1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Plant Pathogenic Fungi

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Gunther Doehlemann1, Bilal Ökmen2, Wenjun Zhu3, Amir Sharon4
  • Editors: Joseph Heitman5, Barbara J. Howlett6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Botanical Institute and Center of Excellence on Plant Sciences (CEPLAS), University of Cologne, BioCenter, D-50674 Cologne, Germany; 2: Botanical Institute and Center of Excellence on Plant Sciences (CEPLAS), University of Cologne, BioCenter, D-50674 Cologne, Germany; 3: Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, 69978, Israel; 4: Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, 69978, Israel; 5: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 6: School of Biosciences, The University of Melbourne, Victoria, NSW 3010, Australia
  • Source: microbiolspec January 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.FUNK-0023-2016
  • Received 20 July 2016 Accepted 27 July 2016 Published 27 January 2017
  • Gunther Doehlemann, g.doehlemann@uni-koeln.de
image of Plant Pathogenic Fungi
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Plant Pathogenic Fungi, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/1/FUNK-0023-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/1/FUNK-0023-2016-2.gif
  • Abstract:

    Fungi are among the dominant causal agents of plant diseases. To colonize plants and cause disease, pathogenic fungi use diverse strategies. Some fungi kill their hosts and feed on dead material (necrotrophs), while others colonize the living tissue (biotrophs). For successful invasion of plant organs, pathogenic development is tightly regulated and specialized infection structures are formed. To further colonize hosts and establish disease, fungal pathogens deploy a plethora of virulence factors. Depending on the infection strategy, virulence factors perform different functions. While basically all pathogens interfere with primary plant defense, necrotrophs secrete toxins to kill plant tissue. In contrast, biotrophs utilize effector molecules to suppress plant cell death and manipulate plant metabolism in favor of the pathogen. This article provides an overview of plant pathogenic fungal species and the strategies they use to cause disease.

  • Citation: Doehlemann G, Ökmen B, Zhu W, Sharon A. 2017. Plant Pathogenic Fungi. Microbiol Spectrum 5(1):FUNK-0023-2016. doi:10.1128/microbiolspec.FUNK-0023-2016.

Key Concept Ranking

Infection and Immunity
0.4801016
Plant Pathogenic Fungi
0.4726043
Tobacco mosaic virus
0.452535
Fungal Proteins
0.40949246
0.4801016

References

1. Agrios GN. 2005. Plant Pathology, 5th ed. Elsevier Academic Press, London, United Kingdom.
2. Avelino J, Cristancho M, Georgiou S, Imbach P, Aguilar L, Bornemann G, Läderach P, Anzueto F, Hruska AJ, Morales C. 2015. The coffee rust crises in Colombia and Central America (2008–2013): impacts, plausible causes and proposed solutions. Food Secur 7:303–321 http://dx.doi.org/10.1007/s12571-015-0446-9.
3. Callaway E. 2016. Devastating wheat fungus appears in Asia for first time. Nature 532:421–422 http://dx.doi.org/10.1038/532421a. [PubMed]
4. Smith RE. 1900. Botrytis and Sclerotinia: their relation to certain plant diseases and to each other. Bot Gaz 29:369–407 http://dx.doi.org/10.1086/328001.
5. Staats M, van Baarlen P, van Kan JA. 2005. Molecular phylogeny of the plant pathogenic genus Botrytis and the evolution of host specificity. Mol Biol Evol 22:333–346 http://dx.doi.org/10.1093/molbev/msi020. [PubMed]
6. Coley-Smith JR, Verhoeff K, Jarvis WR. 1980. The Biology of Botrytis. Academic Press, London, United Kingdom.
7. Walker AS, Gautier AL, Confais J, Martinho D, Viaud M, Le Pecheur P, Dupont J, Fournier E. 2011. Botrytis pseudocinerea, a new cryptic species causing gray mold in French vineyards in sympatry with Botrytis cinerea. Phytopathology 101:1433–1445 http://dx.doi.org/10.1094/PHYTO-04-11-0104.
8. Choquer M, Fournier E, Kunz C, Levis C, Pradier J-M, Simon A, Viaud M. 2007. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277:1–10 http://dx.doi.org/10.1111/j.1574-6968.2007.00930.x. [PubMed]
9. Leroch M, Plesken C, Weber RW, Kauff F, Scalliet G, Hahn M. 2013. Gray mold populations in German strawberry fields are resistant to multiple fungicides and dominated by a novel clade closely related to Botrytis cinerea. Appl Environ Microbiol 79:159–167 http://dx.doi.org/10.1128/AEM.02655-12.
10. Joosten M, de Wit P. 1999. The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant-pathogen interactions. Annu Rev Phytopathol 37:335–367 http://dx.doi.org/10.1146/annurev.phyto.37.1.335.
11. Thomma BP, van Esse HP, Crous PW, de Wit PJ. 2005. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Mol Plant Pathol 6:379–393 http://dx.doi.org/10.1111/j.1364-3703.2005.00292.x.
12. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955 http://dx.doi.org/10.1126/science.1190859.
13. de Wit PJ, 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, 11:e1005775. doi:10.1371/journal.pgen.1005775.) http://dx.doi.org/10.1371/journal.pgen.1003088.
14. Stergiopoulos I, van den Burg HA, Okmen 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.
15. 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.
16. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BP, 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.
17. Talbot NJ. 2003. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57:177–202 http://dx.doi.org/10.1146/annurev.micro.57.030502.090957. [PubMed]
18. Valent B, Chumley FG. 1991. Molecular genetic analysis of the rice blast fungus, Magnaporthe grisea. Annu Rev Phytopathol 29:443–467 http://dx.doi.org/10.1146/annurev.py.29.090191.002303. [PubMed]
19. Wilson RA, Talbot NJ. 2009. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195 http://dx.doi.org/10.1038/nrmicro2032. [PubMed]
20. Cruz CD, Bockus WW, Stack JP, Tang X, Valent B, Pedley KF, Peterson GL. 2012. Preliminary assessment of resistance among U.S. wheat cultivars to the Triticum pathotype of Magnaporthe oryzae. Plant Dis 96:1501–1505 http://dx.doi.org/10.1094/PDIS-11-11-0944-RE.
21. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD. 2012. The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430 http://dx.doi.org/10.1111/j.1364-3703.2011.00783.x. [PubMed]
22. Ebbole DJ. 2007. Magnaporthe as a model for understanding host-pathogen interactions. Annu Rev Phytopathol 45:437–456 http://dx.doi.org/10.1146/annurev.phyto.45.062806.094346. [PubMed]
23. de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ. 1997. Glycerol generates turgor in rice blast. Nature 389:244 http://dx.doi.org/10.1038/38418.
24. Dagdas YF, Yoshino K, Dagdas G, Ryder LS, Bielska E, Steinberg G, Talbot NJ. 2012. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science 336:1590–1595 http://dx.doi.org/10.1126/science.1222934. [PubMed]
25. Kankanala P, Czymmek K, Valent B. 2007. Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19:706–724 http://dx.doi.org/10.1105/tpc.106.046300. [PubMed]
26. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park S-Y, Czymmek K, Kang S, Valent B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388–1403 http://dx.doi.org/10.1105/tpc.109.069666.
27. Zhao X, Xu JR. 2007. A highly conserved MAPK-docking site in Mst7 is essential for Pmk1 activation in Magnaporthe grisea. Mol Microbiol 63:881–894 http://dx.doi.org/10.1111/j.1365-2958.2006.05548.x. [PubMed]
28. Dong Y, Li Y, Zhao M, Jing M, Liu X, Liu M, Guo X, Zhang X, Chen Y, Liu Y, Liu Y, Ye W, Zhang H, Wang Y, Zheng X, Wang P, Zhang Z. 2015. Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98-06 uncover novel effectors and pathogenicity-related genes, revealing gene gain and lose dynamics in genome evolution. PLoS Pathog 11:e1004801. http://dx.doi.org/10.1371/journal.ppat.1004801.
29. Sharpee W, Oh Y, Yi M, Franck W, Eyre A, Okagaki L, Valent B, Dean R. 2016. Identification and characterization of suppressors of plant cell death (SPD) genes from Magnaporthe oryzae. Mol Plant Pathol. [Epub ahead of print.] http://dx.doi.org/10.1111/mpp.12449. [PubMed]
30. 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.
31. Wang Y, Wu J, Kim SG, Tsuda K, Gupta R, Park SY, Kim ST, Kang KY. 2016. Magnaporthe oryzae-secreted protein MSP1 induces cell death and elicits defense responses in rice. Mol Plant Microbe Interact 29:299–312 http://dx.doi.org/10.1094/MPMI-12-15-0266-R.
32. Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R. 2009. Ustilago maydis as a pathogen. Annu Rev Phytopathol 47:423–445 http://dx.doi.org/10.1146/annurev-phyto-080508-081923. [PubMed]
33. Kämper J, et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101 http://dx.doi.org/10.1038/nature05248. [PubMed]
34. Doehlemann G, Wahl R, Vranes M, de Vries RP, Kämper J, Kahmann R. 2008. Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol 165:29–40 http://dx.doi.org/10.1016/j.jplph.2007.05.016. [PubMed][CrossRef]
35. 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 http://dx.doi.org/10.1146/annurev-arplant-043014-114623. [PubMed]
36. Cohen L, Eyal Z. 1993. The histology of processes associated with the infection of resistant and susceptible wheat cultivars with Septoria tritici. Plant Pathol 42:737–743 http://dx.doi.org/10.1111/j.1365-3059.1993.tb01560.x.
37. Duncan KE, Howard RJ. 2000. Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycol Res 104:1074–1082 http://dx.doi.org/10.1017/S0953756299002294.
38. Kema GHJ, Yu DZ, Rijkenberg FHJ, Shaw MW, Baayen RP. 1996. Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86:777–786 http://dx.doi.org/10.1094/Phyto-86-777.
39. Quaedvlieg W, Kema GHJ, Groenewald JZ, Verkley GJM, Seifbarghi S, Razavi M, Mirzadi Gohari A, Mehrabi R, Crous PW. 2011. Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26:57–69 http://dx.doi.org/10.3767/003158511X571841. [PubMed]
40. Suffert F, Sache I, Lannou C. 2011. Early stages of Septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and release of primary inoculum. Plant Pathol 60:166–177 http://dx.doi.org/10.1111/j.1365-3059.2010.02369.x.
41. Cools HJ, Fraaije BA. 2008. Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Manag Sci 64:681–684 http://dx.doi.org/10.1002/ps.1568.
42. Fraaije BA, Cools HJ, Fountaine J, Lovell DJ, Motteram J, West JS, Lucas JA. 2005. Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology 95:933–941 http://dx.doi.org/10.1094/PHYTO-95-0933.
43. Choi Y-E, Goodwin SB. 2011. Gene encoding a c-type cyclin in Mycosphaerella graminicola is involved in aerial mycelium formation, filamentous growth, hyphal swelling, melanin biosynthesis, stress response, and pathogenicity. Mol Plant Microbe Interact 24:469–477 http://dx.doi.org/10.1094/MPMI-04-10-0090.
44. Mehrabi R, Van der Lee T, Waalwijk C, Kema GHJ. 2006. MgSlt2, a cellular integrity MAP kinase gene of the fungal wheat pathogen Mycosphaerella graminicola, is dispensable for penetration but essential for invasive growth. Mol Plant Microbe Interact 19:389–398 http://dx.doi.org/10.1094/MPMI-19-0389.
45. Mehrabi R, Zwiers L-H, de Waard MA, Kema GHJ. 2006. MgHog1 regulates dimorphism and pathogenicity in the fungal wheat pathogen Mycosphaerella graminicola. Mol Plant Microbe Interact 19:1262–1269 http://dx.doi.org/10.1094/MPMI-19-1262.
46. Hamer JE, Howard RJ, Chumley FG, Valent B. 1988. A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239:288–290 http://dx.doi.org/10.1126/science.239.4837.288. [PubMed]
47. DeZwaan TM, Carroll AM, Valent B, Sweigard JA. 1999. Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11:2013–2030 http://dx.doi.org/10.1105/tpc.11.10.2013.
48. Kleemann J, Rincon-Rivera LJ, Takahara H, Neumann U, Ver Loren van Themaat E, van der Does HC, Hacquard S, Stüber K, Will I, Schmalenbach W, Schmelzer E, O’Connell RJ. 2012. Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog 8:e1002643. http://dx.doi.org/10.1371/journal.ppat.1002643.
49. Howard RJ, Valent B. 1996. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu Rev Microbiol 50:491–512 http://dx.doi.org/10.1146/annurev.micro.50.1.491. [PubMed]
50. Howard RJ, Ferrari MA, Roach DH, Money NP. 1991. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci USA 88:11281–11284 http://dx.doi.org/10.1073/pnas.88.24.11281. [PubMed]
51. Saunders DGO, Aves SJ, Talbot NJ. 2010. Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22:497–507 http://dx.doi.org/10.1105/tpc.109.072447. [PubMed]
52. Gupta YK, Dagdas YF, Martinez-Rocha A-L, Kershaw MJ, Littlejohn GR, Ryder LS, Sklenar J, Menke F, Talbot NJ. 2015. Septin-dependent assembly of the exocyst is essential for plant infection by Magnaporthe oryzae. Plant Cell 27:3277–3289 http://dx.doi.org/10.1105/tpc.15.00552.
53. Gourgues M, Brunet-Simon A, Lebrun MH, Levis C. 2004. The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol 51:619–629 http://dx.doi.org/10.1046/j.1365-2958.2003.03866.x.
54. Schirawski J, Böhnert HU, Steinberg G, Snetselaar K, Adamikowa L, Kahmann R. 2005. Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17:3532–3543 http://dx.doi.org/10.1105/tpc.105.036285. [PubMed]
55. Mendoza-Mendoza A, Berndt P, Djamei A, Weise C, Linne U, Marahiel M, Vraneš M, Kämper J, Kahmann R. 2009. Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol Microbiol 71:895–911 http://dx.doi.org/10.1111/j.1365-2958.2008.06567.x.
56. Maheshwari R, Hildebrandt AC. 1967. Directional growth of the urediospore germ tubes and stomatal penetration. Nature 214:1145–1146 http://dx.doi.org/10.1038/2141145a0.
57. Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED. 1987. Signaling for growth orientation and cell differentiation by surface topography in uromyces. Science 235:1659–1662 http://dx.doi.org/10.1126/science.235.4796.1659. [PubMed]
58. Schulze-Lefert P, Panstruga R. 2003. Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641–667 http://dx.doi.org/10.1146/annurev.phyto.41.061002.083300. [PubMed][CrossRef]
59. Petersen RH. 1974. The rust fungus life cycle. Bot Rev 40:453–513 http://dx.doi.org/10.1007/BF02860021.
60. Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kües U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M, Quesneville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan GA, Henrissat B, Van de Peer Y, Rouzé P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA 108:9166–9171 http://dx.doi.org/10.1073/pnas.1019315108.
61. Spanu PD, et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546 http://dx.doi.org/10.1126/science.1194573. [PubMed]
62. Hückelhoven R, Panstruga R. 2011. Cell biology of the plant-powdery mildew interaction. Curr Opin Plant Biol 14:738–746 http://dx.doi.org/10.1016/j.pbi.2011.08.002. [PubMed]
63. Heath MC, Skalamera D. 1997. Cellular interactions between plants and biotrophic fungal parasites, 195–225. In Andrews PR, Tommerup IC (ed), Advances in Botanical Research, vol. 24. Academic Press, San Diego, CA.
64. Struck C. 2015. Amino acid uptake in rust fungi. Front Plant Sci 6:40 http://dx.doi.org/10.3389/fpls.2015.00040. [PubMed]
65. Voegele RT, Mendgen KW. 2011. Nutrient uptake in rust fungi: how sweet is parasitic life? Euphytica 179:41–55 http://dx.doi.org/10.1007/s10681-011-0358-5.
66. 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. [PubMed]
67. Petre B, Kamoun S. 2014. How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biol 12:e1001801. http://dx.doi.org/10.1371/journal.pbio.1001801. [PubMed]
68. Kemen E, Kemen A, Ehlers A, Voegele R, Mendgen K. 2013. A novel structural effector from rust fungi is capable of fibril formation. Plant J 75:767–780 http://dx.doi.org/10.1111/tpj.12237. [PubMed]
69. Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, Hahn M, Voegele RT. 2005. Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microbe Interact 18:1130–1139 http://dx.doi.org/10.1094/MPMI-18-1130. [PubMed]
70. Petre B, Lorrain C, Saunders DG, Win J, Sklenar J, Duplessis S, Kamoun S. 2016. Rust fungal effectors mimic host transit peptides to translocate into chloroplasts. Cell Microbiol 18:453–465 http://dx.doi.org/10.1111/cmi.12530. [PubMed]
71. Wernegreen JJ. 2005. For better or worse: genomic consequences of intracellular mutualism and parasitism. Curr Opin Genet Dev 15:572–583 http://dx.doi.org/10.1016/j.gde.2005.09.013. [PubMed]
72. Links MG, Holub E, Jiang RH, Sharpe AG, Hegedus D, Beynon E, Sillito D, Clarke WE, Uzuhashi S, Borhan MH. 2011. De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genomics 12:503. http://dx.doi.org/10.1186/1471-2164-12-503.
73. Kemen E, Jones JDG. 2012. Obligate biotroph parasitism: can we link genomes to lifestyles? Trends Plant Sci 17:448–457 http://dx.doi.org/10.1016/j.tplants.2012.04.005. [PubMed]
74. Fernandez J, Marroquin-Guzman M, Wilson RA. 2014. Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annu Rev Phytopathol 52:155–174 http://dx.doi.org/10.1146/annurev-phyto-102313-050135. [PubMed][CrossRef]
75. Both M, Csukai M, Stumpf MP, Spanu PD. 2005. Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell 17:2107–2122 http://dx.doi.org/10.1105/tpc.105.032631.
76. Spanu PD. 2006. Why do some fungi give up their freedom and become obligate dependants on their host? New Phytol 171:447–450 http://dx.doi.org/10.1111/j.1469-8137.2006.01802.x. [PubMed]
77. Williams PG. 1984. Obligate parasitism and axenic culture, p 399–430. In Bushnell W (ed), The Cereal Rusts. Academic Press, San Diego, CA. [PubMed]
78. Maclean DJ. 1982. Axenic culture of rust fungi, p 37–120. In Scott K (ed), The Rust Fungi. Academic Press, San Diego, CA. [PubMed]
79. Sohn J, Voegele RT, Mendgen K, Hahn M. 2000. High level activation of vitamin B1 biosynthesis genes in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 13:629–636 http://dx.doi.org/10.1094/MPMI.2000.13.6.629. [PubMed]
80. Jakupović M, Heintz M, Reichmann P, Mendgen K, Hahn M. 2006. Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae. Fungal Genet Biol 43:8–19 http://dx.doi.org/10.1016/j.fgb.2005.09.001. [PubMed]
81. Tudzynski P, Scheffer J. 2004. Claviceps purpurea: molecular aspects of a unique pathogenic lifestyle. Mol Plant Pathol 5:377–388 http://dx.doi.org/10.1111/j.1364-3703.2004.00237.x.
82. Tudzynski P, Tenberge KB. 2003. Molecular aspects of host-pathogen interactions and ergot alkaloid biosynthesis in Claviceps, p 414. In White JF Jr, Bacon CW, Hywel-Jones NL, Spatafora JW (eds), Clavicipitalean Fungi. CRC Press, Boca Raton, FL.
83. Oliver RP, Solomon PS. 2010. New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 13:415–419 http://dx.doi.org/10.1016/j.pbi.2010.05.003. [PubMed]
84. Mengiste T. 2012. Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–294 http://dx.doi.org/10.1146/annurev-phyto-081211-172955. [PubMed]
85. 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. [PubMed]
86. 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.
87. Bolton MD, Thomma BP, Nelson BD. 2006. Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7:1–16 http://dx.doi.org/10.1111/j.1364-3703.2005.00316.x.
88. Amselem J, et al. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230. http://dx.doi.org/10.1371/journal.pgen.1002230.
89. Williamson B, Tudzynski B, Tudzynski P, van Kan JA. 2007. Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580 http://dx.doi.org/10.1111/j.1364-3703.2007.00417.x. [PubMed]
90. Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, Talbot NJ, Sharon A. 2011. Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog 7:e1002185. http://dx.doi.org/10.1371/journal.ppat.1002185.
91. Govrin EM, Levine A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757 http://dx.doi.org/10.1016/S0960-9822(00)00560-1.
92. González C, Brito N, Sharon A. 2016. Infection process and fungal virulence factors, p 229–246. In Fillinger S, Elad Y (ed), Botrytis: the Fungus, the Pathogen and its Management in Agricultural Systems. Springer International Publishing, Heidelberg, Germany. http://dx.doi.org/10.1007/978-3-319-23371-0_12
93. Kabbage M, Williams B, Dickman MB. 2013. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathog 9:e1003287. http://dx.doi.org/10.1371/journal.ppat.1003287. [PubMed][CrossRef]
94. Kim KS, Min JY, Dickman MB. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant Microbe Interact 21:605–612 http://dx.doi.org/10.1094/MPMI-21-5-0605.
95. Minina EA, Bozhkov PV, Hofius D. 2014. Autophagy as initiator or executioner of cell death. Trends Plant Sci 19:692–697 http://dx.doi.org/10.1016/j.tplants.2014.07.007. [PubMed]
96. Heller J, Tudzynski P. 2011. Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49:369–390 http://dx.doi.org/10.1146/annurev-phyto-072910-095355. [PubMed]
97. Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB. 2011. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog 7:e1002107. http://dx.doi.org/10.1371/journal.ppat.1002107.
98. Li C, Barker SJ, Gilchrist DG, Lincoln JE, Cowling WA. 2008. Leptosphaeria maculans elicits apoptosis coincident with leaf lesion formation and hyphal advance in Brassica napus. Mol Plant Microbe Interact 21:1143–1153 http://dx.doi.org/10.1094/MPMI-21-9-1143.
99. Cole JS. 1956. Studies in the physiology of parasitism. XX. The pathogenicity of Botrytis cinerea, Sclerotinia fructigena, and Sclerotinia laxa, with special reference to the part played by pectolytic enzymes. Ann Bot (Lond) 20:15–38.
100. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, Paton NW, Rattray M, Hubbard SJ, Oliver SG, Talbot NJ. 2008. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One 3:e2300. http://dx.doi.org/10.1371/journal.pone.0002300.
101. Kim K-T, Jeon J, Choi J, Cheong K, Song H, Choi G, Kang S, Lee Y-H. 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.
102. McCotter SW, Horianopoulos LC, Kronstad JW. 2016. Regulation of the fungal secretome. Curr Genet 62:533–545 http://dx.doi.org/10.1007/s00294-016-0578-2. [PubMed]
103. Yi M, Valent B. 2013. Communication between filamentous pathogens and plants at the biotrophic interface. Annu Rev Phytopathol 51:587–611 http://dx.doi.org/10.1146/annurev-phyto-081211-172916. [PubMed]
104. O’Connell RJ, et al. 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44:1060–1065 http://dx.doi.org/10.1038/ng.2372.
105. Perfect SE, O’Connell RJ, Green EF, Doering-Saad C, Green JR. 1998. Expression cloning of a fungal proline-rich glycoprotein specific to the biotrophic interface formed in the Colletotrichum-bean interaction. Plant J 15:273–279 http://dx.doi.org/10.1046/j.1365-313X.1998.00196.x.
106. Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K. 2013. Fusarium pathogenomics. Annu Rev Microbiol 67:399–416 http://dx.doi.org/10.1146/annurev-micro-092412-155650. [PubMed][CrossRef]
107. Ploetz RC. 2015. Management of Fusarium wilt of banana: a review with special reference to tropical race 4. Crop Prot 73:7–15 http://dx.doi.org/10.1016/j.cropro.2015.01.007.
108. Fradin EF, Thomma BP. 2006. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7:71–86 http://dx.doi.org/10.1111/j.1364-3703.2006.00323.x. [PubMed]
109. Churchill AC. 2011. Mycosphaerella fijiensis, the black leaf streak pathogen of banana: progress towards understanding pathogen biology and detection, disease development, and the challenges of control. Mol Plant Pathol 12:307–328 http://dx.doi.org/10.1111/j.1364-3703.2010.00672.x.
110. Goodwin SB, et al. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7:e1002070. http://dx.doi.org/10.1371/journal.pgen.1002070.
111. Crouch JA, Beirn LA, Cortese LM, Bonos SA, Clarke BB. 2009. Anthracnose disease of switchgrass caused by the novel fungal species Colletotrichum navitas. Mycol Res 113:1411–1421 http://dx.doi.org/10.1016/j.mycres.2009.09.010.
112. Kubo Y, Harata K, Kodama S, Fukada F. 2016. Development of the infection strategy of the hemibiotrophic plant pathogen, Colletotrichum orbiculare, and plant immunity. Physiol Mol Plant Pathol 95:32–36 http://dx.doi.org/10.1016/j.pmpp.2016.02.008.
113. Peres NA. 2005. Peres NA, Timmer W, Adaskaveg JE, Correll JC. 2005. Lifestyles of Colletotrichum acutatum. Plant Dis 89:784–796 http://dx.doi.org/10.1094/PD-89-0784.
114. Weir BS, Johnston PR, Damm U. 2012. The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180 http://dx.doi.org/10.3114/sim0011. [PubMed]
115. Robinson M, Sharon A. 1999. Transformation of the bioherbicide Colletotrichum gloeosporioides f. sp. aeschynomene by electroporation of germinated conidia. Curr Genet 36:98–104 http://dx.doi.org/10.1007/s002940050478. [PubMed]
116. Barhoom S, Sharon A. 2004. cAMP regulation of “pathogenic” and “saprophytic” fungal spore germination. Fungal Genet Biol 41:317–326 http://dx.doi.org/10.1016/j.fgb.2003.11.011. [PubMed]
117. Barhoom S, Kupiec M, Zhao X, Xu JR, Sharon A. 2008. Functional characterization of CgCTR2, a putative vacuole copper transporter that is involved in germination and pathogenicity in Colletotrichum gloeosporioides. Eukaryot Cell 7:1098–1108 http://dx.doi.org/10.1128/EC.00109-07.
118. Nesher I, Minz A, Kokkelink L, Tudzynski P, Sharon A. 2011. Regulation of pathogenic spore germination by CgRac1 in the fungal plant pathogen Colletotrichum gloeosporioides. Eukaryot Cell 10:1122–1130 http://dx.doi.org/10.1128/EC.00321-10.
119. Li G, Zhou X, Xu JR. 2012. Genetic control of infection-related development in Magnaporthe oryzae. Curr Opin Microbiol 15:678–684 http://dx.doi.org/10.1016/j.mib.2012.09.004. [PubMed]
120. Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ. 2012. Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8:e1002514. http://dx.doi.org/10.1371/journal.ppat.1002514. [PubMed]
121. Heath MC, Valent B, Howard RJ, Chumley FG. 1990. Interactions of two strains of Magnaporthe grisea with rice, goosegrass, and weeping lovegrass. Can J Bot 68:1627–1637 http://dx.doi.org/10.1139/b90-209.
122. Zhang S, Xu JR. 2014. Effectors and effector delivery in Magnaporthe oryzae. PLoS Pathog 10:e1003826. http://dx.doi.org/10.1371/journal.ppat.1003826. [PubMed]
123. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B. 2009. Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21:1273–1290 http://dx.doi.org/10.1105/tpc.107.055228.
124. 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.
125. Mims CW, Vaillancourt LJ. 2002. Ultrastructural characterization of infection and colonization of maize leaves by Colletotrichum graminicola, and by a C. graminicola pathogenicity mutant. Phytopathology 92:803–812 http://dx.doi.org/10.1094/PHYTO.2002.92.7.803.
126. Vargas WA, Martín JM, Rech GE, Rivera LP, Benito EP, Díaz-Mínguez JM, Thon MR, Sukno SA. 2012. Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol 158:1342–1358 http://dx.doi.org/10.1104/pp.111.190397.
127. Gan P, Ikeda K, Irieda H, Narusaka M, O’Connell RJ, Narusaka Y, Takano Y, Kubo Y, Shirasu K. 2013. Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol 197:1236–1249 http://dx.doi.org/10.1111/nph.12085.
128. Sharon A, Shlezinger N. 2013. Fungi infecting plants and animals: killers, non-killers, and cell death. PLoS Pathog 9:e1003517. http://dx.doi.org/10.1371/journal.ppat.1003517. [PubMed]
129. Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R. 2001. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 98:6957–6962 http://dx.doi.org/10.1073/pnas.091108998. (Erratum, 100:11816.)
130. Imani J, Baltruschat H, Stein E, Jia G, Vogelsberg J, Kogel KH, Hückelhoven R. 2006. Expression of barley BAX inhibitor-1 in carrots confers resistance to Botrytis cinerea. Mol Plant Pathol 7:279–284 http://dx.doi.org/10.1111/j.1364-3703.2006.00339.x. [PubMed]
131. Eichmann R, Schultheiss H, Kogel KH, Hückelhoven R. 2004. The barley apoptosis suppressor homologue BAX inhibitor-1 compromises nonhost penetration resistance of barley to the inappropriate pathogen Blumeria graminis f. sp. tritici. Mol Plant Microbe Interact 17:484–490 http://dx.doi.org/10.1094/MPMI.2004.17.5.484. [PubMed]
132. Weis C, Hückelhoven R, Eichmann R. 2013. LIFEGUARD proteins support plant colonization by biotrophic powdery mildew fungi. J Exp Bot 64:3855–3867 http://dx.doi.org/10.1093/jxb/ert217. [PubMed]
133. Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (ed). 2002. The Powdery Mildews: A Comprehensive Treatise. APS Press, Saint Paul, MN.
134. Bowyer P, Clarke BR, Lunness P, Daniels MJ, Osbourn AE. 1995. Host range of a plant pathogenic fungus determined by a saponin detoxifying enzyme. Science 267:371–374 http://dx.doi.org/10.1126/science.7824933. [PubMed][CrossRef]
135. Osbourn AE, Clarke BR, Lunness P, Scott PR, Daniels MJ. 1994. An oat species lacking avenacin is susceptible to infection by Gaeumannomyces graminis var. tritici. Physiol Mol Plant Pathol 45:457–467 http://dx.doi.org/10.1016/S0885-5765(05)80042-6.
136. Nicaise V, Roux M, Zipfel C. 2009. Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150:1638–1647 http://dx.doi.org/10.1104/pp.109.139709.
137. Zipfel C. 2014. Plant pattern-recognition receptors. Trends Immunol 35:345–351 http://dx.doi.org/10.1016/j.it.2014.05.004. [PubMed]
138. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323–329 http://dx.doi.org/10.1038/nature05286. [PubMed]
139. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548 http://dx.doi.org/10.1038/nrg2812. [PubMed]
140. Elmore JM, Lin ZJ, Coaker G. 2011. Plant NB-LRR signaling: upstreams and downstreams. Curr Opin Plant Biol 14:365–371 http://dx.doi.org/10.1016/j.pbi.2011.03.011. [PubMed]
141. Bernoux M, Ellis JG, Dodds PN. 2011. New insights in plant immunity signaling activation. Curr Opin Plant Biol 14:512–518 http://dx.doi.org/10.1016/j.pbi.2011.05.005. [PubMed]
142. Howlett BJ. 2006. Secondary metabolite toxins and nutrition of plant pathogenic fungi. Curr Opin Plant Biol 9:371–375 http://dx.doi.org/10.1016/j.pbi.2006.05.004. [PubMed]
143. Deighton N, Muckenschnabel I, Colmenares AJ, Collado IG, Williamson B. 2001. Botrydial is produced in plant tissues infected by Botrytis cinerea. Phytochemistry 57:689–692 http://dx.doi.org/10.1016/S0031-9422(01)00088-7. [PubMed]
144. Colmenares AJAJ, Aleu J, Durán-Patrón R, Collado IG, Hernández-Galán R. 2002. The putative role of botrydial and related metabolites in the infection mechanism of Botrytis cinerea. J Chem Ecol 28:997–1005 http://dx.doi.org/10.1023/A:1015209817830.
145. Rossi FR, Gárriz A, Marina M, Romero FM, Gonzalez ME, Collado IG, Pieckenstain FL. 2011. The sesquiterpene botrydial produced by Botrytis cinerea induces the hypersensitive response on plant tissues and its action is modulated by salicylic acid and jasmonic acid signaling. Mol Plant Microbe Interact 24:888–896 http://dx.doi.org/10.1094/MPMI-10-10-0248.
146. Siewers V, Viaud M, Jimenez-Teja D, Collado IG, Gronover CS, Pradier JM, Tudzynski B, Tudzynski P. 2005. Functional analysis of the cytochrome P450 monooxygenase gene bcbot1 of Botrytis cinerea indicates that botrydial is a strain-specific virulence factor. Mol Plant Microbe Interact 18:602–612 http://dx.doi.org/10.1094/MPMI-18-0602.
147. Dutton MV, Evans CS. 1996. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can J Microbiol 42:881–895 http://dx.doi.org/10.1139/m96-114.
148. Godoy G, Steadman JR, Dickman MB, Dam R. 1990. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol Mol Plant Pathol 37:179–191 http://dx.doi.org/10.1016/0885-5765(90)90010-U.
149. Cessna SG, Sears VE, Dickman MB, Low PS. 2000. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12:2191–2200 http://dx.doi.org/10.1105/tpc.12.11.2191.
150. Stone JM, Heard JE, Asai T, Ausubel FM. 2000. Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12:1811–1822 http://dx.doi.org/10.1105/tpc.12.10.1811. [PubMed]
151. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM. 2000. Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823–1836 http://dx.doi.org/10.1105/tpc.12.10.1823.
152. Glenn AE, Zitomer NC, Zimeri AM, Williams LD, Riley RT, Proctor RH. 2008. Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings. Mol Plant Microbe Interact 21:87–97 http://dx.doi.org/10.1094/MPMI-21-1-0087.
153. Myung K, Zitomer NC, Duvall M, Glenn AE, Riley RT, Calvo AM. 2012. The conserved global regulator VeA is necessary for symptom production and mycotoxin synthesis in maize seedlings by Fusarium verticillioides. Plant Pathol 61:152–160 http://dx.doi.org/10.1111/j.1365-3059.2011.02504.x.
154. McMullen M, Jones R, Gallenberg D. 1997. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 81:1340–1348 http://dx.doi.org/10.1094/PDIS.1997.81.12.1340.
155. Pestka JJ, Smolinski AT. 2005. Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health B Crit Rev 8:39–69 http://dx.doi.org/10.1080/10937400590889458. [PubMed]
156. Bai GHDA, Desjardins AE, Plattner RD. 2002. Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91–98 http://dx.doi.org/10.1023/A:1014419323550.
157. Desjardins AE. 2003. Gibberella from A (venaceae) to Z (eae). Annu Rev Phytopathol 41:177–198 http://dx.doi.org/10.1146/annurev.phyto.41.011703.115501. [PubMed][CrossRef]
158. Proctor RH, Hohn TM, McCormick SP. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8:593–601 http://dx.doi.org/10.1094/MPMI-8-0593. [PubMed]
159. Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, Xu Q, Zheng D, Wang G, Liu H, Gao X, Ma JW, Kistler HC, Kang Z, Xu JR. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog 7:e1002460. http://dx.doi.org/10.1371/journal.ppat.1002460. [PubMed][CrossRef]
160. Schaller A, Oecking C. 1999. Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–272.
161. Hammond-Kosack KE, Rudd JJ. 2008. Plant resistance signalling hijacked by a necrotrophic fungal pathogen. Plant Signal Behav 3:993–995 http://dx.doi.org/10.4161/psb.6292.
162. 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.
163. 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. [PubMed]
164. Nagy ED, Bennetzen JL. 2008. Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res 18:1918–1923 http://dx.doi.org/10.1101/gr.078766.108.
165. Liu Z, Friesen TL, Ling H, Meinhardt SW, Oliver RP, Rasmussen JB, Faris JD. 2006. The Tsn1-ToxA interaction in the wheat-Stagonospora nodorum pathosystem parallels that of the wheat-tan spot system. Genome 49:1265–1273 http://dx.doi.org/10.1139/g06-088.
166. Liu ZH, Faris JD, Meinhardt SW, Ali S, Rasmussen JB, Friesen TL. 2004. Genetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum. Phytopathology 94:1056–1060 http://dx.doi.org/10.1094/PHYTO.2004.94.10.1056.
167. Friesen TL, Meinhardt SW, Faris JD. 2007. The Stagonospora nodorum-wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. Plant J 51:681–692 http://dx.doi.org/10.1111/j.1365-313X.2007.03166.x.
168. Friesen TL, Zhang Z, Solomon PS, Oliver RP, Faris JD. 2008. Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiol 146:682–693 http://dx.doi.org/10.1104/pp.107.108761.
169. Liu Z, Faris JD, Oliver RP, Tan KC, Solomon PS, McDonald MC, McDonald BA, Nunez A, Lu S, Rasmussen JB, Friesen TL. 2009. SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathog 5:e1000581. http://dx.doi.org/10.1371/journal.ppat.1000581.
170. Zhang Z, Friesen TL, Xu SS, Shi G, Liu Z, Rasmussen JB, Faris JD. 2011. Two putatively homoeologous wheat genes mediate recognition of SnTox3 to confer effector-triggered susceptibility to Stagonospora nodorum. Plant J 65:27–38 http://dx.doi.org/10.1111/j.1365-313X.2010.04407.x.
171. Abeysekara NS, Friesen TL, Keller B, Faris JD. 2009. Identification and characterization of a novel host-toxin interaction in the wheat-Stagonospora nodorum pathosystem. Theor Appl Genet 120:117–126 http://dx.doi.org/10.1007/s00122-009-1163-6. [PubMed]
172. Friesen TL, Chu C, Xu SS, Faris JD. 2012. SnTox5-Snn5: a novel Stagonospora nodorum effector-wheat gene interaction and its relationship with the SnToxA-Tsn1 and SnTox3-Snn3-B1 interactions. Mol Plant Pathol 13:1101–1109 http://dx.doi.org/10.1111/j.1364-3703.2012.00819.x.
173. Gao Y, Faris JD, Liu Z, Kim YM, Syme RA, Oliver RP, Xu SS, Friesen TL. 2015. Identification and characterization of the SnTox6-Snn6 interaction in the Parastagonospora nodorum-wheat pathosystem. Mol Plant Microbe Interact 28:615–625 http://dx.doi.org/10.1094/MPMI-12-14-0396-R.
174. Shi GFT, Saini J, Xu SS, Rasmussen JB, Faris JD. 2015. The wheat Snn7 gene confers susceptibility on recognition of the Parastagonospora nodorum necrotrophic effector SnTox7. Plant Genome 8. http://dx.doi.org/10.3835/plantgenome2015.02.0007.
175. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37(Database):D233–D238 http://dx.doi.org/10.1093/nar/gkn663.
176. Cosgrove DJ. 2005. Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861 http://dx.doi.org/10.1038/nrm1746. [PubMed]
177. Hématy K, Cherk C, Somerville S. 2009. Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413 http://dx.doi.org/10.1016/j.pbi.2009.06.007. [PubMed]
178. Kubicek CP, Starr TL, Glass NL. 2014. Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annu Rev Phytopathol 52:427–451 http://dx.doi.org/10.1146/annurev-phyto-102313-045831. [PubMed]
179. Brito N, Espino JJ, González C. 2006. The endo-beta-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol Plant Microbe Interact 19:25–32 http://dx.doi.org/10.1094/MPMI-19-0025. [PubMed]
180. Yakoby N, Beno-Moualem D, Keen NT, Dinoor A, Pines O, Prusky D. 2001. Colletotrichum gloeosporioides pelB is an important virulence factor in avocado fruit-fungus interaction. Mol Plant Microbe Interact 14:988–995 http://dx.doi.org/10.1094/MPMI.2001.14.8.988.
181. Ben-Daniel BH, Bar-Zvi D, Tsror Lahkim L. 2012. Pectate lyase affects pathogenicity in natural isolates of Colletotrichum coccodes and in pelA gene-disrupted and gene-overexpressing mutant lines. Mol Plant Pathol 13:187–197 http://dx.doi.org/10.1111/j.1364-3703.2011.00740.x.
182. Van Vu B, Itoh K, Nguyen QB, Tosa Y, Nakayashiki H. 2012. Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol Plant Microbe Interact 25:1135–1141 http://dx.doi.org/10.1094/MPMI-02-12-0043-R.
183. ten Have A, Mulder W, Visser J, van Kan JA. 1998. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant Microbe Interact 11:1009–1016 http://dx.doi.org/10.1094/MPMI.1998.11.10.1009. [PubMed]
184. Kars I, Krooshof GH, Wagemakers L, Joosten R, Benen JA, van Kan JA. 2005. Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J 43:213–225 http://dx.doi.org/10.1111/j.1365-313X.2005.02436.x.
185. Misas-Villamil JC, van der Hoorn RA. 2008. Enzyme-inhibitor interactions at the plant-pathogen interface. Curr Opin Plant Biol 11:380–388 http://dx.doi.org/10.1016/j.pbi.2008.04.007.
186. Nürnberger T, Brunner F, Kemmerling B, Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266 http://dx.doi.org/10.1111/j.0105-2896.2004.0119.x. [PubMed]
187. Zhang L, Kars I, Essenstam B, Liebrand TW, Wagemakers L, Elberse J, Tagkalaki P, Tjoitang D, van den Ackerveken G, van Kan JA. 2014. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol 164:352–364 http://dx.doi.org/10.1104/pp.113.230698.
188. Poinssot B, Vandelle E, Bentéjac M, Adrian M, Levis C, Brygoo Y, Garin J, Sicilia F, Coutos-Thévenot P, Pugin A. 2003. The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant Microbe Interact 16:553–564 http://dx.doi.org/10.1094/MPMI.2003.16.6.553.
189. Zhang Y, Zhang Y, Qiu D, Zeng H, Guo L, Yang X. 2015. BcGs1, a glycoprotein from Botrytis cinerea, elicits defence response and improves disease resistance in host plants. Biochem Biophys Res Commun 457:627–634 http://dx.doi.org/10.1016/j.bbrc.2015.01.038.
190. Noda J, Brito N, González C. 2010. The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10:38. http://dx.doi.org/10.1186/1471-2229-10-38. [PubMed]
191. Zhang H, Wu Q, Cao S, Zhao T, Chen L, Zhuang P, Zhou X, Gao Z. 2014. A novel protein elicitor (SsCut) from Sclerotinia sclerotiorum induces multiple defense responses in plants. Plant Mol Biol 86:495–511 http://dx.doi.org/10.1007/s11103-014-0244-3.
192. 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.
193. 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. [PubMed]
194. Hemetsberger C, Mueller AN, Matei A, Herrberger C, Hensel G, Kumlehn J, Mishra B, Sharma R, Thines M, Hückelhoven R, Doehlemann G. 2015. The fungal core effector Pep1 is conserved across smuts of dicots and monocots. New Phytol 206:1116–1126 http://dx.doi.org/10.1111/nph.13304. [PubMed]
195. Mueller AN, Ziemann S, Treitschke S, Aßmann D, Doehlemann G. 2013. Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog 9:e1003177. http://dx.doi.org/10.1371/journal.ppat.1003177.
196. 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.
197. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227 http://dx.doi.org/10.1146/annurev.phyto.43.040204.135923. [PubMed]
198. Vlot AC, Dempsey DA, Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206 http://dx.doi.org/10.1146/annurev.phyto.050908.135202. [PubMed]
199. 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. [PubMed]
200. Redkar A, Villajuana-Bonequi M, Doehlemann G. 2015. Conservation of the Ustilago maydis effector See1 in related smuts. Plant Signal Behav 10:e1086855 http://dx.doi.org/10.1080/15592324.2015.1086855. [PubMed]
201. Brefort T, Tanaka S, Neidig N, Doehlemann G, Vincon V, Kahmann R. 2014. Characterization of the largest effector gene cluster of Ustilago maydis. PLoS Pathog 10:e1003866. http://dx.doi.org/10.1371/journal.ppat.1003866. [PubMed][CrossRef]
202. Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J, Vermerris W, Koenig S, Feussner K, Feussner I, Kahmann R. 2014. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3:e01355 http://dx.doi.org/10.7554/eLife.01355.
203. Stergiopoulos I, de Wit PJ. 2009. Fungal effector proteins. Annu Rev Phytopathol 47:233–263 http://dx.doi.org/10.1146/annurev.phyto.112408.132637. [PubMed][CrossRef]
204. Mesarich CH, Griffiths SA, van der Burgt A, Okmen B, Beenen HG, Etalo DW, Joosten MHAJ, de Wit PJGM. 2014. Transcriptome sequencing uncovers the Avr5 avirulence gene of the tomato leaf mold pathogen Cladosporium fulvum. Mol Plant Microbe Interact 27:846–857 http://dx.doi.org/10.1094/MPMI-02-14-0050-R.
205. Rooney HC, Van’t Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ. 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.
206. Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JD. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744–747 http://dx.doi.org/10.1126/science.1069288.
207. Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn RA, 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.
208. Lozano-Torres JL, Wilbers RH, Gawronski P, Boshoven JC, Finkers-Tomczak A, Cordewener JH, America AH, Overmars HA, Van ’t Klooster JW, Baranowski L, Sobczak M, Ilyas M, van der Hoorn RA, 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.
209. 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.
210. Pliego C, Nowara D, Bonciani G, Gheorghe DM, Xu R, Surana P, Whigham E, Nettleton D, Bogdanove AJ, Wise RP, Schweizer P, Bindschedler LV, Spanu PD. 2013. Host-induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors. Mol Plant Microbe Interact 26:633–642 http://dx.doi.org/10.1094/MPMI-01-13-0005-R.
211. Schmitz AM, Harrison MJ. 2014. Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 56:250–261 http://dx.doi.org/10.1111/jipb.12155. [PubMed]
212. Ahmed AA, Pedersen C, Schultz-Larsen T, Kwaaitaal M, Jørgensen HJ, Thordal-Christensen H. 2015. The barley powdery mildew candidate secreted effector protein CSEP0105 inhibits the chaperone activity of a small heat shock protein. Plant Physiol 168:321–333 http://dx.doi.org/10.1104/pp.15.00278.
213. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091 http://dx.doi.org/10.1073/pnas.0508882103.
214. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214 http://dx.doi.org/10.1111/j.1365-313X.2010.04324.x.
215. Fudal I, Böhnert HU, Tharreau D, Lebrun MH. 2005. Transposition of MINE, a composite retrotransposon, in the avirulence gene ACE1 of the rice blast fungus Magnaporthe grisea. Fungal Genet Biol 42:761–772 http://dx.doi.org/10.1016/j.fgb.2005.05.001. [PubMed]
216. Collemare J, Pianfetti M, Houlle AE, Morin D, Camborde L, Gagey MJ, Barbisan C, Fudal I, Lebrun MH, Böhnert HU. 2008. Magnaporthe grisea avirulence gene ACE1 belongs to an infection-specific gene cluster involved in secondary metabolism. New Phytol 179:196–208 http://dx.doi.org/10.1111/j.1469-8137.2008.02459.x.
217. 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.
218. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014 http://dx.doi.org/10.1093/emboj/19.15.4004. [PubMed]
219. Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, Irieda H, Yoshino K, Yoshida K, Matsumura H, Tosa Y, Win J, Kamoun S, Takano Y, Terauchi R. 2012. Large-scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens. PLoS Pathog 8:e1002711. http://dx.doi.org/10.1371/journal.ppat.1002711.
220. 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. [PubMed]
221. 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. [PubMed]
222. Houterman PM, Speijer D, Dekker HL, DE Koster CG, Cornelissen BJ, 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. [PubMed]
223. Schmidt SM, Houterman PM, Schreiver I, Ma L, Amyotte S, Chellappan B, Boeren S, Takken FLW, Rep M. 2013. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum. BMC Genomics 14:119. http://dx.doi.org/10.1186/1471-2164-14-119.
224. 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.
225. 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.
226. Takken F, Rep M. 2010. The arms race between tomato and Fusarium oxysporum. Mol Plant Pathol 11:309–314 http://dx.doi.org/10.1111/j.1364-3703.2009.00605.x. [PubMed]
227. 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. [PubMed]
228. Gawehns F, Houterman PM, Ichou FA, Michielse CB, Hijdra M, Cornelissen BJ, Rep M, Takken FL. 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.
229. Ma L, Houterman PM, Gawehns F, Cao L, Sillo F, Richter H, Clavijo-Ortiz MJ, Schmidt SM, Boeren S, Vervoort J, Cornelissen BJ, Rep M, Takken FL. 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. [PubMed]
230. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G, Wei Y. 2011. EST mining identifies proteins putatively secreted by the anthracnose pathogen Colletotrichum truncatum. BMC Genomics 12:327. http://dx.doi.org/10.1186/1471-2164-12-327.
231. Bhadauria V, MacLachlan R, Pozniak C, Banniza S. 2015. Candidate effectors contribute to race differentiation and virulence of the lentil anthracnose pathogen Colletotrichum lentis. BMC Genomics 16:628. http://dx.doi.org/10.1186/s12864-015-1836-2.
232. Stephenson SA, Hatfield J, Rusu AG, Maclean DJ, Manners JM. 2000. CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol Plant Microbe Interact 13:929–941 http://dx.doi.org/10.1094/MPMI.2000.13.9.929.
233. Yoshino K, Irieda H, Sugimoto F, Yoshioka H, Okuno T, Takano Y. 2012. Cell death of Nicotiana benthamiana is induced by secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a homologue of CgDN3. Mol Plant Microbe Interact 25:625–636 http://dx.doi.org/10.1094/MPMI-12-11-0316.
234. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G, Wei Y. 2013. Overexpression of a novel biotrophy-specific Colletotrichum truncatum effector, CtNUDIX, in hemibiotrophic fungal phytopathogens causes incompatibility with their host plants. Eukaryot Cell 12:2–11 http://dx.doi.org/10.1128/EC.00192-12.
235. Vargas WA, Sanz-Martín JM, Rech GE, Armijos-Jaramillo VD, Rivera LP, Echeverria MM, Díaz-Mínguez JM, Thon MR, Sukno SA. 2016. A fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development. Mol Plant Microbe Interact 29:83–95 http://dx.doi.org/10.1094/MPMI-09-15-0209-R.
236. Sanz-Martín JM, Pacheco-Arjona JR, Bello-Rico V, Vargas WA, Monod M, Díaz-Mínguez JM, Thon MR, Sukno SA. 2015. A highly conserved metalloprotease effector enhances virulence in the maize anthracnose fungus Colletotrichum graminicola. Mol Plant Pathol 17:1048–1062 http://dx.doi.org/10.1111/mpp.12347.
237. Frías M, Brito N, González M, González C. 2014. The phytotoxic activity of the cerato-platanin BcSpl1 resides in a two-peptide motif on the protein surface. Mol Plant Pathol 15:342–351 http://dx.doi.org/10.1111/mpp.12097.
238. Frías M, González C, Brito N. 2011. BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 192:483–495 http://dx.doi.org/10.1111/j.1469-8137.2011.03802.x.
239. Frías M, Brito N, González C. 2013. The Botrytis cinerea cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application. Mol Plant Pathol 14:191–196 http://dx.doi.org/10.1111/j.1364-3703.2012.00842.x.
240. El Oirdi M, El Rahman TA, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K. 2011. Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23:2405–2421 http://dx.doi.org/10.1105/tpc.111.083394.
241. 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. [PubMed]
242. Zhu W, Wei W, Fu Y, Cheng J, Xie J, Li G, Yi X, Kang Z, Dickman MB, Jiang D. 2013. A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS One 8:e53901. http://dx.doi.org/10.1371/journal.pone.0053901.
243. Xiao X, Xie J, Cheng J, Li G, Yi X, Jiang D, Fu Y. 2014. Novel secretory protein Ss-Caf1 of the plant-pathogenic fungus Sclerotinia sclerotiorum is required for host penetration and normal sclerotial development. Mol Plant Microbe Interact 27:40–55 http://dx.doi.org/10.1094/MPMI-05-13-0145-R.
244. Lyu X, Shen C, Fu Y, Xie J, Jiang D, Li G, Cheng J. 2016. A small secreted virulence-related protein is essential for the necrotrophic interactions of Sclerotinia sclerotiorum with its host plants. PLoS Pathog 12:e1005435. http://dx.doi.org/10.1371/journal.ppat.1005435.
245. Zhang W, Fraiture M, Kolb D, Löffelhardt B, Desaki Y, Boutrot FF, Tör M, Zipfel C, Gust AA, Brunner F. 2013. Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25:4227–4241 http://dx.doi.org/10.1105/tpc.113.117010.
246. Lyu X, Shen C, Fu Y, Xie J, Jiang D, Li G, Cheng J. 2015. Comparative genomic and transcriptional analyses of the carbohydrate-active enzymes and secretomes of phytopathogenic fungi reveal their significant roles during infection and development. Sci Rep 5:15565 http://dx.doi.org/10.1038/srep15565.
247. Dallal Bashi Z, Hegedus DD, Buchwaldt L, Rimmer SR, Borhan MH. 2010. Expression and regulation of Sclerotinia sclerotiorum necrosis and ethylene-inducing peptides (NEPs). Mol Plant Pathol 11:43–53 http://dx.doi.org/10.1111/j.1364-3703.2009.00571.x.
248. Saunders DGO, Aves SJ, Talbot NJ. 2010. Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22:497–507. [PubMed]
249. de Wit PJGM, Testa AC, Oliver RP. 2016. Fungal plant pathogenesis mediated by effectors. Microbiol Spectrum 4(6):FUNK-0021-2016. http://dx.doi.org/10.1128/microbiolspec.FUNK-0021-2016. [PubMed]
microbiolspec.FUNK-0023-2016.citations
cm/5/1
content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0023-2016
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0023-2016
2017-01-27
2017-08-18

Abstract:

Fungi are among the dominant causal agents of plant diseases. To colonize plants and cause disease, pathogenic fungi use diverse strategies. Some fungi kill their hosts and feed on dead material (necrotrophs), while others colonize the living tissue (biotrophs). For successful invasion of plant organs, pathogenic development is tightly regulated and specialized infection structures are formed. To further colonize hosts and establish disease, fungal pathogens deploy a plethora of virulence factors. Depending on the infection strategy, virulence factors perform different functions. While basically all pathogens interfere with primary plant defense, necrotrophs secrete toxins to kill plant tissue. In contrast, biotrophs utilize effector molecules to suppress plant cell death and manipulate plant metabolism in favor of the pathogen. This article provides an overview of plant pathogenic fungal species and the strategies they use to cause disease.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error