The small-secreted cysteine-rich protein CyrA is a virulence factor participating in the attack of Caenorhabditis elegans by Duddingtonia flagrans

Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immob...

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Published inPLoS pathogens Vol. 17; no. 11; p. e1010028
Main Authors Wernet, Nicole, Wernet, Valentin, Fischer, Reinhard
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.11.2021
Public Library of Science (PLoS)
Subjects
Adhesives
Analysis
Animals
Biology and Life Sciences
Caenorhabditis elegans
Caenorhabditis elegans - growth & development
Caenorhabditis elegans - microbiology
CCN Intercellular Signaling Proteins - genetics
CCN Intercellular Signaling Proteins - metabolism
Coelomocytes
Cysteine
Cysteine - chemistry
Duddingtonia - physiology
Fungal Proteins - genetics
Fungal Proteins - metabolism
Fungi
Genes
Genetic transcription
Genomes
Host-Pathogen Interactions
Hyphae
Identification and classification
Infections
Life span
Medicine and Health Sciences
Microorganisms
Nematodes
Observations
Paralysis
Pathogens
Penetration
Peptides
Prevention
Proteins
Research and Analysis Methods
Transcription
Trapping
Virulence
Virulence (Microbiology)
Virulence factors
Germany
Online AccessGet full text
ISSN1553-7374
1553-7366
1553-7374
DOI10.1371/journal.ppat.1010028

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Abstract Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D . flagrans encodes more than 100 of such putative SSPs one of which is the cy steine- r ich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA -deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C . elegans reduced its lifespan. CyrA accumulated in C . elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.
AbstractList Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D . flagrans encodes more than 100 of such putative SSPs one of which is the cy steine- r ich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA -deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C . elegans reduced its lifespan. CyrA accumulated in C . elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.
Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D . flagrans encodes more than 100 of such putative SSPs one of which is the cy steine- r ich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA -deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C . elegans reduced its lifespan. CyrA accumulated in C . elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions. Pathogenic microorganisms are living at the expense of their host organisms and immediate killing of the host may be disadvantageous. Therefore, many bacterial or fungal pathogens developed an arsenal of small-secreted proteins during the colonization to modulate their host for instance to suppress its defense reactions. This allows a biotrophic phase, at least for some time. Some higher eukaryotic “pathogens” also live at the expense of their hosts but are often predators. In this case, quick killing is followed by digestion. In the case of predatory fungi, one could expect a similar situation, quick killing followed by digestion. However, the genome of such fungi encodes many putative small-secreted proteins, and we show here that one of them indeed appears to be secreted into the host and contributes to virulence. The protein is produced in the trapping devices of the fungus and especially in the penetration peg right after entering the nematode. Heterologous expression in Caenorhabditis elegans reduced the lifespan of the worms. This protein is to our knowledge the first characterized small-secreted protein in the predatory relationship between fungi and nematodes.
Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D. flagrans encodes more than 100 of such putative SSPs one of which is the cysteine-rich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA-deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C. elegans reduced its lifespan. CyrA accumulated in C. elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D. flagrans encodes more than 100 of such putative SSPs one of which is the cysteine-rich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA-deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C. elegans reduced its lifespan. CyrA accumulated in C. elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.
Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D. flagrans encodes more than 100 of such putative SSPs one of which is the cysteine-rich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA-deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C. elegans reduced its lifespan. CyrA accumulated in C. elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.
Audience Academic
Author Wernet, Valentin
Wernet, Nicole
Fischer, Reinhard
AuthorAffiliation Karlsruhe Institute of Technology (KIT)—South Campus, Institute for Applied Biosciences, Dept. of Microbiology, Karlsruhe, Germany
Chinese Academy of Sciences, CHINA
AuthorAffiliation_xml – name: Karlsruhe Institute of Technology (KIT)—South Campus, Institute for Applied Biosciences, Dept. of Microbiology, Karlsruhe, Germany
– name: Chinese Academy of Sciences, CHINA
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  surname: Wernet
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  givenname: Reinhard
  orcidid: 0000-0002-6704-2569
  surname: Fischer
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Cites_doi 10.1038/s41586-020-2461-z
10.1128/AEM.01390-13
10.1002/mbo3.304
10.1016/j.exppara.2015.07.006
10.1016/j.exppara.2017.02.009
10.1128/microbiolspec.FUNK-0022-2016
10.1105/tpc.15.00552
10.1146/annurev-arplant-043014-114623
10.1038/175475a0
10.1093/nar/gkj047
10.1186/s12915-016-0256-3
10.1083/jcb.130.2.299
10.1007/BF00418937
10.1073/pnas.1003113107
10.1016/j.cub.2011.06.044
10.1016/j.cub.2013.08.009
10.1038/nsmb1017
10.1007/978-1-4419-5638-5_4
10.1210/endo.142.2.7929
10.1371/journal.ppat.1003866
10.1210/me.2008-0209
10.1038/ncomms5686
10.1111/mpp.12682
10.1096/fj.09-142984
10.1016/j.cvfa.2019.11.007
10.1007/BF02275043
10.1371/journal.ppat.1005921
10.1038/s41467-018-07467-5
10.1038/ncomms2996
10.1186/1471-2164-15-968
10.1016/S0065-2911(08)60178-2
10.1007/S102670200044
10.1007/978-1-4419-8059-5_6
10.1371/journal.pone.0133085
10.2190/25B9-QFMV-Y28P-L736
10.1016/j.cvfa.2017.10.008
10.1385/JMN:22:1-2:63
10.1073/pnas.0702770104
10.1016/S0092-8674(00)80724-2
10.1093/genetics/159.1.133
10.1146/annurev-phyto-082718-100139
10.1111/nph.16563
10.1007/BF02275044
10.1094/PHYTO-09-20-0379-PER
10.1242/jcs.004770
10.1073/pnas.1120915109
10.1128/AEM.00060-06
10.1186/1746-6148-5-46
10.1038/nrmicro.2017.33
10.1080/15592324.2018.1557008
10.1105/tpc.109.069666
10.1038/8967
10.1016/j.zool.2016.06.005
10.1016/0378-1119(95)00875-6
10.1371/journal.pgen.1008029
10.1016/j.cub.2012.11.035
10.1111/j.1462-2920.2007.01457.x
10.1016/j.pbi.2015.09.003
10.1105/tpc.003426
10.3389/fpls.2021.687713
10.1038/s41467-020-19624-w
10.1038/s41467-021-25535-1
10.1146/annurev.phyto.36.1.165
10.7554/eLife.20023
10.1128/mSphere.00408-17
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References KR Barker (ppat.1010028.ref006) 1998; 36
JM Burke (ppat.1010028.ref008) 2020; 36
T Liu (ppat.1010028.ref026) 2014; 5
KM Andersson (ppat.1010028.ref028) 2013; 79
N Mukhi (ppat.1010028.ref060) 2020; 227
M Veenhuis (ppat.1010028.ref042) 1985; 51
A Justesen (ppat.1010028.ref031) 1996; 170
W Zuo (ppat.1010028.ref040) 2019; 57
G Ahmad (ppat.1010028.ref003) 2021
J McGowan (ppat.1010028.ref058) 2017; 2
CS Nodvig (ppat.1010028.ref073) 2015; 10
S Kloppholz (ppat.1010028.ref022) 2011; 21
RD Schulte (ppat.1010028.ref061) 2010; 107
S Kim (ppat.1010028.ref041) 2020; 11
E Kojima (ppat.1010028.ref047) 2002; 43
T Brefort (ppat.1010028.ref064) 2014; 10
K Kiontke (ppat.1010028.ref004) 2013; 23
M Veenhuis (ppat.1010028.ref056) 1989; 56
M Porta-de-la-Riva (ppat.1010028.ref071) 2012
MC Giraldo (ppat.1010028.ref023) 2013; 4
YP Hsueh (ppat.1010028.ref018) 2013; 23
YK Gupta (ppat.1010028.ref024) 2015; 27
I Gallotta (ppat.1010028.ref067) 2020; 584
L Boyer (ppat.1010028.ref021) 2012; 710
JT Blankenship (ppat.1010028.ref057) 2007; 120
LA Thrupp (ppat.1010028.ref005) 1991; 21
GJ Mander (ppat.1010028.ref034) 2006; 72
V Bampidis (ppat.1010028.ref010) 2020; 18
NF Ojeda-Robertos (ppat.1010028.ref011) 2009; 5
O Zugasti (ppat.1010028.ref069) 2016; 14
H Fares (ppat.1010028.ref036) 2001; 159
D Shao (ppat.1010028.ref039) 2021; 12
S Mochizuki (ppat.1010028.ref045) 2015; 4
CH Khang (ppat.1010028.ref044) 2010; 22
X Jiang (ppat.1010028.ref001) 2017; 5
C Fekete (ppat.1010028.ref030) 2008; 10
T Nishimura (ppat.1010028.ref046) 2016; 12
SR Pfeffer (ppat.1010028.ref051) 1999; 1
V Wernet (ppat.1010028.ref012) 2021
C Xue (ppat.1010028.ref032) 2002; 14
YP Hsueh (ppat.1010028.ref017) 2017; 6
SM Ahmed (ppat.1010028.ref054) 2018; 9
I Engelmann (ppat.1010028.ref066) 2010; 708
M Hahn (ppat.1010028.ref065) 2021; 111
DO Ortiz Perez (ppat.1010028.ref013) 2017; 175
E Yang (ppat.1010028.ref062) 2012; 109
P Chardin (ppat.1010028.ref035) 1999; 97
Y Yang (ppat.1010028.ref016) 2007; 104
J Dijksterhuis (ppat.1010028.ref020) 1994; 36
R El Meskini (ppat.1010028.ref048) 2001; 142
Y Liu (ppat.1010028.ref070) 2021
YP Loh (ppat.1010028.ref049) 2004; 22
R Winnenburg (ppat.1010028.ref029) 2006; 34
JJ Park (ppat.1010028.ref050) 2008; 22
G Dong (ppat.1010028.ref052) 2005; 12
SK Park (ppat.1010028.ref068) 2010; 24
DR TerBush (ppat.1010028.ref053) 1995; 130
G Joop (ppat.1010028.ref063) 2016; 119
X Chen (ppat.1010028.ref025) 2015; 28
J Sambrook (ppat.1010028.ref072) 1999
L Lo Presti (ppat.1010028.ref037) 2015; 66
J Sperschneider (ppat.1010028.ref033) 2018; 19
X Yu (ppat.1010028.ref019) 2021; 12
L Zhang (ppat.1010028.ref074) 2015; 142
AM Shepherd (ppat.1010028.ref043) 1955; 175
M Veenhuis (ppat.1010028.ref055) 1985; 51
R. Mankau (ppat.1010028.ref002) 1980; 12
D Lanver (ppat.1010028.ref038) 2017; 15
Y Zhang (ppat.1010028.ref009) 2020; 6
KM Andersson (ppat.1010028.ref027) 2014; 15
L Youssar (ppat.1010028.ref015) 2019; 15
A Buzatti (ppat.1010028.ref014) 2015; 159
L Liu (ppat.1010028.ref059) 2019; 14
TM Craig (ppat.1010028.ref007) 2018; 34
References_xml – volume: 584
  start-page: 410
  issue: 7821
  year: 2020
  ident: ppat.1010028.ref067
  article-title: Extracellular proteostasis prevents aggregation during pathogenic attack
  publication-title: Nature
  doi: 10.1038/s41586-020-2461-z
– volume: 79
  start-page: 4993
  issue: 16
  year: 2013
  ident: ppat.1010028.ref028
  article-title: Proteome of the nematode-trapping cells of the fungus Monacrosporium haptotyla
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.01390-13
– volume: 4
  start-page: 952
  issue: 6
  year: 2015
  ident: ppat.1010028.ref045
  article-title: Live-cell imaging of rice cytological changes reveals the importance of host vacuole maintenance for biotrophic invasion by blast fungus, Magnaporthe oryzae
  publication-title: Microbiologyopen
  doi: 10.1002/mbo3.304
– volume: 159
  start-page: 1
  year: 2015
  ident: ppat.1010028.ref014
  article-title: Duddingtonia flagrans in the control of gastrointestinal nematodes of horses
  publication-title: Exp Parasitol
  doi: 10.1016/j.exppara.2015.07.006
– volume: 175
  start-page: 74
  year: 2017
  ident: ppat.1010028.ref013
  article-title: Using Duddingtonia flagrans in calves under an organic milk farm production system in the Mexican tropics
  publication-title: Exp Parasitol
  doi: 10.1016/j.exppara.2017.02.009
– volume: 5
  issue: 1
  year: 2017
  ident: ppat.1010028.ref001
  article-title: Nematode-trapping fungi
  publication-title: Microbiol Spectr
  doi: 10.1128/microbiolspec.FUNK-0022-2016
– volume: 27
  start-page: 3277
  issue: 11
  year: 2015
  ident: ppat.1010028.ref024
  article-title: Septin-dependent assembly of the exocyst is essential for plant infection by Magnaporthe oryzae
  publication-title: Plant Cell
  doi: 10.1105/tpc.15.00552
– volume: 6
  issue: 4
  year: 2020
  ident: ppat.1010028.ref009
  article-title: Fungi-nematode interactions: diversity, ecology, and biocontrol prospects in agriculture
  publication-title: J Fungi (Basel)
– volume: 66
  start-page: 513
  year: 2015
  ident: ppat.1010028.ref037
  article-title: Fungal effectors and plant susceptibility
  publication-title: Annu Rev Plant Biol
  doi: 10.1146/annurev-arplant-043014-114623
– volume: 175
  start-page: 475
  year: 1955
  ident: ppat.1010028.ref043
  article-title: Formation of the infection bulb in Arthrobotrys oligospora Fresenius
  publication-title: Nature
  doi: 10.1038/175475a0
– volume: 34
  start-page: D459
  year: 2006
  ident: ppat.1010028.ref029
  article-title: PHI-base: a new database for pathogen host interactions
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkj047
– volume: 14
  start-page: 35
  year: 2016
  ident: ppat.1010028.ref069
  article-title: A quantitative genome-wide RNAi screen in C. elegans for antifungal innate immunity genes
  publication-title: BMC Biol
  doi: 10.1186/s12915-016-0256-3
– volume: 130
  start-page: 299
  issue: 2
  year: 1995
  ident: ppat.1010028.ref053
  article-title: Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae
  publication-title: J Cell Biol
  doi: 10.1083/jcb.130.2.299
– volume: 56
  start-page: 251
  issue: 3
  year: 1989
  ident: ppat.1010028.ref056
  article-title: Significance of electron dense microbodies in trap cells of the nematophagous fungus Arthrobotrys oligospora
  publication-title: Ant Leeuw
  doi: 10.1007/BF00418937
– volume: 107
  start-page: 7359
  issue: 16
  year: 2010
  ident: ppat.1010028.ref061
  article-title: Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1003113107
– year: 2021
  ident: ppat.1010028.ref003
  article-title: Biological control: a novel strategy for the control of the plant parasitic nematodes
  publication-title: Ant Leeuw
– start-page: e4019
  issue: 64
  year: 2012
  ident: ppat.1010028.ref071
  article-title: Basic Caenorhabditis elegans methods: synchronization and observation.
  publication-title: J Vis Exp
– volume: 21
  start-page: 1204
  issue: 14
  year: 2011
  ident: ppat.1010028.ref022
  article-title: A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy
  publication-title: Curr Biol
  doi: 10.1016/j.cub.2011.06.044
– volume: 23
  start-page: R862
  issue: 19
  year: 2013
  ident: ppat.1010028.ref004
  article-title: Nematodes
  publication-title: Curr Biol
  doi: 10.1016/j.cub.2013.08.009
– volume: 12
  start-page: 1094
  issue: 12
  year: 2005
  ident: ppat.1010028.ref052
  article-title: The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif
  publication-title: Nat Struct Mol Biol
  doi: 10.1038/nsmb1017
– volume: 710
  start-page: 29
  year: 2012
  ident: ppat.1010028.ref021
  article-title: Bacterial effectors: learning on the fly
  publication-title: Adv Exp Med Biol
  doi: 10.1007/978-1-4419-5638-5_4
– volume: 142
  start-page: 864
  issue: 2
  year: 2001
  ident: ppat.1010028.ref048
  article-title: A signal sequence is sufficient for green fluorescent protein to be routed to regulated secretory granules
  publication-title: Endocrinology
  doi: 10.1210/endo.142.2.7929
– volume: 10
  start-page: e1003866
  issue: 7
  year: 2014
  ident: ppat.1010028.ref064
  article-title: Characterization of the largest effector gene cluster of Ustilago maydis
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1003866
– volume: 22
  start-page: 2583
  issue: 12
  year: 2008
  ident: ppat.1010028.ref050
  article-title: How peptide hormone vesicles are transported to the secretion site for exocytosis
  publication-title: Mol Endocrinol
  doi: 10.1210/me.2008-0209
– volume: 5
  start-page: 4686
  year: 2014
  ident: ppat.1010028.ref026
  article-title: Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis
  publication-title: Nat Commun
  doi: 10.1038/ncomms5686
– volume: 19
  start-page: 2094
  issue: 9
  year: 2018
  ident: ppat.1010028.ref033
  article-title: Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0
  publication-title: Mol Plant Pathol
  doi: 10.1111/mpp.12682
– start-page: 12
  year: 2021
  ident: ppat.1010028.ref070
  article-title: Detection of pathogens and regulation of immunity by the Caenorhabditis elegans nervous system
  publication-title: mBio
– volume: 24
  start-page: 383
  issue: 2
  year: 2010
  ident: ppat.1010028.ref068
  article-title: Life-span extension by dietary restriction is mediated by NLP-7 signaling and coelomocyte endocytosis in C. elegans
  publication-title: FASEB J
  doi: 10.1096/fj.09-142984
– volume: 36
  start-page: 89
  issue: 1
  year: 2020
  ident: ppat.1010028.ref008
  article-title: Sustainable approaches to parasite control in ruminant livestock
  publication-title: Vet Clin North Am Food Anim Pract
  doi: 10.1016/j.cvfa.2019.11.007
– volume: 51
  start-page: 385
  issue: 4
  year: 1985
  ident: ppat.1010028.ref042
  article-title: An electron-microscopical analysis of capture and initial stages of penetration of nematodes by Arthrobotrys oligospora
  publication-title: Ant Leeuw
  doi: 10.1007/BF02275043
– volume: 12
  start-page: e1005921
  issue: 10
  year: 2016
  ident: ppat.1010028.ref046
  article-title: Magnaporthe oryzae glycine-rich secretion protein, rbf1 critically participates in pathogenicity through the focal formation of the biotrophic interfacial Complex
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1005921
– volume: 9
  start-page: 5140
  issue: 1
  year: 2018
  ident: ppat.1010028.ref054
  article-title: Exocyst dynamics during vesicle tethering and fusion
  publication-title: Nat Commun
  doi: 10.1038/s41467-018-07467-5
– volume: 4
  start-page: 1996
  year: 2013
  ident: ppat.1010028.ref023
  article-title: Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae
  publication-title: Nat Commun
  doi: 10.1038/ncomms2996
– volume: 15
  start-page: 968
  year: 2014
  ident: ppat.1010028.ref027
  article-title: Interspecific and host-related gene expression patterns in nematode-trapping fungi
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-15-968
– volume: 142
  start-page: 4374
  issue: 23
  year: 2015
  ident: ppat.1010028.ref074
  article-title: The auxin-inducible degradation (AID) system enables versatile conditional protein depletion in C. elegans
  publication-title: Development
– volume: 36
  start-page: 111
  year: 1994
  ident: ppat.1010028.ref020
  article-title: Nematophagous fungi: physiological aspects and structure-function relationships
  publication-title: Adv Microb Physiol
  doi: 10.1016/S0065-2911(08)60178-2
– volume: 43
  start-page: 299
  issue: 4
  year: 2002
  ident: ppat.1010028.ref047
  article-title: Time-lapse photomicrography and electron microscopy on initiation of infection of nematodes by Dactylella ellipsospora
  publication-title: Mycoscience
  doi: 10.1007/S102670200044
– volume: 708
  start-page: 105
  year: 2010
  ident: ppat.1010028.ref066
  article-title: Innate immunity in C. elegans
  publication-title: Adv Exp Med Biol
  doi: 10.1007/978-1-4419-8059-5_6
– volume: 10
  start-page: e0133085
  issue: 7
  year: 2015
  ident: ppat.1010028.ref073
  article-title: A CRISPR-Cas9 system for genetic engineering of filamentous fungi
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0133085
– volume: 21
  start-page: 731
  issue: 4
  year: 1991
  ident: ppat.1010028.ref005
  article-title: Sterilization of workers from pesticide exposure: the causes and consequences of DBCP-induced damage in Costa Rica and beyond.
  publication-title: Int J Health Serv
  doi: 10.2190/25B9-QFMV-Y28P-L736
– volume: 34
  start-page: 185
  issue: 1
  year: 2018
  ident: ppat.1010028.ref007
  article-title: Gastrointestinal nematodes, diagnosis and control
  publication-title: Vet Clin North Am Food Anim Pract
  doi: 10.1016/j.cvfa.2017.10.008
– volume: 22
  start-page: 63
  issue: 1–2
  year: 2004
  ident: ppat.1010028.ref049
  article-title: Secretory granule biogenesis and neuropeptide sorting to the regulated secretory pathway in neuroendocrine cells
  publication-title: J Mol Neurosci
  doi: 10.1385/JMN:22:1-2:63
– year: 2021
  ident: ppat.1010028.ref012
  article-title: The STRIPAK component SipC is involved in morphology and cell-fate determination in the nematode-trapping fungus Duddingtonia flagrans
  publication-title: Genetics
– volume: 104
  start-page: 8379
  issue: 20
  year: 2007
  ident: ppat.1010028.ref016
  article-title: Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.0702770104
– volume: 97
  start-page: 153
  issue: 2
  year: 1999
  ident: ppat.1010028.ref035
  article-title: Brefeldin A: the advantage of being uncompetitive
  publication-title: Cell
  doi: 10.1016/S0092-8674(00)80724-2
– volume: 159
  start-page: 133
  issue: 1
  year: 2001
  ident: ppat.1010028.ref036
  article-title: Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants
  publication-title: Genetics
  doi: 10.1093/genetics/159.1.133
– volume: 57
  start-page: 411
  year: 2019
  ident: ppat.1010028.ref040
  article-title: Molecular interactions between smut fungi and their host plants
  publication-title: Annu Rev Phytopathol
  doi: 10.1146/annurev-phyto-082718-100139
– volume: 227
  start-page: 326
  issue: 2
  year: 2020
  ident: ppat.1010028.ref060
  article-title: Exploring folds, evolution and host interactions: understanding effector structure/function in disease and immunity
  publication-title: New Phytol
  doi: 10.1111/nph.16563
– volume: 51
  start-page: 399
  issue: 4
  year: 1985
  ident: ppat.1010028.ref055
  article-title: Development of fate of electron-dense microbodies in trap cells of the nematophagous fungus Arthrobotrys oligospora
  publication-title: Ant Leeuw
  doi: 10.1007/BF02275044
– volume: 111
  start-page: 474
  issue: 3
  year: 2021
  ident: ppat.1010028.ref065
  article-title: One cut to change them all: CRISPR/Cas, a groundbreaking tool for genome editing in Botrytis cinerea and other fungal plant pathogens
  publication-title: Phytopathology
  doi: 10.1094/PHYTO-09-20-0379-PER
– volume: 120
  start-page: 3099
  issue: Pt 17
  year: 2007
  ident: ppat.1010028.ref057
  article-title: The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity
  publication-title: J Cell Sci
  doi: 10.1242/jcs.004770
– volume: 109
  start-page: 10960
  issue: 27
  year: 2012
  ident: ppat.1010028.ref062
  article-title: Origin and evolution of carnivorism in the Ascomycota (fungi)
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1120915109
– year: 1999
  ident: ppat.1010028.ref072
– volume: 72
  start-page: 5020
  issue: 7
  year: 2006
  ident: ppat.1010028.ref034
  article-title: Laccase as a novel, versatile reporter gene for filamentous fungi
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.00060-06
– volume: 18
  start-page: e06208
  issue: 7
  year: 2020
  ident: ppat.1010028.ref010
  article-title: Safety and efficacy of BioWorma((R)) (Duddingtonia flagrans NCIMB 30336) as a feed additive for all grazing animals
  publication-title: EFSA J
– volume: 5
  start-page: 46
  year: 2009
  ident: ppat.1010028.ref011
  article-title: Digestibility of Duddingtonia flagrans chlamydospores in ruminants: in vitro and in vivo studies
  publication-title: BMC Vet Res
  doi: 10.1186/1746-6148-5-46
– volume: 15
  start-page: 409
  issue: 7
  year: 2017
  ident: ppat.1010028.ref038
  article-title: Ustilago maydis effectors and their impact on virulence
  publication-title: Nat Rev Microbiol
  doi: 10.1038/nrmicro.2017.33
– volume: 14
  start-page: 1557008
  issue: 2
  year: 2019
  ident: ppat.1010028.ref059
  article-title: Arms race: diverse effector proteins with conserved motifs
  publication-title: Plant Signal Behav
  doi: 10.1080/15592324.2018.1557008
– volume: 22
  start-page: 1388
  issue: 4
  year: 2010
  ident: ppat.1010028.ref044
  article-title: Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement
  publication-title: Plant Cell
  doi: 10.1105/tpc.109.069666
– volume: 1
  start-page: E17
  issue: 1
  year: 1999
  ident: ppat.1010028.ref051
  article-title: Transport-vesicle targeting: tethers before SNAREs
  publication-title: Nat Cell Biol
  doi: 10.1038/8967
– volume: 119
  start-page: 350
  issue: 4
  year: 2016
  ident: ppat.1010028.ref063
  article-title: Coevolution of parasitic fungi and insect hosts
  publication-title: Zoology
  doi: 10.1016/j.zool.2016.06.005
– volume: 170
  start-page: 131
  issue: 1
  year: 1996
  ident: ppat.1010028.ref031
  article-title: Isolation and characterization of two novel genes expressed in germinating conidia of the obligate biotroph Erysiphe graminis f.sp. hordei
  publication-title: Gene
  doi: 10.1016/0378-1119(95)00875-6
– volume: 15
  start-page: e1008029
  issue: 3
  year: 2019
  ident: ppat.1010028.ref015
  article-title: Intercellular communication is required for trap formation in the nematode-trapping fungus Duddingtonia flagrans
  publication-title: PLoS Genet
  doi: 10.1371/journal.pgen.1008029
– volume: 12
  start-page: 244
  issue: 4
  year: 1980
  ident: ppat.1010028.ref002
  article-title: Biocontrol: fungi as nematode control agents
  publication-title: J Nematol
– volume: 23
  start-page: 83
  issue: 1
  year: 2013
  ident: ppat.1010028.ref018
  article-title: Nematode-trapping fungi eavesdrop on nematode pheromones
  publication-title: Curr Biol
  doi: 10.1016/j.cub.2012.11.035
– volume: 10
  start-page: 364
  issue: 2
  year: 2008
  ident: ppat.1010028.ref030
  article-title: Paralysis of nematodes: shifts in the transcriptome of the nematode-trapping fungus Monacrosporium haptotylum during infection of Caenorhabditis elegans
  publication-title: Environ Microbiol
  doi: 10.1111/j.1462-2920.2007.01457.x
– volume: 28
  start-page: 48
  year: 2015
  ident: ppat.1010028.ref025
  article-title: The exocyst complex: delivery hub for morphogenesis and pathogenesis in filamentous fungi
  publication-title: Curr Opin Plant Biol
  doi: 10.1016/j.pbi.2015.09.003
– volume: 14
  start-page: 2107
  issue: 9
  year: 2002
  ident: ppat.1010028.ref032
  article-title: Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus
  publication-title: Plant Cell
  doi: 10.1105/tpc.003426
– volume: 12
  start-page: 687713
  year: 2021
  ident: ppat.1010028.ref039
  article-title: Effectors of plant necrotrophic fungi
  publication-title: Front Plant Sci
  doi: 10.3389/fpls.2021.687713
– volume: 11
  start-page: 5845
  issue: 1
  year: 2020
  ident: ppat.1010028.ref041
  article-title: Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming
  publication-title: Nat Commun
  doi: 10.1038/s41467-020-19624-w
– volume: 12
  start-page: 5462
  year: 2021
  ident: ppat.1010028.ref019
  article-title: Fatal attraction of Caenorhabditis elegans to predatory fungi through 6-methyl-salicylic acid
  publication-title: Nat Commun
  doi: 10.1038/s41467-021-25535-1
– volume: 36
  start-page: 165
  year: 1998
  ident: ppat.1010028.ref006
  article-title: Developing sustainable systems for nematode management
  publication-title: Annu Rev Phytopathol
  doi: 10.1146/annurev.phyto.36.1.165
– volume: 6
  start-page: e20023
  year: 2017
  ident: ppat.1010028.ref017
  article-title: Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey
  publication-title: eLife.
  doi: 10.7554/eLife.20023
– volume: 2
  start-page: e00408
  issue: 6
  year: 2017
  ident: ppat.1010028.ref058
  article-title: Genomic, network, and phylogenetic analysis of the oomycete effector arsenal
  publication-title: mSphere
  doi: 10.1128/mSphere.00408-17
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Snippet Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and...
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StartPage e1010028
SubjectTerms Adhesives
Analysis
Animals
Biology and Life Sciences
Caenorhabditis elegans
Caenorhabditis elegans - growth & development
Caenorhabditis elegans - microbiology
CCN Intercellular Signaling Proteins - genetics
CCN Intercellular Signaling Proteins - metabolism
Coelomocytes
Cysteine
Cysteine - chemistry
Duddingtonia - physiology
Fungal Proteins - genetics
Fungal Proteins - metabolism
Fungi
Genes
Genetic transcription
Genomes
Host-Pathogen Interactions
Hyphae
Identification and classification
Infections
Life span
Medicine and Health Sciences
Microorganisms
Nematodes
Observations
Paralysis
Pathogens
Penetration
Peptides
Prevention
Proteins
Research and Analysis Methods
Transcription
Trapping
Virulence
Virulence (Microbiology)
Virulence factors
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Title The small-secreted cysteine-rich protein CyrA is a virulence factor participating in the attack of Caenorhabditis elegans by Duddingtonia flagrans
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http://dx.doi.org/10.1371/journal.ppat.1010028
Volume 17
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