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Title: Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1

Abstract

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 ofmore » 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.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [3]
  1. Univ. of California, Berkeley, CA (United States); Univ. of Bordeaux, Pessac (France)
  2. Univ. Montpellier (France)
  3. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1591842
Grant/Contract Number:  
AC02-05CH11231; S10RR029668; S10RR027303
Resource Type:
Accepted Manuscript
Journal Name:
Genetics
Additional Journal Information:
Journal Volume: 213; Journal Issue: 4; Journal ID: ISSN 0016-6731
Publisher:
Genetics Society of America
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; neurospora; programmed cell death; allorecognition; heterokaryon; incompatibility; cell fusion

Citation Formats

Daskalov, Asen, Gladieux, Pierre, Heller, Jens, and Glass, N. Louise. Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1. United States: N. p., 2019. Web. doi:10.1534/genetics.119.302617.
Daskalov, Asen, Gladieux, Pierre, Heller, Jens, & Glass, N. Louise. Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1. United States. https://doi.org/10.1534/genetics.119.302617
Daskalov, Asen, Gladieux, Pierre, Heller, Jens, and Glass, N. Louise. Mon . "Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1". United States. https://doi.org/10.1534/genetics.119.302617. https://www.osti.gov/servlets/purl/1591842.
@article{osti_1591842,
title = {Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1},
author = {Daskalov, Asen and Gladieux, Pierre and Heller, Jens and Glass, N. Louise},
abstractNote = {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.},
doi = {10.1534/genetics.119.302617},
journal = {Genetics},
number = 4,
volume = 213,
place = {United States},
year = {Mon Oct 21 00:00:00 EDT 2019},
month = {Mon Oct 21 00:00:00 EDT 2019}
}

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NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi
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Diversity and Variability of NOD-Like Receptors in Fungi
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Identification of Allorecognition Loci in Neurospora crassa by Genomics and Evolutionary Approaches
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  • Zhao, Jiuhai; Gladieux, Pierre; Hutchison, Elizabeth
  • Molecular Biology and Evolution, Vol. 32, Issue 9
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HMMER web server: interactive sequence similarity searching
journal, May 2011

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Genomic sequencing reveals historical, demographic and selective factors associated with the diversification of the fire-associated fungus Neurospora discreta
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Intracellular innate immune surveillance devices in plants and animals
journal, December 2016


Sterilizing immunity in the lung relies on targeting fungal apoptosis-like programmed cell death
journal, September 2017


Hidden Killers: Human Fungal Infections
journal, December 2012


Molecular Trans-Species Polymorphism
journal, November 1998


Automated generation of heuristics for biological sequence comparison
journal, February 2005


EggLib: processing, analysis and simulation tools for population genetics and genomics
journal, January 2012


Characterization of Greenbeard Genes Involved in Long-Distance Kind Discrimination in a Microbial Eukaryote
journal, April 2016


Genome Wide Association Identifies Novel Loci Involved in Fungal Communication
journal, August 2013


Evolution and Diversity of a Fungal Self/Nonself Recognition Locus
journal, November 2010


Vegetative compatibility groups partition variation in the virulence of Verticillium dahliae on strawberry
journal, February 2018


Do fungi have an innate immune response? An NLR-based comparison to plant and animal immune systems
journal, October 2017


Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora tetrasperma
journal, July 2011


Vegetative Incompatibility Loci with Dedicated Roles in Allorecognition Restrict Mycovirus Transmission in Chestnut Blight Fungus
journal, April 2014


A Multilocus Genealogical Approach to Phylogenetic Species Recognition in the Model Eukaryote Neurospora
journal, January 2003

  • Dettman, Jeremy R.; Jacobson, David J.; Taylor, John W.
  • Evolution, Vol. 57, Issue 12
  • DOI: 10.1554/03-073

Regulated Forms of Cell Death in Fungi
journal, September 2017


Allorecognition and chimerism in an invertebrate model organism
journal, October 2008

  • Lakkis, Fadi G.; Dellaporta, Stephen L.; Buss, Leo W.
  • Organogenesis, Vol. 4, Issue 4
  • DOI: 10.4161/org.4.4.7151