An official website of the United States government
Abstract Parasitic fungi produce proteins that modulate virulence, alter host physiology, and trigger host responses. These proteins, classified as a type of “effector,” often act via protein–protein interactions (PPIs). The fungal parasiteOphiocordyceps camponoti-floridani(zombie ant fungus) manipulatesCamponotus floridanus(carpenter ant) behavior to promote transmission. The most striking aspect of this behavioral change is a summit disease phenotype where infected hosts ascend and attach to an elevated position. Plausibly, interspecific PPIs drive aspects ofOphiocordycepsinfection and host manipulation. Machine learning PPI predictions offer high-throughput methods to produce mechanistic hypotheses on how this behavioral manipulation occurs. Using D-SCRIPT to predict host–parasite PPIs, we found ca. 6000 interactions involving 2083 host proteins and 129 parasite proteins, which are encoded by genes upregulated during manipulated behavior. We identified multiple overrepresentations of functional annotations among these proteins. The strongest signals in the host highlighted neuromodulatory G-protein coupled receptors and oxidation–reduction processes. We also detectedCamponotusstructural and gene-regulatory proteins. In the parasite, we found enrichment ofOphiocordycepsproteases and frequent involvement of novel small secreted proteins with unknown functions. From these results, we provide new hypotheses on potential parasite effectors and host targets underlying zombie ant behavioral manipulation.
more »
« less
Characterization of Microbotryum lychnidis-dioicae Secreted Effector Proteins, Their Potential Host Targets, and Localization in a Heterologous Host Plant
Microbotryum lychnidis-dioicae is an obligate fungal species colonizing the plant host, Silene latifolia. The fungus synthesizes and secretes effector proteins into the plant host during infection to manipulate the host for completion of the fungal lifecycle. The goal of this study was to continue functional characterization of such M. lychnidis-dioicae effectors. Here, we identified three putative effectors and their putative host-plant target proteins. MVLG_02245 is highly upregulated in M. lychnidis-dioicae during infection; yeast two-hybrid analysis suggests it targets a tubulin α-1 chain protein ortholog in the host, Silene latifolia. A potential plant protein interacting with MVLG_06175 was identified as CASP-like protein 2C1 (CASPL2C1), which facilitates the polymerization of the Casparian strip at the endodermal cells. Proteins interacting with MVLG_05122 were identified as CSN5a or 5b, involved in protein turnover. Fluorescently labelled MVLG_06175 and MVLG_05122 were expressed in the heterologous plant, Arabidopsis thaliana. MVLG_06175 formed clustered granules at the tips of trichomes on leaves and in root caps, while MVLG_05122 formed a band structure at the base of leaf trichomes. Plants expressing MVLG_05122 alone were more resistant to infection with Fusarium oxysporum. These results indicate that the fungus might affect the formation of the Casparian strip in the roots and the development of trichomes during infection as well as alter plant innate immunity.
more »
« less
- Award ID(s):
- 2007449
- PAR ID:
- 10577559
- Publisher / Repository:
- MDPI
- Date Published:
- Journal Name:
- Journal of Fungi
- Volume:
- 10
- Issue:
- 4
- ISSN:
- 2309-608X
- Page Range / eLocation ID:
- 262
- Subject(s) / Keyword(s):
- Microbotryum lychnidis-dioicae fungal effector protein protein-protein interaction CASPlike protein 2C1 COP9 signalosome subunit 5a/5b trichome
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Mentioned for the first time in an article 1971, the occurrence of the term “Macrophomina phaseolina” has experienced a steep increase in the scientific literature over the past 15 years. Concurrently, incidences ofM. phaseolina-caused crop diseases have been getting more frequent. The high levels of diversity and plasticity observed forM. phasolinagenomes along with a rich equipment of plant cell wall degrading enzymes, secondary metabolites and putative virulence effectors as well as the unusual longevity of microsclerotia, their asexual reproduction structures, make this pathogen very difficult to control and crop protection against it very challenging. During the past years several studies have emerged reporting on host defense measures againstM. phaseolina, as well as mechanisms of pathogenicity employed by this fungal pathogen. While most of these studies have been performed in crop systems, such as soybean or sesame, recently interactions ofM. phaseolinawith the model plant Arabidopsis thaliana have been described. Collectively, results from various studies are hinting at a complex infection cycle ofM. phaseolina, which exhibits an early biotrophic phase and switches to necrotrophy at later time points during the infection process. Consequently, responses of the hosts are complex and seem coordinated by multiple defense-associated phytohormones. However, at this point no robust and strong host defense mechanism againstM. phaseolinahas been described.more » « less
-
Abstract Climate change is rapidly altering the distribution of suitable habitats for many species as well as their pathogenic microbes. For many pathogens, including vector‐borne diseases of humans and agricultural pathogens, climate change is expected to increase transmission and lead to pathogen range expansions. However, if pathogens have a lower heat tolerance than their host, increased warming could generate so‐called thermal refugia for hosts. Predicting the outcomes of warming on disease transmission requires detailed knowledge of the thermal tolerances of both the host and the pathogen. Such thermal tolerance studies are generally lacking for fungal pathogens of wild plant populations, despite the fact that plants form the base of all terrestrial communities. Here, we quantified three aspects of the thermal tolerance (growth, infection, and propagule production) of the naturally occurring fungal pathogenMicrobotryum lychnidis‐dioicae, which causes a sterilizing anther‐smut disease on the herbaceous plantSilene latifolia. We also quantified two aspects of host thermal tolerance: seedling survival and flowering rate. We found that temperatures >30°C reduced the ability of anther‐smut spores to germinate, grow, and conjugate in vitro. In addition, we found that high temperatures (30°C) during or shortly after the time of inoculation strongly reduced the likelihood of infection in seedlings. Finally, we found that high summer temperatures in the field temporarily cured infected plants, likely reducing transmission. Notably, high temperatures did not reduce survival or flowering of the host plants. Taken together, our results show that the fungus is considerably more sensitive to high temperatures than its host plant. A warming climate could therefore result in reduced disease spread or even local pathogen extirpation, leading to thermal refugia for the host.more » « less
-
Extracellular vesicles (EVs) are nano-sized, lipid compartments that mediate the intercellular transport of lipids, proteins, nucleic acids and metabolites. During infectious diseases, EVs released by host cells promote immune responses, while those released by pathogens attempt to subvert host immunity. There is a growing body of research investigating the role of fungal EVs in plant pathosystems. It is becoming clear that EVs released by fungal phytopathogens play a role during infection through the transport of protein effectors, toxic metabolites and RNA. Here, we discuss recent findings on EVs in fungal phytopathogens, including the methods employed in their isolation, their characterization, contents and functionality, as well as the key questions remaining to be addressed.more » « less
-
EndofungalMycetohabitans(formerlyBurkholderia) spp. rely on a type III secretion system to deliver mostly unidentified effector proteins when colonizing their host fungus,Rhizopus microsporus. The one known secreted effector family fromMycetohabitansconsists of homologues of transcription activator-like (TAL) effectors, which are used by plant pathogenicXanthomonasandRalstoniaspp. to activate host genes that promote disease. These ‘BurkholderiaTAL-like (Btl)’ proteins bind corresponding specific DNA sequences in a predictable manner, but their genomic target(s) and impact on transcription in the fungus are unknown. Recent phenotyping of Btl mutants of twoMycetohabitansstrains revealed that the single Btl in oneMycetohabitans endofungorumstrain enhances fungal membrane stress tolerance, while others in aMycetohabitans rhizoxinicastrain promote bacterial colonization of the fungus. The phenotypic diversity underscores the need to assess the sequence diversity and, given that sequence diversity translates to DNA targeting specificity, the functional diversity of Btl proteins. Using a dual approach to maximize capture of Btl protein sequences for our analysis, we sequenced and assembled nineMycetohabitansspp. genomes using long-read PacBio technology and also mined available short-read Illumina fungal–bacterial metagenomes. We show thatbtlgenes are present across diverseMycetohabitansstrains from Mucoromycota fungal hosts yet vary in sequences and predicted DNA binding specificity. Phylogenetic analysis revealed distinct clades of Btl proteins and suggested thatMycetohabitansmight contain more species than previously recognized. Within our data set, Btl proteins were more conserved acrossM. rhizoxinicastrains than acrossM. endofungorum, but there was also evidence of greater overall strain diversity within the latter clade. Overall, the results suggest that Btl proteins contribute to bacterial–fungal symbioses in myriad ways.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/jof10040262
