Annual Review of Phytopathology - Volume 38, 2000

Cornelius Lott Shear was one of the most influential plant pathologists of the early twentieth century. He was first and foremost an excellent mycologist who did pioneering research on pathogenic fungi and, as a senior pathologist with the USDA's Bureau of Plant Industry, studied important crop diseases and offered useful control measures. Shear's successful research enhanced his reputation among his fellow pathologists and allowed him to embark on what was perhaps his most significant contribution to plant pathology, his pivotal role in the creation of the American Phytopathological Society in 1908. Shear felt that an independent society dedicated to the unique needs of plant pathologists would facilitate communication and cooperation among practitioners. Between his scientific research and his role in the creation of APS, Shear stands out for the enormous impact he had on his science.

The twentieth century has been productive for the science of plant pathology and the field of host-parasite interactions—both in understanding how pathogens and plant defense work and in developing more effective means of disease control. Early in the twentieth century, plant pathology adopted a philosophy that encouraged basic scientific investigation of pathogens and disease defense. That philosophy led to the strategy of developing disease-resistant plants as a prima facie disease-control measure—and in the process saved billions of dollars and avoided the use of tons of pesticides. Plant pathology rapidly adopted molecular cloning and its spin-off technologies, and these have fueled major advances in our basic understanding of plant diseases. This knowledge and the development of efficient technologies for producing transgenic plants convey optimism that plant diseases will be more efficiently controlled in the twenty-first century.

Interest in the rust fungi derives from their success as plant pathogens. For example, the epidemic on coffee had serious economic and social impacts on diverse cultures. During the century, research on the rust germling shifted from a study of germling development, including a search for the signals that induce differentiation, to an examination of the genes expressed during host colonization. Research on host resistance was most influenced by Stakman, who studied the genetics and epidemiology of rust disease. His innovations enabled Flor to propose the gene-for-gene hypothesis, a concept that stimulated development of resistant crops, and led to research that gradually shifted during the century to an examination of the molecular basis of rust genetics.

During the twentieth century disease detectives progressed by jagged leaps in understanding patterns of plant disease. With ladders, airplanes, and automatic traps they observed airborne spores, and with meteorological theory they explained takeoff, flight, and landing. They analyzed the grand, logistic rise of epidemics and the roles of horizontal versus vertical resistance. From early experiments on the details of life cycles and weather, they simulated epidemics with new computers. Early in the century they revealed genetic diversity with differential varieties and late in the century with differential fungicides and DNA. They learned the interplay of pest, photosynthesis, and supply and demand to reckon loss. Integrating observations of pest, host, losses, and weather, they placed winning short-term bets for farmer and environment on whether to spray. In the twenty-first century, their goal can be analyses so sound that the world can securely place winning long-term bets.

Plant health management is the science and practice of understanding and overcoming the succession of biotic and abiotic factors that limit plants from achieving their full genetic potential as crops, ornamentals, timber trees, or other uses. Although practiced as long as agriculture itself, as a science-based concept, plant heath management is even younger than integrated pest management (IPM), and includes and builds upon but is not a replacement for IPM. Probably the greatest collection of success stories for plant health management is the number of diseases managed by cleaning up the planting material. The record for root health management is more mixed, with the loss or phase-out of soil fumigants, and practices such as crop rotation and clean tillage being replaced with more intensive cropping and less or no tillage. Perhaps the greatest scientific and technical advances for plant health management have come from the work aimed at management of the pathogens, pests, and other hazards that arrive by air. Flor's work on flax rust, which produced the gene-for-gene model, is possibly the most significant contribution of plant pathology to the life sciences in the twentieth century. Research aimed at the management of foliar pathogens is also the basis for modern theory on epidemiology, population biology, aerobiology, and disease prediction and decision-support systems. Even IPM arose mainly in response to the need to protect crops from pests that arrive by air. If the definition of biological control includes the plant induced or genetically modified to defend itself, as it should, then biological control has been the most significant approach to plant health management during the twentieth century and promises through modern biotechnology to be even more significant in the twenty-first century. Rather than “reducing losses,” the advances are discussed here within the simple framework of achieving the attainable yield by increasing the actual and/or affordable and hence the average yield. Each of these four benchmark yields, as well as the absolute yield for crops, and their significance to the goals and achievements of plant health management are defined. Plant health management is a moving target, which I discuss metaphorically like an American football game, where one team is science and technology and the other is nature, where the S & T team is only beginning to know nature's rules while playing itself with the three sets of rules written to, respectively, satisfy the laws of economics, protect the environment, and gain social acceptance.

Plant viruses have had an impact on the science of virology and on plant pathology ever since the virus concept was discovered with Tobacco mosaic virus at the end of the nineteenth century. In this review, we highlight those discoveries. We have divided plant virus research into a “Classical Discovery Period” from 1883–1951 in which the findings were very descriptive; an “Early Molecular Era” from 1952 to about 1983, in which information was developed that described further properties of the viruses, aided by the development of a number of salient techniques; and the “Recent Period” from 1983 to the present, when techniques have been developed to modify plant virus genomes, to detect nonstructural gene products, to determine the functions of viral gene products, and to transform plants to elicit novel forms of resistance to viral diseases. In this period, plant virology has played a significant role in formulating an understanding of the mechanisms of gene silencing and recombination, plasmodesmatal function, systemic acquired resistance, and in developing methods for pathogen detection. We also attempt to predict the direction plant virology will take in the future.

The vast surface of the plant axis, stretching from root tips occasionally buried deeply in anoxic sediment, to apical meristems held far aloft, provides an extraordinarily diverse habitat for microorganisms. Each zone has to a greater or lesser extent its own cohort of microorganisms, in aggregate comprising representatives from all three primary domains of life—Bacteria, Archaea, and Eucarya. While the plant sets the stage for its microbial inhabitants, they, in turn, have established varied relationships with their large partner. These associations range from relatively inconsequential (transient epiphytic saprophytes) to substantial (epiphytic commensals, mutualistic symbionts, endophytes, or pathogens). Through recent technological breakthroughs, a much better perspective is beginning to emerge on the nature of these relationships, but still relatively little is known about the role of epiphytic microbial associations in the life of the plant.

Several economically important diseases of unknown or recently determined cause are reviewed. Citrus blight (CB), first described over 100 years ago, was shown in 1984 to be transmitted by root-graft inoculations; the cause remains unknown and is controversial. Based on graft transmission, it is considered to be an infectious agent by some; others suggest that the cause of CB is abiotic. Citrus variegated chlorosis, although probably long present in Argentina, where it was considered to be a variant of CB, was identified as a specific disease and shown to be caused by a strain of Xylella fastidiosa after if reached epidemic levels in Brazil in 1987. Citrus psorosis, described in 1933 as the first virus disease of citrus, is perhaps one of the last to be characterized. In 1988, it was shown to be caused by a very unusual virus. The cause of lettuce big vein appears to be a viruslike agent that is transmitted by a soilborne fungus. Double-stranded RNAs were associated with the disease, suggesting it may be caused by an unidentified RNA virus. Rio Grande gummosis, dry rot root, peach tree short life, and some replant diseases may be diseases of complex etiology. Various microorganisms have been isolated from trees with these diseases, but the diseases may be attributable in part to environmental factors. Determination of the cause of these diseases of complex etiology has proven difficult, in part, because they affect only mature trees.

Detection and diagnosis of plant viruses has included serological laboratory tests since the 1960s. Relatively little work was done on serological detection of plant pathogenic bacteria and fungi prior to the development of ELISA and monoclonal antibody technologies. Most applications for laboratory-based tests were directed at virus detection with relatively little emphasis on fungal and bacterial pathogens, though there was some good work done with other groups of plant pathogens. With the advent of molecular biology and the ability to compare regions of genomic DNA representing conserved sequences, the development of laboratory tests increased at an amazing rate for all groups of plant pathogens. Comparison of ITS regions of bacteria, fungi, and nematodes has proven useful for taxonomic purposes. Sequencing of conserved genes has been used to develop PCR-based detection with varying levels of specificity for viruses, fungi, and bacteria. Combinations of ELISA and PCR technologies are used to improve sensitivity of detection and to avoid problems with inhibitors or PCR often found in plants. The application of these technologies in plant pathology has greatly improved our ability to detect plant pathogens and is increasing our understanding of, their ecology and epidemiology.

Lipopolysaccharides (LPSs) are ubiquitous, indispensable components of the cell surface of Gram-negative bacteria that apparently have diverse roles in bacterial pathogenesis of plants. As an outer membrane component, LPS may contribute to the exclusion of plant-derived antimicrobial compounds promoting the ability of a bacterial plant pathogen to infect plants. In contrast, LPS can be recognized by plants to directly trigger some plant defense-related responses. LPS can also alter the response of plants to subsequent bacterial inoculation; these delayed effects include alterations in the expression patterns of genes coding for some pathogenesis-related (PR) proteins, promotion of the synthesis of antimicrobial hydroxycinnamoyl-tyramine conjugates, and prevention of the hypersensitive reaction caused by avirulent bacteria. Prevention of the response may allow expression of resistance in the absence of catastrophic tissue damage. Recognition of LPS (and other nonspecific determinants) may initiate responses in plants that restrict the growth of nonpathogenic bacteria, whereas plant pathogens may possess hrp gene-dependent mechanisms to suppress such responses.

Ralstonia solanacearum causes a lethal bacterial wilt disease of diverse plants. It invades the xylem vessels of roots and disseminates into the stem where it multiplies and wilts by excessive exopolysaccharide production. Many of its key extracytoplasmic virulence and pathogenicity factors are transcriptionally controlled by an extensive network of distinct, interacting signal transduction pathways. The core of this sensory network is the five-gene Phc system that regulates exopolysaccharide, cell-wall-degrading exoenzymes, and other factors in response to a self-produced signal molecule that monitors the pathogen's growth status and environment. Four additional environmentally responsive two-component systems work independently and with the Phc system to fine-tune virulence gene expression. Another critical system is Prh which transduces plant cell-derived signals through a six-gene cascade to activate deployment of the Type III secretion pathway encoded by the hrp pathogenicity genes. Here I summarize knowledge about the regulated targets, signal transduction mechanisms, and crosstalk between Phc, Prh, and other systems. I also provide insight into why R. solanacearum has evolved such a sophisticated sensory apparatus, and how it functions in disease.

The family Closteroviridae comprises more than 30 plant viruses with flexuous, filamentous virions and includes representatives with either mono- or bipartite positive-strand ssRNA genomes. Closteroviruses are transmitted semipersistently by insects from three families of Homoptera, in infected plants are associated with phloem tissue, and demonstrate an astonishing genetic diversity that suggests extensive, on-going evolution. Phylogenetic analyses of their replicative genes as well as the conserved HSP70 demonstrate that closteroviruses co-evolved with their insect vectors, resulting in three major lineages, i.e. aphid-, mealybug-, and whitefly-transmitted viruses. Closteroviruses apparently represent an ancient and diverse virus family that may pose threats to agriculture and needs serious attention.

Although evidence for horizontal gene transfer (HGT) in eukaryotes remains largely anecdotal, literature on HGT in fungi suggests that it may have been more important in the evolution of fungi than in other eukaryotes. Still, HGT in fungi has not been widely accepted because the mechanisms by which it may occur are unknown, because it is usually not directly observed but rather implied as an outcome, and because there are often equally plausible alternative explanations. Despite these reservations, HGT has been justifiably invoked for a variety of sequences including plasmids, introns, transposons, genes, gene clusters, and even whole chromosomes. In some instances HGT has also been confirmed under experimental conditions. It is this ability to address the phenomenon in an experimental setting that makes fungi well suited as model systems in which to study the mechanisms and consequences of HGT in eukaryotic organisms.

The ability of nematodes to live on plant hosts involves multiple parasitism genes. The most pronounced morphological adaptations of nematodes for plant parasitism include a hollow, protrusible stylet (feeding spear) connected to three enlarged esophageal gland cells that express products that are secreted into plant tissues through the stylet. Reverse genetic and expressed sequence tag (EST) approaches are being used to discover the parasitism genes expressed in nematode esophageal gland cells. Some genes cloned from root-knot (Meloidogyne spp.) and cyst (Heterodera and Globodera spp.) nematodes have homologues reported in genomic analyses of Caenorhabditis elegans and animal-parasitic nematodes. To date, however, the candidate parasitism genes endogenous to the esophageal glands of plant nematodes (such as the ß-1,4-endoglucanases) have their greatest similarity to microbial genes, prompting speculation that genes for plant parasitism by nematodes may have been acquired by horizontal gene transfer.

The unique coenocytic anatomy of the mycelia of the filamentous fungi and the formation of anastomoses between hyphae from different mycelia enable the intracellular accumulation and infectious transmission of plasmids and mutant mitochondrial DNAs (mtDNAs) that cause senescence. For reasons that are not fully apparent, mitochondria that are rendered dysfunctional by so-called “suppressive” mtDNA mutations proliferate rapidly in growing cells and gradually displace organelles that contain wild-type mtDNA molecules and are functional. The consequence of this process is senescence and death if the suppressive mtDNA contains a lethal mutation. Suppressive mtDNA mutations and mitochondrial plasmids can elicit cytoplasmically transmissible “mitochondrial hypovirulence” syndromes in at least some of the phytopathogenic fungi. In the chestnut-blight fungus Cryphonectria parasitica, the pattern of asexual transmission of mutant mtDNAs and mitochondrial plasmids resembles the pattern of “infectious” transmission displayed by the attenuating virus that is most commonly used for the biological control of this fungus. At least some of the attenuating mitochondrial hypovirulence factors are inherited maternally in crosses, whereas the viruses are not transmitted sexually. The natural control of blight in an isolated stand of chestnut trees has resulted from the invasion of the local population of C. parasitica by a senescence-inducing mutant mtDNA. Moreover, a mitochondrial plasmid, pCRY1, attenuates at least some virulent strains of C. parasitica, suggesting that such factors could be applied to control plant diseases caused by fungi.

A range of specialist and generalist microorganisms in the rhizosphere attacks plant-parasitic nematodes. Plants have a profound effect on the impact of this microflora on the regulation of nematode populations by influencing both the dynamics of the nematode host and the structure and dynamics of the community of antagonists and parasites in the rhizosphere. In general, those organisms that have a saprophytic phase in their life cycle are most affected by environmental conditions in the rhizosphere, but effects on obligate parasites have also been recorded. Although nematodes influence the colonization of roots by pathogenic and beneficial microorganisms, little is known of such interactions with the natural enemies of nematodes in the rhizosphere. As nematodes influence the quantity and quality of root exudates, they are likely to affect the physiology of those microorganisms in the rhizosphere; such changes may be used as signals for nematode antagonists and parasites. Successful biological control strategies will depend on a thorough understanding of these interactions at the population, organismal, and molecular scale.

All plant-microbe interactions are initiated at the level of the cell. Recently, the light microscope has increased in popularity as an investigative tool in plant cell biology, in part because of the parallel developments of confocal laser scanning and video microscopy, computerized image processing, and an ever-increasing array of fluorescent probes that can be applied to living cells. In addition, transgenic plants and cells can be generated in which specific components are fluorescently labeled without any invasive experimental manipulation. The application of such techniques to plant-microbe interactions has revealed microbe-induced changes in cytosolic calcium levels, the visualization of reactive oxygen species generation, cytoskeleton rearrangements, DNA cleavage, and the detailed resolution of intercellular and intracellular trafficking of viral components. These techniques, integrated with electron microscopy, molecular genetics, and other types of investigations, are likely to play an increasingly important role in future studies of plant responses to microbial pathogens or mutualists.

Plant pathogenic fungi in eight genera produce light-activated perylenequinone toxins that are toxic to plants via the generation of activated oxygen species, particularly singlet oxygen. Studies on the cercosporin toxin produced by Cercospora species have documented an important role for this toxin in pathogenesis of host plants. Cercosporin-generated active oxygen species destroy the membranes of host plants, providing nutrients to support the growth of these intercellular pathogens. Resistance of Cercospora species to the toxic effects of their own toxin has allowed these organisms to be used as a model for understanding the cellular basis of resistance to singlet oxygen and to general oxidative stress. In particular, the recent discovery that pyridoxine (vitamin B6) quenches singlet oxygen has led to the understanding of a novel role for this vitamin in cells as well as the discovery of a novel pathway of biosynthesis.

Wheat (Triticum aestivum L) is grown throughout the grasslands from southern Mexico into the prairie provinces of Canada, a distance of nearly 4200 km. The total area seeded to wheat varies considerably each year; however, from 28 to 32 million ha are planted in the Great Plains of the United States alone. Generally in the central Great Plains, an area from central Texas through central Nebraska, 15 million ha are seeded to winter wheat each year. A wide range of environmental conditions exist throughout this area that may affect the development and final severity of wheat leaf rust (caused by Puccinia triticina L), stripe rust (caused by P. striiformis), and stem rust (caused by P. graminis Pers. f. sp tritici) epidemics and the subsequent reduction in wheat yields. Variation in severity of rust epidemics in this area depends on differences in crop maturity at the time of infection by primary inoculum, host resistance used, and environmental conditions. The interrelationships among time, host, pathogen and environment are complex, and studying the interactions is very difficult. Historically, cultivars with new or different leaf rust resistance genes become ineffective after several years of large-scale production within the Great Plains, and then cultivars carrying new or different resistance genes must be developed and released into production. This is the typical “boom and bust” cycle of the cereal rust resistance genes in the central Great Plains.