Template-Based Modelling of the Structure of Fungal Effector Proteins

Stergiopoulos, I., & de Wit, P. J. G. M. (2009). Fungal effector proteins. Annual Review of Phytopathology, 47(1), 233–263. https://doi.org/10.1146/annurev.phyto.112408.132637 Ballance, G. M., Lamari, L., & Bernier, C. C. (1989). Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici repentis. Physiological and Molecular Plant Pathology, 35(3), 203–213. https://doi.org/10.1016/0885-5765(89)90051-9 Jones, D. A. B., Moolhuijzen, P. M., & Hane, J. K. (2021). Remote homology clustering identifies lowly conserved families of effector proteins in plant-pathogenic fungi. Microbial Genomics, 7(9), 000637. https://doi.org/10.1099/MGEN.0.000637 Kanja, C., & Hammond-Kosack, K. E. (2020). Proteinaceous effector discovery and characterization in filamentous plant pathogens. Molecular Plant Pathology. https://doi.org/10.1111/mpp.12980 Hane, J. K., Rouxel, T., Howlett, B. J., Kema, G. H., Goodwin, S. B., & Oliver, R. P. (2011). A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biology, 12(5), R45. https://doi.org/10.1186/gb-2011-12-5-r45 Testa, A. C., Oliver, R. P., & Hane, J. K. (2016). OcculterCut: A comprehensive survey of at-rich regions in fungal genomes. Genome Biology and Evolution. https://doi.org/10.1093/gbe/evw121 Bertazzoni, S., Williams, A. H., Jones, D. A., Syme, R. A., Tan, K.-C., & Hane, J. K. (2018). Accessories make the outfit: Accessory chromosomes and other dispensable DNA regions in plant-pathogenic fungi. Molecular Plant-Microbe Interactions, 31(8), 779–788. https://doi.org/10.1094/mpmi-06-17-0135-fi Liu, L., Xu, L., Jia, Q., Pan, R., Oelmüller, R., Zhang, W., & Wu, C. (2019). Arms race: Diverse effector proteins with conserved motifs. Plant Signaling and Behavior, 14(2), 1557008. https://doi.org/10.1080/15592324.2018.1557008 Sperschneider, J., & Dodds, P. N. (2022). EffectorP 3.0: Prediction of apoplastic and cytoplasmic effectors in fungi and oomycetes. Molecular Plant-Microbe Interactions, 35(2), 146–156. https://doi.org/10.1094/MPMI-08-21-0201-R Jones, D. A. B., Rozano, L., Debler, J. W., Mancera, R. L., Moolhuijzen, P. M., & Hane, J. K. (2021). An automated and combinative method for the predictive ranking of candidate effector proteins of fungal plant pathogens. Scientific Reports, 11(1), 1–13. https://doi.org/10.1038/s41598-021-99363-0 de Guillen, K., Ortiz-Vallejo, D., Gracy, J., Fournier, E., Kroj, T., & Padilla, A. (2015). Structure analysis uncovers a highly diverse but structurally conserved effector family in phytopathogenic fungi. PLoS Pathogens, 11(10), e1005228. https://doi.org/10.1371/journal.ppat.1005228 Pennington, H. G., Jones, R., Kwon, S., Bonciani, G., Thieron, H., Chandler, T., Luong, P., Morgan, S. N., Przydacz, M., Bozkurt, T., Bowden, S., Craze, M., Wallington, E. J., Garnett, J., Kwaaitaal, M., Panstruga, R., Cota, E., & Spanu, P. D. (2019). The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA. PLoS Pathogens, 15(3), e1007620. https://doi.org/10.1371/journal.ppat.1007620 de Guillen, K., Lorrain, C., Tsan, P., Barthe, P., Petre, B., Saveleva, N., Rouhier, N., Duplessis, S., Padilla, A., & Hecker, A. (2019). Structural genomics applied to the rust fungus Melampsora larici populina reveals two candidate effector proteins adopting cysteine knot and NTF2-like protein folds. Scientific Reports, 9(1), 1–12. https://doi.org/10.1038/s41598-019-53816-9 Outram, M. A., Sung, Y. C., Yu, D., Dagvadorj, B., Rima, S. A., Jones, D. A., Ericsson, D. J., Sperschneider, J., Solomon, P. S., Kobe, B., & Williams, S. J. (2021). The crystal structure of SnTox3 from the necrotrophic fungus Parastagonospora nodorum reveals a unique effector fold and provides insight into Snn3 recognition and pro-domain protease processing of fungal effectors. New Phytologist, 231(6), 2282–2296. https://doi.org/10.1111/nph.17516 Jones, D. A., Bertazzoni, S., Turo, C. J., Syme, R. A., & Hane, J. K. (2018). Bioinformatic prediction of plant–pathogenicity effector proteins of fungi. Current Opinion in Microbiology. https://doi.org/10.1016/j.mib.2018.01.017 Urban, M., Cuzick, A., Seager, J., Wood, V., Rutherford, K., Venkatesh, S. Y., Silva, D. N., Martinez, M. C., Pedro, H., Yates, A. D., Hassani-Pak, K., & Hammond-Kosack, K. E. (2020). PHI-base: The pathogen–host interactions database. Nucleic Acids Research, 48(D1), D613–D620. https://doi.org/10.1093/nar/gkz904 Andreeva, A., Kulesha, E., Gough, J., & Murzin, A. G. (2020). The SCOP database in 2020: Expanded classification of representative family and superfamily domains of known protein structures. Nucleic Acids Research, 48(D1), D376–D382. https://doi.org/10.1093/nar/gkz1064 Varadi, M., Anyango, S., Deshpande, M., Nair, S., Natassia, C., Yordanova, G., Yuan, D., Stroe, O., Wood, G., Laydon, A., Zidek, A., Green, T., Tunyasuvunakool, K., Petersen, S., Jumper, J., Clancy, E., Green, R., Vora, A., Lutfi, M., … Velankar, S. (2022). AlphaFold Protein Structure Database: Massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Research, 50(D1), D439–D444. https://doi.org/10.1093/nar/gkab1061 Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Florian, T. H., de Beer, T. A. P., Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. https://doi.org/10.1093/nar/gky427 Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. E. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10(6), 845–858. https://doi.org/10.1038/nprot.2015.053 Yang, J., & Zhang, Y. (2015). Protein structure and function prediction using I-TASSER. Current Protocols in Bioinformatics. https://doi.org/10.1002/0471250953.bi0508s52 Källberg, M., Wang, H., Wang, S., Peng, J., Wang, Z., Lu, H., & Xu, J. (2012). Template-based protein structure modeling using the RaptorX web server. Nature Protocols, 7(8), 1511–1522. https://doi.org/10.1038/nprot.2012.085 Källberg, M., Margaryan, G., Wang, S., Ma, J., & Xu, J. (2014). RaptorX server: A resource for template-based protein structure modeling (pp. 17–27). Humana Press. https://doi.org/10.1007/978-1-4939-0366-5_2. Hilbert, M., Böhm, G., & Jaenicke, R. (1993). Structural relationships of homologous proteins as a fundamental principle in homology modeling. Proteins: Structure, Function, and Bioinformatics, 17(2), 138–151. https://doi.org/10.1002/PROT.340170204 Seong, K., & Krasileva, K. V. (2021). Computational structural genomics unravels common folds and predicted functions in the secretome of fungal phytopathogen Magnaporthe oryzae. bioRxiv. https://doi.org/10.1101/2021.01.25.427855 Urban, M., Cuzick, A., Rutherford, K., Irvine, A., Pedro, H., Pant, R., Sadanadan, V., Khamari, L., Billal, S., Mohanty, S., & Hammond-Kosack, K. E. (2017). PHI-base: A new interface and further additions for the multi-species pathogen–host interactions database. Nucleic Acids Research, 45(D1), D604–D610. https://doi.org/10.1093/nar/gkw1089 Sperschneider, J., Gardiner, D. M., Dodds, P. N., Tini, F., Covarelli, L., Singh, K. B., Manners, J. M., & Taylor, J. M. (2016). EffectorP: Predicting fungal effector proteins from secretomes using machine learning. New Phytologist, 210(2), 743–761. https://doi.org/10.1111/nph.13794 Sperschneider, J., Dodds, P. N., Gardiner, D. M., Singh, K. B., & Taylor, J. M. (2018). Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Molecular Plant Pathology, 19(9), 2094–2110. https://doi.org/10.1111/mpp.12682 Petersen, T. N., Brunak, S., von Heijne, G., & Nielsen, H. (2011). SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nature Methods, 8(10), 785–786. https://doi.org/10.1038/nmeth.1701 Hall, T. (2011). BioEdit: An important software for molecular biology. GERF Bulletin of Biosciences, 2(1), 60–61. https://www.papers3://publication/uuid/4460861E-549E-43BE-B977-98C413BDC457 Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., Mcgettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947–2948. https://doi.org/10.1093/bioinformatics/btm404 Peng, J., & Xu, J. (2011). RaptorX: Exploiting structure information for protein alignment by statistical inference. Proteins: Structure, Function and Bioinformatics, 79(Suppl. 10), 161–171. https://doi.org/10.1002/prot.23175 Zhang, Y., & Skolnick, J. (2005). TM-align: A protein structure alignment algorithm based on the TM-score. Nucleic Acids Research, 33(7), 2302–2309. https://doi.org/10.1093/nar/gki524 Xu, J., & Zhang, Y. (2010). How significant is a protein structure similarity with TM-score = 0.5? Bioinformatics, 26(7), 889–895. https://doi.org/10.1093/bioinformatics/btq066 Orengo, C., Michie, A., Jones, S., Jones, D., Swindells, M., & Thornton, J. (1997). CATH—A hierarchic classification of protein domain structures. Structure, 5(8), 1093–1109. https://doi.org/10.1016/S0969-2126(97)00260-8 Knudsen, M., & Wiuf, C. (2010). The CATH database. Human Genomics, 4(3), 207–212. https://doi.org/10.1186/1479-7364-4-3-207 Murzin, A. G., Brenner, S. E., Hubbard, T., & Chothia, C. (1995). SCOP: A structural classification of proteins database for the investigation of sequences and structures. Journal of Molecular Biology, 247(4), 536–540. https://doi.org/10.1016/S0022-2836(05)80134-2 Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/s0021889892009944 Praz, C. R., Bourras, S., Zeng, F., Sánchez-Martín, J., Menardo, F., Xue, M., Yang, L., Roffler, S., Boni, R., Herren, G., McNally, K. E., Ben-David, R., Parlange, F., Oberhaensli, S., Fluckiger, S., Schafer, L. K., Wicker, T., Yu, D., & Keller, B. (2017). AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytologist, 213(3), 1301–1314. https://doi.org/10.1111/nph.14372 Bauer, S., Yu, D., Lawson, A. W., Saur, I. M. L., Frantzeskakis, L., Kracher, B., Logemann, E., Chai, J., Maekawa, T., & Schulze-Lefert, P. (2021). The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold. PLoS Pathogens, 17(2), e1009223. https://doi.org/10.1371/JOURNAL.PPAT.1009223 Manser, B., Koller, T., Praz, C. R., Roulin, A. C., Zbinden, H., Arora, S., Steuernagel, B., Wulff, B. B. H., Keller, B., & Sánchez-Martín, J. (2021). Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2. Plant Journal, 106(4), 993–1007. https://doi.org/10.1111/tpj.15214 Sharpee, W., Oh, Y., Yi, M., Franck, W., Eyre, A., Okagaki, L. H., Valent, B., & Dean, R. A. (2017). Identification and characterization of suppressors of plant cell death (SPD) effectors from Magnaporthe oryzae. Molecular Plant Pathology, 18(6), 850–863. https://doi.org/10.1111/mpp.12449 Rawlings, N. D., & Barrett, A. J. (1995). [13] Evolutionary families of metallopeptidases. Methods in Enzymology, 248(C), 183–228. https://doi.org/10.1016/0076-6879(95)48015-3 Sanz-Martín, J. M., Pacheco-Arjona, J. R., Bello-Rico, V., Vargas, W. A., Monod, M., Díaz-Mínguez, J. M., Thon, M. R., & Sukno, S. A. (2016). A highly conserved metalloprotease effector enhances virulence in the maize anthracnose fungus Colletotrichum graminicola. Molecular Plant Pathology, 17(7), 1048–1062. https://doi.org/10.1111/mpp.12347 Brunette, T. J., Parmeggiani, F., Huang, P. S., Bhabha, G., Ekiert, D. C., Tsutakawa, S. E., Hura, G. L., Tainer, J. A., & Baker, D. (2015). Exploring the repeat protein universe through computational protein design. Nature, 528(7583), 580–584. https://doi.org/10.1038/nature16162 Castillo, R. M., Mizuguchi, K., Dhanaraj, V., Albert, A., Blundell, T. L., & Murzin, A. G. (1999). A six-stranded double-psi β barrel is shared by several protein superfamilies. Structure, 7(2), 227–236. https://doi.org/10.1016/S0969-2126(99)80028-8 Bollati, M., Villa, R., Gourlay, L. J., Benedet, M., Dehò, G., Polissi, A., Barbiroli, A., Martorana, A. M., Sperandeo, P., Bolognesi, M., & Nardini, M. (2015). Crystal structure of LptH, the periplasmic component of the lipopolysaccharide transport machinery from Pseudomonas aeruginosa. FEBS Journal, 282(10), 1980–1997. https://doi.org/10.1111/febs.13254 Ge, H., Chen, X., Yang, W., Niu, L., & Teng, M. (2013). Crystal structure of wild-type and mutant human Ap4A hydrolase. Biochemical and Biophysical Research Communications, 432(1), 16–21. https://doi.org/10.1016/J.BBRC.2013.01.095 Li, Y., Han, Y., Qu, M., Chen, J., Chen, X., Geng, X., Wang, Z., & Chen, S. (2020). Apoplastic cell death-inducing proteins of filamentous plant pathogens: Roles in plant–pathogen interactions. Frontiers in Genetics, 11, 661. https://doi.org/10.3389/fgene.2020.00661 Shirke, M. D., Mahesh, H. B., & Gowda, M. (2016). Genome-wide comparison of Magnaporthe species reveals a host-specific pattern of secretory proteins and transposable elements. PLoS ONE, 11(9), e0162458. https://doi.org/10.1371/JOURNAL.PONE.0162458 Kulkarni, R. D., Kelkar, H. S., & Dean, R. A. (2003). An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends in Biochemical Sciences, 28(3), 118–121. https://doi.org/10.1016/S0968-0004(03)00025-2 Nasser, L., Weissman, Z., Pinsky, M., Amartely, H., Dvir, H., & Kornitzer, D. (2016). Structural basis of haem-iron acquisition by fungal pathogens. Nature Microbiology, 1(11), 1–10. https://doi.org/10.1038/nmicrobiol.2016.156 Achari, S. R., Edwards, J., Mann, R. C., Kaur, J. K., Sawbridge, T., & Summerell, B. A. (2021). Comparative transcriptomic analysis of races 1, 2, 5 and 6 of Fusarium oxysporum f. sp. pisi in a susceptible pea host identifies differential pathogenicity profiles. BMC Genomics, 22(1), 1–18. https://doi.org/10.1186/S12864-021-08033-Y Carresi, L., Pantera, B., Zoppi, C., Cappugi, G., Oliveira, A. L., Pertinhez, T. A., Spisni, A., Scala, A., & Pazzagli, L. (2006). Cerato-platanin, a phytotoxic protein from Ceratocystis fimbriata: Expression in Pichia pastoris, purification and characterization. Protein Expression and Purification, 49(2), 159–167. https://doi.org/10.1016/j.pep.2006.07.006 Zhang, P., Li, K., Yang, G., Xia, C., Polston, J. E., Li, G., Li, S., Lin, Z., Yang, L., Bruner, S. D., & Ding, Y. (2017). Cytotoxic protein from the mushroom Coprinus comatus possesses a unique mode for glycan binding and specificity. Proceedings of the National Academy of Sciences of the United States of America, 114(34), 8980–8985. https://doi.org/10.1073/pnas.1706894114 Tanaka, S., Schweizer, G., Rössel, N., Fukada, F., Thines, M., & Kahmann, R. (2018). Neofunctionalization of the secreted Tin2 effector in the fungal pathogen Ustilago maydis. Nature Microbiology, 4(2), 251–257. https://doi.org/10.1038/s41564-018-0304-6 Pao, G. M., & Saier, M. H. (1995). Response regulators of bacterial signal transduction systems: Selective domain shuffling during evolution. Journal of Molecular Evolution, 40(2), 136–154. https://doi.org/10.1007/BF00167109 Wolanin, P. M., Webre, D. J., & Stock, J. B. (2003). Mechanism of phosphatase activity in the chemotaxis response regulator CheY. Biochemistry, 42(47), 14075–14082. https://doi.org/10.1021/bi034883t Mosquera, G., Giraldo, M. C., Khang, C. H., Coughlan, S., & Valent, B. (2009). Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. The Plant Cell, 21(4), 1273–1290. https://doi.org/10.1105/TPC.107.055228 Rozano, L., Mukuka, Y. M., Hane, J. K., & Mancera, R. L. (2023). Ab initio modelling of the structure of ToxA-like and MAX fungal effector proteins. International Journal of Molecular Sciences. Sarma, G. N., Manning, V. A., Ciuffetti, L. M., & Karplus, P. A. (2005). Structure of Ptr ToxA: An RGD-containing host-selective toxin from Pyrenophora tritici repentis. The Plant Cell, 17(11), 3190–3202. https://doi.org/10.1105/TPC.105.034918 Amoozadeh, S., Johnston, J., & Meisrimler, C. N. (2021). Exploiting structural modelling tools to explore host-translocated effector proteins. International Journal of Molecular Sciences, 22(23), 12962. https://doi.org/10.3390/IJMS222312962 Schoonman, M. J. L., Knegtel, R. M. A., & Grootenhuis, P. D. J. (1998). Practical evaluation of comparative modelling and threading methods. Computers and Chemistry, 22(5), 369–375. https://doi.org/10.1016/S0097-8485(98)00006-0