scholarly journals Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1

Genetics ◽  
2019 ◽  
Vol 213 (4) ◽  
pp. 1387-1400 ◽  
Author(s):  
Asen Daskalov ◽  
Pierre Gladieux ◽  
Jens Heller ◽  
N. Louise Glass
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Neurospora Crassa ◽  
Filamentous Fungi ◽  
Fungal Pathogens ◽  
Defense Mechanism ◽  
Balancing Selection ◽  
Nonself Recognition ◽  
Fusion Cell ◽  
Necessary And Sufficient

Nonself recognition following cell fusion between genetically distinct individuals of the same species in filamentous fungi often results in a programmed cell death (PCD) reaction, where the heterokaryotic fusion cell is compartmentalized and rapidly killed. The allorecognition process plays a key role as a defense mechanism that restricts genome exploitation, resource plundering, and the spread of deleterious senescence plasmids and mycoviruses. Although a number of incompatibility systems have been described that function in mature hyphae, less is known about the PCD pathways in asexual spores, which represent the main infectious unit in various human and plant fungal pathogens. Here, we report the identification of regulator of cell death-1 (rcd-1), a novel allorecognition gene, controlling PCD in germinating asexual spores of Neurospora crassa; rcd-1 is one of the most polymorphic genes in the genomes of wild N. crassa isolates. The coexpression of two antagonistic rcd-1-1 and rcd-1-2 alleles was necessary and sufficient to trigger cell death in fused germlings and in hyphae. Based on analysis of wild populations of N. crassa and N. discreta, rcd-1 alleles appeared to be under balancing selection and associated with trans-species polymorphisms. We shed light on genomic rearrangements that could have led to the emergence of the incompatibility system in Neurospora and show that rcd-1 belongs to a much larger gene family in fungi. Overall, our work contributes toward a better understanding of allorecognition and PCD in an underexplored developmental stage of filamentous fungi.

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

2006 ◽  
Vol 5 (12) ◽  
pp. 2161-2173 ◽  
Author(s):  
Karine Dementhon ◽  
Gopal Iyer ◽  
N. Louise Glass
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Neurospora Crassa ◽  
Filamentous Fungi ◽  
Somatic Growth ◽  
Genetic Differences ◽  
Extracellular Proteases ◽  
Hyphal Fusion ◽  
Expression Of Genes ◽  
Nonself Recognition

ABSTRACT 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.

scholarly journals 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

Microbiology ◽  
2009 ◽  
Vol 155 (12) ◽  
pp. 3957-3970 ◽  
Author(s):  
Elizabeth Hutchison ◽  
Sarah Brown ◽  
Chaoguang Tian ◽  
N. Louise Glass
Keyword(s):  
Reactive Oxygen Species ◽  
Cell Death ◽  
Programmed Cell Death ◽  
Neurospora Crassa ◽  
Fungal Infections ◽  
Reactive Oxygen ◽  
Oxygen Species ◽  
Hyphal Fusion ◽  
Heterokaryon Incompatibility ◽  
Nonself Recognition

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.

Binary cell death decision regulated by unequal partitioning of Numb at mitosis

Development ◽  
2002 ◽  
Vol 129 (20) ◽  
pp. 4677-4684 ◽  
Author(s):  
Virginie Orgogozo ◽  
François Schweisguth ◽  
Yohanns Bellaïche
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Daughter Cell ◽  
Asymmetric Cell Divisions ◽  
Daughter Cells ◽  
Cell Divisions ◽  
Specific Manner ◽  
Asymmetric Divisions ◽  
Apoptotic Genes ◽  
Necessary And Sufficient

An important issue in Metazoan development is to understand the mechanisms that lead to stereotyped patterns of programmed cell death. In particular, cells programmed to die may arise from asymmetric cell divisions. The mechanisms underlying such binary cell death decisions are unknown. We describe here a Drosophila sensory organ lineage that generates a single multidentritic neuron in the embryo. This lineage involves two asymmetric divisions. Following each division, one of the two daughter cells expresses the pro-apoptotic genes reaper and grim and subsequently dies. The protein Numb appears to be specifically inherited by the daughter cell that does not die. Numb is necessary and sufficient to prevent apoptosis in this lineage. Conversely, activated Notch is sufficient to trigger death in this lineage. These results show that binary cell death decision can be regulated by the unequal segregation of Numb at mitosis. Our study also indicates that regulation of programmed cell death modulates the final pattern of sensory organs in a segment-specific manner.

Reduced glutathione export during programmed cell death of Neurospora crassa

APOPTOSIS ◽  
2013 ◽  
Vol 18 (8) ◽  
pp. 940-948 ◽  
Author(s):  
Andreia S. Fernandes ◽  
Ana Castro ◽  
Arnaldo Videira
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Neurospora Crassa ◽  
Reduced Glutathione

scholarly journals A novel gene, phcA from Pseudomonas syringae induces programmed cell death in the filamentous fungus Neurospora crassa

2008 ◽  
Vol 68 (3) ◽  
pp. 672-689 ◽  
Author(s):  
Gale Wichmann ◽  
Jianping Sun ◽  
Karine Dementhon ◽  
N. Louise Glass ◽  
Steven E. Lindow
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Neurospora Crassa ◽  
Pseudomonas Syringae ◽  
Filamentous Fungus ◽  
Novel Gene

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

2001 ◽  
Vol 21 (4) ◽  
pp. 1045-1057 ◽  
Author(s):  
Jennifer Wu ◽  
N. Louise Glass
Keyword(s):  
Amino Acid ◽  
Neurospora Crassa ◽  
Filamentous Fungi ◽  
Vegetative Growth ◽  
Molecular Model ◽  
Variable Domain ◽  
Hyphal Fusion ◽  
Nonself Recognition ◽  
Incompatibility Locus ◽  
Specificity Determinants

ABSTRACT 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. InNeurospora 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-cOR, het-cPA , and het-cGR . 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-COR, HET-CPA, and HET-CGR, 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-cspecificity 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.

scholarly journals Comparative analysis of programmed cell death pathways in filamentous fungi

BMC Genomics ◽  
2005 ◽  
Vol 6 (1) ◽  
Author(s):  
Natalie D Fedorova ◽  
Jonathan H Badger ◽  
Geoff D Robson ◽  
Jennifer R Wortman ◽  
William C Nierman
Keyword(s):  
Cell Death ◽  
Comparative Analysis ◽  
Programmed Cell Death ◽  
Filamentous Fungi ◽  
Cell Death Pathways

scholarly journals Molecular characterization of a fungal gasdermin-like protein

2020 ◽  
Vol 117 (31) ◽  
pp. 18600-18607 ◽  
Author(s):  
Asen Daskalov ◽  
Patrick S. Mitchell ◽  
Andrew Sandstrom ◽  
Russell E. Vance ◽  
N. Louise Glass
Keyword(s):  
Cell Death ◽  
Cellular Localization ◽  
Defense Mechanism ◽  
Evolutionary Relationship ◽  
Cell Periphery ◽  
Dependent Cell ◽  
A Cell ◽  
Necessary And Sufficient ◽  
Relationship Of

Programmed cell death (PCD) in filamentous fungi prevents cytoplasmic mixing following fusion between conspecific genetically distinct individuals (allorecognition) and serves as a defense mechanism against mycoparasitism, genome exploitation, and deleterious cytoplasmic elements (i.e., senescence plasmids). Recently, we identifiedregulatorof cell death-1(rcd-1), a gene controlling PCD in germinated asexual spores in the filamentous fungusNeurospora crassa.rcd-1alleles are highly polymorphic and fall into two haplogroups inN. crassapopulations. Coexpression of alleles from the two haplogroups,rcd-1–1andrcd-1–2, is necessary and sufficient to trigger a cell death reaction. Here, we investigated the molecular bases ofrcd-1-dependent cell death. Based on in silico analyses, we found that RCD-1 is a remote homolog of the N-terminal pore-forming domain of gasdermin, the executioner protein of a highly inflammatory cell death reaction termed pyroptosis, which plays a key role in mammalian innate immunity. We show that RCD-1 localizes to the cell periphery and that cellular localization of RCD-1 was correlated with conserved positively charged residues on predicted amphipathic α-helices, as shown for murine gasdermin-D. Similar to gasdermin, RCD-1 binds acidic phospholipids in vitro, notably, cardiolipin and phosphatidylserine, and interacts with liposomes containing such lipids. The RCD-1 incompatibility system was reconstituted in human 293T cells, where coexpression of incompatiblercd-1–1/rcd-1–2alleles triggered pyroptotic-like cell death. Oligomers of RCD-1 were associated with the cell death reaction, further supporting the evolutionary relationship between gasdermin andrcd-1. This report documents an ancient transkingdom relationship of cell death execution modules involved in organismal defense.

Apoptosis-like programmed cell death in the grey mould fungus Botrytis cinerea: genes and their role in pathogenicity

2011 ◽  
Vol 39 (5) ◽  
pp. 1493-1498 ◽  
Author(s):  
Neta Shlezinger ◽  
Adi Doron ◽  
Amir Sharon
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Botrytis Cinerea ◽  
Fungal Pathogens ◽  
Grey Mould ◽  
Fungal Species ◽  
Fungal Virulence ◽  
Mould Fungus ◽  
Apoptosis Protein ◽  
Result Show

A considerable number of fungal homologues of human apoptotic genes have been identified in recent years. Nevertheless, we are far from being able to connect the different pieces and construct a primary structure of the fungal apoptotic regulatory network. To get a better picture of the available fungal components, we generated an automatic search protocol that is based on protein sequences together with a domain-centred approach. We used this protocol to search all the available fungal databases for domains and homologues of human apoptotic proteins. Among all known apoptotic domains, only the BIR [baculovirus IAP (inhibitor of apoptosis protein) repeat] domain was found in fungi. A single protein with one or two BIR domains is present in most (but not all) fungal species. We isolated the BIR-containing protein from the grey mould fungus Botrytis cinerea and determined its role in apoptosis and pathogenicity. We also isolated and analysed BcNMA, a homologue of the yeast NMA11 gene. Partial knockout or overexpression strains of BcBIR1 confirmed that BcBir1 is anti-apoptotic and this activity was assigned to the N′-terminal part of the protein. Plant infection assays showed that the fungus undergoes massive PCD (programmed cell death) during early stages of infection. Further studies showed that fungal virulence was fully correlated with the ability of the fungus to cope with plant-induced PCD. Together, our result show that BcBir1 is a major regulator of PCD in B. cinerea and that proper regulation of the host-induced PCD is essential for pathogenesis in this and other similar fungal pathogens.

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