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 »
- Authors:
-
- Univ. of California, Berkeley, CA (United States); Univ. of Bordeaux, Pessac (France)
- Univ. Montpellier (France)
- 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}
}
Web of Science
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- figshare
Programmed Cell Death in Neurospora crassa Is Controlled by the Allorecognition Determinant rcd-1
dataset, January 2019
- Gladieux, Pierre; Glass, N. Louise; Daskalov, Asen
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Identification of Allorecognition Loci in Neurospora crassa by Genomics and Evolutionary Approaches
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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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Sterilizing immunity in the lung relies on targeting fungal apoptosis-like programmed cell death
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EggLib: processing, analysis and simulation tools for population genetics and genomics
journal, January 2012
- De Mita, Stéphane; Siol, Mathieu
- BMC Genetics, Vol. 13, Issue 1
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy
journal, August 2015
- Emms, David M.; Kelly, Steven
- Genome Biology, Vol. 16, Issue 1
Characterization of Greenbeard Genes Involved in Long-Distance Kind Discrimination in a Microbial Eukaryote
journal, April 2016
- Heller, Jens; Zhao, Jiuhai; Rosenfield, Gabriel
- PLOS Biology, Vol. 14, Issue 4
Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
journal, July 2012
- Sun, Yu; Corcoran, Pádraic; Menkis, Audrius
- PLoS Genetics, Vol. 8, Issue 7
Genome Wide Association Identifies Novel Loci Involved in Fungal Communication
journal, August 2013
- Palma-Guerrero, Javier; Hall, Charles R.; Kowbel, David
- PLoS Genetics, Vol. 9, Issue 8
Evolution and Diversity of a Fungal Self/Nonself Recognition Locus
journal, November 2010
- Hall, Charles; Welch, Juliet; Kowbel, David J.
- PLoS ONE, Vol. 5, Issue 11
Vegetative compatibility groups partition variation in the virulence of Verticillium dahliae on strawberry
journal, February 2018
- Fan, Rong; Cockerton, Helen M.; Armitage, Andrew D.
- PLOS ONE, Vol. 13, Issue 2
Do fungi have an innate immune response? An NLR-based comparison to plant and animal immune systems
journal, October 2017
- Uehling, Jessie; Deveau, Aurélie; Paoletti, Mathieu
- PLOS Pathogens, Vol. 13, Issue 10
Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora tetrasperma
journal, July 2011
- Ellison, Christopher E.; Stajich, Jason E.; Jacobson, David J.
- Genetics, Vol. 189, Issue 1
Vegetative Incompatibility Loci with Dedicated Roles in Allorecognition Restrict Mycovirus Transmission in Chestnut Blight Fungus
journal, April 2014
- Zhang, Dong-Xiu; Spiering, Martin J.; Dawe, Angus L.
- Genetics, Vol. 197, Issue 2
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
Regulated Forms of Cell Death in Fungi
journal, September 2017
- Gonçalves, A. Pedro; Heller, Jens; Daskalov, Asen
- Frontiers in Microbiology, Vol. 8
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