Showing papers in "Annual Review of Phytopathology in 2019"

Fusarium graminearum Trichothecene Mycotoxins: Biosynthesis, Regulation, and Management.

Abstract: Fusarium head blight (FHB) of small grain cereals caused by Fusarium graminearum and other Fusarium species is an economically important plant disease worldwide. Fusarium infections not only result in severe yield losses but also contaminate grain with various mycotoxins, especially deoxynivalenol (DON). With the complete genome sequencing of F. graminearum, tremendous progress has been made during the past two decades toward understanding the basis for DON biosynthesis and its regulation. Here, we summarize the current understanding of DON biosynthesis and the effect of regulators, signal transduction pathways, and epigenetic modifications on DON production and the expression of biosynthetic TRI genes. In addition, strategies for controlling FHB and DON contamination are reviewed. Further studies on these biosynthetic and regulatory systems will provide useful knowledge for developing novel management strategies to prevent FHB incidence and mycotoxin accumulation in cereals.

Resolving Fusarium: Current Status of the Genus

Abstract: The fungal genus Fusarium is one of the most important groups of plant-pathogenic fungi and affects a huge diversity of crops in all climatic zones across the globe. In addition, it is also a human pathogen and produces several extremely important mycotoxins in food products that have deleterious effects on livestock and humans. These fungi have been plagued over the past century by different perspectives of what constitutes the genus Fusarium and how many species occur within the genus. Currently, there are conflicting views on the generic boundaries and what defines a species that impact disease diagnosis, management, and biosecurity legislation. An approach to defining and identifying Fusarium that places the needs of the community of users (especially, in this case, phytopathologists) to the forefront is presented in this review.

Surviving in a Hostile World: Plant Strategies to Resist Pests and Diseases

Abstract: As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.

Molecular Dialog Between Parasitic Plants and Their Hosts.

Abstract: Parasitic plants steal sugars, water, and other nutrients from host plants through a haustorial connection. Several species of parasitic plants such as witchweeds (Striga spp.) and broomrapes (Orob...

Ecology and Evolution of the Sudden Oak Death Pathogen Phytophthora ramorum.

Abstract: The sudden oak and sudden larch death pathogen Phytophthora ramorum emerged simultaneously in the United States on oak and in Europe on Rhododendron in the 1990s. This pathogen has had a devastatin...

Activity and Phylogenetics of the Broadly Occurring Family of Microbial Nep1-Like Proteins

Abstract: Necrosis- and ethylene-inducing peptide 1 (Nep1)-like proteins (NLP) have an extremely broad taxonomic distribution; they occur in bacteria, fungi, and oomycetes. NLPs come in two forms, those that are cytotoxic to eudicot plants and those that are noncytotoxic. Cytotoxic NLPs bind to glycosyl inositol phosphoryl ceramide (GIPC) sphingolipids that are abundant in the outer leaflet of plant plasma membranes. Binding allows the NLP to become cytolytic in eudicots but not monocots. The function of noncytotoxic NLPs remains enigmatic, but the expansion of NLP genes in oomycete genomes suggests they are important. Several plant species have evolved the capacity to recognize NLPs as molecular patterns and trigger plant immunity, e.g., Arabidopsis thaliana detects nlp peptides via the receptor-like protein RLP23. In this review, we provide a historical perspective from discovery to understanding of molecular mechanisms and describe the latest developments in the NLP field to shed light on these fascinating microbial proteins.

Genome Editing, Gene Drives, and Synthetic Biology: Will They Contribute to Disease-Resistant Crops, and Who Will Benefit?

Abstract: Genetically engineered crops have been grown for more than 20 years, resulting in widespread albeit variable benefits for farmers and consumers. We review current, likely, and potential genetic eng...

Molecular Interactions Between Smut Fungi and Their Host Plants

Abstract: Smut fungi are a large group of biotrophic plant pathogens that infect mostly monocot species, including economically relevant cereal crops. For years, Ustilago maydis has stood out as the model system to study the genetics and cell biology of smut fungi as well as the pathogenic development of biotrophic plant pathogens. The identification and functional characterization of secreted effectors and their role in virulence have particularly been driven forward using the U. maydis-maize pathosystem. Today, advancing tools for additional smut fungi such as Ustilago hordei and Sporisorium reilianum, as well as an increasing number of available genome sequences, provide excellent opportunities to investigate in parallel the effector function and evolution associated with different lifestyles and host specificities. In addition, genome analyses revealed similarities in the genomic signature between pathogenic smuts and epiphytic Pseudozyma species. This review elaborates on how knowledge about fungal lifestyles, genome biology, and functional effector biology has helped in understanding the biology of this important group of fungal pathogens. We highlight the contribution of the U. maydis model system but also discuss the differences from other smut fungi, which raises the importance of comparative genomic and genetic analyses in future research.

Pathways of DNA Transfer to Plants from Agrobacterium tumefaciens and Related Bacterial Species

Abstract: Genetic transformation of host plants by Agrobacterium tumefaciens and related species represents a unique model for natural horizontal gene transfer. Almost five decades of studying the molecular interactions between Agrobacterium and its host cells have yielded countless fundamental insights into bacterial and plant biology, even though several steps of the DNA transfer process remain poorly understood. Agrobacterium spp. may utilize different pathways for transferring DNA, which likely reflects the very wide host range of Agrobacterium. Furthermore, closely related bacterial species, such as rhizobia, are able to transfer DNA to host plant cells when they are provided with Agrobacterium DNA transfer machinery and T-DNA. Homologs of Agrobacterium virulence genes are found in many bacterial genomes, but only one non-Agrobacterium bacterial strain, Rhizobium etli CFN42, harbors a complete set of virulence genes and can mediate plant genetic transformation when carrying a T-DNA-containing plasmid.

Revisiting the Concept of Host Range of Plant Pathogens.

Abstract: Strategies to manage plant disease-from use of resistant varieties to crop rotation, elimination of reservoirs, landscape planning, surveillance, quarantine, risk modeling, and anticipation of disease emergences-all rely on knowledge of pathogen host range. However, awareness of the multitude of factors that influence the outcome of plant-microorganism interactions, the spatial and temporal dynamics of these factors, and the diversity of any given pathogen makes it increasingly challenging to define simple, all-purpose rules to circumscribe the host range of a pathogen. For bacteria, fungi, oomycetes, and viruses, we illustrate that host range is often an overlapping continuum-more so than the separation of discrete pathotypes-and that host jumps are common. By setting the mechanisms of plant-pathogen interactions into the scales of contemporary land use and Earth history, we propose a framework to assess the frontiers of host range for practical applications and research on pathogen evolution.

Plant Virus Vectors 3.0: Transitioning into Synthetic Genomics.

Abstract: Plant viruses were first implemented as heterologous gene expression vectors more than three decades ago. Since then, the methodology for their use has varied, but we propose it was the merging of technologies with virology tools, which occurred in three defined steps discussed here, that has driven viral vector applications to date. The first was the advent of molecular biology and reverse genetics, which enabled the cloning and manipulation of viral genomes to express genes of interest (vectors 1.0). The second stems from the discovery of RNA silencing and the development of high-throughput sequencing technologies that allowed the convenient and widespread use of virus-induced gene silencing (vectors 2.0). Here, we briefly review the events that led to these applications, but this treatise mainly concentrates on the emerging versatility of gene-editing tools, which has enabled the emergence of virus-delivered genetic queries for functional genomics and virology (vectors 3.0).

Boxwood Blight: Threat to Ornamentals

Abstract: Boxwood blight, caused by Calonectria pseudonaviculata and Calonectria henricotiae, has had devastating effects in gardens since its first appearance in the United Kingdom in 1994. The disease affe...

Durability of Quantitative Resistance in Crops: Greater Than We Know?

Abstract: Quantitative resistance (QR) to crop diseases has usually been much more durable than major-gene, effector-triggered resistance. It has been observed that the effectiveness of some QR has eroded as pathogens adapt to it, especially when deployment is extensive and epidemics occur regularly, but it generally declines more slowly than effector-triggered resistance. Changes in aggressiveness and specificity of diverse pathogens on cultivars with QR have been recorded, along with experimental data on fitness costs of pathogen adaptation to QR, but there is little information about molecular mechanisms of adaptation. Some QR has correlated or antagonistic effects on multiple diseases. Longitudinal data on cultivars' disease ratings in trials over several years can be used to assess the significance of QR for durable resistance in crops. It is argued that published data likely underreport the durability of QR, owing to publication bias. The implications of research on QR for plant breeding are discussed.

A Decade Decoded: Spies and Hackers in the History of TAL Effectors Research

Abstract: Transcription activator-like effectors (TALEs) from the genus Xanthomonas are proteins with the remarkable ability to directly bind the promoters of genes in the plant host to induce their expression, which often helps bacterial colonization. Metaphorically, TALEs act as spies that infiltrate the plant disguised as high-ranking civilians (transcription factors) to trick the plant into activating weak points that allow an invasion. Current knowledge of how TALEs operate allows researchers to predict their activity (counterespionage) and exploit their function, engineering them to do our bidding (a Manchurian agent). This has been possible thanks particularly to the discovery of their DNA binding mechanism, which obeys specific amino acid-DNA correspondences (the TALE code). Here, we review the history of how researchers discovered the way these proteins work and what has changed in the ten years since the discovery of the code. Recommended music for reading this review can be found in the Supplemental Material.

Paving the Way to Tospovirus Infection: Multilined Interplays with Plant Innate Immunity.

Abstract: Tospoviruses are among the most important plant pathogens and cause serious crop losses worldwide. Tospoviruses have evolved to smartly utilize the host cellular machinery to accomplish their life cycle. Plants mount two layers of defense to combat their invasion. The first one involves the activation of an antiviral RNA interference (RNAi) defense response. However, tospoviruses encode an RNA silencing suppressor that enables them to counteract antiviral RNAi. To further combat viral invasion, plants also employ intracellular innate immune receptors (e.g., Sw-5b and Tsw) to recognize different viral effectors (e.g., NSm and NSs). This leads to the triggering of a much more robust defense against tospoviruses called effector-triggered immunity (ETI). Tospoviruses have further evolved their effectors and can break Sw-5b-/Tsw-mediated resistance. The arms race between tospoviruses and both layers of innate immunity drives the coevolution of host defense and viral genes involved in counter defense. In this review, a state-of-the-art overview is presented on the tospoviral life cycle and the multilined interplays between tospoviruses and the distinct layers of defense.

Never Walk Alone: Clathrin-Coated Vesicle (CCV) Components in Plant Immunity

Abstract: At the host-pathogen interface, the protein composition of the plasma membrane (PM) has important implications for how a plant cell perceives and responds to invading microbial pathogens. A plant's ability to modulate its PM composition is critical for regulating the strength, duration, and integration of immune responses. One mechanism by which plant cells reprogram their cell surface is vesicular trafficking, including secretion and endocytosis. These trafficking processes add or remove cargo proteins (such as pattern-recognition receptors, transporters, and other proteins with immune functions) to or from the PM via small, membrane-bound vesicles. Clathrin-coated vesicles (CCVs) that form at the PM and trans-Golgi network/early endosomes have emerged as the prominent vesicle type in the regulation of plant immune responses. In this review, we discuss the roles of the CCV core, adaptors, and accessory components in plant defense signaling and immunity against various microbial pathogens.

Mangroves in the Leaves: Anatomy, Physiology, and Immunity of Epithemal Hydathodes.

Abstract: Hydathodes are organs found on aerial parts of a wide range of plant species that provide almost direct access for several pathogenic microbes to the plant vascular system. Hydathodes are better known as the site of guttation, which is the release of droplets of plant apoplastic fluid to the outer leaf surface. Because these organs are only described through sporadic allusions in the literature, this review aims to provide a comprehensive view of hydathode development, physiology, and immunity by compiling a historic and contemporary bibliography. In particular, we refine the definition of hydathodes.We illustrate their important roles in the maintenance of plant osmotic balance, nutrient retrieval, and exclusion of deleterious chemicals from the xylem sap. Finally, we present our current understanding of the infection of hydathodes by adapted vascular pathogens and the associated plant immune responses.

Interactions and Coadaptation in Plant Metaorganisms

Abstract: Plants associate with a wide diversity of microorganisms. Some microorganisms engage in intimate associations with the plant host, collectively forming a metaorganism. Such close coexistence with plants requires specific adaptations that allow microorganisms to overcome plant defenses and inhabit plant tissues during growth and reproduction. New data suggest that the plant immune system has a broader role beyond pathogen recognition and also plays an important role in the community assembly of the associated microorganism. We propose that core microorganisms undergo coadaptation with their plant host, notably in response to the plant immune system allowing them to persist and propagate in their host. Microorganisms, which are vertically transmitted from generation to generation via plant seeds, putatively compose highly adapted species and may have plant-beneficial functions. The extent to which plant domestication has impacted the underlying genetics of plant-microbe associations remains poorly understood. We propose that the ability of domesticated plants to select and maintain advantageous microbial partners may have been affected. In this review, we discuss factors that impact plant metaorganism assembly and function. We underline the importance of microbe-microbe interactions in plant tissues, as they are still poorly studied but may have a great impact on plant health.

The Evolution, Ecology, and Mechanisms of Infection by Gram-Positive, Plant-Associated Bacteria

Abstract: Gram-positive bacteria are prominent members of plant-associated microbial communities. Although many are hypothesized to be beneficial, some are causative agents of economically important diseases...

Understanding Adaptation, Coevolution, Host Specialization, and Mating System in Castrating Anther-Smut Fungi by Combining Population and Comparative Genomics.

Abstract: Anther-smut fungi provide a powerful system to study host-pathogen specialization and coevolution, with hundreds of Microbotryum species specialized on diverse Caryophyllaceae plants, castrating their hosts through manipulation of the hosts' reproductive organs to facilitate disease transmission. Microbotryum fungi have exceptional genomic characteristics, including dimorphic mating-type chromosomes, that make this genus anexcellent model for studying the evolution of mating systems and their influence on population genetics structure and adaptive potential. Important insights into adaptation, coevolution, host specialization, and mating system evolution have been gained using anther-smut fungi, with new insights made possible by the recent advent of genomic approaches. We illustrate with Microbotryum case studies how using a combination of comparative genomics, population genomics, and transcriptomics approaches enables the integration of different evolutionary perspectives across different timescales. We also highlight current challenges and suggest future studies that will contribute to advancing our understanding of the mechanisms underlying adaptive processes in populations of fungal pathogens.

Current Status of Potato Cyst Nematodes in North America.

Abstract: The potato cyst nematodes (PCNs) Globodera rostochiensis and Globodera pallida are internationally recognized quarantine pests. Although not widely distributed in either the United States or Canada, both are present and are regulated by the national plant protection organizations (NPPOs) of each country. G. rostochiensis was first discovered in New York in the 1940s, and G. pallida was first detected in a limited area of Idaho in 2006. In Canada, G. rostochiensis and G. pallida were first detected in Newfoundland in 1962 and 1977, respectively, and further detections of G. rostochiensis occurred in British Columbia and Quebec, most recently in 2006. Adherence to a stringent NPPO-agreed-upon phytosanitary program has prevented the spread of PCNs to other potato-growing areas in both countries. The successful research and regulatory PCN programs in both countries rely on a network of state, federal, university, and private industry cooperatorspursuing a common goal of containment, management/eradication, and regulation. The regulatory and research efforts of these collaborative groups spanning from the 1940s to the present are highlighted in this review.

Stealth Pathogens: The Sooty Blotch and Flyspeck Fungal Complex.

Abstract: Sooty blotch and flyspeck (SBFS) fungi produce superficial, dark-colored colonies on fruits, stems, and leaves of many plant genera. These blemishes are economically damaging on fruit, primarily ap...

Lessons from a Life in Time and Space.

Abstract: A research career investigating epidemiological and evolutionary patterns in both natural and crop host-pathogen systems emphasizes the need for flexibility in thinking and a willingness to adopt ideas from a wide diversity of subdisciplines. Here, I reflect on the pivotal issues, research areas, and interactions, including the role of science management, that shaped my career in the hope of demonstrating that career paths and collaborations in science can be as diverse and unpredictable as the natural world in which we study our organisms of choice.