Fatal Attraction: Nonself Recognition and Heterokaryon Incompatibility in Filamentous Fungi

Glass, N. Louise; Kaneko, Isao

doi:10.1128/ec.2.1.1-8.2003

Cited by 240 publications

(226 citation statements)

References 82 publications

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“…Another intriguing possibility concerns the effects of genetic background on the efficiency of nuclear fusion. It is still too early to ascertain whether C. albicans has a set of genes controlling heterokaryon incompatibility, as has been well documented for certain filamentous ascomycete fungi (for reviews, see Saupe, 2000;Glass and Kaneko, 2003), but it appears that the efficiency of nuclear fusion is not linked to how similar the genetic backgrounds of the two mating strains are. A more likely possibility is that some natural isolates of C. albicans are defective in the expression of components required for nuclear fusion.…”

Section: Discussionmentioning

confidence: 99%

Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene

Bennett

Miller

Chua

et al. 2005

Molecular Microbiology

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SummaryIt is now well established that mating can occur between diploid a and a a a a cells of Candida albicans . There is, however, controversy over when, and with what efficiency, nuclear fusion follows cell fusion to create stable tetraploid a/ a a a a cells. In this study, we have analysed the mating process between C. albicans strains using both cytological and genetic approaches. Using strains derived from SC5314, we used a number of techniques, including time-lapse microscopy, to demonstrate that efficient nuclear fusion occurs in the zygote before formation of the first daughter cell. Consistent with these observations, zygotes micromanipulated from mating mixes gave rise to mononuclear tetraploid cells, even when no selection for successful mating was applied to them. Mating between different clinical isolates of C. albicans revealed that while all isolates could undergo nuclear fusion, the efficiency of nuclear fusion varied in different crosses. We also show that nuclear fusion in C. albicans requires the Kar3 microtubule motor protein. Deletion of the CaKAR3 gene from both mating partners had little or no effect on zygote formation but reduced the formation of stable tetraploids more than 600-fold, as determined by quantitative mating assays. These findings demonstrate that nuclear fusion is an active process that can occur in C. albicans at high frequency to produce stable, mononucleate mating products.

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Section: Discussionmentioning

confidence: 99%

Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene

Bennett

Miller

Chua

et al. 2005

Molecular Microbiology

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“…Self/ nonself discrimination becomes critical for filamentous fungi during hyphal fusion, which enables the exchange of cytoplasm and nuclei during the assimilative growth phase (1)(2)(3)(4). Nonself recognition triggers a postfusion, programmed cell death process known as vegetative incompatibility, which leads to heterokaryon death.…”

mentioning

confidence: 99%

“…het genes exhibit extensive polymorphism and generally encode proteins carrying a HET domain (1)(2)(3)(4). Originally, this domain was linked to the het-c2 gene of P. anserina, where it was shown to encode a protein similar in size and with limited sequence homology to mammalian glycolipid transfer proteins (GLTPs) 5 (5,6).…”

mentioning

confidence: 99%

Structural Determination and Tryptophan Fluorescence of Heterokaryon Incompatibility C2 Protein (HET-C2), a Fungal Glycolipid Transfer Protein (GLTP), Provide Novel Insights into Glycolipid Specificity and Membrane Interaction by the GLTP Fold

Kenoth

Simanshu

Kamlekar

et al. 2010

Journal of Biological Chemistry

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HET-C2 is a fungal protein that transfers glycosphingolipids between membranes and has limited sequence homology with human glycolipid transfer protein (GLTP). The human GLTP fold is unique among lipid binding/transfer proteins, defining the GLTP superfamily. Herein, GLTP fold formation by HET-C2, its glycolipid transfer specificity, and the functional role(s) of its two Trp residues have been investigated. X-ray diffraction (1.9 Å ) revealed a GLTP fold with all key sugar headgroup recognition residues (Asp 66 , Asn 70 , Lys 73 , Trp 109 , and His 147 ) conserved and properly oriented for glycolipid binding. Far-UV CD showed secondary structure dominated by ␣-helices and a cooperative thermal unfolding transition of 49°C, features consistent with a GLTP fold. Environmentally induced optical activity of Trp/Tyr/Phe (2:4:12) detected by near-UV CD was unaffected by membranes containing glycolipid but was slightly altered by membranes lacking glycolipid. Trp fluorescence was maximal at ϳ355 nm and accessible to aqueous quenchers, indicating free exposure to the aqueous milieu and consistent with surface localization of the two Trps. Interaction with membranes lacking glycolipid triggered significant decreases in Trp emission intensity but lesser than decreases induced by membranes containing glycolipid. Binding of glycolipid (confirmed by electrospray injection mass spectrometry) resulted in a blue-shifted emission wavelength maximum (ϳ6 nm) permitting determination of binding affinities. The unique positioning of Trp 208 at the HET-C2 C terminus revealed membrane-induced conformational changes that precede glycolipid uptake, whereas key differences in residues of the sugar headgroup recognition center accounted for altered glycolipid specificity and suggested evolutionary adaptation for the simpler glycosphingolipid compositions of filamentous fungi.Self/nonself recognition is a universally important process, encompassing intercellular interactions ranging from vertebrate immune responses to somatic chimera formation in protists, filamentous fungi, sponges, ascidians, and tunicates. Self/ nonself discrimination becomes critical for filamentous fungi during hyphal fusion, which enables the exchange of cytoplasm and nuclei during the assimilative growth phase (1-4). Nonself recognition triggers a postfusion, programmed cell death process known as vegetative incompatibility, which leads to heterokaryon death. The benefits of vegetative incompatibility include prevention of transmission of deleterious cytoplasmic elements (i.e. viruses) as well as restriction of plundering by parasitic genotypes.het genes are known to play a major role in vegetative incompatibility processes that occur in Neurospora crassa and Podospora anserina. het genes exhibit extensive polymorphism and generally encode proteins carrying a HET domain (1-4). Originally, this domain was linked to the het-c2 gene of P. anserina, where it was shown to encode a protein similar in size and with limited sequence homology to mammalian glycolipid transfer...

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“…PCD is also involved in eukaryotic nonself recognition, where cell death is triggered in infected plant and animal cells to prevent the spread of the infection to surrounding tissue (Greenberg and Yao, 2004;Hückelhoven, 2007). In fungi, PCD associated with nonself recognition or "PCD by incompatibility" limits vegetative hyphal fusion between genetically different individuals (Worral, 1997;Saupe, 2000;Glass and Kaneko, 2003). Although the exact biological function of PCD associated with the nonself recognition system in fungi is not yet clear, it has recently been suggested that it may also be involved in pathogen recognition (Chevanne et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…One method has been to use mutations that suppress PCD by incompatibility (Glass and Kaneko, 2003;Dementhon et al, 2004). For example, a mutation in the vib-1 (for vegetative incompatibility block) gene of N. crassa partly suppresses mating-type associated cell death, as well as het-c/pin-c induced cell death (Glass and Kaneko, 2003;Dementhon et al, 2004). Another approach has been to study differentially expressed genes that are specifically up-regulated during vegetative incompatibility, which led to the discovery of the induced during incompatibilty (idi) genes in P. anserina (Bourges et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Gene expression associated with vegetative incompatibility in Amylostereum areolatum

Nest¹,

Steenkamp²,

Slippers³

et al. 2011

Fungal Genetics and Biology

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In filamentous fungi, vegetative compatibility among individuals of the same species is determined by the genes encoded at the heterokaryon incompatibility (het) loci. The hyphae of genetically similar individuals that share the same allelic specificities at their het loci are able to fuse and intermingle, while different allelic specificities at the het loci result in cell death of the interacting hyphae. In this study, suppression subtractive hybridization (SSH) followed by pyrosequencing and quantitative reverse transcription PCR were used to identify genes that are selectively expressed when vegetatively incompatible individuals of Amylostereum areolatum interact. The SSH library contained genes associated with various cellular processes, including cell-cell adhesion, stress and defence responses, as well as cell death. Some of the transcripts encoded proteins that were previously implicated in the stress and defence responses associated with vegetative incompatibility. Other transcripts encoded proteins known to be associated with programmed cell death, but have not previously been linked with vegetative incompatibility.Results of this study have considerably increased our knowledge of the processes underlying vegetative incompatibility in Basidiomycetes in general and A. areolatum in particular.

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Fatal Attraction: Nonself Recognition and Heterokaryon Incompatibility in Filamentous Fungi

Cited by 240 publications

References 82 publications

Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene

Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene

Structural Determination and Tryptophan Fluorescence of Heterokaryon Incompatibility C2 Protein (HET-C2), a Fungal Glycolipid Transfer Protein (GLTP), Provide Novel Insights into Glycolipid Specificity and Membrane Interaction by the GLTP Fold

Gene expression associated with vegetative incompatibility in Amylostereum areolatum

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