Annual Review of Phytopathology - Volume 36, 1998

Xanthomonas campestris pv. vesicatoria, causal agent of bacterial spot of tomato and pepper, had been considered for nearly 70 years to be a relatively homogeneous organism. However, in the past decade this bacterium was determined to be composed of two genetically and phenotypically distinct groups. The two groups, designated A and B, were distinguished based on amylolytic activity, expression of unique protein bands, reaction on differential hosts (tomato races T1 and T2), reaction patterns with monoclonal antibodies, DNA restriction profiles, and DNA:DNA hybridization. The A and B groups were placed into X. axonopodis pv. vesicatoria and X. vesicatoria, respectively. A third group, designated C, was pathogenically (race T3) and serologically distinct from A and B strains, and formed unique DNA restriction profiles. DNA:DNA hybridization data suggest that C is distinct but related to A strains and may represent a subspecies of A. A final group, designated D, consisted of X. gardneri, an organism identified in Yugoslavia in 1957, and also found in Costa Rica. Group D was determined to be genetically distinct from strains within the other two groups; it represents a third Xanthomonas species pathogenic on tomato and pepper.

A growing body of evidence indicates that elicitation of primary active defense responses results from a recognition event frequently involving protein-protein interactions. Most pathogen avirulence determinants eliciting resistance gene–dependent responses have been shown to be proteins with no apparent enzymic activity. Disruption of the tertiary and quaternary structure of these proteins abolishes their elicitor activity. Critical to their elicitor activity is their display by the pathogen. Resistance genes are proposed to function as receptors for the eliciting proteins. The most consistent feature of resistance gene products is the presence of potential protein binding domains in the form of leucine-rich repeat regions, and there is direct evidence for the physical interaction of elicitor proteins and receptor proteins in several cases. Thus in many but not all cases the primary recognition event eliciting an active defense response during incompatible interactions appears to be a protein-protein interaction occurring between a specific pathogen protein and a strategically placed receptor protein in the host cell. The interaction of elicitor protein with the receptor protein activates a signal transduction pathway leading to programmed cell death and an oxidative burst.

Over the past 70 years a destructive blight of Cupressus macrocarpa and other Cupressaceae, caused by Seiridium cardinale, has spread worldwide from California, devastating forests, plantations, and ornamental cypresses. The epidemic has been particularly severe in the Mediterranean region, on C. sempervirens. A similar destructive blight induced by Lepteutypa cupressi, which caused serious losses to Monterey cypresses in East Africa in the 1940s, has now also spread to distant continents, albeit to a lesser extent. There is yet a third wave of canker disease induced by S. unicorne, although this is a milder type.

This review deals with problems related to identification of the pathogens, their taxonomy, pathogenesis and role of fungal toxins, and early screening of cypress clones or hybrids for resistance to the pathogens and tolerance to their toxins.

In ascomycetes, the single mating type locus (MAT) controls sexual development. This locus is structurally unusual because the two alternate forms (“alleles”) are completely dissimilar sequences, encoding different transcription factors, yet they occupy the same chromosomal position. Recently developed procedures allow efficient cloning of MAT genes from a wide array of filamentous ascomycetes, thereby providing MAT-based technology for application to several ongoing issues in fungal biology. This article first outlines the basic nature of MAT genes, then addresses the following topics: efficient cloning of MAT genes; the unusual molecular characteristics of these genes; phylogenetics using MAT; the issues of why some fungi are self-sterile, others self-fertile, and yet others asexual; the long-standing mystery of possible mating type switching in filamentous fungi; and finally the evolutionary origins of pathogenic capability.

Viruses in the genus Tenuivirus (Tenuiviruses) cause a number of important diseases in economically important crop plants including rice and maize. Tenuiviruses are transmitted from plant to plant by specific planthopper vectors, and their transmission relationship is circulative-propagative. Thus, Tenuiviruses have host ranges including plants and animals (planthoppers). Four or five characteristic, circular ribonucleoprotein particles (RNPs), each containing a single Tenuivirus genomic RNA, can be isolated from Tenuivirus-infected plants. The genomic RNAs range in size from ca 9.0 kb to 1.3 kb and together give a total genome size of ca 18–19 kb. The genomic RNAs are either negative-sense or ambisense, and expression of the ambisense RNAs utilizes cap-snatching during mRNA transcription. The combination of characteristics exhibited by Tenuiviruses are quite different than those found for most plant viruses and are more similar to vertebrate-infecting viruses in the genus Phlebovirus of the Bunyaviridae.

Early researchers identified key concepts and developed tactics for multiple-option management of nematodes. Although the emphasis on integrated pest management over the past three decades has promoted strategies and tactics for nematode management, comprehensive studies on the related soil biology–ecology are relatively recent. Traditional management tactics include host resistance (where available), cultural tactics such as rotation with nonhosts, sanitation and avoidance, and destruction of residual crop roots, and the judicious use of nematicides. There have been advances in biological control of nematodes, but field-scale exploitation of this tactic remains to be realized. New technologies and resources are currently becoming central to the development of sustainable systems for nematode-pest-crop management: molecular diagnostics for nematode identification, genetic engineering for host resistance, and the elucidation and application of soil biology for general integrated cropping systems. The latter strategy includes the use of nematode-pest antagonistic cover crops, animal wastes, and limited tillage practices that favor growth-promoting rhizobacteria, earthworms, predatory mites, and other beneficial organisms while suppressing parasitic nematodes and other plant pathogens. Certain rhizobacteria may induce systemic host resistance to nematodes and, in some instances, to foliage pathogens. The systems focusing on soil biology hold great promise for sustainable crop-nematode management, but only a few research programs are currently involved in this labor-intensive endeavor.

Many plant-associated bacteria produce and utilize diffusible N-acyl-homoserine lactones (AHLs) to regulate the expression of specific bacterial genes and operons. AHL-mediated regulation utilizes two genes that encode proteins similar to the LuxI/LuxR system originally studied in the marine symbiont Vibrio fischeri. The LuxI-type proteins are AHL synthases that assemble the diffusible AHL signal. The LuxR-type proteins are AHL-responsive transcriptional regulatory proteins. LuxR proteins control the transcription of specific bacterial genes in response to the levels of AHL signal. To date, AHL-mediated gene regulation has been identified in a broad range of gram-negative bacteria, most of which are host-associated. However, it seems unlikely that such a widely conserved regulatory mechanism would be limited only to host-microbe interactions. These signals probably play central roles in ecological interactions among organisms in microbial communities by affecting communication among bacterial populations as well as between bacterial populations and their eukaryotic hosts.

Suppression of the blossom-blight phase of fire blight is a key point in the management of this destructive and increasingly important disease of apple and pear. For blossom infection to occur, the causal bacterium, Erwinia amylovora, needs to increase its population size through an epiphytic phase that occurs on stigmatic surfaces. Knowledge of the ecology of the pathogen on stigmas has been key to the development of predictive models for infection and optimal timing of antibiotic sprays. Other bacterial epiphytes also colonize stigmas where they can interact with and suppress epiphytic growth of the pathogen. A commercially available bacterial antagonist of E. amylovora (BlightBan, Pseudomonas fluorescens A506) can be included in antibiotic spray programs. Integration of bacterial antagonists with chemical methods suppresses populations of the pathogen and concomitantly, fills the ecological niche provided by the stigma with a nonpathogenic, competing microorganism. Further integration of biologically based methods with conventional management of blossom blight may be achievable by increasing the diversity of applied antagonists, by refining predictive models to incorporate antagonist use, and by gaining an improved understanding of the interactions that occur among indigenous and applied bacterial epiphytes, antibiotics, and the physical environment.

The heterothallic ascomycete, Magnaporthe grisea, is the blast pathogen of rice and about 50 other grasses, and has potential for sexual and asexual reproduction. In most populations, data from mating type, fertility assays, and genotypic diversity strongly suggest that the pathogen is asexual. However, parasexual recombination cannot be ruled out. Chromosome length polymorphisms and translocations may prevent successful meiosis in most populations. Pathogens of millets and some grasses growing with rice appear to be largely genetically isolated, though some gene flow may occur. Sexual fertility has repeatedly been reported in rice pathogens from mountainous regions of South and East Asia. Several means by which sexual fertility may be lost in an agricultural setting are advanced.

The gene Mi, which confers resistance to several species of root-knot nematode, is present in many modern tomato cultivars. Recent cloning of this gene revealed that it encodes a member of the plant resistance protein family characterized by the presence of a putative nucleotide binding site and a leucine-rich repeat. Analysis of transgenic plants revealed the unexpected result that Mi also confers resistance to potato aphids. Although highly effective in many conditions, Mi fails to confer resistance at high soil temperature, and Mi-virulent nematode isolates have been identified in many areas of the world. These findings have stimulated efforts to identify new sources of root-knot nematode resistance. Resistance genes that differ from Mi in properties and genetic position have been identified in Lycopersicon peruvianum. These genes, as well as the cloned Mi gene, provide a resource for broadening the base of root-knot nematode resistance in tomato and other crops.

Satellite tobacco mosaic virus (STMV) is a small, spherical ssRNA virus common in a natural wild plant, Nicotiana glauca or tree tobacco, in southern California and is one of the best-studied satellite viruses. It is the only satellite virus that has rod-shaped viruses (tobamoviruses) for its helper. In addition to describing the general properties of STMV, this review focuses on (a) the structural properties of the virus particle including the RNA within the particle that is partially double stranded; (b) the genetic diversity within the type strain before and after serial passage and between different field isolates; (c) the effect of experimental mutation on infectivity, replication, and symptomatology; and (d) the genetic changes that occur when the satellite virus adapts to different helper tobamoviruses.

Plants dedicate a large amount of energy to the regulated production of living cells programmed to separate from roots into the external environment. This unusual process may be worth the cost because it enables the plant to dictate which species will share its ecological niche. For example, border cells can rapidly attract and stimulate growth in some microorganisms and repel and inhibit the growth of others. Such specificity may provide a way to control the dynamics of adjacent microbial populations in the soil to foster beneficial associations and inhibit pathogenic invasion. Plant genes controlling the delivery of border cells and the expression of their unique properties provide tools to genetically engineer plants with altered border cell quality and quantity. Such variants are being used to test the hypothesis that the function of border cells is to protect plant health by controlling the ecology of the root system.

Aflatoxins are the most thoroughly studied mycotoxins. Elegant early research on the biosynthetic scheme of the pathway has allowed a molecular characterization of aflatoxin biosynthesis and its regulation. Genetic studies on aflatoxin biosynthesis in Aspergillus flavus and A. parasiticus, and sterigmatocystin biosynthesis in A. nidulans, led to the cloning of 17 genes responsible for 12 enzymatic conversions in the AF/ST pathways. Pathway-specific regulation is by a Zn(II)2Cys6 DNA-binding protein that regulates the transcription of all pathway genes. Less is known about the global factors that regulate aflatoxin biosynthesis, but there is a clear link between development and aflatoxin biosynthesis. There is also a large body of information on physiological factors involved in aflatoxin biosynthesis, but it has been difficult to understand their role in the regulation of this pathway. This chapter discusses current knowledge on the molecular biology and genetics of the pathway, and provides a summary of the physiological factors known to influence aflatoxin formation.

Among many interesting and sophisticated mechanisms used by bacterial pathogens to subvert eukaryotic hosts is a class of specialized protein secretion systems (known as type III protein secretion systems) that deliver bacterial virulence proteins directly into the host cell. Recent studies have revealed four important features of these secretion systems. First, they are widespread among plant and animal bacterial pathogens, and mutations affecting type III protein secretion often eliminate bacterial virulence completely. Second, at least eight type III secretion components share sequence similarities with those of the flagellar assembly machinery and flagellum-like structures are associated with type III secretion, raising the possibility that these secretion systems are derived from the presumably more ancient flagellar assembly apparatus. Third, type III secretion is activated in vivo upon contact with host cells. Fourth, the type III secretion mechanism is Sec-independent and the effector proteins may possess mRNA-based targeting signals. This review highlights the similarities and differences among type III secretion systems of selected model plant and animal pathogenic bacteria.

The interaction of pathogens with plants leads to a disruption in cellular homeostasis, often leading to cell death, in both compatible and incompatible relationships. The mechanistic basis of this cellular disruption and consequent death is complex and poorly characterized, but it is established that host responses to pathogens are dependent on gene expression, involve signal transduction, and require energy. Recent data suggest that in animals, a genetically regulated, signal transduction–dependent programmed cell death process, commonly referred to as apoptosis, is conserved over a wide range of phyla. The basic function of apoptosis is to direct the selective elimination of certain cells during development, but it also is a master template that is involved in host responses to many pathogens. Programmed cell death in plants, while widely observed, has not been studied extensively at either the biochemical or genetic level. Current data suggest that activation or suppression of programmed cell death may underlie diseases in plants as it does in animals. This review describes some of the fundamental characteristics of apoptosis in animals and points to a number of connections to programmed cell death in plants that may lead to both a better understanding of disease processes and novel strategies for engineering disease resistance in plants.

The papaya crop is severely affected by papaya ringspot virus (PSRV) worldwide. This review focuses on efforts to control the destructiveness of the disease caused by PSRV in Hawaii, starting from the use of cross protection to parasite-derived resistance with transgenic papaya expressing the PSRV coat protein gene. A chronology of the research effort is given and related to the development of technologies and the pressing need to control PSRV in Hawaii. The development of commercial virus-resistant transgenic papaya provides a tangible approach to control PSRV in Hawaii. Moreover, the development of transgenic papaya by other laboratories and employment of a mechanism of effective technology transfer to different countries hold promise for control of PSRV worldwide.

Root cortices remain as the last frontier for the biocontrol agents to protect the vascular elements from the invader, where the virulent pathogen has breached the bulk soil, rhizosphere, and rhizoplane. Root cortices are commonly colonized by a variety of soilborne fungi. Many nonmycorrhizal biocontrol fungi that occupy the rhizosphere appear to extend their activity into the live cells of the cortex. It has been proposed that the occupation of the cortices by biocontrol fungi introduced on seed at sowing could extend their activity in time and space. The biology and ecology of such fungi with parasitic competency to colonize live cortical cells are discussed in relation to a case study involving a sterile cortical fungus.

Nonpathogenic rhizobacteria can induce a systemic resistance in plants that is phenotypically similar to pathogen-induced systemic acquired resistance (SAR). Rhizobacteria-mediated induced systemic resistance (ISR) has been demonstrated against fungi, bacteria, and viruses in Arabidopsis, bean, carnation, cucumber, radish, tobacco, and tomato under conditions in which the inducing bacteria and the challenging pathogen remained spatially separated. Bacterial strains differ in their ability to induce resistance in different plant species, and plants show variation in the expression of ISR upon induction by specific bacterial strains. Bacterial determinants of ISR include lipopolysaccharides, siderophores, and salicylic acid (SA). Whereas some of the rhizobacteria induce resistance through the SA-dependent SAR pathway, others do not and require jasmonic acid and ethylene perception by the plant for ISR to develop. No consistent host plant alterations are associated with the induced state, but upon challenge inoculation, resistance responses are accelerated and enhanced. ISR is effective under field conditions and offers a natural mechanism for biological control of plant disease.