease research and the beginning of plant pathology at the University of Minnesota has been overshadowed largely by the enormous prestige of his student, E.C. Stakman. During the first decade of the twentieth century, Freeman was responsible for the transferral from Europe to the United States and the subsequent nurturing of important conceptual and technical developments in the area of cereal disease pathology. Under Freeman's leadership, these ideas would come to shape the direction of plant pathology research at the University of Minnesota for decades to follow.

Rhodococcus fascians infects a wide range of plants, initiating the formation of leafy galls that consist of centers of shoot amplification and shoot growth inhibition. R. fascians is an epiphyte but it also can establish endophytic populations. Bacterial signals involved in symptom development initiate de novo cell division and shoot meristem formation in differentiated tissues. The R. fascians signals exert activities that are distinct from mere cytokinin effects, and the evidence points to a process that adopted cytokinin biosynthetic enzymes to form derivatives with unique activity. Genes implicated in leafy gall formation are located on a linear plasmid and are subject to a highly controlling, complex regulatory network, integrating autoregulatory compounds and environmental signals. Leafy galls are considered as centers with specific metabolic features, a niche where populations of R. fascians experience a selective advantage. Such “metabolic habitat modification” might be universal for gall-inducing bacteria.

Most apomictic root-knot nematodes (RKN; Meloidogyne spp.) have host ranges that encompass the majority of flowering plants, and M. incognita is possibly the world's most damaging crop pathogen. The ancestors, age, and origins of the polyphagous RKN are obscure, but there is increasing evidence that M. incognita, M. javanica, and M. arenaria are closely related, heterogeneous species with a recent, hybrid (reticulate) origin. If so, they must owe much of their current worldwide distributions to spread by agriculture. Host resistance appears to be generally durable in the field, but laboratory studies suggest that apomixis does not prevent evolution in response to selection by a parasitic bacterium (Pasteuria penetrans) and host resistance. Maintaining general fitness may be the evolutionary priority for most populations of polyphagous RKN, and a wide host range, important in the field but not in the laboratory, may be conserved by apomixis. Several factors may help confer a wide host range, including suppression of host resistance, perhaps as a consequence of the strength of the induced susceptible response. Resistance genes effective against RKN appear not to have resulted from coevolution. Rates of juvenile invasion and/or development are low in many wild and some crop plants, with the result that they are both poor hosts and sustain less damage. Overall, it is suggested that greater coordination, particularly of fundamental research, is required.

Nineteen single dominant genes (R genes) for resistance to viruses, nematodes, and fungi have been positioned on the molecular map of potato using DNA markers. Fourteen of those genes are located in five “hotspots” for resistance in the potato genome. Quantitative trait loci (QTL) for resistance to late blight caused by the oomycete Phytophthora infestans, to tuber rot caused by the bacterium Erwinia carotovora ssp. atroseptica, and to root cyst nematodes have been identified on all 12 potato chromosomes. Some QTL for resistance to different pathogens are linked to each other and/or to resistance hotspots. Based on the genetic clustering with R genes, we propose that some QTL for resistance have a molecular basis similar to single R genes. Mapping potato genes with sequence similarity to cloned R genes of other plants and other defense-related genes reveals linkage between candidate genes, R genes, and resistance QTL. To explain the molecular basis of polygenic resistance in potato we propose (a) genes having structural similarity with cloned R genes and (b) genes involved in the defense response. The “candidate gene approach” enables the identification of markers highly useful for marker-assisted selection in potato breeding.

The controlled environment of greenhouses, the high value of the crops, and the limited number of registered fungicides offer a unique niche for the biological control of plant diseases. During the past ten years, over 80 biocontrol products have been marketed worldwide. A large percentage of these have been developed for greenhouse crops. Products to control soilborne pathogens such as Sclerotinia, Pythium, Rhizoctonia and Fusarium include Coniothyrium minitans, species of Gliocladium, Trichoderma, Streptomyces, and Bacillus, and nonpathogenic Fusarium. Products containing Trichoderma, Ampelomyces quisqualis, Bacillus, and Ulocladium are being developed to control the primary foliar diseases, Botrytis and powdery mildew. The development of Pseudomonas for the control of Pythium diseases in hydroponics and Pseudozyma flocculosa for the control of powdery mildew by two Canadian research programs is presented. In the future, biological control of diseases in greenhouses could predominate over chemical pesticides, in the same way that biological control of greenhouse insects predominates in the United Kingdom. The limitations in formulation, registration, and commercialization are discussed, along with suggested future research priorities.

The role of the professional disease diagnostician has become increasingly important in turf management. Responsible turfgrass disease diagnosis must incorporate the possibility of biotic, as well as abiotic, disorders and should consist of three components: the interview, identification of the stress factor, and a management recommendation. The concept of management groups is introduced to facilitate delivery of the rapid and effective solution required by turf managers. Recent advances in diagnostics, including immunoassay, PCR kits, and distance diagnostics, have had minimal effect on turfgrass diagnostic practices to date. However, continued emphasis on the application of technology rather than knowledge-based diagnostic procedures is contributing to the demise of applied plant pathology. Nevertheless, the demand for turfgrass disease diagnostic services continues to increase, making the future for the applied plant pathologist somewhat uncertain, but full of opportunities.

Populations of plant viruses, like all other living beings, are genetically heterogeneous, a property long recognized in plant virology. Only recently have the processes resulting in genetic variation and diversity in virus populations and genetic structure been analyzed quantitatively. The subject of this review is the analysis of genetic variation, its quantification in plant virus populations, and what factors and processes determine the genetic structure of these populations and its temporal change. The high potential for genetic variation in plant viruses, through either mutation or genetic exchange by recombination or reassortment of genomic segments, need not necessarily result in high diversity of virus populations. Selection by factors such as the interaction of the virus with host plants and vectors and random genetic drift may in fact reduce genetic diversity in populations. There is evidence that negative selection results in virus-encoded proteins being not more variable than those of their hosts and vectors. Evidence suggests that small population diversity, and genetic stability, is the rule. Populations of plant viruses often consist of a few genetic variants and many infrequent variants. Their distribution may provide evidence of a population that is undifferentiated, differentiated by factors such as location, host plant, or time, or that fluctuates randomly in composition, depending on the virus.

Host plant resistance has been used extensively for disease control in many crop species; however, the resistance conferred by many sources is not durable as a result of rapid changes in the pathogen. Although many resistance genes have been identified in plant germplasm, there is no easy way to predict the quality or durability of these resistance genes. In this review, we revisit the hypothesis that resistance genes imposing a high penalty to the pathogen for adaptation will likely be durable. By elucidating the molecular changes involved in pathogen adaptation and the associated fitness cost, a proactive approach may be developed to predict the durability of resistance genes available for deployment.

The Burkholderia cepacia complex (Bcc) consists of several species of closely related and extremely versatile gram-negative bacteria found naturally in soil, water, and the rhizosphere of plants. Strains of Bcc have been used in biological control of plant diseases and bioremediation, while some strains are plant pathogens or opportunistic pathogens of humans with cystic fibrosis. The ecological versatility of these bacteria is likely due to their unusually large genomes, which are often comprised of several (typically two or three) large replicons, as well as their ability to use a large array of compounds as sole carbon sources. The original species B. cepacia has been split into eight genetic species (genomovars), including five named species, but taxonomic distinctions have not enabled biological control strains to be clearly distinguished from human pathogenic strains. This has led to a reassessment of the risk of several strains registered by the U.S. Environmental Protection Agency for biological control. We review the biology of Bcc bacteria, especially how our growing knowledge of Bcc ecology and pathogenicity might be used in risk assessment. The capability of this bacterial complex to cause disease in plants and humans, as well as to control plant diseases, affords a rare opportunity to explore traits that may function in all three environments.

The vast evolutionary gulf between plants and animals—in terms of structure, composition, and many environmental factors—would seem to preclude the possibility that these organisms could act as receptive hosts to the same microorganism. However, some pathogens are capable of establishing themselves and thriving in members of both the plant and animal kingdoms. The identification of functionally conserved virulence mechanisms required to infect hosts of divergent evolutionary origins demonstrates the remarkable conservation in some of the underlying virulence mechanisms of pathogenesis and is changing researchers' thinking about the evolution of microbial pathogenesis.

More than 30 genes have been characterized from different plant species that provide resistance to a variety of different pathogen and pest species. The structures of most are consistent with a role in pathogen recognition and defense response signaling. Resistance genes are very abundant in plant genomes and most belong to tightly linked gene families. Evolution of R genes is driven by selection on allelic variation created by mutation and re-assorted by recombination between alleles and sometimes between different gene family members. Selection favors genes that can recognize pathogen avr gene products that are present in pathogen populations. Selection at linked gene families favors haplotypes with useful combinations of genes but a limited physiological cost to the plant. Future utilization of R genes will include transfer between related genera and identification or construction of genes that condition durable resistance to variable pathogens. Genes with durable resistance may interact with conserved pathogen elicitors or condition resistance responses that are independent of specific Avr gene interactions.

Polygalacturonase-inhibiting proteins (PGIPs) are extracellular plant proteins capable of inhibiting fungal endopolygalacturonases (PGs). Plants have evolved different PGIPs with specific recognition abilities against the many PGs produced by fungi. The genes encoding PGIPs are organized into families, and different members of each family may encode proteins with nearly identical characteristics but different specificities and regulation. PGIPs are typically induced by pathogen infection and stress-related signals. The recognition ability of PGIPs resides in their LRR (leucine-rich repeat) structure, where solvent-exposed residues in the β-strand/β-turn motifs of the LRRs are determinants of specificity. Manipulation of the primary structure of PGIPs is expected to generate more efficient PGIPs with novel recognition specificities to protect crop plants against pathogens.

The fungi are the most economically important plant pathogens and continue to be the focus of extensive research with a wide variety of methodologies. Enhancements in microscopy techniques have increased our ability to visualize the intimate interaction of fungi and their host plants. Improving methods allow pharmacological inhibition and genetic dissection of the determinants of fungal pathogenicity in a gene-by-gene approach. Identification and analysis of genes differentially transcribed in ways pertinent to pathogenicity continues to be a frequent research approach. Genome-wide analysis is gaining favor in biological research and fungal plant pathogens are no exception. Several industrial research groups are exploring fungal plant pathogenesis based on genomic sequence data and genome-wide mutagenesis. In March 2001 the first publicly available complete genome of a filamentous fungus (Neurospora crassa) was released. N. crassa is of course a saprophyte and there is no complete sequence available for a plant pathogenic fungus in public databases. However, freely accessible entire genome sequences for both plant pathogenic fungi and their hosts are on the horizon. Sequence availability promises to revolutionize the rate at which data relevant to disease processes will be accrued. In this review we describe approaches currently applied to the study of plant pathogenic fungi and explore developments of potential future benefit with existing technologies not yet applied to this group of important organisms.

Yellow rust of barley is an invasive disease that was found in the past 10 years in North America. The causal agent, Puccinia striiformis f. sp. hordei, was introduced into Colombia, South America, from Europe in 1975. It spread to all major barley-producing areas in South America by 1982. In 1988 it was found in Mexico and in 1991 in Texas. Since then it has been found in all major barley-producing areas of the American West. Originally described as race (R) 24, barley yellow rust in North America is now known to be a very heterogeneous population. Resistance has been identified, evaluated, and is being introduced into commercial malting and other barley cultivars. Cultural and chemical controls are effective and available. An integrated approach using general field resistance and other tactics is described for sustainable management of barley yellow rust.

Fungal pathogens cause many of the most serious crop diseases. One of the principal reasons for the success of this group is their ability to locate and perceive appropriate host surfaces and then to elaborate specialized infection structures. Here we review the processes implicated in surface attachment, germ tube elongation, and development of appressoria. The involvement of surface-acting proteins such as fungal hydrophobins and integrins in these processes is evaluated, along with a description of studies that have revealed the existence of conserved signaling pathways that regulate appressorium formation. Finally, we anticipate the prospect of genome-level analysis of fungal pathogens and the key research questions that will need to be addressed.

This article summarizes studies of viral coat (capsid) proteins (CPs) of RNA plant viruses. In addition, we discuss and seek to interpret the knowledge accumulated to date. CPs are named for their primary function; to encapsidate viral genomic nucleic acids. However, encapsidation is only one feature of an extremely diverse array of structural, functional, and ecological roles played during viral infection and spread. Herein, we consider the evolution of viral CPs and their multitude of interactions with factors encoded by the virus, host plant, or viral vector (biological transmission agent) that influence the infection and epidemiological facets of plant disease. In addition, applications of today's understanding of CPs in the protection of crops from viral infection and use in the manufacture of valuable compounds are considered.

Rhizosphere colonization is one of the first steps in the pathogenesis of soilborne microorganisms. It can also be crucial for the action of microbial inoculants used as biofertilizers, biopesticides, phytostimulators, and bioremediators. Pseudomonas, one of the best root colonizers, is therefore used as a model root colonizer. This review focuses on (a) the temporal-spatial description of root-colonizing bacteria as visualized by confocal laser scanning microscopal analysis of autofluorescent microorganisms, and (b) bacterial genes and traits involved in root colonization. The results show a strong parallel between traits used for the colonization of roots and of animal tissues, indicating the general importance of such a study. Finally, we identify several noteworthy areas for future research.