Annual Review of Phytopathology - Volume 55, 2017

This article recounts the experiences that shaped my career as a molecular plant pathologist. It focuses primarily on technical and conceptual developments in molecular phytobacteriology, shares some personal highlights and untold stories that impacted my professional development, and describes the early years of agricultural biotechnology. Writing this article required reflection on events occurring over several decades that were punctuated by a mid-career relocation across the Atlantic. I hope it will still be useful, informative, and enjoyable to read. An extended version of the abstract is provided in the Supplemental Materials, available online.

The Fusarium oxysporum species complex (FOSC) comprises a multitude of strains that cause vascular wilt diseases of economically important crops throughout the world. Although sexual reproduction is unknown in the FOSC, horizontal gene transfer may contribute to the observed diversity in pathogenic strains. Development of disease in a susceptible crop requires F. oxysporum to advance through a series of transitions, beginning with spore germination and culminating with establishment of a systemic infection. In principle, each transition presents an opportunity to influence the risk of disease. This includes modifications of the microbial community in soil, which can affect the ability of pathogen propagules to survive, germinate, and infect plant roots. In addition, many host attributes, including the composition of root exudates, the structure of the root cortex, and the capacity to recognize and respond quickly to invasive growth of a pathogen, can impede development of F. oxysporum.

The evidential basis for disease management decision making is provided by data relating to risk factors. The decision process involves an assessment of the evidence leading to taking (or refraining from) action on the basis of a prediction. The primary objective of the decision process is to identify—at the time the decision is made—the control action that provides the best predicted end-of-season outcome, calculated in terms of revenue or another appropriate metric. Data relating to disease risk factors may take a variety of forms (e.g., continuous, discrete, categorical) on measurement scales in a variety of units. Log10-likelihood ratios provide a principled basis for the accumulation of evidence based on such data and allow predictions to be made via Bayesian updating of prior probabilities.

Plants are colonized on their surfaces and in the rhizosphere and phyllosphere by a multitude of different microorganisms and are inhabited internally by endophytes. Most endophytes act as commensals without any known effect on their plant host, but multiple bacteria and fungi establish a mutualistic relationship with plants, and some act as pathogens. The outcome of these plant-microbe interactions depends on biotic and abiotic environmental factors and on the genotype of the host and the interacting microorganism. In addition, endophytic microbiota and the manifold interactions between members, including pathogens, have a profound influence on the function of the system plant and the development of pathobiomes. In this review, we elaborate on the differences and similarities between nonpathogenic and pathogenic endophytes in terms of host plant response, colonization strategy, and genome content. We furthermore discuss environmental effects and biotic interactions within plant microbiota that influence pathogenesis and the pathobiome.

Silicon (Si) plays a pivotal role in the nutritional status of a wide variety of monocot and dicot plant species and helps them, whether directly or indirectly, counteract abiotic and/or biotic stresses. In general, plants with a high root or shoot Si concentration are less prone to pest attack and exhibit enhanced tolerance to abiotic stresses such as drought, low temperature, or metal toxicity. However, the most remarkable effect of Si is the reduction in the intensities of a number of seedborne, soilborne, and foliar diseases in many economically important crops that are caused by biotrophic, hemibiotrophic, and necrotrophic plant pathogens. The reduction in disease symptom expression is due to the effect of Si on some components of host resistance, including incubation period, lesion size, and lesion number. The mechanical barrier formed by the polymerization of Si beneath the cuticle and in the cell walls was the first proposed hypothesis to explain how this element reduced the severity of plant diseases. However, new insights have revealed that many plant species supplied with Si have the phenylpropanoid and terpenoid pathways potentiated and have a faster and stronger transcription of defense genes and higher activities of defense enzymes. Photosynthesis and the antioxidant system are also improved for Si-supplied plants. Although the current understanding of how this overlooked element improves plant reaction against pathogen infections, pest attacks, and abiotic stresses has advanced, the exact mechanism(s) by which it modulates plant physiology through the potentiation of host defense mechanisms still needs further investigation at the genomic, metabolomic, and proteomic levels.

Pathogen- or microbe-associated molecular patterns (PAMPs/MAMPs) are detected as nonself by host pattern recognition receptors (PRRs) and activate pattern-triggered immunity (PTI). Microbial invasions often trigger the production of host-derived endogenous signals referred to as danger- or damage-associated molecular patterns (DAMPs), which are also perceived by PRRs to modulate PTI responses. Collectively, PTI contributes to host defense against infections by a broad range of pathogens. Remarkable progress has been made toward demonstrating the cellular and physiological responses upon pattern recognition, elucidating the molecular, biochemical, and genetic mechanisms of PRR activation, and dissecting the complex signaling networks that orchestrate PTI responses. In this review, we present an update on the current understanding of how plants recognize and respond to nonself patterns, a process from which the seemingly chaotic responses form into a harmonic defense.

During the past decade, knowledge of pathogen life history has greatly benefited from the advent and development of molecular epidemiology. This branch of epidemiology uses information on pathogen variation at the molecular level to gain insights into a pathogen's niche and evolution and to characterize pathogen dispersal within and between host populations. Here, we review molecular epidemiology approaches that have been developed to trace plant virus dispersal in landscapes. In particular, we highlight how virus molecular epidemiology, nourished with powerful sequencing technologies, can provide novel insights at the crossroads between the blooming fields of landscape genetics, phylogeography, and evolutionary epidemiology. We present existing approaches and their limitations and contributions to the understanding of plant virus epidemiology.

Toxin-antitoxin (TA) systems are gene modules that are ubiquitous in free-living prokaryotes. Diverse in structure, cellular function, and fitness roles, TA systems are defined by the presence of a toxin gene that suppresses bacterial growth and a toxin-neutralizing antitoxin gene, usually encoded in a single operon. Originally viewed as DNA maintenance modules, TA systems are now thought to function in many roles, including bacterial stress tolerance, virulence, phage defense, and biofilm formation. However, very few studies have investigated the significance of TA systems in the context of plant-microbe interactions. This review discusses the potential impact and application of TA systems in plant-associated bacteria, guided by insights gained from animal-pathogenic model systems.

Fungicides should be used to the extent required to minimize economic costs of disease in a given field in a given season. The maximum number of treatments and maximum dose per treatment are set by fungicide manufacturers and regulators at a level that provides effective control under high disease pressure. Lower doses are economically optimal under low or moderate disease pressure, or where other control measures such as resistant cultivars constrain epidemics. Farmers in many countries often apply reduced doses, although they may still apply higher doses than the optimum to insure against losses in high disease seasons. Evidence supports reducing the number of treatments and reducing the applied dose to slow the evolution of fungicide resistance. The continuing research challenge is to improve prediction of future disease damage and account for the combined effect of integrated control measures to estimate the optimum number of treatments and the optimum dose needed to minimize economic costs. The theory for optimizing dose is well developed but requires translation into decision tools because the current basis for farmers’ dose decisions is unclear.

The first plant disease resistance (R) genes were identified and cloned more than two decades ago. Since then, many more R genes have been identified and characterized in numerous plant pathosystems. Most of these encode members of the large family of intracellular NLRs (NOD-like receptors), which also includes animal immune receptors. New discoveries in this expanding field of research provide new elements for our understanding of plant NLR function. But what do we know about plant NLR function today? Genetic, structural, and functional analyses have uncovered a number of commonalities and differences in pathogen recognition strategies as well as how NLRs are regulated and activate defense signaling, but many unknowns remain. This review gives an update on the latest discoveries and breakthroughs in this field, with an emphasis on structural findings and some comparison to animal NLRs, which can provide additional insights and paradigms in plant NLR function.

Cucumber green mottle mosaic virus (CGMMV) was first described in 1935 infecting cucumber, making it one of the first plant viruses to be studied. Its initial distribution occurred out of England to other countries. This was followed by its distribution from England and these other countries to additional countries. This process increased slowly between 1935 and 1985, faster between 1986 and 2006, and rapidly between 2007 and 2016. The discovery that it diminished cucurbit fruit yields and quality, especially of watermelon, prompted a substantial research effort in worst-affected countries. These efforts included obtaining insight into its particle and genome characteristics, evolution, and epidemiology. CGMMV's particle stability, ease of contact transmission, and seed transmissibility, which are typical tobamovirus characteristics, explained its complex disease cycle and its ability to spread locally or over long distances without a vector. Knowledge of its disease etiology and epidemiology enabled development of integrated disease management approaches that rely heavily on diverse phytosanitary measures. Dispersal of seed-borne infection through the international seed trade following cucurbit seed crop production in tropical or subtropical countries explains its recent rapid dispersion worldwide.

Plants are constantly exposed to would-be pathogens and pests, and thus have a sophisticated immune system to ward off these threats, which otherwise can have devastating ecological and economic consequences on ecosystems and agriculture. Plants employ receptor kinases (RKs) and receptor-like proteins (RLPs) as pattern recognition receptors (PRRs) to monitor their apoplastic environment and detect non-self and damaged-self patterns as signs of potential danger. Plant PRRs contribute to both basal and non-host resistances, and treatment with pathogen-/microbe-associated molecular patterns (PAMPs/MAMPs) or damage-associated molecular patterns (DAMPs) recognized by plant PRRs induces both local and systemic immunity. Here, we comprehensively review known PAMPs/DAMPs recognized by plants as well as the plant PRRs described to date. In particular, we describe the different methods that can be used to identify PAMPs/DAMPs and PRRs. Finally, we emphasize the emerging biotechnological potential use of PRRs to improve broad-spectrum, and potentially durable, disease resistance in crops.

Many living organisms on Earth have evolved the ability to integrate environmental and internal signals to determine time and thereafter adjust appropriately their metabolism, physiology, and behavior. The circadian clock is the endogenous timekeeper critical for multiple biological processes in many organisms. A growing body of evidence supports the importance of the circadian clock for plant health. Plants activate timed defense with various strategies to anticipate daily attacks of pathogens and pests and to modulate responses to specific invaders in a time-of-day-dependent manner (gating). Pathogen infection is also known to reciprocally modulate clock activity. Such a cross talk likely reflects the adaptive nature of plants to coordinate limited resources for growth, development, and defense. This review summarizes recent progress in circadian regulation of plant innate immunity with a focus on the molecular events linking the circadian clock and defense. More and better knowledge of clock-defense cross talk could help to improve disease resistance and productivity in economically important crops.

It is becoming abundantly clear that the microbes associated with plants and insects can profoundly influence plant-insect interactions. Here, we focus on recent findings and propose directions for future research that involve microbe-induced changes to plant defenses and nutritive quality as well as the consequences of these changes for the behavior and fitness of insect herbivores. Insect (herbivore and parasitoid)-associated microbes can favor or improve insect fitness by suppressing plant defenses and detoxifying defensive phytochemicals. Phytopathogens can influence or manipulate insect behavior and fitness by altering plant quality and defense. Plant-beneficial microbes can promote plant growth and influence plant nutritional and phytochemical composition that can positively or negatively influence insect fitness. Lastly, we suggest that entomopathogens have the potential to influence plant defenses directly as endophytes or indirectly by altering insect physiology.

Plant parasitism has evolved independently on at least four separate occasions in the phylum Nematoda. The application of next-generation sequencing (NGS) to plant-parasitic nematodes has allowed a wide range of genome- or transcriptome-level comparisons, and these have identified genome adaptations that enable parasitism of plants. Current genome data suggest that horizontal gene transfer, gene family expansions, evolution of new genes that mediate interactions with the host, and parasitism-specific gene regulation are important adaptations that allow nematodes to parasitize plants. Sequencing of a larger number of nematode genomes, including plant parasites that show different modes of parasitism or that have evolved in currently unsampled clades, and using free-living taxa as comparators would allow more detailed analysis and a better understanding of the organization of key genes within the genomes. This would facilitate a more complete understanding of the way in which parasitism has shaped the genomes of plant-parasitic nematodes.

Iron is an essential nutrient for most life on Earth because it functions as a crucial redox catalyst in many cellular processes. However, when present in excess iron can lead to the formation of harmful hydroxyl radicals. Hence, the cellular iron balance must be tightly controlled. Perturbation of iron homeostasis is a major strategy in host-pathogen interactions. Plants use iron-withholding strategies to reduce pathogen virulence or to locally increase iron levels to activate a toxic oxidative burst. Some plant pathogens counteract such defenses by secreting iron-scavenging siderophores that promote iron uptake and alleviate iron-regulated host immune responses. Mutualistic root microbiota can also influence plant disease via iron. They compete for iron with soil-borne pathogens or induce a systemic resistance that shares early signaling components with the root iron-uptake machinery. This review describes the progress in our understanding of the role of iron homeostasis in both pathogenic and beneficial plant-microbe interactions.

The introduction of Pseudomonas syringae pv. actinidiae (Psa) severely damaged the New Zealand kiwifruit industry, which in 2010 was based on only two cultivars. Despite an extraordinarily quick and strong response by industry, government, and scientists to minimize the economic and social impacts, the economic consequences of this outbreak were severe. Although our understanding of Psa epidemiology and control methods increased substantively over the past six years, the kiwifruit industry largely recovered because of the introduction of a less-susceptible yellow-fleshed cultivar. The New Zealand population of Psa is clonal but has evolved rapidly since its introduction by exchanging mobile genetic elements, including integrative conjugative elements (ICEs), with the local bacterial populations. In some cases, this has led to copper resistance. It is currently believed that the center of origin of the pathogen is Japan or Korea, but biovar 3, which is responsible for the global outbreak, originated in China.

Studies with model plants such as Arabidopsis thaliana have revealed that phytohormones are central regulators of plant defense. The intricate network of phytohormone signaling pathways enables plants to activate appropriate and effective defense responses against pathogens as well as to balance defense and growth. The timing of the evolution of most phytohormone signaling pathways seems to coincide with the colonization of land, a likely requirement for plant adaptations to the more variable terrestrial environments, which included the presence of pathogens. In this review, we explore the evolution of defense hormone signaling networks by combining the model plant-based knowledge about molecular components mediating phytohormone signaling and cross talk with available genome information of other plant species. We highlight conserved hubs in hormone cross talk and discuss evolutionary advantages of defense hormone cross talk. Finally, we examine possibilities of engineering hormone cross talk for improvement of plant fitness and crop production.

Many fungi can live both saprophytically and as endophyte or pathogen inside a living plant. In both environments, complex organic polymers are used as sources of nutrients. Propagation inside a living host also requires the ability to respond to immune responses of the host. We review current knowledge of how plant-pathogenic fungi do this. First, we look at how fungi change their global gene expression upon recognition of the host environment, leading to secretion of effectors, enzymes, and secondary metabolites; changes in metabolism; and defense against toxic compounds. Second, we look at what is known about the various cues that enable fungi to sense the presence of living plant cells. Finally, we review literature on transcription factors that participate in gene expression in planta or are suspected to be involved in that process because they are required for the ability to cause disease.

“Candidatus Liberibacter” species are associated with economically devastating diseases of citrus, potato, and many other crops. The importance of these diseases as well as the proliferation of new diseases on a wider host range is likely to increase as the insects vectoring the “Ca. Liberibacter” species expand their territories worldwide. Here, we review the progress on understanding pathogenesis mechanisms of “Ca. Liberibacter” species and the control approaches for diseases they cause. We discuss the Liberibacter virulence traits, including secretion systems, putative effectors, and lipopolysaccharides (LPSs), as well as other important traits likely to contribute to disease development, e.g., flagella, prophages, and salicylic acid hydroxylase. The pathogenesis mechanisms of Liberibacters are discussed. Liberibacters secrete Sec-dependent effectors (SDEs) or other virulence factors into the phloem elements or companion cells to interfere with host targets (e.g., proteins or genes), which cause cell death, necrosis, or other phenotypes of phloem elements or companion cells, leading to localized cell responses and systemic malfunction of phloem. Receptors on the remaining organelles in the phloem, such as plastid, vacuole, mitochondrion, or endoplasmic reticulum, interact with secreted SDEs and/or other virulence factors secreted or located on the Liberibacter outer membrane to trigger cell responses. Some of the host genes or proteins targeted by SDEs or other virulence factors of Liberibacters serve as susceptibility genes that facilitate compatibility (e.g., promoting pathogen growth or suppressing immune responses) or disease development. In addition, Liberibacters trigger plant immunity response via pathogen-associated molecular patterns (PAMPs, such as lipopolysaccharides), which leads to premature cell death, callose deposition, or phloem protein accumulation, causing a localized response and/or systemic effect on phloem transportation. Physical presence of Liberibacters and their metabolic activities may disturb the function of phloem, via disrupting osmotic gradients, or the integrity of phloem conductivity. We also review disease management strategies, including promising new technologies. Citrus production in the presence of Huanglongbing is possible if the most promising management approaches are integrated. HLB management is discussed in the context of local, area-wide, and regional Huanglongbing/Asian Citrus Psyllid epidemiological zones. For zebra chip disease control, aggressive psyllid management enables potato production, although insecticide resistance is becoming an issue. Meanwhile, new technologies such as clustered regularly interspaced short palindromic repeat (CRISPR)-derived genome editing provide an unprecedented opportunity to provide long-term solutions.