Showing papers in "Annual Review of Phytopathology in 2014"

Induced systemic resistance by beneficial microbes

Abstract: Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth–promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.

Plant Cell Wall–Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi

Abstract: Approximately a tenth of all described fungal species can cause diseases in plants. A common feature of this process is the necessity to pass through the plant cell wall, an important barrier against pathogen attack. To this end, fungi possess a diverse array of secreted enzymes to depolymerize the main structural polysaccharide components of the plant cell wall, i.e., cellulose, hemicellulose, and pectin. Recent advances in genomic and systems-level studies have begun to unravel this diversity and have pinpointed cell wall-degrading enzyme (CWDE) families that are specifically present or enhanced in plant-pathogenic fungi. In this review, we discuss differences between the CWDE arsenal of plant-pathogenic and non-plant-pathogenic fungi, highlight the importance of individual enzyme families for pathogenesis, illustrate the secretory pathway that transports CWDEs out of the fungal cell, and report the transcriptional regulation of expression of CWDE genes in both saprophytic and phytopathogenic fungi.

Susceptibility genes 101: how to be a good host.

Abstract: To confer resistance against pathogens and pests in plants, typically dominant resistance genes are deployed. However, because resistance is based on recognition of a single pathogen-derived molecular pattern, these narrow-spectrum genes are usually readily overcome. Disease arises from a compatible interaction between plant and pathogen. Hence, altering a plant gene that critically facilitates compatibility could provide a more broad-spectrum and durable type of resistance. Here, such susceptibility (S) genes are reviewed with a focus on the mechanisms underlying loss of compatibility. We distinguish three groups of S genes acting during different stages of infection: early pathogen establishment, modulation of host defenses, and pathogen sustenance. The many examples reviewed here show that S genes have the potential to be used in resistance breeding. However, because S genes have a function other than being a compatibility factor for the pathogen, the side effects caused by their mutation demands a one...

Novel insights into rice innate immunity against bacterial and fungal pathogens.

Abstract: Rice feeds more than half of the world's population. Rice blast, caused by the fungal pathogen Magnaporthe oryzae, and bacterial blight, caused by the bacterial pathogen Xanthomonas oryzae pv. oryzae, are major constraints to rice production worldwide. Genome sequencing and extensive molecular analysis has led to the identification of many new pathogen-associated molecular patterns (PAMPs) and avirulence and virulence effectors in both pathogens, as well as effector targets and receptors in the rice host. Characterization of these effectors, host targets, and resistance genes has provided new insight into innate immunity in plants. Some of the new findings, such as the binding activity of X. oryzae transcriptional activator–like (TAL) effectors to specific rice genomic sequences, are being used for the development of effective disease control methods and genome modification tools. This review summarizes the recent progress toward understanding the recognition and signaling events that govern rice innate i...

New Insights into Mycoviruses and Exploration for the Biological Control of Crop Fungal Diseases

Abstract: Mycoviruses are viruses that infect fungi. A growing number of novel mycoviruses have expanded our knowledge of virology, particularly in taxonomy, ecology, and evolution. Recent progress in the study of mycoviruses has comprehensively improved our understanding of the properties of mycoviruses and has strengthened our confidence to explore hypovirulence-associated mycoviruses that control crop diseases. In this review, the advantages of using hypovirulence-associated mycoviruses to control crop diseases are discussed, and, as an example, the potential for Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1) to control the stem rot of rapeseed (Brassica napus) is also introduced. Fungal vegetative incompatibility is likely to be the key factor that limits the wide utilization of mycoviruses to control crop diseases; however, there are suggested strategies for resolving this problem.

Predisposition in Plant Disease: Exploiting the Nexus in Abiotic and Biotic Stress Perception and Response

Abstract: Predisposition results from abiotic stresses occurring prior to infection that affect susceptibility of plants to disease The environment is seldom optimal for plant growth, and even mild, episodic stresses can predispose plants to inoculum levels they would otherwise resist Plant responses that are adaptive in the short term may conflict with those for resisting pathogens Abiotic and biotic stress responses are coordinated by complex signaling networks involving phytohormones and reactive oxygen species (ROS) Abscisic acid (ABA) is a global regulator in stress response networks and an important phytohormone in plant-microbe interactions with systemic effects on resistance and susceptibility However, extensive cross talk occurs among all the phytohormones during stress events, and the challenge is discerning those interactions that most influence disease Identifying convergent points in the stress response circuitry is critically important in terms of understanding the fundamental biology that under

Small RNAs: A New Paradigm in Plant-Microbe Interactions

Abstract: A never-ending arms race drives coevolution between pathogens and hosts. In plants, pathogen attacks invoke multiple layers of host immune responses. Many pathogens deliver effector proteins into host cells to suppress host immunity, and many plants have evolved resistance proteins to recognize effectors and trigger robust resistance. Here, we discuss findings on noncoding small RNAs (sRNAs) from plants and pathogens, which regulate host immunity and pathogen virulence. Recent discoveries have unveiled the role of noncoding sRNAs from eukaryotic pathogens and bacteria in pathogenicity in both plant and animal hosts. The discovery of fungal sRNAs that are delivered into host cells to suppress plant immunity added sRNAs to the list of pathogen effectors. Similar to protein effector genes, many of these sRNAs are generated from transposable element (TE) regions, which are likely to contribute to rapidly evolving virulence and host adaptation. We also discuss RNA silencing that occurs between organisms.

Protein Kinases in Plant-Pathogenic Fungi: Conserved Regulators of Infection

Abstract: Phytopathogenic fungi have evolved an amazing diversity of infection modes and nutritional strategies, yet the signaling pathways that govern pathogenicity are remarkably conserved. Protein kinases (PKs) catalyze the reversible phosphorylation of proteins, regulating a variety of cellular processes. Here, we present an overview of our current understanding of the different classes of PKs that contribute to fungal pathogenicity on plants and of the mechanisms that regulate and coordinate PK activity during infection-related development. In addition to the well-studied PK modules, such as MAPK (mitogen-activated protein kinase) and cAMP (cyclic adenosine monophosphate)-PKA (protein kinase A) cascades, we also discuss new PK pathways that have emerged in recent years as key players of pathogenic development and disease. Understanding how conserved PK signaling networks have been recruited during the evolution of fungal pathogenicity not only advances our knowledge of the highly elaborate infection process bu...

The activation and suppression of plant innate immunity by parasitic nematodes.

Abstract: Plant-parasitic nematodes engage in prolonged and intimate relationships with their host plants, often involving complex alterations in host cell morphology and function. It is puzzling how nematodes can achieve this, seemingly without activating the innate immune system of their hosts. Secretions released by infective juvenile nematodes are thought to be crucial for host invasion, for nematode migration inside plants, and for feeding on host cells. In the past, much of the research focused on the manipulation of developmental pathways in host plants by plant-parasitic nematodes. However, recent findings demonstrate that plant-parasitic nematodes also deliver effectors into the apoplast and cytoplasm of host cells to suppress plant defense responses. In this review, we describe the current insights in the molecular and cellular mechanisms underlying the activation and suppression of host innate immunity by plant-parasitic nematodes along seven critical evolutionary and developmental transitions in plant parasitism.

Governing Principles Can Guide Fungicide-Resistance Management Tactics

Abstract: Fungicide-resistance management would be more effective if principles governing the selection of resistant strains could be determined and validated. Such principles could then be used to predict whether a proposed change to a fungicide application program would decrease selection for resistant strains. In this review, we assess a governing principle that appears to have good predictive power. The principle states that reducing the product of the selection coefficient (defined as the difference between the per capita rate of increase of the sensitive and resistant strains) and the exposure time of the pathogen to the fungicide reduces the selection for resistance. We show that observations as well as modeling studies agree with the predicted effect (i.e., that a specific change to a fungicide program increased or decreased selection or was broadly neutral in its effect on selection) in 84% of the cases and that only 5% of the experimental results contradict predictions. We argue that the selection coefficient and exposure time principle can guide the development of resistance management tactics.

Horizontal Gene Transfer in Eukaryotic Plant Pathogens

Abstract: Gene transfer has been identified as a prevalent and pervasive phenomenon and an important source of genomic innovation in bacteria. The role of gene transfer in microbial eukaryotes seems to be of a reduced magnitude but in some cases can drive important evolutionary innovations, such as new functions that underpin the colonization of different niches. The aim of this review is to summarize published cases that support the hypothesis that horizontal gene transfer (HGT) has played a role in the evolution of phytopathogenic traits in fungi and oomycetes. Our survey of the literature identifies 46 proposed cases of transfer of genes that have a putative or experimentally demonstrable phytopathogenic function. When considering the life-cycle steps through which a pathogen must progress, the majority of the HGTs identified are associated with invading, degrading, and manipulating the host. Taken together, these data suggest HGT has played a role in shaping how fungi and oomycetes colonize plant hosts.

Plant-Parasitic Nematode Infections in Rice: Molecular and Cellular Insights

Abstract: Being one of the major staple foods in the world, and an interesting model monocot plant, rice (Oryza sativa L.) has recently received attention from molecular nematologists studying the cellular and molecular aspects of the interaction between this crop and plant-parasitic nematodes. In this review, we highlight recent advances in this field, with a focus on the best-studied root-knot nematodes. Histological studies have revealed the cellular changes inside root-knot nematode-induced feeding sites, both in the compatible interaction with Oryza sativa and the incompatible interaction with the related species Oryza glaberrima. After comparing the published data from transcriptome analyses, mutant studies, and exogenous hormone applications, we provide a comprehensive model showing the role and interaction of plant hormone pathways in defense of this monocot crop against root nematodes, where jasmonate seems to play a key role. Finally, recent evidence indicates that effectors secreted from rice-infecting nematodes can suppress plant defense.

Localizing Viruses in Their Insect Vectors

Abstract: The mechanisms and impacts of the transmission of plant viruses by insect vectors have been studied for more than a century. The virus route within the insect vector is amply documented in many cases, but the identity, the biochemical properties, and the structure of the actual molecules (or molecule domains) ensuring compatibility between them remain obscure. Increased efforts are required both to identify receptors of plant viruses at various sites in the vector body and to design competing compounds capable of hindering transmission. Recent trends in the field are opening questions on the diversity and sophistication of viral adaptations that optimize transmission, from the manipulation of plants and vectors ultimately increasing the chances of acquisition and inoculation, to specific “sensing” of the vector by the virus while still in the host plant and the subsequent transition to a transmission-enhanced state.

Altering the Cell Wall and Its Impact on Plant Disease: From Forage to Bioenergy

Abstract: The individual sugars found within the major classes of plant cell wall polymers are dietary components of herbivores and are targeted for release in industrial processes for fermentation to liquid biofuels. With a growing understanding of the biosynthesis of the complex cell wall polymers, genetic modification strategies are being developed to target the cell wall to improve the digestibility of forage crops and to render lignocellulose less recalcitrant for bioprocessing. This raises concerns as to whether altering cell wall properties to improve biomass processing traits may inadvertently make plants more susceptible to diseases and pests. Here, we review the impacts of cell wall modification on plant defense, as assessed from studies in model plants utilizing mutants or transgenic modification and in crop plants specifically engineered for improved biomass or bioenergy traits. Such studies reveal that cell wall modifications can indeed have unintended impacts on plant defense, but these are not always negative.

The Role of Trees in Agroecology and Sustainable Agriculture in the Tropics

Abstract: Shifting agriculture in the tropics has been replaced by sedentary smallholder farming on a few hectares of degraded land. To address low yields and low income both, the soil fertility, the agroecosystem functions, and the source of income can be restored by diversification with nitrogen-fixing trees and the cultivation of indigenous tree species that produce nutritious and marketable products. Biodiversity conservation studies indicate that mature cash crop systems, such as cacao and coffee with shade trees, provide wildlife habitat that supports natural predators, which, in turn, reduce the numbers of herbivores and pathogens. This review offers suggestions on how to examine these agroecological processes in more detail for the most effective rehabilitation of degraded land. Evidence from agroforestry indicates that in this way, productive and environmentally friendly farming systems that provide food and nutritional security, as well as poverty alleviation, can be achieved in harmony with wildlife.

The ABCs and 123s of Bacterial Secretion Systems in Plant Pathogenesis

Abstract: Bacteria have many export and secretion systems that translocate cargo into and across biological membranes. Seven secretion systems contribute to pathogenicity by translocating proteinaceous cargos that can be released into the extracellular milieu or directly into recipient cells. In this review, we describe these secretion systems and how their complexities and functions reflect differences in the destinations, states, functions, and sizes of the translocated cargos as well as the architecture of the bacterial cell envelope. We examine the secretion systems from the perspective of pathogenic bacteria that proliferate within plant tissues and highlight examples of translocated proteins that contribute to the infection and disease of plant hosts.

Harnessing Population Genomics to Understand How Bacterial Pathogens Emerge, Adapt to Crop Hosts, and Disseminate

Abstract: Crop diseases emerge without warning. In many cases, diseases cross borders, or even oceans, before plant pathologists have time to identify and characterize the causative agents. Genome sequencing, in combination with intensive sampling of pathogen populations and application of population genetic tools, is now providing the means to unravel how bacterial crop pathogens emerge from environmental reservoirs, how they evolve and adapt to crops, and what international and intercontinental routes they follow during dissemination. Here, we introduce the field of population genomics and review the population genomics research of bacterial plant pathogens over the past 10 years. We highlight the potential of population genomics for investigating plant pathogens, using examples of population genomics studies of human pathogens. We also describe the complementary nature of the fields of population genomics and molecular plant-microbe interactions and propose how to translate new insights into improved disease pre...

Fifty years since Silent Spring.

Abstract: Rachel Carson's 1962 Silent Spring exposed both observed and potential environmental and health externalities of the increasing organochlorine and organophosphate insecticide use in the United States post–World War II. Silent Spring was a critical component in a popular movement that resulted in increased regulation and the development of safer pesticides. Most changes in pesticide use in the global north have involved pesticide substitutions, although riskier pesticides remain in use. Many ideas in Silent Spring are compatible with the theory of integrated pest management (IPM), and IPM has been broadly embraced in the United States and internationally as a strategy for achieving least-use and/or least-risk pesticide use in agriculture. IPM is a politically feasible policy that purports to reduce pesticide use and/or risk in agriculture but often does not, except in extreme cases of pesticide overuse that result in negative agricultural/economic consequences for growers.

Mechanisms of Nutrient Acquisition and Utilization During Fungal Infections of Leaves

Abstract: Foliar fungal pathogens challenge global food security, but how they optimize growth and development during infection is understudied. Despite adopting several lifestyles to facilitate nutrient acquisition from colonized cells, little is known about the genetic underpinnings governing pathogen adaption to host-derived nutrients. Homologs of common global and pathway-specific gene regulatory elements are likely to be involved, but their contribution to pathogenicity, and how they are connected to broader genetic networks, is largely unspecified. Here, we focus on carbon and nitrogen metabolism in foliar pathogens and consider what is known, and what is not known, about fungal exploitation of host nutrient and ask how common metabolic regulators have been co-opted to the plant-pathogenic lifestyle as well as how nutrients are utilized to drive infection.

Networks and plant disease management: Concepts and applications

Abstract: A network is a natural structure with which to describe many aspects of a plant pathosystem. The article seeks to set out in a nonmathematical way some of the network concepts that promise to be useful in managing plant disease. The field has been stimulated by developments designed to help understand and manage animal and human disease, and by technical infrastructures, such as the internet. It overlaps partly with landscape ecology. The study of networks has helped identify likely ways to reduce the flow of disease in traded plants, to find the best sites to monitor as warning sites for annually reinvading diseases, and to understand the fundamentals of how a pathogen spreads in different structures. A tension between the free flow of goods or species down communication channels and free flow of pathogens down the same pathways is highlighted.

Network Modeling to Understand Plant Immunity

Abstract: Deciphering the networks that underpin complex biological processes using experimental data remains a significant, but promising, challenge, a task made all the harder by the added complexity of host-pathogen interactions. The aim of this article is to review the progress in understanding plant immunity made so far by applying network modeling algorithms and to show how this computational/mathematical strategy is facilitating a systems view of plant defense. We review the different types of network modeling that have been used, the data required, and the type of insight that such modeling can provide. We discuss the current challenges in modeling the regulatory networks that underlie plant defense and the future developments that may help address these challenges.

Speciation in Fungal and Oomycete Plant Pathogens

Abstract: The process of speciation, by definition, involves evolution of one or more reproductive isolating mechanisms that split a single species into two that can no longer interbreed. Determination of which processes are responsible for speciation is important yet challenging. Several studies have proposed that speciation in pathogens is heavily influenced by host-pathogen dynamics and that traits that mediate such interactions (e.g., host mobility, reproductive mode of the pathogen, complexity of the life cycle, and host specificity) must lead to reproductive isolation and ultimately affect speciation rates. In this review, we summarize the main evolutionary processes that lead to speciation of fungal and oomycete plant pathogens and provide an outline of how speciation can be studied rigorously, including novel genetic/genomic developments.

Meta-analysis and other approaches for synthesizing structured and unstructured data in plant pathology.

Abstract: The term data deluge is used widely to describe the rapidly accelerating growth of information in the technical literature, in scientific databases, and in informal sources such as the Internet and social media The massive volume and increased complexity of information challenge traditional methods of data analysis but at the same time provide unprecedented opportunities to test hypotheses or uncover new relationships via mining of existing databases and literature In this review, we discuss analytical approaches that are beginning to be applied to help synthesize the vast amount of information generated by the data deluge and thus accelerate the pace of discovery in plant pathology We begin with a review of meta-analysis as an established approach for summarizing standardized (structured) data across the literature We then turn to examples of synthesizing more complex, unstructured data sets through a range of data-mining approaches, including the incorporation of 'omics data in epidemiological analy

Virus infection cycle events coupled to RNA replication.

Abstract: Replication, the process by which the genetic material of a virus is copied to generate multiple progeny genomes, is the central part of the virus infection cycle. For an infection to be productive, it is essential that this process is coordinated with other aspects of the cycle, such as translation of the viral genome, encapsidation, and movement of the genome between cells. In the case of positive-strand RNA viruses, this represents a particular challenge, as the infecting genome must not only be replicated but also serve as an mRNA for the production of the replication-associated proteins. In recent years, it has become apparent that in positive-strand RNA plant viruses all the aspects of the infection cycle are intertwined. This article reviews the current state of knowledge regarding replication-associated events in such viruses.

How way leads on to way.

Abstract: In this article, I briefly recount the historical events in my native country that led me to become a plant pathologist. I started as a field pathologist specializing in fungal diseases of legumes, moved to biochemical research on virulence factors, and then on to molecular plant-microbe interactions. I describe the impact my graduate studies at the University of California (UC)-Davis had on my career. My life's work and teaching can be said to reflect the development in plant pathology during the past 40 years. I have included a concise review of the development of plant pathology in Israel and the ways it is funded. Dealing with administrative duties while conducting research has contributed to my belief in the importance of multidisciplinary approaches and of preserving the applied approach in the teaching of plant pathology.