Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa

Marek, Stephen M.; Wu, Jennifer D.; Glass, N. Louise; Gilchrist, David G.; Bostock, Richard M.

doi:10.1016/s1087-1845(03)00086-0

Cited by 59 publications

(45 citation statements)

References 74 publications

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“…A het-c-incompatible heterokaryon (FGSC 4564 ϩ JH1) grew ϳ2 cm/day and showed 30% hyphal death throughout the colony, similar to previous results (36,52,87). A mat-incompatible heterokaryon (JH1 ϩ C9-2) grew ϳ1 cm/day and showed 34% hyphal death.…”

Section: Vib-1 Is a Nucleus-localized Proteinsupporting

confidence: 89%

VIB-1 Is Required for Expression of Genes Necessary for Programmed Cell Death in Neurospora crassa

2006

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Nonself recognition during somatic growth is an essential and ubiquitous phenomenon in both prokaryotic and eukaryotic species. In filamentous fungi, nonself recognition is also important during vegetative growth. Hyphal fusion between genetically dissimilar individuals results in rejection of heterokaryon formation and in programmed cell death of the fusion compartment. In filamentous fungi, such as Neurospora crassa, nonself recognition and heterokaryon incompatibility (HI) are regulated by genetic differences at het loci. In N. crassa, mutations at the vib-1 locus suppress nonself recognition and HI mediated by genetic differences at het-c/pin-c, mat, and un-24/het-6. vib-1 is a homolog of Saccharomyces cerevisiae NDT80, which is a transcriptional activator of genes during meiosis. For this study, we determined that vib-1 encodes a nuclear protein and showed that VIB-1 localization varies during asexual reproduction and during HI. vib-1 is required for the expression of genes involved in nonself recognition and HI, including pin-c, tol, and het-6; all of these genes encode proteins containing a HET domain. vib-1 is also required for the production of downstream effectors associated with HI, including the production of extracellular proteases upon carbon and nitrogen starvation. Our data support a model in which mechanisms associated with starvation and nonself recognition/HI are interconnected. VIB-1 is a major regulator of responses to nitrogen and carbon starvation and is essential for the expression of genes involved in nonself recognition and death in N. crassa.Nonself recognition during somatic growth is an essential and ubiquitous phenomenon in both prokaryotic and eukaryotic species. In vertebrate species, self/nonself recognition relies on the major histocompatibility complex (MHC), which is an array of polymorphic genetic loci that generate proteins important in pathogen recognition and the activation of defense mechanisms (37). In filamentous fungi, nonself recognition is important during vegetative growth. Hyphal fusion between genetically dissimilar individuals results in rejection of heterokaryon formation and in programmed cell death of the fusion compartment (Fig. 1), an event analogous to nonself recognition following fusion in colonial marine invertebrates, such as Hydractinia and Botryllus (32, 73), and nonself recognition and death following fusion of plasmodia in the slime mold Physarum polycephalum (9). Nonself recognition during heterokaryon formation in filamentous fungi is regulated genetically by het loci (for heterokaryon incompatibility [HI]) (29,70,86). In the filamentous fungus Neurospora crassa, 11 het loci mediate nonself recognition and HI (28, 63); each het locus has two or three alternative allelic specificities. Since these het loci are effectively unlinked, the number of possible het genotypes within a segregating population is at least 2 11 genotypes, thus forming an effective barrier to heterokaryon formation between genetically different isolates. HI in filamentous fungi...

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Section: Vib-1 Is a Nucleus-localized Proteinsupporting

confidence: 89%

VIB-1 Is Required for Expression of Genes Necessary for Programmed Cell Death in Neurospora crassa

2006

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“…8 and 9 need to be studied in more detail in C. heterostrophus and other fungi for which signal transduction mutants are available. Similar patterns of DNA staining have been observed in N. crassa strains undergoing vegetative incompatibility, suggesting that the interaction of incompatible het alleles leads to programmed cell death (24). There is precedent in the animal cell literature for either the promotion or the inhibition of apoptosis by G-protein signaling pathways.…”

Section: Discussionmentioning

confidence: 53%

G-Protein β Subunit of Cochliobolus heterostrophus Involved in Virulence, Asexual and Sexual Reproductive Ability, and Morphogenesis

Ganem

Lee

et al. 2004

Eukaryot Cell

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Previous work established that mutations in mitogen-activated protein (MAP) kinase (CHK1) and heterotrimeric G-protein ␣ (G␣) subunit (CGA1) genes affect the development of several stages of the life cycle of the maize pathogen Cochliobolus heterostrophus. The effects of mutating a third signal transduction pathway gene, CGB1, encoding the G␤ subunit, are reported here. CGB1 is the sole G␤ subunit-encoding gene in the genome of this organism. cgb1 mutants are nearly wild type in vegetative growth rate; however, Cgb1 is required for appressorium formation, female fertility, conidiation, regulation of hyphal pigmentation, and wild-type virulence on maize. Young hyphae of cgb1 mutants grow in a straight path, in contrast to those of the wild type, which grow in a wavy pattern. Some of the phenotypes conferred by mutations in CGA1 are found in cgb1 mutants, suggesting that Cgb1 functions in a heterotrimeric G protein; however, there are also differences. In contrast to the deletion of CGA1, the loss of CGB1 is not lethal for ascospores, evidence that there is a G␤ subunit-independent signaling role for Cga1 in mating. Furthermore, not all of the phenotypes conferred by mutations in the MAP kinase CHK1 gene are found in cgb1 mutants, implying that the G␤ heterodimer is not the only conduit for signals to the MAP kinase CHK1 module. The additional phenotypes of cgb1 mutants, including severe loss of virulence on maize and of the ability to produce conidia, are consistent with CGB1 being unique in the genome. Fluorescent DNA staining showed that there is often nuclear degradation in mature hyphae of cgb1 mutants, while comparable wild-type cells have intact nuclei. These data may be genetic evidence for a novel cell death-related function of the G␤ subunit in filamentous fungi.

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“…Although HI displays some downstream characteristics of apoptosis observed in metazoans (Jacobson et al, 1998;Leslie & Zeller, 1996;Marek et al, 2003), the induction of death via nonself recognition and HI may occur by a filamentous-fungal-specific process. Many genes required for HI in filamentous fungi encode proteins containing a HET domain (PF06985), including PIN-C (Kaneko et al, 2006), and which are ubiquitous in the genomes of filamentous ascomycete species, but are notably absent from all other eukaryotic and prokaryotic species.…”

Section: Dncu09882mentioning

confidence: 99%

“…The stability of heterokaryons formed by nonself fusion events is dependent on allelic specificity at nonself recognition loci termed het (for heterokaryon) or vcg (for vegetative compatibility group) (Garnjobst & Wilson, 1956;Leslie & Zeller, 1996;Saupe, 2000). If individuals that differ in het allelic specificity undergo hyphal fusion, the fusion cell is rapidly compartmentalized by septal plugging and dies (Biella et al, 2002;Jacobson et al, 1998;Marek et al, 2003). Heterokaryon incompatibility (HI) is associated with restriction of viral transfer between fungal individuals and prevention of resource plundering (Biella et al, 2002;Debets & Griffiths, 1998;Debets et al, 1994;van Diepeningen et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

“…Heterokaryon incompatibility (HI) is associated with restriction of viral transfer between fungal individuals and prevention of resource plundering (Biella et al, 2002;Debets & Griffiths, 1998;Debets et al, 1994;van Diepeningen et al, 1997). Hyphal death during HI shows some features that are similar to apoptosis in mammalian cells, including shrinkage of plasma membrane, membrane-bound vesicle formation, DNA condensation and TUNEL-positive nuclei (Biella et al, 2002;Jacobson et al, 1998;Leslie & Zeller, 1996;Marek et al, 2003). Markers associated with apoptosis have also been reported upon exposure of various filamentous fungi to treatment with H 2 O 2 , acetic acid, farnesol, sphingolipids and amphotericin B (Castro et al, 2008;Chen & Dickman, 2005;Cheng et al, 2003;Leiter et al, 2005;Mousavi & Robson, 2004;Phillips et al, 2003;Semighini et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death

et al. 2009

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Heterokaryon incompatibility (HI) is a nonself recognition phenomenon occurring in filamentous fungi that is important for limiting resource plundering and restricting viral transfer between strains. Nonself recognition and HI occurs during hyphal fusion between strains that differ at het loci. If two strains undergo hyphal fusion, but differ in allelic specificity at a het locus, the fusion cell is compartmentalized and undergoes a rapid programmed cell death (PCD). Incompatible heterokaryons show a macroscopic phenotype of slow growth and diminished conidiation, and a microscopic phenotype of hyphal compartmentation and cell death. To understand processes associated with HI and PCD, we used whole-genome microarrays for Neurospora crassa to assess transcriptional differences associated with induction of HI mediated by differences in het-c pin-c haplotype. Our data show that HI is a dynamic and transcriptionally active process. The production of reactive oxygen species is implicated in the execution of HI and PCD in N. crassa, as are several genes involved in phosphatidylinositol and calcium signalling pathways. However, genes encoding mammalian homologues of caspases or apoptosis-inducing factor (AIF) are not required for HI or programmed cell death. These data indicate that PCD during HI occurs via a novel and possibly fungal-specific mechanism, making this pathway an attractive drug target for control of fungal infections.

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Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa

Cited by 59 publications

References 74 publications

VIB-1 Is Required for Expression of Genes Necessary for Programmed Cell Death in Neurospora crassa

VIB-1 Is Required for Expression of Genes Necessary for Programmed Cell Death in Neurospora crassa

G-Protein β Subunit of Cochliobolus heterostrophus Involved in Virulence, Asexual and Sexual Reproductive Ability, and Morphogenesis

Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death

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