The aim of this review was to survey all fungal pathologists with an association with the journal Molecular Plant Pathology and ask them to nominate which fungal pathogens they would place in a 'Top 10' based on scientific/economic importance. The survey generated 495 votes from the international community, and resulted in the generation of a Top 10 fungal plant pathogen list for Molecular Plant Pathology. The Top 10 list includes, in rank order, (1) Magnaporthe oryzae; (2) Botrytis cinerea; (3) Puccinia spp.; (4) Fusarium graminearum; (5) Fusarium oxysporum; (6) Blumeria graminis; (7) Mycosphaerella graminicola; (8) Colletotrichum spp.; (9) Ustilago maydis; (10) Melampsora lini, with honourable mentions for fungi just missing out on the Top 10, including Phakopsora pachyrhizi and Rhizoctonia solani. This article presents a short resume of each fungus in the Top 10 list and its importance, with the intent of initiating discussion and debate amongst the plant mycology community, as well as laying down a bench-mark. It will be interesting to see in future years how perceptions change and what fungi will comprise any future Top 10.

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The Top 10 fungal pathogens in molecular plant pathology

Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.

/pdf/comparative-genomics-reveals-mobile-pathogenicity-4un6wxzvar.pdf

Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium

SUMMARY
The rapid global re-emergence of Fusarium head blight disease of wheat and barley in the last decade along with contamination of grains with mycotoxins attributable to the disease have spurred basic research on the fungal causal agent. As a result, Fusarium graminearum quickly has become one of the most intensively studied fungal plant pathogens. This review briefly summarizes current knowledge on the pathogenicity, population genetics, evolution and genomics of Fusarium graminearum.

Taxonomy:  Based on the sexual state Gibberella zeae (Schwein.) Petch: Superkingdom Eukaryota; Kingdom Fungi; Phylum Ascomycota; Subphylum Pezizomycotina; Class Sordariomycetidae; Subclass Hypocreomycetidae; Order Hypocreales; Family Nectriaceae; Genus Gibberella.

Host range:  The pathogen is capable of causing head blight or ‘scab’ on wheat (Triticum), barley (Hordeum), rice (Oryza), oats (Avena) and Gibberella stalk and ear rot disease on maize (Zea). The fungus also may infect other plant species without causing disease symptoms. Other host genera cited for Gibberella zeae or F. graminearum sensu lato (see below) are Agropyron, Agrostis, Bromus, Calamagrostis, Cenchrus, Cortaderia, Cucumis, Echinochloa, Glycine, Hierochloe, Lolium, Lycopersicon, Medicago, Phleum, Poa, Schizachyrium, Secale, Setaria, Sorghum, Spartina and Trifolium.

Disease symptoms and signs:  For wheat, brown, dark purple to black necrotic lesions form on the exterior surface of the florets and glume (Fig. 1). Although these lesion symptoms sometimes are referred to as scab, they are not formally related to the hyperplasia and hypertrophic epidermal growth associated with other scab diseases such as apple scab. Peduncles immediately below the inflorescence may become discoloured brown/purple. With time, tissue of the inflorescence often becomes blighted, appearing bleached and tan, while the grain within atrophies. Awns often become deformed, twisted and curved downward. In barley, infections are not always readily apparent in the field. Infected spikelets may show a browning or water-soaked appearance. Infected barley kernels show a tan to dark brown discolouration that can be similar to that caused by other kernel blighting organisms. During prolonged wet periods, pink to salmon-orange spore masses of the fungus are often seen on infected spikelets, glumes and kernels in both wheat and barley. For maize ear rot, infection occurs by way of colonizing silk and thus symptoms first appear at the ear apex. White mycelium, turning pink to red with time, colonizes kernels and may progress basipetally, covering the entire ear.



Figure 1. 

Field-grown wheat inflorescence showing symptoms of Fusarium head blight. The third spikelet from the bottom shows a darkened necrotic lesion (‘scab’) whereas the second and fifth spikelets demonstrate tissue bleaching (‘blight’) symptoms. Photograph courtesy of Jacki Morrison, USDA ARS Cereal Disease Laboratory.


Useful websites: http://www.broad.mit.edu/annotation/fungi/fusarium/mips.gsf.de/genre/proj/fusarium/

http://www.cdl.umn.edu/scab/gz-consort.html

http://www.scabusa.org/

Heading for disaster: Fusarium graminearum on cereal crops.

The plant hormones abscisic acid (ABA), jasmonic acid (JA), and ethylene are involved in diverse plant processes, including the regulation of gene expression during adaptive responses to abiotic and biotic stresses. Previously, ABA has been implicated in enhancing disease susceptibility in various plant species, but currently very little is known about the molecular mechanisms underlying this phenomenon. In this study, we obtained evidence that a complex interplay between ABA and JA-ethylene signaling pathways regulate plant defense gene expression and disease resistance. First, we showed that exogenous ABA suppressed both basal and JA-ethylene–activated transcription from defense genes. By contrast, ABA deficiency as conditioned by the mutations in the ABA1 and ABA2 genes, which encode enzymes involved in ABA biosynthesis, resulted in upregulation of basal and induced transcription from JA-ethylene responsive defense genes. Second, we found that disruption of AtMYC2 (allelic to JASMONATE INSENSITIVE1 [JIN1]), encoding a basic helix-loop-helix Leu zipper transcription factor, which is a positive regulator of ABA signaling, results in elevated levels of basal and activated transcription from JA-ethylene responsive defense genes. Furthermore, the jin1/myc2 and aba2-1 mutants showed increased resistance to the necrotrophic fungal pathogen Fusarium oxysporum. Finally, using ethylene and ABA signaling mutants, we showed that interaction between ABA and ethylene signaling is mutually antagonistic in vegetative tissues. Collectively, our results indicate that the antagonistic interactions between multiple components of ABA and the JA-ethylene signaling pathways modulate defense and stress responsive gene expression in response to biotic and abiotic stresses.

/pdf/antagonistic-interaction-between-abscisic-acid-and-jasmonate-17on35agpu.pdf

Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis

Fusarium species cause a broad spectrum of infections in humans, including superficial, locally invasive, and disseminated infections. The clinical form of fusariosis depends largely on the immune status of the host and the portal of entry, with superficial and localized disease occurring mostly in immunocompetent patients and invasive and disseminated disease affecting immunocompromised patients. Risk factors for severe fusariosis include prolonged neutropenia and T-cell immunodeficiency, especially in hematopoietic stem cell transplant recipients with severe graft-versus-host disease. The most frequent presentation of disseminated fusariosis is a combination of characteristic cutaneous lesions and positive blood cultures, with or without lung or sinus involvement. The prognosis is poor and is determined largely by degree of immunosuppression and extent of infection, with virtually a 100% death rate among persistently neutropenic patients with disseminated disease. These infections may be clinically suspected on the basis of a constellation of clinical and laboratory findings, which should lead to prompt therapy. Treatment options include the lipid formulations of amphotericin B, voriconazole, and posaconazole. Prevention of fusarial infection among high-risk patients should be considered.

Fusarium Infections in Immunocompromised Patients

SUMMARY
Taxonomy: Vascular wilt fungus; Ascomycete although sexual stage is yet to be found. The most closely related teleomorphic group, Gibberella, is classified within the Pyrenomycetes.

 Host range: Very broad at the species level. More than 120 different formae speciales have been identified based on specificity to host species belonging to a wide range of plant families.

 Disease symptoms: Initial symptoms of vascular wilt include vein clearing and leaf epinasty, followed by stunting, yellowing of the lower leafs, progressive wilting of leaves and stem, defoliation and finally death of the plant. In cross-sections of the stem, a brown ring is evident in the area of the vascular bundles. Some formae speciales are not primarily vascular pathogens but cause foot- and rootrot or bulbrot.

 Economic importance: Causes severe losses on most vegetables and flowers, several field crops such as cotton and tobacco, plantation crops such as banana, plantain, coffee and sugarcane, and a few shade trees.

 Control: Use of resistant varieties is the only practical measure for controlling the disease in the field. Under greenhouse conditions, soil sterilization can be performed. Alternative control methods with potential for the future include soil solarization and biological control with antagonistic bacteria or fungi.

 Useful websites: http://www.fgsc.net/fus.htm, http://www-genome.wi.mit.edu/annotation/fungi/fusarium/, http://www.cbs.knaw.nl/fusarium/database.html

Fusarium oxysporum: exploring the molecular arsenal of a vascular wilt fungus

Fungal pathogens cause disease in plant and animal hosts. The extent to which infection mechanisms are conserved between both classes of hosts is unknown. We present a dual plant-animal infection system based on a single strain of Fusarium oxysporum, the causal agent of vascular wilt disease in plants and an emerging opportunistic human pathogen. Injection of microconidia of a well-characterized tomato pathogenic isolate (isolate 4287) into the lateral tail vein of immunodepressed mice resulted in disseminated infection of multiple organs and death of the animals. Knockout mutants in genes encoding a mitogen-activated protein kinase, a pH response transcription factor, or a class V chitin synthase previously shown to be implicated in virulence on tomato plants were tested in the mouse model. The results indicate that some of these virulence factors play functionally distinct roles during the infection of tomato plants and mice. Thus, a single F. oxysporum strain can be used to study fungal virulence mechanisms in plant and mammalian pathogenesis.

https://iai.asm.org/content/iai/72/3/1760.full.pdf

Fusarium oxysporum as a Multihost Model for the Genetic Dissection of Fungal Virulence in Plants and Mammals

Fusarium as a model for studying virulence in soilborne plant pathogens

Three structural chitin synthase genes, chs1, chs2 and chs3, were identified in the genome of Fusarium oxysporum f. sp. lycopersici, a soilborne pathogen causing vascular wilt disease in tomato plants. Based on amino acid identities with related fungal species, chs1, chs2 and chs3 encode structural chitin synthases (CSs) of class I, class II and class III, respectively. A gene (chs7) encoding a chaperone-like protein was identified by comparison of the deduced protein with Chs7p from Saccharomyces cerevisiae, an endoplasmic reticulum (ER) protein required for the export of ScChs3p (class IV) from the ER. So far no CS gene belonging to class IV has been isolated from F. oxysporum, although it probably contains more than one gene of this class, based on the genome data of the closely related species Fusarium graminearum. F. oxysporum chs1-, chs2- and chs7-deficient mutants were constructed through targeted gene disruption by homologous recombination. No compensatory mechanism seems to exist between the CS genes studied, since chitin content determination and expression analysis of the chs genes showed no differences between the disruption mutants and the wild-type strain. By fluorescence microscopy using Calcofluor white and DAPI staining, the wild-type strain and Δchs2 and Δchs7 mutants showed similar septation and even nuclear distribution, with each hyphal compartment containing only one nucleus, whereas the Δchs1 mutant showed compartments containing up to four nuclei. Pathogenicity assays on tomato plants indicated reduced virulence of Δchs2 and Δchs7 null mutants. Stress conditions affected normal development in Δchs2 but not in Δchs1 or Δchs7 disruptants, and the three chs-deficient mutants showed increased hyphal hydrophobicity compared to the wild-type strain when grown in sorbitol-containing medium. The chitin synthase mutants will be useful for elucidating cell wall biogenesis in F. oxysporum and the relationship between fungal cell wall integrity and pathogenicity.

/pdf/role-of-chitin-synthase-genes-in-fusarium-oxysporum-d0s7poku7u.pdf

Role of chitin synthase genes in Fusarium oxysporum.

Glycosylphosphatidylinositol-anchored (beta)-1,3-glucanosyltransferases play active roles in fungal cell wall biosynthesis and morphogenesis and have been implicated in virulence on mammals. The role of beta-1,3-glucanosyltransferases in pathogenesis to plants has not been explored so far. Here, we report the cloning and mutational analysis of the gas1 gene encoding a putative beta-1,3-glucanosyltransferase from the vascular wilt fungus Fusarium oxysporum. In contrast to Candida albicans, expression of gas1 in F. oxysporum was independent of ambient pH and of the pH response transcription factor PacC. Gene knockout mutants lacking a functional gas1 allele grew in a way similar to the wildtype strain in submerged culture but exhibited restricted colony growth on solid substrates. The restricted growth phenotype was relieved by the osmotic stabilizer sorbitol, indicating that it may be related to structural alterations in the cell wall. Consistent with this hypothesis, deltagas1 mutants exhibited enhanced resistance to cell wall-degrading enzymes and increased transcript levels of chsV and rho1, encoding a class V chitin synthase and a small monomeric G protein, respectively. The deltagas1 mutants showed dramatically reduced virulence on tomato, both in a root infection assay and in a fruit tissue-invasion model, thus providing the first evidence for an essential role of fungal beta-1,3-glucanosyltransferases during plant infection.

https://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI-18-1140

Marta P. Madrid

Papers

Fusarium oxysporum: exploring the molecular arsenal of a vascular wilt fungus

Fusarium oxysporum as a Multihost Model for the Genetic Dissection of Fungal Virulence in Plants and Mammals

Fusarium as a model for studying virulence in soilborne plant pathogens

Role of chitin synthase genes in Fusarium oxysporum.

Fusarium oxysporum gas1 encodes a putative beta-1,3-glucanosyltransferase required for virulence on tomato plants