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Fungal Plant Pathogenesis Mediated by Effectors

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  • Authors: Pierre J.G.M. De Wit1, Alison C. Testa2, Richard P. Oliver3
  • Editors: Joseph Heitman4, Neil A. R. Gow5
    Affiliations: 1: Laboratory of Phytopathology, Wageningen University, Wageningen, The Netherlands; 2: Center for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia; 3: Center for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia; 4: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 5: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0021-2016
  • Received 05 July 2016 Accepted 11 August 2016 Published 18 November 2016
  • Richard Oliver, [email protected]
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  • Abstract:

    The interactions between fungi and plants encompass a spectrum of ecologies ranging from saprotrophy (growth on dead plant material) through pathogenesis (growth of the fungus accompanied by disease on the plant) to symbiosis (growth of the fungus with growth enhancement of the plant). We consider pathogenesis in this article and the key roles played by a range of pathogen-encoded molecules that have collectively become known as effectors.

  • Citation: De Wit P, Testa A, Oliver R. 2016. Fungal Plant Pathogenesis Mediated by Effectors. Microbiol Spectrum 4(6):FUNK-0021-2016. doi:10.1128/microbiolspec.FUNK-0021-2016.


1. Birnbaumer L. 1992. Receptor-to-effector signaling through G proteins: roles for β γ dimers as well as α subunits. Cell 71:1069–1072 http://dx.doi.org/10.1016/S0092-8674(05)80056-X.
2. Kjemtrup S, Nimchuk Z, Dangl JL. 2000. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr Opin Microbiol 3:73–78 http://dx.doi.org/10.1016/S1369-5274(99)00054-5.
3. Fiegen M, Gierlich A, Hermann H, Li V, Rohe M, Knogge W. 1996. NIP1, a bifunctional signal molecule from the barley pathogen, Rhynchosporium secalis, p 89–92. In Stacey G, Mullin B, Gresshoff PM (ed), Biology of Plant-Microbe Interactions, vol 1. APS Press, St. Paul, MN.
4. De Wit PJGM, Joosten MHAJ, Thomma BPHJ, Stergiopoulos I. 2009. Gene-for-gene models and beyond: the Cladosporium fulvum-tomato pathosystem, p 135–156. In Deising HB (ed), The Mycota, vol 5. Springer, Berlin, Germany http://dx.doi.org/10.1007/978-3-540-87407-2_7.
5. Zipfel C. 2008. Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16 http://dx.doi.org/10.1016/j.coi.2007.11.003.
6. Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S, Kahmann R. 2015. Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545.
7. Bakkeren G, Jiang G, Warren RL, Butterfield Y, Shin H, Chiu R, Linning R, Schein J, Lee N, Hu G, Kupfer DM, Tang Y, Roe BA, Jones S, Marra M, Kronstad JW. 2006. Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet Biol 43:655–666 http://dx.doi.org/10.1016/j.fgb.2006.04.002.
8. Liu Z, Holmes DJ, Faris JD, Chao S, Brueggeman RS, Edwards MC, Friesen TL. 2015. Necrotrophic effector-triggered susceptibility (NETS) underlies the barley- Pyrenophora teres f. teres interaction specific to chromosome 6H. Mol Plant Pathol 16:188–200 http://dx.doi.org/10.1111/mpp.12172.
9. Baldrich P, Campo S, Wu MT, Liu TT, Hsing YI, San Segundo B. 2015. MicroRNA-mediated regulation of gene expression in the response of rice plants to fungal elicitors. RNA Biol 12:847–863 http://dx.doi.org/10.1080/15476286.2015.1050577.
10. Tan KC, Oliver RP, Solomon PS, Moffat CS. 2010. Proteinaceous necrotrophic effectors in fungal virulence. Funct Plant Biol 37:907–912 http://dx.doi.org/10.1071/FP10067.
11. Voegele RT, Struck C, Hahn M, Mendgen K. 2001. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98:8133–8138 http://dx.doi.org/10.1073/pnas.131186798.
12. Oliveira-Garcia E, Valent B. 2015. How eukaryotic filamentous pathogens evade plant recognition. Curr Opin Microbiol 26:92–101 http://dx.doi.org/10.1016/j.mib.2015.06.012.
13. Stotz HU, Mitrousia GK, de Wit PJ, Fitt BDL. 2014. Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci 19:491–500 http://dx.doi.org/10.1016/j.tplants.2014.04.009.
14. Balmer D, Planchamp C, Mauch-Mani B. 2013. On the move: induced resistance in monocots. J Exp Bot 64:1249–1261 http://dx.doi.org/10.1093/jxb/ers248.
15. Zhao C, Waalwijk C, de Wit PJGM, Tang D, van der Lee T. 2013. RNA-Seq analysis reveals new gene models and alternative splicing in the fungal pathogen Fusarium graminearum. BMC Genomics 14:21. http://dx.doi.org/10.1186/1471-2164-14-21.
16. Spanu PD. 2012. The genomics of obligate (and nonobligate) biotrophs. Annu Rev Phytopathol 50:91–109 http://dx.doi.org/10.1146/annurev-phyto-081211-173024.
17. Collemare J, Griffiths S, Iida Y, Karimi Jashni M, Battaglia E, Cox RJ, de Wit PJGM. 2014. Secondary metabolism and biotrophic lifestyle in the tomato pathogen Cladosporium fulvum. PLoS One 9:e85877. http://dx.doi.org/10.1371/journal.pone.0085877.
18. Jashni MK, Dols IHM, Iida Y, Boeren S, Beenen HG, Mehrabi R, Collemare J, de Wit PJGM. 2015. Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence. Mol Plant Microbe Interact 28:996–1008 http://dx.doi.org/10.1094/MPMI-04-15-0074-R.
19. Ökmen B, Etalo DW, Joosten MHAJ, Bouwmeester HJ, de Vos RCH, Collemare J, de Wit PJGM. 2013. Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato. New Phytol 198:1203–1214 http://dx.doi.org/10.1111/nph.12208.
20. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–329 http://dx.doi.org/10.1038/nature05286.
21. Liebrand TWH, van den Burg HA, Joosten MHAJ. 2014. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19:123–132 http://dx.doi.org/10.1016/j.tplants.2013.10.003.
22. Liebrand TWH, van den Berg GCM, Zhang Z, Smit P, Cordewener JHG, America AHP, Sklenar J, Jones AME, Tameling WIL, Robatzek S, Thomma BPHJ, Joosten MHAJ. 2013. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci USA 110:10010–10015 http://dx.doi.org/10.1073/pnas.1220015110. (Erratum, 110:13228.)
23. Macho AP, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–272 http://dx.doi.org/10.1016/j.molcel.2014.03.028. [CrossRef]
24. Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, Martinez-Rocha AL, Saitoh H, Terauchi R, Talbot NJ, Valent B. 2013. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun 4:1996. http://dx.doi.org/10.1038/ncomms2996.
25. Stergiopoulos I, de Wit PJGM. 2009. Fungal effector proteins. Annu Rev Phytopathol 47:233–263 http://dx.doi.org/10.1146/annurev.phyto.112408.132637. [CrossRef]
26. Bakkeren G, Valent B. 2014. Do pathogen effectors play peek-a-boo? Front Plant Sci 5:731 http://dx.doi.org/10.3389/fpls.2014.00731.
27. Oliver R, Lichtenzveig J, Tan KC, Waters O, Rybak K, Lawrence J, Friesen T, Burgess P. 2014. Absence of detectable yield penalty associated with insensitivity to Pleosporales necrotrophic effectors in wheat grown in the West Australian wheat belt. Plant Pathol 63:1027–1032 http://dx.doi.org/10.1111/ppa.12191.
28. Vleeshouwers VGAA, Oliver RP. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol Plant Microbe Interact 27:196–206 http://dx.doi.org/10.1094/MPMI-10-13-0313-IA.
29. Flor HH. 1971. Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296 http://dx.doi.org/10.1146/annurev.py.09.090171.001423.
30. van Kan JAL, van den Ackerveken GFJM, de Wit PJGM. 1991. Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact 4:52–59 http://dx.doi.org/10.1094/MPMI-4-052.
31. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793 http://dx.doi.org/10.1126/science.7973631.
32. Van den Ackerveken GFJM, Dunn RM, Cozijnsen AJ, Vossen JPMJ, Van den Broek HWJ, De Wit PJGM. 1994. Nitrogen limitation induces expression of the avirulence gene avr9 in the tomato pathogen Cladosporium fulvum. Mol Gen Genet 243:277–285 http://dx.doi.org/10.1007/BF00301063.
33. Pérez-García A, Snoeijers SS, Joosten MHAJ, Goosen T, De Wit PJGM. 2001. Expression of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by the global nitrogen response factor NRF1. Mol Plant Microbe Interact 14:316–325 http://dx.doi.org/10.1094/MPMI.2001.14.3.316.
34. Thomma BPHJ, Bolton MD, Clergeot PH, DE Wit PJGM. 2006. Nitrogen controls in planta expression of Cladosporium fulvum Avr9 but no other effector genes. Mol Plant Pathol 7:125–130 http://dx.doi.org/10.1111/j.1364-3703.2006.00320.x.
35. Flor HH. 1942. Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–669.
36. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183 http://dx.doi.org/10.1126/science.1119409.
37. Van Der Biezen EA, Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456 http://dx.doi.org/10.1016/S0968-0004(98)01311-5.
38. van Esse HP, Van’t Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, Boeren S, Vervoort J, de Wit PJGM, Thomma BPHJ. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948–1963 http://dx.doi.org/10.1105/tpc.108.059394.
39. Rooney HCE, Van’t Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Wit PJGM. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–1786 http://dx.doi.org/10.1126/science.1111404.
40. Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn RAL, Kamoun S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci USA 106:1654–1659 http://dx.doi.org/10.1073/pnas.0809201106.
41. Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A, Cordewener JHG, America AHP, Overmars HA, Van’t Klooster JW, Baranowski L, Sobczak M, Ilyas M, van der Hoorn RAL, Schots A, de Wit PJ, Bakker J, Goverse A, Smant G. 2012. Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc Natl Acad Sci USA 109:10119–10124 http://dx.doi.org/10.1073/pnas.1202867109.
42. Jashni MK, Mehrabi R, Collemare J, Mesarich CH, de Wit PJGM. 2015. The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant-pathogen interactions. Front Plant Sci 6:584 http://dx.doi.org/10.3389/fpls.2015.00584.
43. van den Hooven HW, Appelman AWJ, Zey T, de Wit PJGM, Vervoort J. 1999. Folding and conformational analysis of AVR9 peptide elicitors of the fungal tomato pathogen Cladosporium fulvum. Eur J Biochem 264:9–18 http://dx.doi.org/10.1046/j.1432-1327.1999.00503.x.
44. van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, de Wit PJGM. 2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19:1420–1430 http://dx.doi.org/10.1094/MPMI-19-1420.
45. van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJGM, Thomma BPHJ. 2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20:1092–1101 http://dx.doi.org/10.1094/MPMI-20-9-1092.
46. Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J, Hammond-Kosack KE, Thomma BPHJ, Rudd JJ. 2011. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 156:756–769 http://dx.doi.org/10.1104/pp.111.176347.
47. Stergiopoulos I, van den Burg HA, Ökmen B, Beenen HG, van Liere S, Kema GHJ, de Wit PJGM. 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc Natl Acad Sci USA 107:7610–7615 http://dx.doi.org/10.1073/pnas.1002910107.
48. Becker M, Becker Y, Green K, Scott B. 2016. The endophytic symbiont Epichloë festucae establishes an epiphyllous net on the surface of Lolium perenne leaves by development of an expressorium, an appressorium-like leaf exit structure. New Phytol 211:240–254 http://dx.doi/org/10.1111/nph.13931.
49. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12:2019–2032 http://dx.doi.org/10.1105/tpc.12.11.2019.
50. Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, McAdams SA, Faulk KN, Donaldson GK, Tarchini R, Valent B. 2000. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12:2033–2046 http://dx.doi.org/10.1105/tpc.12.11.2033.
51. Pareja-Jaime Y, Roncero MIG, Ruiz-Roldán MC. 2008. Tomatinase from Fusarium oxysporum f. sp. lycopersici is required for full virulence on tomato plants. Mol Plant Microbe Interact 21:728–736 http://dx.doi.org/10.1094/MPMI-21-6-0728.
52. Tanaka S, Han X, Kahmann R. 2015. Microbial effectors target multiple steps in the salicylic acid production and signaling pathway. Front Plant Sci 6:349 http://dx.doi.org/10.3389/fpls.2015.00349.
53. Park CH, Chen S, Shirsekar G, Zhou B, Khang CH, Songkumarn P, Afzal AJ, Ning Y, Wang R, Bellizzi M, Valent B, Wang GL. 2012. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 24:4748–4762 http://dx.doi.org/10.1105/tpc.112.105429.
54. Kim KT, Jeon J, Choi J, Cheong K, Song H, Choi G, Kang S, Lee YH. 2016. Kingdom-wide analysis of fungal small secreted proteins (SSPs) reveals their potential role in host association. Front Plant Sci 7:186 http://dx.doi.org/10.3389/fpls.2016.00186.
55. Houterman PM, Cornelissen BJC, Rep M. 2008. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 4:e1000061. http://dx.doi.org/10.1371/journal.ppat.1000061.
56. Houterman PM, Ma L, van Ooijen G, de Vroomen MJ, Cornelissen BJC, Takken FLW, Rep M. 2009. The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. Plant J 58:970–978 http://dx.doi.org/10.1111/j.1365-313X.2009.03838.x.
57. Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM, Dekker HL, de Koster CG, Cornelissen BJC. 2004. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol Microbiol 53:1373–1383 http://dx.doi.org/10.1111/j.1365-2958.2004.04177.x.
58. Ma L, Houterman PM, Gawehns F, Cao L, Sillo F, Richter H, Clavijo-Ortiz MJ, Schmidt SM, Boeren S, Vervoort J, Cornelissen BJC, Rep M, Takken FLW. 2015. The AVR2-SIX5 gene pair is required to activate I-2-mediated immunity in tomato. New Phytol 208:507–518 http://dx.doi.org/10.1111/nph.13455.
59. Gawehns F, Houterman PM, Ichou FA, Michielse CB, Hijdra M, Cornelissen BJC, Rep M, Takken FLW. 2014. The Fusarium oxysporum effector Six6 contributes to virulence and suppresses I-2-mediated cell death. Mol Plant Microbe Interact 27:336–348 http://dx.doi.org/10.1094/MPMI-11-13-0330-R.
60. Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, Van der Lee T, Bleeker M, Onstenk J, de Both M, Haring M, Mes J, Cornelissen B, Zabeau M, Vos P. 1998. Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055–1068 http://dx.doi.org/10.1105/tpc.10.6.1055.
61. Catanzariti AM, Lim GTT, Jones DA. 2015. The tomato I-3 gene: a novel gene for resistance to Fusarium wilt disease. New Phytol 207:106–118 http://dx.doi.org/10.1111/nph.13348.
62. Gonzalez-Cendales Y, Catanzariti AM, Baker B, Mcgrath DJ, Jones DA. 2016. Identification of I-7 expands the repertoire of genes for resistance to Fusarium wilt in tomato to three resistance gene classes. Mol Plant Pathol 17:448–463 http://dx.doi.org/10.1111/mpp.12294.
63. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma BP. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109:5110–5115 http://dx.doi.org/10.1073/pnas.1119623109.
64. Adhikari TB, Mamidi S, Gurung S, Bonman JM. 2015. Mapping of new quantitative trait loci (QTL) for resistance to Septoria tritici blotch in spring wheat ( Triticum aestivum L.). Euphytica 205:699–706 http://dx.doi.org/10.1007/s10681-015-1393-4.
65. Wolpert TJ, Dunkle LD, Ciuffetti LM. 2002. Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285 http://dx.doi.org/10.1146/annurev.phyto.40.011402.114210.
66. Vincent D, Du Fall LA, Livk A, Mathesius U, Lipscombe RJ, OliverRP, Friesen TL, Solomon PS. 2012. A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat. Mol Plant Pathol 13:467–482 http://dx.doi.org/10.1111/j.1364-3703.2011.00763.x.
67. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, Tzeng SC, Maier CS, Wolpert TJ. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659–662 http://dx.doi.org/10.1126/science.1226743.
68. Krupinsky JM, Tanaka DL. 2001. Leaf spot diseases on winter wheat influenced by nitrogen, tillage, and haying after a grass-alfalfa mixture inthe Conservation Reserve Program. Plant Dis 85:785–789 http://dx.doi.org/10.1094/PDIS.2001.85.7.785.
69. Brooks P, Fuertes G, Murray RZ, Bose S, Knecht E, Rechsteiner MC, Hendil KB, Tanaka K, Dyson J, Rivett J. 2000. Subcellular localization of proteasomes and their regulatory complexes in mammalian cells. Biochem J 346:155–161 http://dx.doi.org/10.1042/bj3460155.
70. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H. 2013. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–66 http://dx.doi.org/10.1111/j.1574-6976.2012.00350.x.
71. Akagi Y, Akamatsu H, Otani H, Kodama M. 2009. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738 http://dx.doi.org/10.1128/EC.00135-09.
72. Lorang JM, Carkaci-Salli N, Wolpert TJ. 2004. Identification and characterization of victorin sensitivity in Arabidopsis thaliana. Mol Plant Microbe Interact 17:577–582 http://dx.doi.org/10.1094/MPMI.2004.17.6.577.
73. Lorang JM, Sweat TA, Wolpert TJ. 2007. Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci USA 104:14861–14866 http://dx.doi.org/10.1073/pnas.0702572104.
74. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, Tzeng S-C, Maier CS, Wolpert TJ. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659–662 http://dx.doi.org/10.1126/science.1226743.
75. Carapito R, Hatsch D, Vorwerk S, Petkovski E, Jeltsch JM, Phalip V. 2008. Gene expression in Fusarium graminearum grown on plant cell wall. Fungal Genet Biol 45:738–748 http://dx.doi.org/10.1016/j.fgb.2007.12.002.
76. Braun CJ, Siedow JN, Levings CS III. 1990. Fungal toxins bind to the URF13 protein in maize mitochondria and Escherichia coli. Plant Cell 2:153–161 http://dx.doi.org/10.1105/tpc.2.2.153.
77. Levings CS III, Rhoads DM, Siedow JN. 1995. Molecular interactions of Bipolaris maydis T-toxin and maize. Can J Bot 73(S1) :483–489 http://dx.doi.org/10.1139/b95-286.
78. Anderson JP, Lichtenzveig J, Gleason C, Oliver RP, Singh KB. 2010. The B-3 ethylene response factor MtERF1-1 mediates resistance to a subset of root pathogens in Medicago truncatula without adversely affecting symbiosis with rhizobia. Plant Physiol 154:861–873 http://dx.doi.org/10.1104/pp.110.163949.
79. Friesen TL, Faris JD, Lai Z, Steffenson BJ. 2006. Identification and chromosomal location of major genes for resistance to Pyrenophora teres in a doubled-haploid barley population. Genome 49:855–859 http://dx.doi.org/10.1139/G06-024.
80. Cervera MI, Portolés T, Pitarch E, Beltrán J, Hernández F. 2012. Application of gas chromatography time-of-flight mass spectrometry for target and non-target analysis of pesticide residues in fruits and vegetables. J Chromatogr A 1244:168–177 http://dx.doi.org/10.1016/j.chroma.2012.04.063.
81. Chu C-G, Faris JD, Xu SS, Friesen TL. 2010. Genetic analysis of disease susceptibility contributed by the compatible Tsn1-SnToxA and Snn1-SnTox1 interactions in the wheat- Stagonospora nodorum pathosystem. Theor Appl Genet 120:1451–1459 http://dx.doi.org/10.1007/s00122-010-1267-z.
82. Manning VA, Hardison LK, Ciuffetti LM. 2007. Ptr ToxA interacts with a chloroplast-localized protein. Mol Plant Microbe Interact 20:168–177 http://dx.doi.org/10.1094/MPMI-20-2-0168.
83. Sarma GN, Manning VA, Ciuffetti LM, Karplus PA. 2005. Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell 17:3190–3202 http://dx.doi.org/10.1105/tpc.105.034918. [CrossRef]
84. Manning VA, Hamilton SM, Karplus PA, Ciuffetti LM. 2008. The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization. Mol Plant Microbe Interact 21:315–325 http://dx.doi.org/10.1094/MPMI-21-3-0315.
85. Amogan HP, Martinez JP, Ciuffetti LM, Field KG, Reno PW. 2006. Karyotype and genome size of Nadelspora canceri determined by pulsed field gel electrophoresis. Acta Protozool 45:249–254.
86. Girard V, Dieryckx C, Job C, Job D. 2013. Secretomes: the fungal strike force. Proteomics 13:597–608 http://dx.doi.org/10.1002/pmic.201200282. [CrossRef]
87. Aboukhaddour R, Cloutier S, Ballance GM, Lamari L. 2009. Genome characterization of Pyrenophora tritici-repentis isolates reveals high plasticity and independent chromosomal location of ToxA and ToxB. Mol Plant Pathol 10:201–212 http://dx.doi.org/10.1111/j.1364-3703.2008.00520.x.
88. Abu Qamar M, Liu ZH, Faris JD, Chao S, Edwards MC, Lai Z, Franckowiak JD, Friesen TL. 2008. A region of barley chromosome 6H harbors multiple major genes associated with net type net blotch resistance. Theor Appl Genet 117:1261–1270 http://dx.doi.org/10.1007/s00122-008-0860-x.
89. Mead O, Thynne E, Winterberg B, Solomon PS. 2013. Characterising the role of GABA and its metabolism in the wheat pathogen Stagonospora nodorum. PLoS One 8:e78368. http://dx.doi.org/10.1371/journal.pone.0078368. [CrossRef]
90. Fudal I, Collemare J, Böhnert HU, Melayah D, Lebrun MH. 2007. Expression of Magnaporthe grisea avirulence gene ACE1 is connected to the initiation of appressorium-mediated penetration. Eukaryot Cell 6:546–554 http://dx.doi.org/10.1128/EC.00330-05.
91. Berger GL, Liu S, Hall MD, Brooks WS, Chao S, Muehlbauer GJ, Baik BK, Steffenson B, Griffey CA. 2012. Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor Appl Genet 126:693–710.
92. Cockram J, Scuderi A, Barber T, Furuki E, Gardner KA, Gosman N, Kowalczyk R, Phan HP, Rose GA, Tan KC, Oliver RP, Mackay IJ. 2015. Fine-mapping the wheat Snn1 locus conferring sensitivity to the Parastagonospora nodorum necrotrophic effector SnTox1 using an eight founder multiparent advanced generation inter-cross population. G3 (Bethesda) 5:2257–2266 http://dx.doi.org/10.1534/g3.115.021584.
93. Schürch S, Linde CC, Knogge W, Jackson LF, McDonald BA. 2004. Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol Plant Microbe Interact 17:1114–1125 http://dx.doi.org/10.1094/MPMI.2004.17.10.1114.
94. Rohe M, Gierlich A, Hermann H, Hahn M, Schmidt B, Rosahl S, Knogge W. 1995. The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J 14:4168–4177.
95. Schouten A, van Baarlen P, van Kan JAL. 2008. Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytol 177:493–505.
96. Staats M, van Baarlen P, Schouten A, van Kan JAL. 2007. Functional analysis of NLP genes from Botrytis elliptica. Mol Plant Pathol 8:209–214 http://dx.doi.org/10.1111/j.1364-3703.2007.00382.x.
97. Staats M, van Baarlen P, Schouten A, van Kan JAL, Bakker FT. 2007. Positive selection in phytotoxic protein-encoding genes of Botrytis species. Fungal Genet Biol 44:52–63 http://dx.doi.org/10.1016/j.fgb.2006.07.003.
98. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123 http://dx.doi.org/10.1126/science.1239705.
99. Weiberg A, Wang M, Bellinger M, Jin HL. 2014. Small RNAs: a new paradigm in plant-microbe interactions. Annu Rev Phytopathol 52:495–516. http://dx.doi.org/10.1146/annurev-phyto-102313-045933
100. Ellwood SR, Syme RA, Moffat CS, Oliver RP. 2012. Evolution of three Pyrenophora cereal pathogens: recent divergence, speciation and evolution of non-coding DNA. Fungal Genet Biol 49:825–829 http://dx.doi.org/10.1016/j.fgb.2012.07.003.
101. Hane JK, Rouxel T, Howlett BJ, Kema GH, Goodwin SB, Oliver RP. 2011. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 12:R45 http://dx.doi.org/10.1186/gb-2011-12-5-r45. [CrossRef]
102. Van de Wouw AP, Cozijnsen AJ, Hane JK, Brunner PC, McDonald BA, Oliver RP, Howlett BJ. 2010. Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6:e1001180. http://dx.doi.org/10.1371/journal.ppat.1001180.
103. Deller S, Hammond-Kosack KE, Rudd JJ. 2011. The complex interactions between host immunity and non-biotrophic fungal pathogens of wheat leaves. J Plant Physiol 168:63–71 http://dx.doi.org/10.1016/j.jplph.2010.05.024.
104. Martinez JP, Oesch NW, Ciuffetti LM. 2004. Characterization of the multiple-copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis. Mol Plant Microbe Interact 17:467–474 http://dx.doi.org/10.1094/MPMI.2004.17.5.467.
105. Inderbitzin P, Asvarak T, Turgeon BG. 2010. Six new genes required for production of T-toxin, a polyketide determinant of high virulence of Cochliobolus heterostrophus to maize. Mol Plant Microbe Interact 23:458–472 http://dx.doi.org/10.1094/MPMI-23-4-0458.
106. Stukenbrock EH, McDonald BA. 2007. Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol Plant Pathol 8:321–332 http://dx.doi.org/10.1111/j.1364-3703.2007.00396.x.
107. Liu ZH, Zhong S, Stasko AK, Edwards MC, Friesen TL. 2012. Virulence profile and genetic structure of a North Dakota population of Pyrenophora teres f. teres, the causal agent of net form net blotch of barley. Phytopathology 102:539–546 http://dx.doi.org/10.1094/PHYTO-09-11-0243.
108. Tan KC, Ferguson-Hunt M, Rybak K, Waters ODC, Stanley WA, Bond CS, Stukenbrock EH, Friesen TL, Faris JD, McDonald BA, Oliver RP. 2012. Quantitative variation in effector activity of ToxA isoforms from Stagonospora nodorum and Pyrenophora tritici-repentis. Mol Plant Microbe Interact 25:515–522 http://dx.doi.org/10.1094/MPMI-10-11-0273.
109. Marcet-Houben M, Gabaldón T. 2010. Acquisition of prokaryotic genes by fungal genomes. Trends Genet 26:5–8 http://dx.doi.org/10.1016/j.tig.2009.11.007.
110. Oliver RP, Solomon PS. 2008. Recent fungal diseases of crop plants: is lateral gene transfer a common theme? Mol Plant Microbe Interact 21:287–293 http://dx.doi.org/10.1094/MPMI-21-3-0287.
111. Perez-Nadales E, Almeida Nogueira MF, Baldin C, Castanheira S, El Ghalid M, Grund E, Lengeler K, Marchegiani E, Mehrotra PV, Moretti M, Naik V, Oses-Ruiz M, Oskarsson T, Schäfer K, Wasserstrom L, Brakhage AA, Gow NAR, Kahmann R, Lebrun MH, Perez-Martin J, Di Pietro A, Talbot NJ, Toquin V, Walther A, Wendland J. 2014. Fungal model systems and the elucidation of pathogenicity determinants. Fungal Genet Biol 70:42–67 http://dx.doi.org/10.1016/j.fgb.2014.06.011.
112. Tan KC, Phan HTT, Rybak K, John E, Chooi YH, Solomon PS, Oliver RP. 2015. Functional redundancy of necrotrophic effectors - consequences for exploitation for breeding. Front Plant Sci 6:501. http://dx.doi.org/10.3389/fpls.2015.00501.
113. Price CL, Parker JE, Warrilow AG, Kelly DE, Kelly SL. 2015. Azole fungicides: understanding resistance mechanisms in agricultural fungal pathogens. Pest Manag Sci 71:1054–1058 http://dx.doi.org/10.1002/ps.4029.
114. Howlett BJ, Lowe RG, Marcroft SJ, van de Wouw AP. 2015. Evolution of virulence in fungal plant pathogens: exploiting fungal genomics to control plant disease. Mycologia 107:441–451 http://dx.doi.org/10.3852/14-317.
115. Hubbard A, Lewis CM, Yoshida K, Ramirez-Gonzalez RH, de Vallavieille-Pope C, Thomas J, Kamoun S, Bayles R, Uauy C, Saunders DG. 2015. Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol 16:23. doi:10.1186/s13059-015-0590-8.
116. Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG. 2004. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16:755–768 http://dx.doi.org/10.1105/tpc.020040.
117. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243–256 http://dx.doi.org/10.1105/tpc.105.035980.
118. Liermann JC, Opatz T, Kolshorn H, Antelo L, Hof C, Anke H. 2009.Omphalotins E-I, five oxidatively modified nematicidal cyclopeptides from Omphalotus olearius. Eur J Org Chem 2009:1256–1262 http://dx.doi.org/10.1002/ejoc.200801068.
119. Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JDG, Brown JKM. 2006. Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18:2402–2414 http://dx.doi.org/10.1105/tpc.106.043307.
120. Zhang WJ, Pedersen C, Kwaaitaal M, Gregersen PL, Mørch SM, Hanisch S, Kristensen A, Fuglsang AT, Collinge DB, Thordal-Christensen H. 2012. Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Mol Plant Pathol 13:1110–1119 http://dx.doi.org/10.1111/j.1364-3703.2012.00820.x.
121. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, Chintha R, Harzen A, Colby T, Kamoun S, van der Hoorn RAL. 2008. Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 20:1169–1183 http://dx.doi.org/10.1105/tpc.107.056325.
122. Ilyas M, Hörger AC, Bozkurt TO, van den Burg HA, Kaschani F, Kaiser M, Belhaj K, Smoker M, Joosten MHAJ, Kamoun S, van der Hoorn RAL. 2015. Functional divergence of two secreted immune proteases of tomato. Curr Biol 25:2300–2306 http://dx.doi.org/10.1016/j.cub.2015.07.030. [CrossRef]
123. van den Burg HA, Spronk CAEM, Boeren S, Kennedy MA, Vissers JPC, Vuister GW, de Wit PJGM, Vervoort J. 2004. Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein-protein interactions: the chitin-binding site of AVR4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J Biol Chem 279:16786–16796 http://dx.doi.org/10.1074/jbc.M312594200.
124. van der Ackerveken AFJM. 1993. Molecular aspects of avirulence and pathogenicity of the tomato pathogen Cladosporium fulvum. PhD thesis. Wageningen University, Wageningen, The Netherlands.
125. Vervoort J, van den Hooven HW, Berg A, Vossen P, Vogelsang R, Joosten MHAJ, de Wit PJGM. 1997. The race-specific elicitor AVR9 of the tomato pathogen Cladosporium fulvum: a cystine knot protein. Sequence-specific 1H NMR assignments, secondary structure and global fold of the protein. FEBS Lett 404:153–158 http://dx.doi.org/10.1016/S0014-5793(97)00117-8.
126. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, Stulemeijer IJE, van den Berg GCM, Borrás-Hidalgo O, Dekker HL, de Koster CG, de Wit PJGM, Joosten MHAJ, Thomma BPHJ. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69:119–136 http://dx.doi.org/10.1111/j.1365-2958.2008.06270.x.
127. de Jonge R, Thomma BPHJ. 2009. Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 17:151–157 http://dx.doi.org/10.1016/j.tim.2009.01.002.
128. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395–398 http://dx.doi.org/10.1038/nature10454.
129. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. 2012. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 8:e1002684. http://dx.doi.org/10.1371/journal.ppat.1002684.
130. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5:e1000290. http://dx.doi.org/10.1371/journal.ppat.1000290.
131. Doehlemann G, Reissmann S, Assmann D, Fleckenstein M, Kahmann R. 2011. Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation. Mol Microbiol 81:751–766 http://dx.doi.org/10.1111/j.1365-2958.2011.07728.x.
132. Khang CH, Park SY, Lee YH, Valent B, Kang S. 2008. Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol Plant Microbe Interact 21:658–670 http://dx.doi.org/10.1094/MPMI-21-5-0658.
133. Kang S, Sweigard JA, Valent B. 1995. The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 8:939–948 http://dx.doi.org/10.1094/MPMI-8-0939.
134. Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, Valent B. 1995. Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7:1221–1233 http://dx.doi.org/10.1105/tpc.7.8.1221.
135. Böhnert HU, Fudal I, Dioh W, Tharreau D, Notteghem JL, Lebrun MH. 2004. A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell 16:2499–2513 http://dx.doi.org/10.1105/tpc.104.022715.
136. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BPHJ, Talbot NJ. 2012. Effector-mediated suppression of chitin-triggered immunity by magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322–335 http://dx.doi.org/10.1105/tpc.111.092957.
137. Houterman PM, Speijer D, Dekker HL, DE Koster CG, Cornelissen BJC, Rep M. 2007. The mixed xylem sap proteome of Fusarium oxysporum-infected tomato plants. Mol Plant Pathol 8:215–221 http://dx.doi.org/10.1111/j.1364-3703.2007.00384.x.
138. Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP. 2010. Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187:911–919 http://dx.doi.org/10.1111/j.1469-8137.2010.03362.x.
139. Figueroa M, Manning VA, Pandelova I, Ciuffetti LM. 2015. Persistence of the host-selective toxin Ptr ToxB in the apoplast. Mol Plant Microbe Interact 28:1082–1090 http://dx.doi.org/10.1094/MPMI-05-15-0097-R.
140. Ciuffetti LM, Tuori RP, Gaventa JM. 1997. A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9:135–144 http://dx.doi.org/10.1105/tpc.9.2.135.
141. Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci USA 107:13544–13549 http://dx.doi.org/10.1073/pnas.1004090107.
142. Oome S, Van den Ackerveken G. 2014. Comparative and functional analysis of the widely occurring family of Nep1-like proteins. Mol Plant Microbe Interact 27:1081–1094 http://dx.doi.org/10.1094/MPMI-04-14-0118-R.
143. Weiberg A, Wang M, Bellinger M, Jin HL. 2014. Small RNAs: a new paradigm in plant-microbe interactions. Annu Rev Phytopathol 52:495–516. http://dx.doi.org/10.1146/annurev-phyto-102313-045933
144. Baker SE, Kroken S, Inderbitzin P, Asvarak T, Li BY, Shi L, Yoder OC, Turgeon BG. 2006. Two polyketide synthase-encoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol Plant Microbe Interact 19:139–149 http://dx.doi.org/10.1094/MPMI-19-0139.
145. Walton JD. 2006. HC-toxin. Phytochemistry 67:1406–1413 http://dx.doi.org/10.1016/j.phytochem.2006.05.033.
146. Wolpert TJ, Lorang JM. 2016. Victoria blight, defense turned upside down. Physiol Mol Plant Pathol 95:8–13 http://dx.doi.org/10.1016/j.pmpp.2016.03.006.
147. de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA, Aerts AL, Bahkali AH, Beenen HG, Chettri P, Cox MP, Datema E, de Vries RP, Dhillon B, Ganley AR, Griffiths SA, Guo Y, Hamelin RC, Henrissat B, Kabir MS, Jashni MK, Kema G, Klaubauf S, Lapidus A, Levasseur A, Lindquist E, Mehrabi R, Ohm RA, Owen TJ, Salamov A, Schwelm A, Schijlen E, Sun H, van den Burg HA, van Ham RC, Zhang S, Goodwin SB, Grigoriev IV, Collemare J, Bradshaw RE. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet 8:e1003088. (Erratum, doi:info:doi/10.1371/journal.pgen.1005775.) http://dx.doi.org/10.1371/journal.pgen.1003088.

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The interactions between fungi and plants encompass a spectrum of ecologies ranging from saprotrophy (growth on dead plant material) through pathogenesis (growth of the fungus accompanied by disease on the plant) to symbiosis (growth of the fungus with growth enhancement of the plant). We consider pathogenesis in this article and the key roles played by a range of pathogen-encoded molecules that have collectively become known as effectors.

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Typical penetration, feeding, and reproductive structures associated with three contrasting fungal pathogens. Barley powdery mildew, f.sp. (courtesy C. Ge). Epiphytic hyphae penetrating through the epidermis and the finger-like haustoria in the epidermal cell. Conidiophores bearing abundant conidia. Wheat septoria nodorum blotch, (courtesy K. Rybak). Epiphytic hyphae penetrating via hyphopodia (arrows) or through stomata. A green fluorescent protein-expressing strain under epifluorescence. The arrow shows a pycnidium containing abundant pycnidia. Tomato leaf mold, (Courtesy JC and PdW). Penetration of a stoma by adventitious (runner) hyphae. Growth of hyphae around tomato mesophyll cells. Conidiophores bearing abundant conidia on the underside of an otherwise healthy tomato leaflet.

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0021-2016
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Interactions of fungal effectors with targets in plant host cells in biotrophic, hemibiotrophic, and necrotrophic diseases. The fungal cell interacts with the host cell via the yellow space, which represents either the extrahaustorial, matrix surrounding the haustorium, or the apoplast. Effectors from a range of fungi are presented in yellow, and their plant targets in green. Additional information is provided in Table 1 . Adapted from reference 6 .

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0021-2016
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Effectors from obligate biotrophic, hemibiotrophic, and necrotrophic fungal pathogens whose intrinsic function, host target, or matching resistance gene is known

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0021-2016

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