Jump to content

Fungal effectors: Difference between revisions

Add links
From Wikipedia, the free encyclopedia
Browse history interactively
← Previous editNext edit →
Content deleted Content added
VisualWikitext
m v2.05b - Bot T18 CW#553 - Fix errors for CW project (<nowiki> tags)
Nolanna (talk | contribs)
66 edits
Added a table summarising some pathogens and their known effectors. Made minor changes to the main text.
Line 1: Line 1:
'''Fungal effector proteins''' or '''fungal effectors''' are proteins secreted by [[Pathogenic fungus|pathogenic fungi]] into a host organism in order to modulate the host's immune response.<ref>{{cite journal|last1=Bent|first1=A. F.|last2=Mackey|first2=D.|year=2007|title=Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions|journal=Annual Review of Phytopathology|volume=45|pages=399–436|doi=10.1146/annurev.phyto.45.062806.094427|pmid=17506648 }}</ref><ref>{{cite journal|last1=Stergiopoulos|first1=I.|last2=de Wit|first2=P. J.|year=2009|title=Fungal effector proteins|journal=Annual Review of Phytopathology|volume=47|pages=233–263|doi=10.1146/annurev.phyto.112408.132637|pmid=19400631 }}</ref>
'''Fungal effectors''' are proteins or non-proteinaceous molecules (such as RNAs or small molecules) secreted by [[Pathogenic fungus|pathogenic fungi]] into a host organism in order to modulate the host's immune response.<ref>{{cite journal|last1=Bent|first1=A. F.|last2=Mackey|first2=D.|year=2007|title=Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions|journal=Annual Review of Phytopathology|volume=45|pages=399–436|doi=10.1146/annurev.phyto.45.062806.094427|pmid=17506648 }}</ref><ref>{{cite journal|last1=Stergiopoulos|first1=I.|last2=de Wit|first2=P. J.|year=2009|title=Fungal effector proteins|journal=Annual Review of Phytopathology|volume=47|pages=233–263|doi=10.1146/annurev.phyto.112408.132637|pmid=19400631 }}</ref><ref>{{Cite journal |last=Shao |first=Dandan |last2=Smith |first2=Damon L. |last3=Kabbage |first3=Mehdi |last4=Roth |first4=Mitchell G. |date=2021 |title=Effectors of Plant Necrotrophic Fungi |url=https://www.frontiersin.org/articles/10.3389/fpls.2021.687713 |journal=Frontiers in Plant Science |volume=12 |doi=10.3389/fpls.2021.687713 |issn=1664-462X |pmc=PMC8213389 |pmid=34149788}}</ref>


== Fungal effectors of plant pathogenic fungi ==
== Fungal effectors of plant pathogenic fungi ==
Line 6: Line 6:
In order to counteract PTI, fungal pathogens secrete effector proteins into the host, some of which may directly inhibit components of the innate immune response cascade. One example is the conserved effector NIS1, present in fungal pathogens from the [[Ascomycota]] and [[Basidiomycota]] phyla. NIS1 blocks PAMP-triggered immune responses by interacting with the PRR-associated kinases BAK1 and BIK1 and preventing these kinases from interacting with their downstream partners.<ref>{{Cite journal |last=Irieda |first=Hiroki |last2=Inoue |first2=Yoshihiro |last3=Mori |first3=Masashi |last4=Yamada |first4=Kohji |last5=Oshikawa |first5=Yuu |last6=Saitoh |first6=Hiromasa |last7=Uemura |first7=Aiko |last8=Terauchi |first8=Ryohei |last9=Kitakura |first9=Saeko |last10=Kosaka |first10=Ayumi |last11=Singkaravanit-Ogawa |first11=Suthitar |last12=Takano |first12=Yoshitaka |date=2019-01-08 |title=Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases |url=https://pnas.org/doi/full/10.1073/pnas.1807297116 |journal=Proceedings of the National Academy of Sciences |language=en |volume=116 |issue=2 |pages=496–505 |doi=10.1073/pnas.1807297116 |issn=0027-8424 |pmc=6329965 |pmid=30584105}}</ref> To protect themselves from the actions of effector proteins, plants have evolved resistance proteins (R proteins), which may in turn recognise an effector and trigger a second tier of immune responses, known as [[effector-triggered immunity]] (ETI).
In order to counteract PTI, fungal pathogens secrete effector proteins into the host, some of which may directly inhibit components of the innate immune response cascade. One example is the conserved effector NIS1, present in fungal pathogens from the [[Ascomycota]] and [[Basidiomycota]] phyla. NIS1 blocks PAMP-triggered immune responses by interacting with the PRR-associated kinases BAK1 and BIK1 and preventing these kinases from interacting with their downstream partners.<ref>{{Cite journal |last=Irieda |first=Hiroki |last2=Inoue |first2=Yoshihiro |last3=Mori |first3=Masashi |last4=Yamada |first4=Kohji |last5=Oshikawa |first5=Yuu |last6=Saitoh |first6=Hiromasa |last7=Uemura |first7=Aiko |last8=Terauchi |first8=Ryohei |last9=Kitakura |first9=Saeko |last10=Kosaka |first10=Ayumi |last11=Singkaravanit-Ogawa |first11=Suthitar |last12=Takano |first12=Yoshitaka |date=2019-01-08 |title=Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases |url=https://pnas.org/doi/full/10.1073/pnas.1807297116 |journal=Proceedings of the National Academy of Sciences |language=en |volume=116 |issue=2 |pages=496–505 |doi=10.1073/pnas.1807297116 |issn=0027-8424 |pmc=6329965 |pmid=30584105}}</ref> To protect themselves from the actions of effector proteins, plants have evolved resistance proteins (R proteins), which may in turn recognise an effector and trigger a second tier of immune responses, known as [[effector-triggered immunity]] (ETI).


== Fungal effectors based on their site of action ==
The pathogenic fungi in plants use two distinct effector secretion systems and each secretory pathway is specific to an effector family:
Plant pathogenic fungi use two distinct effector secretion systems and each secretory pathway is specific to an effector family:


* '''apoplastic effectors''' : proteins which stay into the [[apoplast]], they are translocated and accumulated into a distinct compartment enclosing the growing hypha named the [[EIHM]] (extra-invasive hyphal membrane).
* '''apoplastic effectors''' act in the [[apoplast]], the extracellular space outside the host plant's cells. In the model pathogen ''[[Magnaporthe grisea|Magnaporthe oryzae]],'' apoplastic effectors are secreted into a distinct compartment enclosing the growing hypha named the [[EIHM]] (extra-invasive hyphal membrane).<ref name=":3">{{Cite web |url=https://academic.oup.com/plcell/article/22/4/1388/6096968 |access-date=2023-02-27 |website=academic.oup.com |doi=10.1105/tpc.109.069666 |pmc=PMC2879738 |pmid=20435900}}</ref>
* '''cytoplasmic effectors''' : proteins which enter the host cytoplasm, they are accumulated into a complex plant-derived structure named the biotrophic interfacial complex (BIC) and they are later translocated across the [[EIHM]] inside the plant cell. It has been shown that cytoplasmic effectors can move through a few layers of plant cells, probably a way to prepare them for hyphal invasion.<ref>{{Cite journal |last1=De Wit |first1=Pierre J. G. M. |last2=Mehrabi |first2=Rahim |last3=Van Den Burg |first3=Harrold A. |last4=Stergiopoulos |first4=Ioannis |date=November 2009 |title=Fungal effector proteins: past, present and future |journal=Molecular Plant Pathology |language=en |volume=10 |issue=6 |pages=735–747 |doi=10.1111/j.1364-3703.2009.00591.x |pmc=6640362 |pmid=19849781}}</ref>
* '''cytoplasmic effectors''' enter the host cells' cytoplasm. Cytoplasmic effectors of the pathogen ''[[Magnaporthe grisea|Magnaporthe oryzae]]'' are accumulated into a complex plant-derived structure named the biotrophic interfacial complex (BIC) and they are later translocated across the [[EIHM]] inside the plant cell.<ref name=":3" /> It has been shown that cytoplasmic effectors can move through a few layers of plant cells, probably a way to prepare them for hyphal invasion.<ref>{{Cite journal |last1=De Wit |first1=Pierre J. G. M. |last2=Mehrabi |first2=Rahim |last3=Van Den Burg |first3=Harrold A. |last4=Stergiopoulos |first4=Ioannis |date=November 2009 |title=Fungal effector proteins: past, present and future |journal=Molecular Plant Pathology |language=en |volume=10 |issue=6 |pages=735–747 |doi=10.1111/j.1364-3703.2009.00591.x |pmc=6640362 |pmid=19849781}}</ref>

== Fungal pathogens and their known effectors ==
{| class="wikitable"
!Pathogen nutrition
!Pathogen species
!Plant disease and host plant species
!Known effectors and their functions
|-
| rowspan="2" |Biotrophic
|[[Blumeria graminis|''Blumeria graminis'' f. sp. ''hordei'']] ''(Bgh)''
|Powdery mildew on barley
|'''AVR<sub>A10</sub>''' - recognized by the MLA10 R-protein from barley. <ref name=":0">{{Cite journal |last=Shen |first=Qian-Hua |last2=Saijo |first2=Yusuke |last3=Mauch |first3=Stefan |last4=Biskup |first4=Christoph |last5=Bieri |first5=Stéphane |last6=Keller |first6=Beat |last7=Seki |first7=Hikaru |last8=Ülker |first8=Bekir |last9=Somssich |first9=Imre E. |last10=Schulze-Lefert |first10=Paul |date=2007-02-23 |title=Nuclear Activity of MLA Immune Receptors Links Isolate-Specific and Basal Disease-Resistance Responses |url=https://www.science.org/doi/10.1126/science.1136372 |journal=Science |language=en |volume=315 |issue=5815 |pages=1098–1103 |doi=10.1126/science.1136372 |issn=0036-8075}}</ref>
'''AVR<sub>K1</sub>''' - recognized by the MLK1 R-protein from barley.<ref name=":0" />
|-
|''[[Passalora fulva|Cladosporium fulvum]]''
|Leaf mould on tomato
|'''Ecp6''' - sequesters chitin, making less chitin available to bind PRRs.<ref name=":1">{{Cite journal |last=Sánchez-Vallet |first=Andrea |last2=Tian |first2=Hui |last3=Rodriguez-Moreno |first3=Luis |last4=Valkenburg |first4=Dirk-Jan |last5=Saleem-Batcha |first5=Raspudin |last6=Wawra |first6=Stephan |last7=Kombrink |first7=Anja |last8=Verhage |first8=Leonie |last9=Jonge |first9=Ronnie de |last10=Esse |first10=H. Peter van |last11=Zuccaro |first11=Alga |last12=Croll |first12=Daniel |last13=Mesters |first13=Jeroen R. |last14=Thomma |first14=Bart P. H. J. |date=2020-06-23 |title=A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization |url=https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1008652 |journal=PLOS Pathogens |language=en |volume=16 |issue=6 |pages=e1008652 |doi=10.1371/journal.ppat.1008652 |issn=1553-7374 |pmc=PMC7337405 |pmid=32574207}}</ref>
'''Avr4''' - binds to chitin oligomers in the fungal cell wall, protecting it from degradation by chitinases.<ref name=":1" />
|-
| rowspan="2" |Hemibiotrophic
|[[Fusarium oxysporum f.sp. lycopersici|''Fusarium oxysporum'' f. sp. ''lycopersici'']]
|Tomato vascular wilt
|'''Six1 (Avr3)''' - recognised by the R-protein I-3 from tomato, and when this happens local cell death is triggered as a defense mechanism.<ref name=":2">{{Cite journal |last=Gawehns |first=F. |last2=Houterman |first2=P. M. |last3=Ichou |first3=F. Ait |last4=Michielse |first4=C. B. |last5=Hijdra |first5=M. |last6=Cornelissen |first6=B. J. C. |last7=Rep |first7=M. |last8=Takken |first8=F. L. W. |date=2014-04-01 |title=The Fusarium oxysporum Effector Six6 Contributes to Virulence and Suppresses I-2-Mediated Cell Death |url=https://apsjournals.apsnet.org/doi/10.1094/MPMI-11-13-0330-R |journal=Molecular Plant-Microbe Interactions® |volume=27 |issue=4 |pages=336–348 |doi=10.1094/MPMI-11-13-0330-R |issn=0894-0282}}</ref>
'''Six3 (Avr2) -''' recognised by the R-protein I-2, triggering local cell death.<ref name=":2" />
'''Six4 (Avr1) -''' suppresses I-2 and I-3-mediated cell death; in resistant tomato varieties Avr1 is recognised and neutralised by I and I-1.<ref name=":2" />

'''Six6 -''' suppresses I-2 and I-3-mediated cell death. <ref name=":2" />
|-
|''[[Leptosphaeria maculans]]''
|Blackleg disease on Brassica crops.<ref>{{Cite journal |last=Robin |first=Arif Hasan Khan |last2=Laila |first2=Rawnak |last3=Abuyusuf |first3=Md. |last4=Park |first4=Jong-In |last5=Nou |first5=Ill-Sup |date=2020 |title=Leptosphaeria maculans Alters Glucosinolate Accumulation and Expression of Aliphatic and Indolic Glucosinolate Biosynthesis Genes in Blackleg Disease-Resistant and -Susceptible Cabbage Lines at the Seedling Stage |url=https://www.frontiersin.org/articles/10.3389/fpls.2020.01134 |journal=Frontiers in Plant Science |volume=11 |doi=10.3389/fpls.2020.01134 |issn=1664-462X |pmc=PMC7406797 |pmid=32849695}}</ref>
|'''AvrLm1AvrLm2AvrLm3'''
|-
| rowspan="2" |Necrotrophic
|''[[Pyrenophora tritici-repentis]]''
|Tan spot of wheat.<ref>{{Cite journal |last=Andersen |first=Ethan J. |last2=Nepal |first2=Madhav P. |last3=Ali |first3=Shaukat |date=2021-04-01 |title=Necrotrophic Fungus Pyrenophora tritici-repentis Triggers Expression of Multiple Resistance Components in Resistant and Susceptible Wheat Cultivars |url=http://ppjonline.org/journal/view.php?doi=10.5423/PPJ.OA.06.2020.0109 |journal=The Plant Pathology Journal |language=en |volume=37 |issue=2 |pages=99–114 |doi=10.5423/PPJ.OA.06.2020.0109 |issn=1598-2254 |pmc=PMC8053848 |pmid=33866753}}</ref>
|'''PtrToxAPtrToxB'''
|-
|''[[Parastognospora nodorum]]''
|Septoria nodorum blotch in wheat.<ref>{{Cite journal |last=Hafez |first=Mohamed |last2=Gourlie |first2=Ryan |last3=Despins |first3=Therese |last4=Turkington |first4=Thomas K. |last5=Friesen |first5=Timothy L. |last6=Aboukhaddour |first6=Reem |date=2020-12-01 |title=Parastagonospora nodorum and Related Species in Western Canada: Genetic Variability and Effector Genes |url=https://apsjournals.apsnet.org/doi/10.1094/PHYTO-05-20-0207-R |journal=Phytopathology® |volume=110 |issue=12 |pages=1946–1958 |doi=10.1094/PHYTO-05-20-0207-R |issn=0031-949X}}</ref>
|'''SnToxASnTox1SnTox2SnTox3SnTox4SnTox5SnTox6SnTox7SnTox8'''
|}


== References ==
== References ==

Revision as of 15:50, 27 February 2023

Fungal effectors are proteins or non-proteinaceous molecules (such as RNAs or small molecules) secreted by pathogenic fungi into a host organism in order to modulate the host's immune response.[1][2][3]

Fungal effectors of plant pathogenic fungi

In the first stages of infection, conserved molecules from the fungal pathogen's cell wall, such as polysaccharides and chitin, are recognised by membrane-localised pattern recognition receptors (PRRs) on the plant host's side. Such conserved molecules are generally described as pathogen-associated molecular patterns (PAMPs) or microbe-associated molecular patterns (MAMPs) and the initial innate immune response that their recognition triggers is known as PAMP-triggered immunity (PTI).[4]

In order to counteract PTI, fungal pathogens secrete effector proteins into the host, some of which may directly inhibit components of the innate immune response cascade. One example is the conserved effector NIS1, present in fungal pathogens from the Ascomycota and Basidiomycota phyla. NIS1 blocks PAMP-triggered immune responses by interacting with the PRR-associated kinases BAK1 and BIK1 and preventing these kinases from interacting with their downstream partners.[5] To protect themselves from the actions of effector proteins, plants have evolved resistance proteins (R proteins), which may in turn recognise an effector and trigger a second tier of immune responses, known as effector-triggered immunity (ETI).

Fungal effectors based on their site of action

Plant pathogenic fungi use two distinct effector secretion systems and each secretory pathway is specific to an effector family:

  • apoplastic effectors act in the apoplast, the extracellular space outside the host plant's cells. In the model pathogen Magnaporthe oryzae, apoplastic effectors are secreted into a distinct compartment enclosing the growing hypha named the EIHM (extra-invasive hyphal membrane).[6]
  • cytoplasmic effectors enter the host cells' cytoplasm. Cytoplasmic effectors of the pathogen Magnaporthe oryzae are accumulated into a complex plant-derived structure named the biotrophic interfacial complex (BIC) and they are later translocated across the EIHM inside the plant cell.[6] It has been shown that cytoplasmic effectors can move through a few layers of plant cells, probably a way to prepare them for hyphal invasion.[7]

Fungal pathogens and their known effectors

Pathogen nutrition Pathogen species Plant disease and host plant species Known effectors and their functions
Biotrophic Blumeria graminis f. sp. hordei (Bgh) Powdery mildew on barley AVRA10 - recognized by the MLA10 R-protein from barley. [8]

AVRK1 - recognized by the MLK1 R-protein from barley.[8]

Cladosporium fulvum Leaf mould on tomato Ecp6 - sequesters chitin, making less chitin available to bind PRRs.[9]

Avr4 - binds to chitin oligomers in the fungal cell wall, protecting it from degradation by chitinases.[9]

Hemibiotrophic Fusarium oxysporum f. sp. lycopersici Tomato vascular wilt Six1 (Avr3) - recognised by the R-protein I-3 from tomato, and when this happens local cell death is triggered as a defense mechanism.[10]

Six3 (Avr2) - recognised by the R-protein I-2, triggering local cell death.[10] Six4 (Avr1) - suppresses I-2 and I-3-mediated cell death; in resistant tomato varieties Avr1 is recognised and neutralised by I and I-1.[10]

Six6 - suppresses I-2 and I-3-mediated cell death. [10]

Leptosphaeria maculans Blackleg disease on Brassica crops.[11] AvrLm1AvrLm2AvrLm3
Necrotrophic Pyrenophora tritici-repentis Tan spot of wheat.[12] PtrToxAPtrToxB
Parastognospora nodorum Septoria nodorum blotch in wheat.[13] SnToxASnTox1SnTox2SnTox3SnTox4SnTox5SnTox6SnTox7SnTox8

References

  1. ^ Bent, A. F.; Mackey, D. (2007). "Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions". Annual Review of Phytopathology. 45: 399–436. doi:10.1146/annurev.phyto.45.062806.094427. PMID 17506648.
  2. ^ Stergiopoulos, I.; de Wit, P. J. (2009). "Fungal effector proteins". Annual Review of Phytopathology. 47: 233–263. doi:10.1146/annurev.phyto.112408.132637. PMID 19400631.
  3. ^ Shao, Dandan; Smith, Damon L.; Kabbage, Mehdi; Roth, Mitchell G. (2021). "Effectors of Plant Necrotrophic Fungi". Frontiers in Plant Science. 12. doi:10.3389/fpls.2021.687713. ISSN 1664-462X. PMC 8213389. PMID 34149788.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  4. ^ Selin, Carrie; de Kievit, Teresa R.; Belmonte, Mark F.; Fernando, W. G. Dilantha (2016-04-27). "Elucidating the Role of Effectors in Plant-Fungal Interactions: Progress and Challenges". Frontiers in Microbiology. 7. doi:10.3389/fmicb.2016.00600. ISSN 1664-302X. PMC 4846801. PMID 27199930.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  5. ^ Irieda, Hiroki; Inoue, Yoshihiro; Mori, Masashi; Yamada, Kohji; Oshikawa, Yuu; Saitoh, Hiromasa; Uemura, Aiko; Terauchi, Ryohei; Kitakura, Saeko; Kosaka, Ayumi; Singkaravanit-Ogawa, Suthitar; Takano, Yoshitaka (2019-01-08). "Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases". Proceedings of the National Academy of Sciences. 116 (2): 496–505. doi:10.1073/pnas.1807297116. ISSN 0027-8424. PMC 6329965. PMID 30584105.
  6. ^ a b academic.oup.com. doi:10.1105/tpc.109.069666. PMC 2879738. PMID 20435900 https://academic.oup.com/plcell/article/22/4/1388/6096968. Retrieved 2023-02-27. {{cite web}}: Missing or empty |title= (help)CS1 maint: PMC format (link)
  7. ^ De Wit, Pierre J. G. M.; Mehrabi, Rahim; Van Den Burg, Harrold A.; Stergiopoulos, Ioannis (November 2009). "Fungal effector proteins: past, present and future". Molecular Plant Pathology. 10 (6): 735–747. doi:10.1111/j.1364-3703.2009.00591.x. PMC 6640362. PMID 19849781.
  8. ^ a b Shen, Qian-Hua; Saijo, Yusuke; Mauch, Stefan; Biskup, Christoph; Bieri, Stéphane; Keller, Beat; Seki, Hikaru; Ülker, Bekir; Somssich, Imre E.; Schulze-Lefert, Paul (2007-02-23). "Nuclear Activity of MLA Immune Receptors Links Isolate-Specific and Basal Disease-Resistance Responses". Science. 315 (5815): 1098–1103. doi:10.1126/science.1136372. ISSN 0036-8075.
  9. ^ a b Sánchez-Vallet, Andrea; Tian, Hui; Rodriguez-Moreno, Luis; Valkenburg, Dirk-Jan; Saleem-Batcha, Raspudin; Wawra, Stephan; Kombrink, Anja; Verhage, Leonie; Jonge, Ronnie de; Esse, H. Peter van; Zuccaro, Alga; Croll, Daniel; Mesters, Jeroen R.; Thomma, Bart P. H. J. (2020-06-23). "A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization". PLOS Pathogens. 16 (6): e1008652. doi:10.1371/journal.ppat.1008652. ISSN 1553-7374. PMC 7337405. PMID 32574207.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  10. ^ a b c d Gawehns, F.; Houterman, P. M.; Ichou, F. Ait; Michielse, C. B.; Hijdra, M.; Cornelissen, B. J. C.; Rep, M.; Takken, F. L. W. (2014-04-01). "The Fusarium oxysporum Effector Six6 Contributes to Virulence and Suppresses I-2-Mediated Cell Death". Molecular Plant-Microbe Interactions®. 27 (4): 336–348. doi:10.1094/MPMI-11-13-0330-R. ISSN 0894-0282.
  11. ^ Robin, Arif Hasan Khan; Laila, Rawnak; Abuyusuf, Md.; Park, Jong-In; Nou, Ill-Sup (2020). "Leptosphaeria maculans Alters Glucosinolate Accumulation and Expression of Aliphatic and Indolic Glucosinolate Biosynthesis Genes in Blackleg Disease-Resistant and -Susceptible Cabbage Lines at the Seedling Stage". Frontiers in Plant Science. 11. doi:10.3389/fpls.2020.01134. ISSN 1664-462X. PMC 7406797. PMID 32849695.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  12. ^ Andersen, Ethan J.; Nepal, Madhav P.; Ali, Shaukat (2021-04-01). "Necrotrophic Fungus Pyrenophora tritici-repentis Triggers Expression of Multiple Resistance Components in Resistant and Susceptible Wheat Cultivars". The Plant Pathology Journal. 37 (2): 99–114. doi:10.5423/PPJ.OA.06.2020.0109. ISSN 1598-2254. PMC 8053848. PMID 33866753.{{cite journal}}: CS1 maint: PMC format (link)
  13. ^ Hafez, Mohamed; Gourlie, Ryan; Despins, Therese; Turkington, Thomas K.; Friesen, Timothy L.; Aboukhaddour, Reem (2020-12-01). "Parastagonospora nodorum and Related Species in Western Canada: Genetic Variability and Effector Genes". Phytopathology®. 110 (12): 1946–1958. doi:10.1094/PHYTO-05-20-0207-R. ISSN 0031-949X.
Retrieved from "https://en.wikipedia.org/w/index.php?title=Fungal_effectors&oldid=1141924056"