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Title: NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi

Abstract

In plants and metazoans, intracellular receptors that belong to the NOD-like receptor (NLR) family are major contributors to innate immunity. Filamentous fungal genomes contain large repertoires of genes encoding for proteins with similar architecture to plant and animal NLRs with mostly unknown function. Here, we identify and molecularly characterize patatin-like phospholipase-1 (PLP-1), an NLR-like protein containing an N-terminal patatin-like phospholipase domain, a nucleotide-binding domain (NBD), and a C-terminal tetratricopeptide repeat (TPR) domain. PLP-1 guards the essential SNARE protein SEC-9; genetic differences at plp-1 and sec-9 function to trigger allorecognition and cell death in two distantly related fungal species, Neurospora crassa and Podospora anserina . Analyses of Neurospora population samples revealed that plp-1 and sec-9 alleles are highly polymorphic, segregate into discrete haplotypes, and show transspecies polymorphism. Upon fusion between cells bearing incompatible sec-9 and plp-1 alleles, allorecognition and cell death are induced, which are dependent upon physical interaction between SEC-9 and PLP-1. The central NBD and patatin-like phospholipase activity of PLP-1 are essential for allorecognition and cell death, while the TPR domain and the polymorphic SNARE domain of SEC-9 function in conferring allelic specificity. Our data indicate that fungal NLR-like proteins function similar to NLR immune receptors in plants andmore » animals, showing that NLRs are major contributors to innate immunity in plants and animals and for allorecognition in fungi.« less

Authors:
; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE; LBNL Laboratory Directed Research and Development (LDRD) Program; National Inst. of Health (NIH) (United States); German Research Foundation (DFG)
OSTI Identifier:
1421894
Alternate Identifier(s):
OSTI ID: 1506298
Grant/Contract Number:  
AC02-05CH11231; P01 GM068087; R01 GM060468; S10RR029668; S10RR027303; HE 7254/1-1
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 10; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; allorecognition; NOD-like receptors; SEC-9 SNARE; Neurospora; Podospora

Citation Formats

Heller, Jens, Clavé, Corinne, Gladieux, Pierre, Saupe, Sven J., and Glass, N. Louise. NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi. United States: N. p., 2018. Web. doi:10.1073/pnas.1719705115.
Heller, Jens, Clavé, Corinne, Gladieux, Pierre, Saupe, Sven J., & Glass, N. Louise. NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi. United States. doi:10.1073/pnas.1719705115.
Heller, Jens, Clavé, Corinne, Gladieux, Pierre, Saupe, Sven J., and Glass, N. Louise. Tue . "NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi". United States. doi:10.1073/pnas.1719705115.
@article{osti_1421894,
title = {NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi},
author = {Heller, Jens and Clavé, Corinne and Gladieux, Pierre and Saupe, Sven J. and Glass, N. Louise},
abstractNote = {In plants and metazoans, intracellular receptors that belong to the NOD-like receptor (NLR) family are major contributors to innate immunity. Filamentous fungal genomes contain large repertoires of genes encoding for proteins with similar architecture to plant and animal NLRs with mostly unknown function. Here, we identify and molecularly characterize patatin-like phospholipase-1 (PLP-1), an NLR-like protein containing an N-terminal patatin-like phospholipase domain, a nucleotide-binding domain (NBD), and a C-terminal tetratricopeptide repeat (TPR) domain. PLP-1 guards the essential SNARE protein SEC-9; genetic differences at plp-1 and sec-9 function to trigger allorecognition and cell death in two distantly related fungal species, Neurospora crassa and Podospora anserina . Analyses of Neurospora population samples revealed that plp-1 and sec-9 alleles are highly polymorphic, segregate into discrete haplotypes, and show transspecies polymorphism. Upon fusion between cells bearing incompatible sec-9 and plp-1 alleles, allorecognition and cell death are induced, which are dependent upon physical interaction between SEC-9 and PLP-1. The central NBD and patatin-like phospholipase activity of PLP-1 are essential for allorecognition and cell death, while the TPR domain and the polymorphic SNARE domain of SEC-9 function in conferring allelic specificity. Our data indicate that fungal NLR-like proteins function similar to NLR immune receptors in plants and animals, showing that NLRs are major contributors to innate immunity in plants and animals and for allorecognition in fungi.},
doi = {10.1073/pnas.1719705115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 10,
volume = 115,
place = {United States},
year = {2018},
month = {2}
}

Journal Article:
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DOI: 10.1073/pnas.1719705115

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Works referenced in this record:

Regulation of Nod1-mediated signaling pathways
journal, December 2006

  • da Silva Correia, J.; Miranda, Y.; Leonard, N.
  • Cell Death & Differentiation, Vol. 14, Issue 4
  • DOI: 10.1038/sj.cdd.4402070

HAM-5 Functions As a MAP Kinase Scaffold during Cell Fusion in Neurospora crassa
journal, November 2014


Neurospora V. A Synthetic Medium Favoring Sexual Reproduction
journal, December 1947

  • Westergaard, Mogens; Mitchell, Herschel K.
  • American Journal of Botany, Vol. 34, Issue 10
  • DOI: 10.2307/2437339

Cytochrome c and dATP-mediated Oligomerization of Apaf-1 Is a Prerequisite for Procaspase-9 Activation
journal, June 1999

  • Saleh, Ayman; Srinivasula, Srinivasa M.; Acharya, Samir
  • Journal of Biological Chemistry, Vol. 274, Issue 25
  • DOI: 10.1074/jbc.274.25.17941

Fungal incompatibility: Evolutionary origin in pathogen defense?
journal, November 2009


Intracellular innate immune surveillance devices in plants and animals
journal, December 2016


Gene deletion and allelic replacement in the filamentous fungus Podospora anserina
journal, February 2008


Arabidopsis immune secretory pathways to powdery mildew fungi
journal, August 2016


Programmed cell death correlates with virus transmission in a filamentous fungus
journal, November 2002

  • Biella, Silvia; Smith, Myron L.; Aist, James R.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 269, Issue 1506
  • DOI: 10.1098/rspb.2002.2148

Rice Exo70 interacts with a fungal effector , AVR-Pii, and is required for AVR-Pii-triggered immunity
journal, August 2015

  • Fujisaki, Koki; Abe, Yoshiko; Ito, Akiko
  • The Plant Journal, Vol. 83, Issue 5
  • DOI: 10.1111/tpj.12934

Basic Local Alignment Search Tool
journal, October 1990


Direct targeting of membrane fusion by SNARE mimicry: Convergent evolution of Legionella effectors
journal, July 2016

  • Shi, Xingqi; Halder, Partho; Yavuz, Halenur
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 31
  • DOI: 10.1073/pnas.1608755113

Identification of the pollen determinant of S-RNase-mediated self-incompatibility
journal, May 2004

  • Sijacic, Paja; Wang, Xi; Skirpan, Andrea L.
  • Nature, Vol. 429, Issue 6989
  • DOI: 10.1038/nature02523

Secondary Evolution of a Self-Incompatibility Locus in the Brassicaceae Genus Leavenworthia
journal, May 2013


AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints
journal, July 2005

  • Stanke, M.; Morgenstern, B.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki458

SNARE Protein Mimicry by an Intracellular Bacterium
journal, March 2008


Pathogen perception by NLRs in plants and animals: Parallel worlds
journal, June 2016


SNARE motif: A common motif used by pathogens to manipulate membrane fusion
journal, July 2010


Primitive immune systems: Are your ways my ways?
journal, April 2004


Phylogeny.fr: robust phylogenetic analysis for the non-specialist
journal, May 2008

  • Dereeper, A.; Guignon, V.; Blanc, G.
  • Nucleic Acids Research, Vol. 36, Issue Web Server
  • DOI: 10.1093/nar/gkn180

Analysis of SEC9 Suppression Reveals a Relationship of SNARE Function to Cell Physiology
journal, May 2009


Genomic sequencing reveals historical, demographic and selective factors associated with the diversification of the fire-associated fungus Neurospora discreta
journal, November 2015

  • Gladieux, Pierre; Wilson, Benjamin A.; Perraudeau, Fanny
  • Molecular Ecology, Vol. 24, Issue 22
  • DOI: 10.1111/mec.13417

Molecular mechanisms of allorecognition in a basal chordate
journal, February 2010


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

The plant immune system
journal, November 2006

  • Jones, Jonathan D. G.; Dangl, Jeffery L.
  • Nature, Vol. 444, Issue 7117
  • DOI: 10.1038/nature05286

Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein
journal, August 2017

  • El Kasmi, Farid; Chung, Eui-Hwan; Anderson, Ryan G.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 35
  • DOI: 10.1073/pnas.1708288114

Phytophthora infestans RXLR effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity
journal, September 2015


The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events
journal, January 2017

  • Urbach, Jonathan M.; Ausubel, Frederick M.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 5
  • DOI: 10.1073/pnas.1619730114

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


A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system
journal, September 2014


SNARE Proteins Are Required for Macroautophagy
journal, July 2011


Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis
journal, December 2014


Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes
journal, September 2000


A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors
journal, June 2006

  • Colot, H. V.; Park, G.; Turner, G. E.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
  • DOI: 10.1073/pnas.0601456103

trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons
journal, September 2011


Legionella effector Lpg1137 shuts down ER-mitochondria communication through cleavage of syntaxin 17
journal, May 2017

  • Arasaki, Kohei; Mikami, Yumi; Shames, Stephanie R.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms15406

The social evolution of somatic fusion
journal, November 2008

  • Aanen, Duur K.; Debets, Alfons J. M.; de Visser, J. Arjan G. M.
  • BioEssays, Vol. 30, Issue 11-12
  • DOI: 10.1002/bies.20840

Identification of Allorecognition Loci in Neurospora crassa by Genomics and Evolutionary Approaches
journal, May 2015

  • Zhao, Jiuhai; Gladieux, Pierre; Hutchison, Elizabeth
  • Molecular Biology and Evolution, Vol. 32, Issue 9
  • DOI: 10.1093/molbev/msv125

Cyclosporin A-resistance based gene placement system for Neurospora crassa
journal, May 2007


The genome sequence of the filamentous fungus Neurospora crassa
journal, April 2003

  • Galagan, James E.; Calvo, Sarah E.; Borkovich, Katherine A.
  • Nature, Vol. 422, Issue 6934
  • DOI: 10.1038/nature01554

The pepper patatin-like phospholipase CaPLP1 functions in plant cell death and defense signaling
journal, October 2013


Wheel of Life, Wheel of Death: A Mechanistic Insight into Signaling by STAND Proteins
journal, February 2009

  • Danot, Olivier; Marquenet, Emélie; Vidal-Ingigliardi, Dominique
  • Structure, Vol. 17, Issue 2
  • DOI: 10.1016/j.str.2009.01.001

The Arabidopsis Patatin-Like Protein 2 (PLP2) Plays an Essential Role in Cell Death Execution and Differentially Affects Biosynthesis of Oxylipins and Resistance to Pathogens
journal, April 2009

  • Camera, Sylvain La; Balagué, Claudine; Göbel, Cornelia
  • Molecular Plant-Microbe Interactions, Vol. 22, Issue 4
  • DOI: 10.1094/MPMI-22-4-0469

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


GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa
journal, October 2004

  • Freitag, Michael; Hickey, Patrick C.; Raju, Namboori B.
  • Fungal Genetics and Biology, Vol. 41, Issue 10
  • DOI: 10.1016/j.fgb.2004.06.008

Burning Down the House: Cellular Actions during Pyroptosis
journal, December 2013


Estimating Divergence Times from Molecular Data on Phylogenetic and Population Genetic Timescales
journal, November 2002


The complex domain architecture of SAMD9 family proteins, predicted STAND-like NTPases, suggests new links to inflammation and apoptosis
journal, May 2017


Diversity and Variability of NOD-Like Receptors in Fungi
journal, December 2014

  • Dyrka, Witold; Lamacchia, Marina; Durrens, Pascal
  • Genome Biology and Evolution, Vol. 6, Issue 12
  • DOI: 10.1093/gbe/evu251

Population genomics and local adaptation in wild isolates of a model microbial eukaryote
journal, January 2011

  • Ellison, C. E.; Hall, C.; Kowbel, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 7
  • DOI: 10.1073/pnas.1014971108

Role of a Mitogen-Activated Protein Kinase Pathway during Conidial Germination and Hyphal Fusion in Neurospora crassa
journal, April 2004


The Crystal Structure, Mutagenesis, and Activity Studies Reveal that Patatin Is a Lipid Acyl Hydrolase with a Ser-Asp Catalytic Dyad
journal, June 2003

  • Rydel, Timothy J.; Williams, Jennifer M.; Krieger, Elysia
  • Biochemistry, Vol. 42, Issue 22
  • DOI: 10.1021/bi027156r

NLRs join TLRs as innate sensors of pathogens
journal, August 2005


Plant NBS-LRR proteins in pathogen sensing and host defense
journal, November 2006

  • DeYoung, Brody J.; Innes, Roger W.
  • Nature Immunology, Vol. 7, Issue 12
  • DOI: 10.1038/ni1410

Fusion PCR and gene targeting in Aspergillus nidulans
journal, December 2006

  • Szewczyk, Edyta; Nayak, Tania; Oakley, C. Elizabeth
  • Nature Protocols, Vol. 1, Issue 6
  • DOI: 10.1038/nprot.2006.405

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