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. 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, showingmore »
- Authors:
-
[1]
- The Plant and Microbial Biology Department, University of California, Berkeley, CA 94720-3102,, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720,
- Institut de Biochimie et de Génétique Cellulaire, CNRS, Université de Bordeaux, 33077 Bordeaux, France,
- Biologie et Génétique des Interactions Plante-Parasite, University of Montpellier, Institut National de la Recherche Agronomique, Centre de Coopération Internationale en Recherche Agronomique pour le Dévelopement, Montpellier SupAgro, F-34398 Montpellier, France
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (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. https://doi.org/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. https://doi.org/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. 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 = {Tue Feb 20 00:00:00 EST 2018},
month = {Tue Feb 20 00:00:00 EST 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1719705115
https://doi.org/10.1073/pnas.1719705115
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 50 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
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
HAM-5 Functions As a MAP Kinase Scaffold during Cell Fusion in Neurospora crassa
journal, November 2014
- Jonkers, Wilfried; Leeder, Abigail C.; Ansong, Charles
- PLoS Genetics, Vol. 10, Issue 11
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
Fungal incompatibility: Evolutionary origin in pathogen defense?
journal, November 2009
- Paoletti, Mathieu; Saupe, Sven J.
- BioEssays, Vol. 31, Issue 11
Intracellular innate immune surveillance devices in plants and animals
journal, December 2016
- Jones, J. D. G.; Vance, R. E.; Dangl, J. L.
- Science, Vol. 354, Issue 6316
Gene deletion and allelic replacement in the filamentous fungus Podospora anserina
journal, February 2008
- El-Khoury, Riyad; Sellem, Carole H.; Coppin, Evelyne
- Current Genetics, Vol. 53, Issue 4
Arabidopsis immune secretory pathways to powdery mildew fungi
journal, August 2016
- Yun, Hye Sup; Kang, Bin Goo; Kwon, Chian
- Plant Signaling & Behavior, Vol. 11, Issue 10
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
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
The Saccharomyces cerevisiae PRM1 Homolog in Neurospora crassa Is Involved in Vegetative and Sexual Cell Fusion Events but Also Has Postfertilization Functions
journal, December 2008
- Fleißner, André; Diamond, Spencer; Glass, N. Louise
- Genetics, Vol. 181, Issue 2
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
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
Secondary Evolution of a Self-Incompatibility Locus in the Brassicaceae Genus Leavenworthia
journal, May 2013
- Chantha, Sier-Ching; Herman, Adam C.; Platts, Adrian E.
- PLoS Biology, Vol. 11, Issue 5
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
SNARE Protein Mimicry by an Intracellular Bacterium
journal, March 2008
- Delevoye, Cédric; Nilges, Michael; Dehoux, Pierre
- PLoS Pathogens, Vol. 4, Issue 3
Pathogen perception by NLRs in plants and animals: Parallel worlds
journal, June 2016
- Duxbury, Zane; Ma, Yan; Furzer, Oliver J.
- BioEssays, Vol. 38, Issue 8
SNARE motif: A common motif used by pathogens to manipulate membrane fusion
journal, July 2010
- Wesolowski, Jordan; Paumet, Fabienne
- Virulence, Vol. 1, Issue 4
Primitive immune systems: Are your ways my ways?
journal, April 2004
- Rinkevich, Baruch
- Immunological Reviews, Vol. 198, Issue 1
Enabling a Community to Dissect an Organism: Overview of the Neurospora Functional Genomics Project
book, March 2007
- Dunlap, Jay C.; Borkovich, Katherine A.; Henn, Matthew R.
- Fungal Genomics
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
Analysis of SEC9 Suppression Reveals a Relationship of SNARE Function to Cell Physiology
journal, May 2009
- Williams, Daniel C.; Novick, Peter J.
- PLoS ONE, Vol. 4, Issue 5
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
Molecular mechanisms of allorecognition in a basal chordate
journal, February 2010
- McKitrick, Tanya R.; De Tomaso, Anthony W.
- Seminars in Immunology, Vol. 22, Issue 1
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
The plant immune system
journal, November 2006
- Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature, Vol. 444, Issue 7117
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
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
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
A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system
journal, September 2014
- Corcoran, Pádraic; Dettman, Jeremy R.; Sun, Yu
- Molecular Phylogenetics and Evolution, Vol. 78
SNARE Proteins Are Required for Macroautophagy
journal, July 2011
- Nair, Usha; Jotwani, Anjali; Geng, Jiefei
- Cell, Vol. 146, Issue 2
Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis
journal, December 2014
- Chae, Eunyoung; Bomblies, Kirsten; Kim, Sang-Tae
- Cell, Vol. 159, Issue 6
Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes
journal, September 2000
- Saupe, S. J.
- Microbiology and Molecular Biology Reviews, Vol. 64, Issue 3
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
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons
journal, September 2011
- Ranwez, Vincent; Harispe, Sébastien; Delsuc, Frédéric
- PLoS ONE, Vol. 6, Issue 9
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
Neurospora v. a Synthetic Medium Favoring Sexual Reproduction
journal, December 1947
- Westergaard, Mogens; Mitchell, Herschel K.
- American Journal of Botany, Vol. 34, Issue 10
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
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
Cyclosporin A-resistance based gene placement system for Neurospora crassa
journal, May 2007
- Bardiya, Nirmala; Shiu, Patrick K. T.
- Fungal Genetics and Biology, Vol. 44, Issue 5
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
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
The pepper patatin-like phospholipase CaPLP1 functions in plant cell death and defense signaling
journal, October 2013
- Kim, Dae Sung; Jeun, Yongchull; Hwang, Byung Kook
- Plant Molecular Biology, Vol. 84, Issue 3
Genetic and morphological analyses reveal a critical interaction between the C-termini of two SNARE proteins and a parallel four helical arrangement for the exocytic SNARE complex
journal, November 1998
- Katz, Luba; Hanson, Phyllis I.; Heuser, John E.
- The EMBO Journal, Vol. 17, Issue 21
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
Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis
journal, October 1994
- Brennwald, P.
- Cell, Vol. 79, Issue 2
Molecular Characterization of Vegetative Incompatibility Genes That Restrict Hypovirus Transmission in the Chestnut Blight Fungus Cryphonectria parasitica
journal, October 2011
- Choi, Gil H.; Dawe, Angus L.; Churbanov, Alexander
- Genetics, Vol. 190, Issue 1
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
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
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
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
Burning Down the House: Cellular Actions during Pyroptosis
journal, December 2013
- LaRock, Christopher N.; Cookson, Brad T.
- PLoS Pathogens, Vol. 9, Issue 12
Estimating Divergence Times from Molecular Data on Phylogenetic and Population Genetic Timescales
journal, November 2002
- Arbogast, Brian S.; Edwards, Scott V.; Wakeley, John
- Annual Review of Ecology and Systematics, Vol. 33, Issue 1
The complex domain architecture of SAMD9 family proteins, predicted STAND-like NTPases, suggests new links to inflammation and apoptosis
journal, May 2017
- Mekhedov, Sergei L.; Makarova, Kira S.; Koonin, Eugene V.
- Biology Direct, Vol. 12, Issue 1
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
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
Role of a Mitogen-Activated Protein Kinase Pathway during Conidial Germination and Hyphal Fusion in Neurospora crassa
journal, April 2004
- Pandey, Amita; Roca, M. Gabriela; Read, Nick D.
- Eukaryotic Cell, Vol. 3, Issue 2
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
NLRs join TLRs as innate sensors of pathogens
journal, August 2005
- Martinon, F.; Tschopp, J.
- Trends in Immunology, Vol. 26, Issue 8
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
Fusion PCR and gene targeting in Aspergillus nidulans
journal, December 2006
- Szewczyk, Edyta; Nayak, Tania; Oakley, C. Elizabeth
- Nature Protocols, Vol. 1, Issue 6