Annual Review of Phytopathology - Volume 45, 2007

My job at Pullman, Washington, starting in 1965, was to control the root diseases of wheat and barley, focusing first on fusarium root and crown rot, then including take-all and pythium and rhizoctonia root rots. In the absence of viable alternatives, the agronomic approaches used were implemented through design of cereal-based cropping systems. Starting in the late 1970s, the mission focused further on cereal-intensive direct-seed (no-till) cropping systems. A team effort demonstrated the role of indigenous antibiotic-producing fluorescent pseudomonads in the widespread decline of take-all in response to monoculture wheat (or barley-wheat sequences). Today, the suppression of take-all by these beneficial rhizobacteria is the centerpiece of an integrated system that augments take-all decline while limiting pythium and rhizoctonia root rots and fusarium root and crown rot in direct-seed systems. In such systems, “crop rotation” takes the form of different sequences of winter and spring wheat, barley and triticale varieties, and market classes, all susceptible to all four root diseases.

Noel T. Keen (1940–2002) made pioneering contributions to molecular plant pathology during a period when the study of disease mechanisms was transformed by the new tools of molecular genetics. His primary contributions involved race-specific elicitors of plant defenses and bacterial pectic enzymes. In collaboration with Brian J. Staskawicz and Frances Jurnak, respectively, Noel cloned the first avirulence gene and determined that pectate lyase C possessed a novel structural motif, known as the parallel β-helix. Noel received his B.S. and M.S. from Iowa State University in Ames and his Ph.D. from the Department of Plant Pathology at the University of Wisconsin in Madison in 1968. He joined the faculty of the Department of Plant Pathology at the University of California at Riverside the same year and remained there his entire career. He served as Chair of the department from 1983 to 1989 and in 1997 assumed the William and Sue Johnson Endowed Chair in Molecular Plant Pathology. He became a Fellow of the American Phytopathological Society in 1991, a Fellow of the American Association for the Advancement of Science in 1996, a Fellow of the American Academy of Microbiology in 1997, and a member of the National Academy of Sciences in 1997. He was serving as President of the American Phytopathological Society (2001–2002) at the time of his death.

Gene-for-gene resistance in plants is based on the presence of a resistance (R) gene in the host and a matching Avirulence (Avr) gene in the pathogen. Many R genes have been cloned over the past two decades, mostly from the Solanaceae. The gene products, called R proteins, display modular domain structures. R protein function has recently been shown to require dynamic interactions between the various domains. In addition to these intramolecular interactions, R proteins interact with other proteins to form signaling complexes that are able to activate an innate immune response that arrests proliferation of the invading pathogen, thereby conferring disease resistance. In this review, we summarize current understanding of R protein structure and function, as well as the molecular mechanisms underlying the activation of defense signaling processes. As well as being a rich source for R genes, Solanaceae are a leading model system in which to study inter- and intramolecular interactions of R proteins.

The plant virus family Flexiviridae includes the definitive genera Potexvirus, Mandarivirus, Allexivirus, Carlavirus, Foveavirus, Capillovirus, Vitivirus, Trichovirus, the putative genus Citrivirus, and some unassigned species. Its establishment was based on similarities in virion morphology, common features in genome type and organization, and strong phylogenetic relationships between replicational and structural proteins. In this review, we provide a brief account of the main biological and molecular properties of the members of the family, with special emphasis on the relationships within and among the genera. In phylogenetic analyses the potexvirus-like replicases were more closely related to tymoviruses than to carlaviruses. We postulate a common evolutionary ancestor for the family Tymoviridae and the two distinct evolutionary clusters of the Flexiviridae, i.e., a plant virus with a polyadenylated genome, filamentous virions, and a triple gene block of movement proteins. Subsequent recombination and gene loss would then have generated a very diverse group of plant and fungal viruses.

The plant cuticle and cell wall separate microbial pathogens from the products of plant metabolism. While microbial pathogens try to breach these barriers for colonization, plants respond to attempted penetration by a battery of wall-associated defense reactions. Successful pathogens circumvent or suppress plant nonself recognition and basal defense during penetration and during microbial reproduction. Additionally, accommodation of fungal infection structures within intact cells requires host reprogramming. Recent data highlight that both early plant defense to fungal penetration and host reprogramming for susceptibility can function at the host cell periphery. Genetic evidence has also widened our understanding of how fungal pathogens are restricted during penetration at the plant cell wall. This review summarizes the current view of how plants monitor and model their cell periphery during interaction with microbial invaders.

Plasmids are common residents of phytopathogenic bacteria and contribute significantly to host evolution in a multi-faceted manner. Plasmids tend to encode determinants of virulence and ecological fitness that can enhance adaptation to a specific niche or can influence niche expansion. Many of these determinants appear to have been acquired from other bacteria via horizontal transfer, illustrating an important function of plasmids in the acquisition of sequences that enable rapid evolution. These genes can ultimately be delivered to the host chromosome through plasmid integration events, thus stabilizing important acquired determinants within the genome. Most plasmids characterized in phytopathogenic bacteria are self-transmissible and possess suites of genes encoding type IV secretion systems. In addition, the phytopathogenic bacterial plasmid “mobilome” includes insertion sequence and other transposable elements that contribute to the movement of sequences within and between genomes. Possession of mosaic and ever-changing plasmids allows phytopathogenic bacteria to maintain a dynamic, flexible genome and possible advantage in host-pathogen and other environmental interactions that belies the concept of plasmids as apparently selfish genetic elements.

Suppressive soils hold considerable potential for managing soilborne pathogens. When the suppressiveness has a biological origin, identifying the causal organisms is the crucial step in realizing this potential. Armed with such knowledge, it may be possible to develop effective and sustainable pest management strategies through application of these organisms or agronomic practices that influence their population densities. This chapter focuses on the development and utilization of a population-based approach for identifying microorganisms involved in specific pathogen suppression. Key experimental design principles of the approach are explored by examining experiments characterizing the biological nature of take-all decline. We also describe how this approach was used to identify microorganisms that suppress the sugarbeet cyst nematode. Additional experimental design considerations and future directions for such investigations are also discussed.

Potential safety issues have been raised with the development and release of virus-resistant transgenic plants. This review focuses on safety assessment with a special emphasis on crops that have been commercialized or extensively tested in the field such as squash, papaya, plum, grape, and sugar beet. We discuss topics commonly perceived to be of concern to the environment and to human health—heteroencapsidation, recombination, synergism, gene flow, impact on nontarget organisms, and food safety in terms of allergenicity. The wealth of field observations and experimental data is critically evaluated to draw inferences on the most relevant issues. We also express inside views on the safety and benefits of virus-resistant transgenic plants, and recommend realistic risk assessment approaches to assist their timely deregulation and release.

Plant disease cycles represent pathogen biology as a series of interconnected stages of development including dormancy, reproduction, dispersal, and pathogenesis. The progression through these stages is determined by a continuous sequence of interactions among host, pathogen, and environment. The stages of the disease cycle form the basis of many plant disease prediction models. The relationship of temperature and moisture to disease development and pathogen reproduction serve as the basis for most contemporary plant disease prediction systems. Pathogen dormancy and inoculum dispersal are considered less frequently. We found extensive research efforts evaluating the performance of prediction models as part of operation disease management systems. These efforts appear to be greater than just a few decades ago, and include novel applications of Bayesian decision theory. Advances in information technology have stimulated innovations in model application. This trend must accelerate to provide the disease management strategies needed to maintain global food supplies.

Virus infections are the cause of numerous plant disease syndromes that are generally characterized by the induction of disease symptoms such as developmental abnormalities, chlorosis, and necrosis. How viruses induce these disease symptoms represents a long-standing question in plant pathology. Recent studies indicate that symptoms are derived from specific interactions between virus and host components. Many of these interactions have been found to contribute to the successful completion of the virus life-cycle, although the role of other interactions in the infection process is not yet known. However, all share the potential to disrupt host physiology. From this information we are beginning to decipher the progression of events that lead from specific virus-host interactions to the establishment of disease symptoms. This review highlights our progress in understanding the mechanisms through which virus-host interactions affect host physiology. The emerging picture is one of complexity involving the individual effects of multiple virus-host interactions.

The use of phages for disease control is a fast expanding area of plant protection with great potential to replace the chemical control measures now prevalent. Phages can be used effectively as part of integrated disease management strategies. The relative ease of preparing phage treatments and low cost of production of these agents make them good candidates for widespread use in developing countries as well. However, the efficacy of phages, as is true of many biological control agents, depends greatly on prevailing environmental factors as well as on susceptibility of the target organism. Great care is necessary during development, production and application of phage treatments. In addition, constant monitoring for the emergence of resistant bacterial strains is essential. Phage-based disease control management is a dynamic process with a need for continuous adjustment of the phage preparation in order to effectively fight potentially adapting pathogenic bacteria.

The reniform nematode, Rotylenchulus reniformis, is an emerging problem in U.S. cotton. The impact of this nematode and the extent to which it has and will continue to spread across the U.S. cotton belt are controversial. Long-term changes in cotton production and unique biological attributes of R. reniformis are key factors. Expert opinion surveys indicate that R. reniformis has replaced the root-knot nematode (Meloidogyne incognita) as the major nematode of cotton in Mississippi, Louisiana, and Alabama. In neighboring states the incidence of heavily infested fields has increased during the past 10 years. Estimated annual loss to the U.S. cotton crop is $130M. Crop rotation and nematicides can reduce losses. Introgression of genetic resistance from primitive accessions of other cotton species offers the most promising opportunity to effectively control this pathogen in the long term. Laboratories in several institutions are currently pursuing this goal, with the promise of resistant cultivars adapted to U.S. cotton production regions within three years.

Genetic studies of the flax-flax rust interaction led to the formulation of the gene-for-gene hypothesis and identified resistance genes (R) in the host plant and pathogenicity genes, including avirulence (Avr) and inhibitor of avirulence genes (I), in the rust pathogen. R genes have now been cloned from four of the five loci in flax and all encode proteins of the Toll, Interleukin-1 receptor, R gene-nucleotide binding site-leucine-rich repeat (TIR-NBS-LRR) class. Avr genes have been cloned from four loci in flax rust and encode small secreted proteins with no between locus similarity and no close homologs in current data bases. It is postulated that Avr proteins enter the host cell, have virulence effector functions, and in resistant host genotypes, are recognized by direct and specific interaction with host R proteins, leading to activation of rust resistance defense responses. Direct interaction between R and Avr proteins is the basis of gene-for-gene specificity in the flax-flax rust system and both R and Avr genes have the signatures of diversifying selection, suggesting the existence of a coevolutionary arms race between the host plant and its obligate rust pathogen.

Many factors affect the development and application of diagnostic techniques. Plant viruses are an inherently diverse group that, unlike cellular pathogens, possess no nucleotide sequence type (e.g., ribosomal RNA sequences) in common. Detection of plant viruses is becoming more challenging as globalization of trade, particularly in ornamentals, and the potential effects of climate change enhance the movement of viruses and their vectors, transforming the diagnostic landscape. Techniques for assessing seed, other propagation materials and field samples for the presence of specific viruses include biological indexing, electron microscopy, antibody-based detection, including enzyme-linked immunosorbent assay (ELISA), polymerase chain reaction (PCR), and microarray detection. Of these, microarray detection provides the greatest capability for parallel yet specific testing, and can be used to detect individual, or combinations of viruses and, using current approaches, to do so with a sensitivity comparable to ELISA. Methods based on PCR provide the greatest sensitivity among the listed techniques but are limited in parallel detection capability even in “multiplexed” applications. Various aspects of microarray technology, including probe development, array fabrication, assay target preparation, hybridization, washing, scanning, and interpretation are presented and discussed, for both current and developing technology.

Using genomic technologies, it is now possible to address research hypotheses in the context of entire developmental or biochemical pathways, gene networks, and chromosomal location of relevant genes and their inferred evolutionary history. Through a range of platforms, researchers can survey an entire transcriptome under a variety of experimental and field conditions. Interpretation of such data has led to new insights and revealed previously undescribed phenomena. In the area of plant-pathogen interactions, transcript profiling has provided unparalleled perception into the mechanisms underlying gene-for-gene resistance and basal defense, host vs nonhost resistance, biotrophy vs necrotrophy, and pathogenicity of vascular vs nonvascular pathogens, among many others. In this way, genomic technologies have facilitated a system-wide approach to unifying themes and unique features in the interactions of hosts and pathogens.

Although seed production has been moved to semiarid regions to escape seedborne pathogens, seedborne bacterial diseases continue to be problematic and cause significant economic losses worldwide. Infested seeds are responsible for the re-emergence of diseases of the past, movement of pathogens across international borders, or the introduction of diseases into new areas. Considerable attention has been paid to improving the sensitivity and selectivity of seed health assays by using techniques such as flow cytometry and the polymerase chain reaction. There has also been progress in understanding infection thresholds and how they influence seed sample size determination and ultimately the reliability of seed health testing. Disease development and dissemination of pathogens from contaminated seedlots can be predicted using formulas that take into account inoculum density and environmental pressures. In general, seeds infested with bacterial pathogens are distributed within a Poisson distribution. In a subset of contaminated seeds, bacteria are distributed in non-Gaussian distributions, e.g., a lognormal distribution.

The plant basal immune system can detect broadly present microbe-associated molecular patterns (MAMPs, also called PAMPs) and induce defenses, but adapted microbes express a suite of effector proteins that often act to suppress these defenses. Plants have evolved other receptors (R proteins) that detect these pathogen effectors and activate strong defenses. Pathogens can subsequently alter or delete their recognized effectors to avoid defense elicitation, at risk of a fitness cost associated with loss of those effectors. Significant research progress is revealing, among other things, mechanisms of MAMP perception, the host defense processes and specific host proteins that pathogen effectors target, the mechanisms of R protein activation, and the ways in which pathogen effector suites and R genes evolve. These findings carry practical ramifications for resistance durability and for future resistance engineering. The present review uses numerous questions to help clarify what we know and to identify areas that are ripe for further investigation.

The rice blast pathosystem has been the subject of intense interest in part because of the importance of the disease to world agriculture, but also because both Magnaporthe oryzae and its host are amenable to advanced experimental approaches. The goal of this review is to provide an overview of the system and to point out recent significant studies that update our understanding of the biology of M. orzyae. The genome sequence of M. oryzae has provided insight into how genome structure and pathogen population genetic variability has been shaped by transposable elements. The sequence allows systematic approaches to long-standing areas of investigation, including pathogen development and the molecular basis of compatible and incompatible interactions with its host. Rice blast provides an integrated system to illustrate most of the important concepts governing fungal/plant interactions and serves as an excellent starting point for gaining a broad perspective of issues in plant pathology.

A major challenge facing agricultural scientists today is the need to secure food for an increasing world population. This growth occurs predominantly in developing, mostly tropical countries, where the majority of hungry people live. Reducing yield losses caused by pathogens of tropical agricultural crops is one measure that can contribute to increased food production. Although plant-parasitic nematodes are often not as important as some other biotic and nonbiotic constraints on crop production in the tropics, they can nevertheless cause extensive damage and substantial yield losses. The effects of agricultural, environmental, socioeconomic, and policy changes on the occurrence of plant-parasitic nematodes in the tropics and the losses these pathogens cause are largely undocumented. Recent developments pose new challenges to tropical nematology. The increased application of molecular diagnostics may widen the knowledge gap between nematologists working in developed countries and in the tropics. Uncertainties concerning the validity of nematode species will lead to practical problems related to quarantine measures and nematode management. The study of interactions between nematodes and other pathogens in disease complexes provide opportunities for multidisciplinary research with scientists from other disciplines but remain underexploited. Difficulties in recognizing emerging nematode threats prevent the timely implementation of management strategies, thus increasing yield losses. Research is needed to address these challenges. Examples are presented mainly but not exclusively from banana, peanut, and rice nematology.