Vegetative incompatibility in filamentous fungi: het genes begin to talk

Bégueret, Joël; Turcq, Béatrice; Clavé, Corinne

doi:10.1016/0168-9525(94)90115-5

Cited by 92 publications

(53 citation statements)

References 30 publications

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“…Work on the genetics of incompatibility in other ascomycetes will only be mentioned marginally. These aspects have been discussed more thoroughly in previous reviews (8,41,53).…”

Section: Scope Of the Reviewmentioning

confidence: 98%

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Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes

Saupe

2000

Microbiol Mol Biol Rev

312

284

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SUMMARY Filamentous fungi spontaneously undergo vegetative cell fusion events within but also between individuals. These cell fusions (anastomoses) lead to cytoplasmic mixing and to the formation of vegetative heterokaryons (i.e., cells containing different nuclear types). The viability of these heterokaryons is genetically controlled by specific loci termed het loci (for heterokaryon incompatibility). Heterokaryotic cells formed between individuals of unlike het genotypes undergo a characteristic cell death reaction or else are severely inhibited in their growth. The biological significance of this phenomenon remains a puzzle. Heterokaryon incompatibility genes have been proposed to represent a vegetative self/nonself recognition system preventing heterokaryon formation between unlike individuals to limit horizontal transfer of cytoplasmic infectious elements. Molecular characterization of het genes and of genes participating in the incompatibility reaction has been achieved for two ascomycetes, Neurospora crassa and Podospora anserina. These analyses have shown that het genes are diverse in sequence and do not belong to a gene family and that at least some of them perform cellular functions in addition to their role in incompatibility. Divergence between the different allelic forms of a het gene is generally extensive, but single-amino-acid differences can be sufficient to trigger incompatibility. In some instances het gene evolution appears to be driven by positive selection, which suggests that the het genes indeed represent recognition systems. However, work on nonallelic incompatibility systems in P. anserina suggests that incompatibility might represent an accidental activation of a cellular system controlling adaptation to starvation.

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“…Work on the genetics of incompatibility in other ascomycetes will only be mentioned marginally. These aspects have been discussed more thoroughly in previous reviews (8,41,53).…”

Section: Scope Of the Reviewmentioning

confidence: 98%

“…This rapidly generates extensive polymorphism. It has been proposed that "genes evolving by concerted evolution produce a selective force on the gene of their cognate interacting protein" (8). This requires no external forces.…”

Section: Nonallelic Incompatibilitymentioning

confidence: 99%

Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes

Saupe

2000

Microbiol Mol Biol Rev

312

284

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“…Alternatively, heterocomplex formation between HET-C proteins may result in the formation of a "poison" complex that affects normal cellular function of either the plasma membrane or endomembrane system. In P. anserina, a poison heteromeric complex model, in which heteromeric complexes between the products of incompatible genes are lethal to the cell, has been proposed for mediating vegetative incompatibility (2). The formation of such a complex may result in general growth inhibition and morphological changes, until a threshold of HET-C heterocomplex is formed and HCD is triggered.…”

Section: Discussionmentioning

confidence: 99%

Identification of Specificity Determinants and Generation of Alleles with Novel Specificity at the het-cHeterokaryon Incompatibility Locus of Neurospora crassa

Glass

2001

Molecular and Cellular Biology

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The capacity for nonself recognition is a ubiquitous and essential aspect of biology. In filamentous fungi, nonself recognition during vegetative growth is believed to be mediated by genetic differences at heterokaryon incompatibility (het) loci. Filamentous fungi are capable of undergoing hyphal fusion to form mycelial networks and with other individuals to form vegetative heterokaryons, in which genetically distinct nuclei occupy a common cytoplasm. In Neurospora crassa, 11 het loci have been identified that affect the viability of such vegetative heterokaryons. The het-c locus has at least three mutually incompatible alleles, termed het-c OR , het-c PA , and het-c GR . Hyphal fusion between strains that are of alternative het-c specificity results in vegetative heterokaryons that are aconidial and which show growth inhibition and hyphal compartmentation and death. A 34-to 48-amino-acid variable domain, which is dissimilar in HET-C OR , HET-C PA , and HET-C GR , confers allelic specificity. To assess requirements for allelic specificity, we constructed chimeras between the het-c variable domain from 24 different isolates that displayed amino acid and insertion or deletion variations and determined their het-c specificity by introduction into N. crassa. We also constructed a number of artificial alleles that contained novel het-c specificity domains. By this method, we identified four additional and novel het-c specificities. Our results indicate that amino acid and length variations within the insertion or deletion motif are the primary determinants for conferring het-c allelic specificity. These results provide a molecular model for nonself recognition in multicellular eucaryotes.The ability to distinguish self from nonself is a critical feature in most multicellular eucaryotic organisms for maintenance of integrity and individuality. In filamentous fungi, nonself recognition during vegetative growth is mediated through a system known as vegetative or heterokaryon incompatibility (22,29,37). A filamentous fungal individual grows as an interconnected network of multinuclear hyphal filaments that are formed via hyphal self-fusion. Filamentous fungi also possess the remarkable attribute of being able to undergo hyphal fusion between different individuals to form vegetative heterokaryons (genetically different nuclei in a common cytoplasm). However, if fungal individuals undergo hyphal fusion but differ in allelic specificity at any one of a number of heterokaryon incompatibility loci (het; sometimes referred to as vic for vegetative incompatibility), the hyphal fusion cell is compartmentalized and dies (Fig.

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“…Such interactions are commonly re- ported in other fungi, including Neurospora crassa and other ascomycetes (4,17) and in some myxomycetes (5). In those cases, the fungal population which has established growth actively inhibits coinfection by another strain of the same fungus.…”

Section: Discussionmentioning

confidence: 99%

“…In some fungal systems, the addition of a second fungal population to a host or artificial medium colonized by another population with a similar genetic background results in a destructive process causing organism loss in one or both populations (4,17). Since most P. carinii f. sp.…”

Section: Fig 5 Organism Burdens From Rats Inoculated With Combinationsmentioning

confidence: 99%

Time between Inoculations and Karyotype Forms ofPneumocystis cariniif. sp.cariniiInfluence Outcome of Experimental Coinfections in Rats

et al. 2001

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The prevalence of Pneumocystis carinii pneumonia (PCP) in humans caused by more than a single genotype has been reported to range from 10 to 67%, depending on the method used for detection (3, 19). Most coinfections were associated with primary rather than recurrent disease. To better understand the factors influencing the development of coinfections, the time periods between inoculations and the genotype of the infecting organisms were evaluated in the chronically immunosuppressed-inoculated rat model of PCP. P. carinii f. sp. carinii infecting rats differentiated by karyotypic profiles exhibit the same low level of genetic divergence manifested by organisms infecting humans. P. carinii f. sp. carinii karyotype forms 1, 2, and 6 were inoculated into immunosuppressed rats, individually and in dual combinations, spaced 0, 10, and 20 days apart. Infections comprised of both organism forms resulted from admixtures inoculated at the same time. In contrast, coinfections did not develop in most rats, where a 10-or 20-day gap was inserted between inoculations; only the first organism form inoculated was detected by pulsed-field gel electrophoresis in the resultant infection. Organism burdens were reduced with combinations of forms 1 and 2 spaced 20 days apart but not in rats inoculated with forms 1 and 6. A role for the host response in the elimination of the second population and in reduction of the organism burden was suggested by the lack of direct killing of forms 1 and 2 in an in vitro ATP assay, by reduction of the burden by autoclaved organisms, and by the specific reactions of forms 1 and 2 but not forms 1 and 6. These studies showed that the time between inoculations was critical in establishing coinfections and P. carinii f. sp. carinii karyotype profiles were associated with differences in biological responses. This model provides a useful method for the study of P. carinii coinfections and their transmission in humans.Organisms termed Pneumocystis carinii were placed in the Fungal kingdom more than 10 years ago on the basis of gene sequence comparisons (14, 29), yet much of their basic biological processes remains poorly understood, due in large part to their poor growth outside the mammalian lung environment (11). Recent genetic comparisons (32), as well as animal inoculation studies (16) and antigenic analyses (2, 15), provide strong evidence that "P. carinii" is actually a family of organisms that, although related, exhibit species specificity among its mammalian hosts.Comparisons at five genetic loci suggest three levels of genetic divergence are present among P. carinii organism populations (30). The highest level of divergence, class III, was observed among Pneumocystis populations isolated from different mammalian hosts and ranged from 5 to 50% divergence in nucleotide sequence at these selected loci, with the internal transcribed sequence (ITS) regions being most divergent. Class II divergence ranged from 4 to 7% for all genes, with a 20 to 30% difference at the ITS regions. Organisms demonstrating ...

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Vegetative incompatibility in filamentous fungi: het genes begin to talk

Cited by 92 publications

References 30 publications

Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes

Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes

Identification of Specificity Determinants and Generation of Alleles with Novel Specificity at the het-cHeterokaryon Incompatibility Locus of Neurospora crassa

Time between Inoculations and Karyotype Forms ofPneumocystis cariniif. sp.cariniiInfluence Outcome of Experimental Coinfections in Rats

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