Advances and Challenges in Computational Prediction of Effectors from Plant Pathogenic Fungi

1. Garnica DP, Nemri A, Upadhyaya NM, Rathjen JP, Dodds PN (2014) The ins and outs of rust haustoria. PLoS Pathog 10: e1004329. doi: 10.1371/journal.ppat.1004329 25211126

2. Zhang S, Xu JR (2014) Effectors and effector delivery in Magnaporthe oryzae. PLoS Pathog 10: e1003826. doi: 10.1371/journal.ppat.1003826 24391496

3. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, et al. (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69: 119–136. doi: 10.1111/j.1365-2958.2008.06270.x 18452583

4. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, et al. (2011) Metabolic priming by a secreted fungal effector. Nature 478: 395–398. doi: 10.1038/nature10454 21976020

5. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, et al. (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142: 284–295. doi: 10.1016/j.cell.2010.06.008 20655469

6. Godfrey D, Bohlenius H, Pedersen C, Zhang Z, Emmersen J, Thordal-Christensen H. (2010) Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 11: 317. doi: 10.1186/1471-2164-11-317 20487537

7. Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, et al. (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A 108: 9166–9171. doi: 10.1073/pnas.1019315108 21536894

8. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373. doi: 10.1038/nature08850 20237561

9. Sperschneider J, Gardiner DM, Taylor JM, Hane JK, Singh KB, Manners JM. (2013) A comparative hidden Markov model analysis pipeline identifies proteins characteristic of cereal-infecting fungi. BMC Genomics 14: 807. doi: 10.1186/1471-2164-14-807 24252298

10. 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. doi: 10.1094/MPMI-21-3-0315 18257681

11. Rafiqi M, Gan PH, Ravensdale M, Lawrence GJ, Ellis JG, Jones D, et al. (2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22: 2017–2032. doi: 10.1105/tpc.109.072983 20525849

12. Win J, Krasileva KV, Kamoun S, Shirasu K, Staskawicz BJ, Banfield M. (2012) Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathog 8: e1002400. doi: 10.1371/journal.ppat.1002400 22253591

13. Pedersen C, Ver Loren van Themaat E, McGuffin LJ, Abbott JC, Burgis TA, Barton G, et al. (2012) Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13: 694. doi: 10.1186/1471-2164-13-694 23231440

14. Wang CI, Guncar G, Forwood JK, Teh T, Catanzariti AM, Lawrencec G, et al. (2007) Crystal structures of flax rust avirulence proteins AvrL567-A and-D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 19: 2898–2912. 17873095

15. 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. 16214901

16. Zhang ZM, Zhang X, Zhou ZR, Hu HY, Liu M, Zhou B, et al. (2013) Solution structure of the Magnaporthe oryzae avirulence protein AvrPiz-t. J Biomol NMR 55: 219–223. doi: 10.1007/s10858-012-9695-5 23334361

17. Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47: 233–263. doi: 10.1146/annurev.phyto.112408.132637 19400631

18. de Jonge R (2012) In silico identification and characterization of effector catalogs. Methods Mol Biol 835: 415–425. doi: 10.1007/978-1-61779-501-5_25 22183668

19. Hacquard S, Joly DL, Lin YC, Tisserant E, Feau N, Delaruelle C, et al. (2012) A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). Mol Plant Microbe Interact 25: 279–293. doi: 10.1094/MPMI-09-11-0238 22046958

20. Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, et al. (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 60: 67–80. 16556221

21. Saunders DG, Win J, Cano LM, Szabo LJ, Kamoun S, Raffaele S. (2012) Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS One 7: e29847. doi: 10.1371/journal.pone.0029847 22238666

22. Upadhyaya NM, Mago R, Staskawicz BJ, Ayliffe M, Ellis J, Dodds PN. (2013) A Bacterial Type III Secretion Assay for Delivery of Fungal Effector Proteins into Wheat. Mol Plant Microbe Interact.

23. Nemri A, Saunders DG, Anderson C, Upadhyaya NM, Win J, Lawrence GJ, et al. (2014) The genome sequence and effector complement of the flax rust pathogen Melampsora lini. Front Plant Sci 5: 98. doi: 10.3389/fpls.2014.00098 24715894

24. Cantu D, Segovia V, MacLean D, Bayles R, Chen X, Kamoun S, et al. (2013) Genome analyses of the wheat yellow (stripe) rust pathogen Puccinia striiformis f. sp. tritici reveal polymorphic and haustorial expressed secreted proteins as candidate effectors. BMC Genomics 14: 270. doi: 10.1186/1471-2164-14-270 23607900

25. Sperschneider J, Ying H, Dodds PN, Gardiner DM, Upadhyaya NM, Singh KB, et al. (2014) Diversifying selection in the wheat stem rust fungus acts predominantly on pathogen-associated gene families and reveals candidate effectors. Front Plant Sci 5: 372. doi: 10.3389/fpls.2014.00372 25225496

26. Guyon K, Balague C, Roby D, Raffaele S (2014) Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 15: 336. doi: 10.1186/1471-2164-15-336 24886033

27. Syme RA, Hane JK, Friesen TL, Oliver RP (2013) Resequencing and comparative genomics of Stagonospora nodorum: sectional gene absence and effector discovery. G3 (Bethesda) 3: 959–969. doi: 10.1534/g3.112.004994 23589517

28. Rovenich H, Boshoven JC, Thomma BP (2014) Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr Opin Plant Biol 20: 96–103. doi: 10.1016/j.pbi.2014.05.001 24879450

29. Liu T, Song T, Zhang X, Yuan H, Su L, Li W, et al. (2014) Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun 5: 4686. doi: 10.1038/ncomms5686 25156390

30. Sharon A, Shlezinger N (2013) Fungi infecting plants and animals: killers, non-killers, and cell death. PLoS Pathog 9: e1003517. doi: 10.1371/journal.ppat.1003517 24009499

31. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786. doi: 10.1038/nmeth.1701 21959131