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The Use of Caenorhabditis elegans as a Model for Plant-Parasitic Nematodes: What Have We Learned?

Nematoda is a diverse phylum that is estimated to contain more than a million species. More than 4,100 of these species have the ability to parasitize plants and cause agricultural losses estimated at US $173 billion annually. This has led to considerable research into their biology to minimize crop losses via control methods. At the infancy of plant-parasitic nematode molecular biology, researchers compared nematode genomes, genes, and biological processes to the model nematode species Caenorhabditis elegans, which is a free-living bacterial feeder. This well-annotated and researched model nematode assisted the molecular biology research, e.g., with genome assemblies, of plant-parasitic nematodes. However, as research into these plant parasites progressed, the necessity of relying on the free-living relative as a reference has reduced. This is partly driven by revealing the considerable divergence between the two types of nematodes both genomically and anatomically, forcing comparisons to be redundant as well as the increased quality of molecular plant nematology proposing more suitable model organisms for this clade of nematode. The major irregularity between the two types of nematodes is the unique anatomical structure and effector repertoire that plant nematodes utilize to establish parasitism, which C. elegans lacks, therefore reducing its value as a heterologous system to investigate parasitic processes. Despite this, C. elegans remains useful for investigating conserved genes via its utility as an expression system because of the current inability to transform plant-parasitic nematodes. Unfortunately, owing to the expertise that this requires, it is not a common and/or accessible tool. Furthermore, we believe that the application of C. elegans as an expression system for plant nematodes will be redundant once tools are established for stable reverse-genetics in these plant parasites. This will remove the restraints on molecular plant nematology and allow it to excel on par with the capabilities of C. elegans research.

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Re-Envisioning the Plant Disease Triangle: Full Integration of the Host Microbiota and a Focal Pivot to Health Outcomes.

The disease triangle is a structurally simple but conceptually rich model that is used in plant pathology and other fields of study to explain infectious disease as an outcome of the three-way relationship between a host, a pathogen, and their environment. It also serves as a guide for finding solutions to treat, predict, and prevent such diseases. With the omics-driven, evidence-based realization that the abundance and activity of a pathogen are impacted by proximity to and interaction with a diverse multitude of other microorganisms colonizing the same host, the disease triangle evolved into a tetrahedron shape, which features an added fourth dimension representing the host-associated microbiota. Another variant of the disease triangle emerged from the recently formulated pathobiome paradigm, which deviates from the classical "one pathogen" etiology of infectious disease in favor of a scenario in which disease represents a conditional outcome of complex interactions between and among a host, its microbiota (including microbes with pathogenic potential), and the environment. The result is a version of the original disease triangle where "pathogen" is substituted with "microbiota." Here, as part of a careful and concise review of the origin, history, and usage of the disease triangle, I propose a next step in its evolution, which is to replace the word "disease" in the center of the host-microbiota-environment triad with the word "health." This triangle highlights health as a desirable outcome (rather than disease as an unwanted state) and as an emergent property of host-microbiota-environment interactions. Applied to the discipline of plant pathology, the health triangle offers an expanded range of targets and approaches for the diagnosis, prediction, restoration, and maintenance of plant health outcomes. Its applications are not restricted to infectious diseases only, and its underlying framework is more inclusive of all microbial contributions to plant well-being, including those by mycorrhizal fungi and nitrogen-fixing bacteria, for which there never was a proper place in the plant disease triangle. The plant health triangle also may have an edge as an education and communication tool to convey and stress the importance of healthy plants and their associated microbiota to a broader public and stakeholdership.

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Molecular Dialogue During Host Manipulation by the Vascular Wilt Fungus Fusarium oxysporum.

Vascular wilt fungi are a group of hemibiotrophic phytopathogens that infect diverse crop plants. These pathogens have adapted to thrive in the nutrient-deprived niche of the plant xylem. Identification and functional characterization of effectors and their role in the establishment of compatibility across multiple hosts, suppression of plant defense, host reprogramming, and interaction with surrounding microbes have been studied mainly in model vascular wilt pathogens Fusarium oxysporum and Verticillium dahliae. Comparative analysis of genomes from fungal isolates has accelerated our understanding of genome compartmentalization and its role in effector evolution. Also, advances in recent years have shed light on the cross talk of root-infecting fungi across multiple scales from the cellular to the ecosystem level, covering their interaction with the plant microbiome as well as their interkingdom signaling. This review elaborates on our current understanding of the cross talk between vascular wilt fungi and the host plant, which eventually leads to a specialized lifestyle in the xylem. We particularly focus on recent findings in F. oxysporum, including multihost associations, and how they have contributed to understanding the biology of fungal adaptation to the xylem. In addition, we discuss emerging research areas and highlight open questions and future challenges.

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