Fungal effectors

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A diagram showing the infecting structures and effector delivery strategies of a model hemibiotrophic pathogen, Phytophthora infestans.

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]

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).

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

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]

Ustilago maydis Corn smut (maize) Pep1; Pit2; Cmu1; Tin2; See1
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] AvrLm1; AvrLm2; AvrLm3
Magnaporthe oryzae Rice blast disease Cytoplasmic effectors:

Avr-Pizt - interacts with the E3 ubiquitin ligase APIP6, which indirectly leads to reduced Reactive Oxygen Species (ROS) production and suppresses the expression of defence-related genes.[12] Pwl1, Pwl2, Bas1, Avr-Pita, MC69

Apoplastic effectors: Slp1 - binds to and sequesters chitin oligosaccharides. As a result, chitin is unavailable to bind to the host's chitin elicitor binding protein (CEBiP) and elicit PAMP-triggered defence responses.[13] BAS4, BAS113

Phytophthora infestans Potato blight AVR3a - cytoplasmic effector interacting with and stabilising the plant E3 ubiquitin ligase CMPG1. As a result CMPG1 is unable to get degraded and trigger cell death, allowing the pathogen to obtain nutrients from living host cells (biotrophy).

AVRblb2 - a cytoplasmic effector preventing the secretion of a papain-like cysteine protease (C14) from the host, which would otherwise serve to degrade fungal effector proteins.[14]

Necrotrophic Pyrenophora tritici-repentis Tan spot of wheat.[15] PtrToxA; PtrToxB
Parastognospora nodorum Septoria nodorum blotch in wheat.[16] SnToxA; SnTox1; SnTox2; SnTox3; SnTox4; SnTox5; SnTox6; SnTox7; SnTox8
Cochliobolus heterostrophus Southern corn leaf blight (maize)[17] ChToxA - in maize varieties sensitive to ToxA it induces leaf necrosis in response to light.[18]
Cochliobolus sativus BsToxA
Corynespora cassiicola Corynespora leaf fall disease in rubber trees[19] Cassiicolin - disrupts the membranes of host plant cells, causing leaf necrosis.[19]
Cochliobolus victoriae victorin

References

  1. ^ Bent AF, 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 PJ (2009). "Fungal effector proteins". Annual Review of Phytopathology. 47: 233–263. doi:10.1146/annurev.phyto.112408.132637. PMID 19400631.
  3. ^ Shao D, Smith DL, Kabbage M, Roth MG (2021). "Effectors of Plant Necrotrophic Fungi". Frontiers in Plant Science. 12: 687713. doi:10.3389/fpls.2021.687713. PMC 8213389. PMID 34149788.
  4. ^ Selin C, de Kievit TR, Belmonte MF, Fernando WG (2016-04-27). "Elucidating the Role of Effectors in Plant-Fungal Interactions: Progress and Challenges". Frontiers in Microbiology. 7: 600. doi:10.3389/fmicb.2016.00600. PMC 4846801. PMID 27199930.
  5. ^ Irieda H, Inoue Y, Mori M, Yamada K, Oshikawa Y, Saitoh H, et al. (January 2019). "Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases". Proceedings of the National Academy of Sciences of the United States of America. 116 (2): 496–505. Bibcode:2019PNAS..116..496I. doi:10.1073/pnas.1807297116. PMC 6329965. PMID 30584105.
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  9. ^ a b Sánchez-Vallet A, Tian H, Rodriguez-Moreno L, Valkenburg DJ, Saleem-Batcha R, Wawra S, et al. (June 2020). "A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization". PLOS Pathogens. 16 (6): e1008652. doi:10.1371/journal.ppat.1008652. PMC 7337405. PMID 32574207.
  10. ^ a b c d Gawehns F, Houterman PM, Ichou FA, Michielse CB, Hijdra M, Cornelissen BJ, et al. (April 2014). "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. PMID 24313955.
  11. ^ Robin AH, Laila R, Abuyusuf M, Park JI, Nou IS (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: 1134. doi:10.3389/fpls.2020.01134. PMC 7406797. PMID 32849695.
  12. ^ Park, Chan-Ho; Chen, Songbiao; Shirsekar, Gautam; Zhou, Bo; Khang, Chang Hyun; Songkumarn, Pattavipha; Afzal, Ahmed J.; Ning, Yuese; Wang, Ruyi; Bellizzi, Maria; Valent, Barbara; Wang, Guo-Liang (November 2012). "The Magnaporthe oryzae Effector AvrPiz-t Targets the RING E3 Ubiquitin Ligase APIP6 to Suppress Pathogen-Associated Molecular Pattern–Triggered Immunity in Rice". The Plant Cell. 24 (11): 4748–4762. doi:10.1105/tpc.112.105429. ISSN 1040-4651. PMC 3531864. PMID 23204406.
  13. ^ Mentlak, Thomas A.; Kombrink, Anja; Shinya, Tomonori; Ryder, Lauren S.; Otomo, Ippei; Saitoh, Hiromasa; Terauchi, Ryohei; Nishizawa, Yoko; Shibuya, Naoto; Thomma, Bart P.H.J.; Talbot, Nicholas J. (2012-01-01). "Effector-Mediated Suppression of Chitin-Triggered Immunity by Magnaporthe oryzae Is Necessary for Rice Blast Disease". The Plant Cell. 24 (1): 322–335. doi:10.1105/tpc.111.092957. ISSN 1532-298X. PMC 3289562. PMID 22267486.
  14. ^ Pradhan, Amrita; Ghosh, Srayan; Sahoo, Debashis; Jha, Gopaljee (2020-11-04). "Fungal effectors, the double edge sword of phytopathogens". Current Genetics. 67 (1): 27–40. doi:10.1007/s00294-020-01118-3. ISSN 0172-8083. PMID 33146780. S2CID 226251352.
  15. ^ Andersen EJ, Nepal MP, Ali S (April 2021). "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. PMC 8053848. PMID 33866753.
  16. ^ Hafez M, Gourlie R, Despins T, Turkington TK, Friesen TL, Aboukhaddour R (December 2020). "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. PMID 32689900. S2CID 220671230.
  17. ^ Kang IJ, Shim HK, Roh JH, Heu S, Shin DB (August 2018). "Simple Detection of Cochliobolus Fungal Pathogens in Maize". The Plant Pathology Journal. 34 (4): 327–334. doi:10.5423/PPJ.FT.10.2017.0209. PMC 6097825. PMID 30140186.
  18. ^ Lu S, Gillian Turgeon B, Edwards MC (August 2015). "A ToxA-like protein from Cochliobolus heterostrophus induces light-dependent leaf necrosis and acts as a virulence factor with host selectivity on maize". Fungal Genetics and Biology. 81: 12–24. doi:10.1016/j.fgb.2015.05.013. PMID 26051492.
  19. ^ a b Ngo KX, Nguyen PD, Furusho H, Miyata M, Shimonaka T, Chau NN, et al. (July 2022). "Unraveling the Host-Selective Toxic Interaction of Cassiicolin with Lipid Membranes and Its Cytotoxicity". Phytopathology. 112 (7): 1524–1536. doi:10.1094/PHYTO-09-21-0397-R. PMID 35238604. S2CID 247221286.
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