The Genetics of Hyphal Fusion and Vegetative Incompatibility in Filamentous Ascomycete Fungi

Abstract Trans-species polymorphism, meaning the presence of alleles in different species that are more similar to each other than they are to alleles in the same species, has been found at loci associated with vegetative incompatibility in filamentous fungi. If individuals differ at one or more of these loci (termed het for heterokaryon), they cannot form stable heterokaryons after vegetative fusion. At the het-c locus in Neurospora crassa and related species there is clear evidence of trans-species polymorphism: three alleles have persisted for ∼30 million years. We analyze a population genetic model of multilocus vegetative incompatibility and find the conditions under which trans-species polymorphism will occur. In the model, several unlinked loci determine the vegetative compatibility group (VCG) of an individual. Individuals of different VCGs fail to form productive heterokaryons, while those of the same VCG form viable heterokaryons. However, viable heterokaryon formation between individuals of the same VCG results in a loss in fitness, presumably via transfer of infectious agents by hyphal fusion or exploitation by aggressive genotypes. The result is a form of balancing selection on all loci affecting an individual's VCG. We analyze this model by making use of a Markov chain/strong selection, weak mutation (SSWM) approximation. We find that trans-species polymorphism of the type that has been found at the het-c locus is expected to occur only when the appearance of new incompatibility alleles is strongly constrained, because the rate of mutation to such alleles is very low, because the number of possible incompatibility alleles at each locus is restricted, or because the number of incompatibility loci is limited.

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The ham-2 Locus, Encoding a Putative Transmembrane Protein, Is Required for Hyphal Fusion in Neurospora crassa

Genetics ◽

10.1093/genetics/160.1.169 ◽

2002 ◽

Vol 160 (1) ◽

pp. 169-180

Author(s):

Qijun Xiang ◽

Carolyn Rasmussen ◽

N Louise Glass

Keyword(s):

Neurospora Crassa ◽

Somatic Cell ◽

Molecular Mechanism ◽

Cell Fusion ◽

Deletion Mutant ◽

Transmembrane Protein ◽

Wild Type ◽

Vegetative Incompatibility ◽

Hyphal Fusion ◽

Aerial Hyphae

Abstract Somatic cell fusion is common during organogenesis in multicellular eukaryotes, although the molecular mechanism of cell fusion is poorly understood. In filamentous fungi, somatic cell fusion occurs during vegetative growth. Filamentous fungi grow as multinucleate hyphal tubes that undergo frequent hyphal fusion (anastomosis) during colony expansion, resulting in the formation of a hyphal network. The molecular mechanism of the hyphal fusion process and the role of networked hyphae in the growth and development of these organisms are unexplored questions. We use the filamentous fungus Neurospora crassa as a model to study the molecular mechanism of hyphal fusion. In this study, we identified a deletion mutant that was restricted in its ability to undergo both self-hyphal fusion and fusion with a different individual to form a heterokaryon. This deletion mutant displayed pleiotropic defects, including shortened aerial hyphae, altered conidiation pattern, female sterility, slow growth rate, lack of hyphal fusion, and suppression of vegetative incompatibility. Complementation with a single open reading frame (ORF) within the deletion region in this mutant restored near wild-type growth rates, female fertility, aerial hyphae formation, and hyphal fusion, but not vegetative incompatibility and wild-type conidiation pattern. This ORF, which we named ham-2 (for hyphal anastomosis), encodes a putative transmembrane protein that is highly conserved, but of unknown function among eukaryotes.

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Unique Patterns of Mating Pheromone Presence and Absence could Result in the Ambiguous Sexual Behaviours of Colletotrichum Species

10.21203/rs.3.rs-112807/v1 ◽

2020 ◽

Author(s):

Andrea Melissa Wilson ◽

RV Lelwala ◽

PWJ Taylor ◽

MJ Wingfield ◽

BD WINGFIELD

Keyword(s):

Mating Type ◽

Molecular Mechanisms ◽

Mating Strategies ◽

Mating Partner ◽

Filamentous Ascomycete ◽

Sexual Behaviours ◽

History Of ◽

Ascomycete Fungi ◽

Presence And Absence ◽

Sexual Progeny

Abstract Background: Colletotrichum species are known to engage in unique sexual behaviours that differ significantly from the mating strategies of other filamentous ascomycete species. Most ascomycete fungi require the expression of both the MAT1-1-1 and MAT1-2-1 genes to regulate mating type and induce sexual reproduction. In contrast, all isolates of Colletotrichum are known to harbour only the MAT1-2-1 gene and yet, are capable of recognizing suitable mating partners and producing sexual progeny. The molecular mechanisms contributing to mating types and behaviours in Colletotrichum are thus unknown. Results: A comparative genomics approach analysing genomes from 47 Colletotrichum isolates was used to elucidate a putative molecular mechanism underlying the unique sexual behaviours observed in Colletotrichum species. The existence of only the MAT1-2 idiomorph was confirmed across all species included in this study. Comparisons at the loci harbouring the two mating pheromones and their cognate receptors revealed interesting patterns of gene presence and absence as well as gene loss. The results also showed that these genes have been lost multiple times over the evolutionary history of this genus. Conclusion: The multiple losses of the pheromone genes in these species suggest strong selection against the typical mating strategies seen in other species. This further suggests that these pheromones no longer play a role in mating type determination and that the species of this genus have undiscovered mechanisms by which to control mating type and mating partner recognition. This research thus provides a base from which further interrogation of this topic can take place.

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Mechanisms of Manganese(II) Oxidation by Filamentous Ascomycete Fungi Vary With Species and Time as a Function of Secretome Composition

Frontiers in Microbiology ◽

10.3389/fmicb.2021.610497 ◽

2021 ◽

Vol 12 ◽

Author(s):

Carolyn A. Zeiner ◽

Samuel O. Purvine ◽

Erika Zink ◽

Si Wu ◽

Ljiljana Paša-Tolić ◽

...

Keyword(s):

Physiological Role ◽

Oxidative Capacity ◽

White Rot ◽

Lignocellulose Degradation ◽

Filamentous Ascomycete ◽

Solid Substrates ◽

Gmc Oxidoreductase ◽

Ascomycete Fungi ◽

Species Specific ◽

Glyoxal Oxidase

Manganese (Mn) oxides are among the strongest oxidants and sorbents in the environment, and Mn(II) oxidation to Mn(III/IV) (hydr)oxides includes both abiotic and microbially-mediated processes. While white-rot Basidiomycete fungi oxidize Mn(II) using laccases and manganese peroxidases in association with lignocellulose degradation, the mechanisms by which filamentous Ascomycete fungi oxidize Mn(II) and a physiological role for Mn(II) oxidation in these organisms remain poorly understood. Here we use a combination of chemical and in-gel assays and bulk mass spectrometry to demonstrate secretome-based Mn(II) oxidation in three phylogenetically diverse Ascomycetes that is mechanistically distinct from hyphal-associated Mn(II) oxidation on solid substrates. We show that Mn(II) oxidative capacity of these fungi is dictated by species-specific secreted enzymes and varies with secretome age, and we reveal the presence of both Cu-based and FAD-based Mn(II) oxidation mechanisms in all 3 species, demonstrating mechanistic redundancy. Specifically, we identify candidate Mn(II)-oxidizing enzymes as tyrosinase and glyoxal oxidase in Stagonospora sp. SRC1lsM3a, bilirubin oxidase in Stagonospora sp. and Paraconiothyrium sporulosum AP3s5-JAC2a, and GMC oxidoreductase in all 3 species, including Pyrenochaeta sp. DS3sAY3a. The diversity of the candidate Mn(II)-oxidizing enzymes identified in this study suggests that the ability of fungal secretomes to oxidize Mn(II) may be more widespread than previously thought.

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SO, a Protein Involved in Hyphal Fusion in Neurospora crassa, Localizes to Septal Plugs

Eukaryotic Cell ◽

10.1128/ec.00268-06 ◽

2006 ◽

Vol 6 (1) ◽

pp. 84-94 ◽

Cited By ~ 56

Author(s):

André Fleiβner ◽

N. Louise Glass

Keyword(s):

Cell Death ◽

Neurospora Crassa ◽

Colony Development ◽

Independent Manner ◽

Hyphal Fusion ◽

Filamentous Ascomycete ◽

Sealing Material ◽

Woronin Body ◽

Local Injury ◽

Extensive Damage

ABSTRACT The colony of a filamentous ascomycete fungus typically grows as a multinucleate syncytium. While this syncytial organization has developmental advantages, it bears the risk of extensive damage caused by local injury of hyphae. Loss of cytoplasm in injured hyphae is restricted by the fast and efficient sealing of the central pores of hyphal crosswalls, or septa, by a peroxisome-derived organelle called the Woronin body. The formation of septal plugs is also associated with development and leads to separation of certain parts of the colony. Septal plugs associated with developmental processes or aging hyphae typically occur by the accumulation of sealing material. Here we report that in Neurospora crassa, a protein necessary for hyphal fusion and proper colony development called SO (SOFT) localizes to septal plugs. In response to injury, SO accumulates at the septal plug in a Woronin body-independent manner. However, the presence of the Woronin body affects the speed of accumulation of SO at the septal pore. We determined that SO contributes to, but is not essential for, septal plugging. SO accumulation was also observed at septal plugs formed during hyphal aging and during programmed cell death mediated by genetic differences at heterokaryon incompatibility (het) loci.

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The so Locus Is Required for Vegetative Cell Fusion and Postfertilization Events in Neurospora crassa

Eukaryotic Cell ◽

10.1128/ec.4.5.920-930.2005 ◽

2005 ◽

Vol 4 (5) ◽

pp. 920-930 ◽

Cited By ~ 93

Author(s):

André Fleißner ◽

Sovan Sarkar ◽

David J. Jacobson ◽

M. Gabriela Roca ◽

Nick D. Read ◽

...

Keyword(s):

Neurospora Crassa ◽

Cell Fusion ◽

Protein Interactions ◽

Cell Communication ◽

Model Organism ◽

Female Sterility ◽

Wild Type ◽

Hyphal Fusion ◽

Filamentous Ascomycete ◽

Ascomycete Yeast

ABSTRACT The process of cell fusion is a basic developmental feature found in most eukaryotic organisms. In filamentous fungi, cell fusion events play an important role during both vegetative growth and sexual reproduction. We employ the model organism Neurospora crassa to dissect the mechanisms of cell fusion and cell-cell communication involved in fusion processes. In this study, we characterized a mutant with a mutation in the gene so, which exhibits defects in cell fusion. The so mutant has a pleiotropic phenotype, including shortened aerial hyphae, an altered conidiation pattern, and female sterility. Using light microscopy and heterokaryon tests, the so mutant was shown to possess defects in germling and hyphal fusion. Although so produces conidial anastomosis tubes, so germlings did not home toward wild-type germlings nor were wild-type germlings attracted to so germlings. We employed a trichogyne attraction and fusion assay to determine whether the female sterility of the so mutant is caused by impaired communication or fusion failure between mating partners. so showed no defects in attraction or fusion between mating partners, indicating that so is specific for vegetative hyphal fusion and/or associated communication events. The so gene encodes a protein of unknown function, but which contains a WW domain; WW domains are predicted to be involved in protein-protein interactions. Database searches showed that so was conserved in the genomes of filamentous ascomycete fungi but was absent in ascomycete yeast and basidiomycete species.

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