Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant
species. Nat Rev Genet 8:382–393
Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C,
Dangl JL, Weigel D (2007) Autoimmune response
as a mechanism for a Dobzhansky-Muller-type
incompatibility syndrome in plants. PLoS Biol 5:
e236
Brodersen P, Petersen M, Pike HM, Olszak B, Skov S,
Odum N, Jorgensen LB, Brown RE, Mundy J (2002)
Knockout of Arabidopsis accelerated-cell-death11
encoding a sphingosine transfer protein causes
activation of programmed cell death and defense.
Genes Dev 16:490–502
Cai X, Chen J, Xu H, Liu S, Jiang QX, Halfmann R, Chen
ZJ (2014) Prion-like polymerization underlies signal transduction in antiviral immune defense and
inflammasome activation. Cell 156:1207–1222
Cayley DM (1923) The phenonenon of mutual aversion
between mono-spore mycelia of the same fungus
(Diaporthe perniciosa march.) with a discussion
on sex heterothallism in fungi. Jour Gen
13:353–370
Chae E, Bomblies K, Kim ST, Karelina D, Zaidem M,
Ossowski S, Martin-Pizarro C, Laitinen RA, Rowan
BA, Tenenboim H et al (2014) Species-wide genetic
incompatibility analysis identifies immune genes
as hot spots of deleterious epistasis. Cell 159:1341–
1351
Chevanne D, Bastiaans E, Debets A, Saupe SJ, Clave C,
Paoletti M (2009) Identification of the het-r vegetative incompatibility gene of Podospora anserina
as a member of the fast evolving HNWD gene
family. Curr Genet 55:93–102
Chevanne D, Saupe SJ, Clave C, Paoletti M (2010) WDrepeat instability and diversification of the Podospora anserina hnwd non-self recognition gene
family. BMC Evol Biol 10:134
Choi GH, Dawe AL, Churbanov A, Smith ML, Milgroom
MG, Nuss DL (2012) Molecular characterization of
vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus
Cryphonectria parasitica. Genetics 190:113–127
Daskalov A, Saupe SJ (2015) As a toxin dies a prion
comes to life: a tentative natural history of the
[Het-s] prion. Prion 9:184–189
Daskalov A, Paoletti M, Ness F, Saupe SJ (2012) Genomic clustering and homology between HET-S and
the NWD2 STAND protein in various fungal genomes. PLoS One 7:e34854
Daskalov A, Dyrka W, Saupe SJ (2015a) Theme and
variations: evolutionary diversification of the
HET-s functional amyloid motif. Sci Rep 5:12494
Daskalov A, Habenstein B, Martinez D, Debets AJ,
Sabate R, Loquet A, Saupe SJ (2015b) Signal transduction by a fungal NOD-like receptor based on
propagation of a prion amyloid fold. PLoS Biol 13:
e1002059
Daskalov A, Habenstein B, Sabate R, Berbon M, Martinez D, Chaignepain S, Coulary-Salin B, Hofmann
K, Loquet A, Saupe SJ (2016) Identification of a
novel cell death-inducing domain reveals that fungal amyloid-controlled programmed cell death is
related to necroptosis. Proc Natl Acad Sci U S A
113:2720–2725
Daskalov A, Heller J, Herzog S, Fleissner A, Glass NL
(2017) Molecular mechanisms regulating cell
fusion and heterokaryon formation in filamentous
fungi. Microbiol Spectr 5(2). https://doi.org/
10.1128/microbiolspec.FUNK-0015-2016
Dunin-Horkawicz S, Kopec KO, Lupas AN (2014) Prokaryotic ancestry of eukaryotic protein networks
mediating innate immunity and apoptosis. J Mol
Biol 426:1568–1582
Duxbury Z, Ma Y, Furzer OJ, Huh SU, Cevik V, Jones
JD, Sarris PF (2016) Pathogen perception by NLRs
in plants and animals: parallel worlds. BioEssays
38:769–781
Dyrka W, Lamacchia M, Durrens P, Kobe B, Daskalov
A, Paoletti M, Sherman DJ, Saupe SJ (2014) Diversity and variability of NOD-like receptors in fungi.
Genome Biol Evol 6:3137–3158
Espagne E, Balhadere P, Penin ML, Barreau C, Turcq B
(2002) HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative
incompatibility specificity in the fungus Podospora
anserina. Genetics 161:71–81
Esser K (1965) Heterogenic incompatibility. In: Esser K,
Raper JR (eds) Incompatibility in fungi. Springer,
New York, pp 6–12
Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo
P, Anderson MJ, Crabtree J, Silva JC, Badger JH,
Albarraq A et al (2008) Genomic islands in the
pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046
Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han GZ
(2018) Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:82–89
Garnjobst L, Wilson JF (1956) Heterocaryosis and protoplasmic incompatibility in Neurospora crassa.
Proc Natl Acad Sci U S A 42:613–618
Glass NL, Vollmer SJ, Staben C, Grotelueschen J, Metzenberg RL, Yanofsky C (1988) DNAs of the two
mating-type alleles of Neurospora crassa are highly
dissimilar. Science 241:570–573
Gould JS, Vrba ES (1982) Exaptation-a missing term in
the science of form. Paleobiology 8:4–15
Graziani S, Silar P, Daboussi MJ (2004) Bistability and
hysteresis of the ‘Secteur’ differentiation are controlled by a two-gene locus in Nectria haematococca. BMC Biol 2:18
Hamada M, Shoguchi E, Shinzato C, Kawashima T,
Miller DJ, Satoh N (2013) The complex NOD-like
receptor repertoire of the coral Acropora digitifera
includes novel domain combinations. Mol Biol
Evol 30:167–176
6 NLR Function in Fungi as Revealed by the Study of Self/Non-self Recognition Systems
139
species. Nat Rev Genet 8:382–393
Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C,
Dangl JL, Weigel D (2007) Autoimmune response
as a mechanism for a Dobzhansky-Muller-type
incompatibility syndrome in plants. PLoS Biol 5:
e236
Brodersen P, Petersen M, Pike HM, Olszak B, Skov S,
Odum N, Jorgensen LB, Brown RE, Mundy J (2002)
Knockout of Arabidopsis accelerated-cell-death11
encoding a sphingosine transfer protein causes
activation of programmed cell death and defense.
Genes Dev 16:490–502
Cai X, Chen J, Xu H, Liu S, Jiang QX, Halfmann R, Chen
ZJ (2014) Prion-like polymerization underlies signal transduction in antiviral immune defense and
inflammasome activation. Cell 156:1207–1222
Cayley DM (1923) The phenonenon of mutual aversion
between mono-spore mycelia of the same fungus
(Diaporthe perniciosa march.) with a discussion
on sex heterothallism in fungi. Jour Gen
13:353–370
Chae E, Bomblies K, Kim ST, Karelina D, Zaidem M,
Ossowski S, Martin-Pizarro C, Laitinen RA, Rowan
BA, Tenenboim H et al (2014) Species-wide genetic
incompatibility analysis identifies immune genes
as hot spots of deleterious epistasis. Cell 159:1341–
1351
Chevanne D, Bastiaans E, Debets A, Saupe SJ, Clave C,
Paoletti M (2009) Identification of the het-r vegetative incompatibility gene of Podospora anserina
as a member of the fast evolving HNWD gene
family. Curr Genet 55:93–102
Chevanne D, Saupe SJ, Clave C, Paoletti M (2010) WDrepeat instability and diversification of the Podospora anserina hnwd non-self recognition gene
family. BMC Evol Biol 10:134
Choi GH, Dawe AL, Churbanov A, Smith ML, Milgroom
MG, Nuss DL (2012) Molecular characterization of
vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus
Cryphonectria parasitica. Genetics 190:113–127
Daskalov A, Saupe SJ (2015) As a toxin dies a prion
comes to life: a tentative natural history of the
[Het-s] prion. Prion 9:184–189
Daskalov A, Paoletti M, Ness F, Saupe SJ (2012) Genomic clustering and homology between HET-S and
the NWD2 STAND protein in various fungal genomes. PLoS One 7:e34854
Daskalov A, Dyrka W, Saupe SJ (2015a) Theme and
variations: evolutionary diversification of the
HET-s functional amyloid motif. Sci Rep 5:12494
Daskalov A, Habenstein B, Martinez D, Debets AJ,
Sabate R, Loquet A, Saupe SJ (2015b) Signal transduction by a fungal NOD-like receptor based on
propagation of a prion amyloid fold. PLoS Biol 13:
e1002059
Daskalov A, Habenstein B, Sabate R, Berbon M, Martinez D, Chaignepain S, Coulary-Salin B, Hofmann
K, Loquet A, Saupe SJ (2016) Identification of a
novel cell death-inducing domain reveals that fungal amyloid-controlled programmed cell death is
related to necroptosis. Proc Natl Acad Sci U S A
113:2720–2725
Daskalov A, Heller J, Herzog S, Fleissner A, Glass NL
(2017) Molecular mechanisms regulating cell
fusion and heterokaryon formation in filamentous
fungi. Microbiol Spectr 5(2). https://doi.org/
10.1128/microbiolspec.FUNK-0015-2016
Dunin-Horkawicz S, Kopec KO, Lupas AN (2014) Prokaryotic ancestry of eukaryotic protein networks
mediating innate immunity and apoptosis. J Mol
Biol 426:1568–1582
Duxbury Z, Ma Y, Furzer OJ, Huh SU, Cevik V, Jones
JD, Sarris PF (2016) Pathogen perception by NLRs
in plants and animals: parallel worlds. BioEssays
38:769–781
Dyrka W, Lamacchia M, Durrens P, Kobe B, Daskalov
A, Paoletti M, Sherman DJ, Saupe SJ (2014) Diversity and variability of NOD-like receptors in fungi.
Genome Biol Evol 6:3137–3158
Espagne E, Balhadere P, Penin ML, Barreau C, Turcq B
(2002) HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative
incompatibility specificity in the fungus Podospora
anserina. Genetics 161:71–81
Esser K (1965) Heterogenic incompatibility. In: Esser K,
Raper JR (eds) Incompatibility in fungi. Springer,
New York, pp 6–12
Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo
P, Anderson MJ, Crabtree J, Silva JC, Badger JH,
Albarraq A et al (2008) Genomic islands in the
pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046
Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han GZ
(2018) Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:82–89
Garnjobst L, Wilson JF (1956) Heterocaryosis and protoplasmic incompatibility in Neurospora crassa.
Proc Natl Acad Sci U S A 42:613–618
Glass NL, Vollmer SJ, Staben C, Grotelueschen J, Metzenberg RL, Yanofsky C (1988) DNAs of the two
mating-type alleles of Neurospora crassa are highly
dissimilar. Science 241:570–573
Gould JS, Vrba ES (1982) Exaptation-a missing term in
the science of form. Paleobiology 8:4–15
Graziani S, Silar P, Daboussi MJ (2004) Bistability and
hysteresis of the ‘Secteur’ differentiation are controlled by a two-gene locus in Nectria haematococca. BMC Biol 2:18
Hamada M, Shoguchi E, Shinzato C, Kawashima T,
Miller DJ, Satoh N (2013) The complex NOD-like
receptor repertoire of the coral Acropora digitifera
includes novel domain combinations. Mol Biol
Evol 30:167–176
6 NLR Function in Fungi as Revealed by the Study of Self/Non-self Recognition Systems
139