Comparative Genomic Analysis of Plant Pathogenic Colletotrichum Fungi

Akcapinar, G.B., Kappel, L., Sezerman, O.U., Seidl-Seiboth, V., 2015. Molecular diversity of LysM carbohydrate-binding motifs in fungi. Curr. Genet. 61, 103–113.

Asai, S., Shirasu, K., 2015. Plant cells under siege: plant immune system versus pathogen effectors. Curr. Opin. Plant Biol. 28, 1–8.

Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., Schulze-Lefert, P., 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073–2076.

Bailly-Bechet, M., Haudry, A., Lerat, E., 2014. “One code to find them all”: a perl tool to conveniently parse RepeatMasker output files. Mob. DNA 5, 13.

Bao, J., Chen, M., Zhong, Z., Tang, W., Lin, L., Zhang, X., Jiang, H., Zhang, D., Miao, C., Tang, H., Zhang, J., Lu, G., Ming, R., Norvienyeku, J., Wang, B., Wang, Z., 2017. PacBio sequencing reveals transposable elements as a key contributor to genomic plasticity and virulence variation in Magnaporthe oryzae. Mol. Plant 10, 1465–1468.

Bao, W., Kojima, K.K., Kohany, O., 2015. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob. DNA 6, 11.

Bao, Z., Eddy, S.R., 2002. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 12, 1269–76.

Baroncelli, R., Amby, D.B., Zapparata, A., Sarrocco, S., Vannacci, G., Le Floch, G., Harrison, R.J., Holub, E., Sukno, S.A., Sreenivasaprasad, S., Thon, M.R., 2016. Gene family expansions and contractions are associated with host range in plant pathogens of the genus Colletotrichum. BMC Genomics 17, 555.

Baroncelli, R., Sreenivasaprasad, S., Sukno, S.A., Thon, M.R., Holub, E., 2014. Draft genome sequence of Colletotrichum acutatum Sensu Lato (Colletotrichum fioriniae). Genome Announc. 2, e00112-14.

Bendtsen, J.D., Nielsen, H., von Heijne, G., Brunak, S., 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783–95.

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.

Birker, D., Heidrich, K., Takahara, H., Narusaka, M., Deslandes, L., Narusaka, Y., Reymond, M., Parker, J.E., O’Connell, R., 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 60, 602–613.

Cannon, P.F., Damm, U., Johnston, P.R., Weir, B.S., 2012. Colletotrichum - current status and future directions. Stud. Mycol. 73, 181–213.

Capella-Gutiérrez, S., Silla-Martínez, J.M., Gabaldón, T., 2009. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973.

Castanera, R., López-Varas, L., Borgognone, A., LaButti, K., Lapidus, A., Schmutz, J., Grimwood, J., Pérez, G., Pisabarro, A.G., Grigoriev, I. V., Stajich, J.E., Ramírez, L., 2016. Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLoS Genet. 12, 1–27.

Chaverri, P., Salgado, C., Hirooka, Y., Rossman, A.Y., Samuels, G.J., 2011. Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon-like anamorphs. Stud. Mycol. 68, 57–78.

Chin, C.-S., Alexander, D.H., Marks, P., Klammer, A.A., Drake, J., Heiner, C., Clum, A., Copeland, A., Huddleston, J., Eichler, E.E., Turner, S.W., Korlach, J., 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569.

Chisholm, S.T., Coaker, G., Day, B., Staskawicz, B.J., 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.

Chuma, I., Isobe, C., Hotta, Y., Ibaragi, K., Futamata, N., Kusaba, M., Yoshida, K., Terauchi, R., Fujita, Y., Nakayashiki, H., Valent, B., Tosa, Y., 2011. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog. 7, e1002147.

Chuma, I., Tosa, Y., Taga, M., Nakayashiki, H., Mayama, S., 2003. Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae. Curr. Genet. 43, 191–198.

Croll, D., McDonald, B.A., 2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog. 8, e1002608.

Croll, D., Zala, M., McDonald, B.A., 2013. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet. 9, e1003567.

Crouch, J., Beirn, L.A., 2009. Anthracnose of cereals and grasses. Fungal Divers. 2006, 19–44.

Crouch, J., O’Connell, R., Gan, P., Buiate, E., Torres, M.F., Beirn, L., Shirasu, K., Vaillancourt, L., 2014. The genomics of Colletotrichum. in: Dean, RA., Lichens-Park, A., Kole, C. (Eds), Genomics of Plant-Associated Fungi: Monocot Pathogens. Springer, Berlin Heidelberg, pp. 69–102.

Damm, U., O’Connell, R.J., Groenewald, J.Z., Crous, P.W., 2014. The Colletotrichum destructivum species complex - hemibiotrophic pathogens of forage and field crops. Stud. Mycol. 79, 49–84.

De Jonge, R., Bolton, M.D., Kombrink, A., Van Den Berg, G.C.M., Yadeta, K.A., Thomma, B.P.H.J., 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23, 1271–1282. de Jonge, R., Peter van Esse, H., Maruthachalam, K., Bolton, M.D., Santhanam, P., Saber, M.K., Zhang, Z., Usami, T., Lievens, B., Subbarao, K. V., Thomma, B.P.H.J., 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U. S. A. 109, 5110–5115.

Dean, R., Van Kan, J.A.L., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R., Ellis, J., Foster, G.D., 2012. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414–430.

Deslandes, L., Rivas, S., 2012. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644–655.

Dodds, P.N., Lawrence, G.J., Catanzariti, A.-M., Teh, T., Wang, C.-I.A., Ayliffe, M.A., Kobe, B., Ellis, J.G., 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U. S. A. 103, 8888–93.

Dodds, P.N., Rathjen, J.P., 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539–548.

Dong, S., Raffaele, S., Kamoun, S., 2015. The two-speed genomes of filamentous pathogens: waltz with plants. Curr. Opin. Genet. Dev. 35, 57–65.

Dong, S., Stam, R., Cano, L.M., Song, J., Sklenar, J., Yoshida, K., Bozkurt, T.O., Oliva, R., Liu, Z., Tian, M., Win, J., Banfield, M.J., Jones, A.M.E., van der Hoorn, R.A.L., Kamoun, S., 2014. Effector specialization in a lineage of the Irish potato famine pathogen. Science. 343, 552–555.

Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.

Eisenhaber, B., Schneider, G., Wildpaner, M., Eisenhaber, F., 2004. A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studiesfor Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae

and Schizosaccharomyces pombe. J. Mol. Biol. 337, 243–253.

Ellinghaus, D., Kurtz, S., Willhoeft, U., 2008. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9, 18.

Emms, D.M., Kelly, S., 2015. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157.

Fabro, G., Steinbrenner, J., Coates, M., Ishaque, N., Baxter, L., Studholme, D.J., Körner, E., Allen, R.L., Piquerez, S.J.M., Rougon-Cardoso, A., Greenshields, D., Lei, R., Badel, J.L., Caillaud, M.C., Sohn, K.H., Van den Ackerveken, G., Parker, J.E., Beynon, J., Jones, J.D.G., 2011. Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity. PLoS Pathog. 7, e1002348.

Faino, L., Seidl, M.F., Shi-Kunne, X., Pauper, M., Van Den Berg, G.C.M., Wittenberg, A.H.J., Thomma, B.P.H.J., 2016. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res. 26, 1091–1100.

Falk, A., Feys, B.J., Frost, L.N., Jones, J.D.G., Daniels, M.J., Parker, J.E., 1999. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. U. S. A. 96, 3292–3297.

Feldman, D., Kowbel, D.J., Glass, N.L., Yarden, O., Hadar, Y., 2017. A role for small secreted proteins (SSPs) in a saprophytic fungal lifestyle: Ligninolytic enzyme regulation in Pleurotus ostreatus. Sci. Rep. 7, 14553.

Finn, R.D., Attwood, T.K., Babbitt, P.C., Bateman, A., Bork, P., Bridge, A.J., Chang, H.-Y., Dosztányi, Z., El-Gebali, S., Fraser, M., Gough, J., Haft, D., Holliday, G.L., Huang, H., Huang, X., Letunic, I., Lopez, R., Lu, S., Marchler-Bauer, A., Mi, H., Mistry, J., Natale, D.A., Necci, M., Nuka, G., Orengo, C.A., Park, Y., Pesseat, S., Piovesan, D., Potter, S.C., Rawlings, N.D., Redaschi, N., Richardson, L., Rivoire, C., Sangrador-Vegas, A., Sigrist, C., Sillitoe, I., Smithers, B., Squizzato, S., Sutton, G., Thanki, N., Thomas, P.D., Tosatto, S.C.E., Wu, C.H., Xenarios, I., Yeh, L.-S., Young, S.-Y., Mitchell, A.L., 2017. InterPro in 2017—beyond protein family and domain annotations. Nucleic Acids Res. 45, D190–D199.

Fisher, M.C., Henk, D. a., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L., Gurr, S.J., 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194.

Flor, H.H., 1971. Current Status of the Gene-For-Gene Concept. Annu. Rev. Phytopathol. 9, 275–296.

Frantzeskakis, L., Kracher, B., Kusch, S., Yoshikawa-Maekawa, M., Bauer, S., Pedersen, C., Spanu, P.D., Maekawa, T., Schulze-Lefert, P., Panstruga, R., 2018. Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen. BMC Genomics 19, 381.

Freese, N.H., Norris, D.C., Loraine, A.E., 2016. Integrated genome browser: visual analytics platform for genomics. Bioinformatics 32, 2089–2095.

Frey, T.J., Weldekidan, T., Colbert, T., Wolters, P.J.C.C., Hawk, J.A., 2011. Fitness evaluation of Rcg1, a locus that confers resistance to Colletotrichum graminicola (Ces.) G.W. Wils. using near-isogenic maize hybrids. Crop Sci. 51, 1551–1563.

Gan, P., Ikeda, K., Irieda, H., Narusaka, M., O’Connell, R.J., 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.

Gan, P., Narusaka, M., Kumakura, N., Tsushima, A., Takano, Y., Narusaka, Y., Shirasu, K., 2016.

Genus-wide comparative genome analyses of Colletotrichum species reveal specific gene family losses and gains during adaptation to specific infection lifestyles. Genome Biol. Evol. 8, 1467–1481.

Gan, P., Narusaka, M., Tsushima, A., Narusaka, Y., Takano, Y., Shirasu, K., 2017. Draft genome assembly of Colletotrichum chlorophyti, a pathogen of herbaceous plants. Genome Announc. 5, e01733-16.

Geib, S.M., Hall, B., Derego, T., Bremer, F.T., Cannoles, K., Sim, S.B., 2018. Genome Annotation Generator: a simple tool for generating and correcting WGS annotation tables for NCBI submission.

Gigascience 7, 1–5.Giraldo, M.C., Valent, B., 2013. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11, 800–814.

Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J.W., Robatzek, S., 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824–1832.

Gomes, R.R., Glienke, C., Videira, S.I.R., Lombard, L., Groenewald, J.Z., Crous, P.W., 2013. Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31, 1–41.

Grandaubert, J., Lowe, R.G., Soyer, J.L., Schoch, C.L., Van de Wouw, A.P., Fudal, I., Robbertse, B., Lapalu, N., Links, M.G., Ollivier, B., Linglin, J., Barbe, V., Mangenot, S., Cruaud, C., Borhan, H., Howlett, B.J., Balesdent, M.-H., Rouxel, T., 2014. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics 15, 891.

Griffis, A.H.N., Groves, N.R., Zhou, X., Meier, I., 2014. Nuclei in motion: movement and positioning of plant nuclei in development, signaling, symbiosis, and disease. Front. Plant Sci. 5,129.

Gross, P., Julius, C., Schmelzer, E., Hahlbrock, K., 1993. Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defence gene activation in infected, cultured parsley cells. EMBO J. 12, 1735–1744.

Hacquard, S., Kracher, B., Hiruma, K., Münch, P.C., Garrido-Oter, R., Thon, M.R., Weimann, A., Damm, U., Dallery, J.-F., Hainaut, M., Henrissat, B., Lespinet, O., Sacristán, S., Ver Loren van Themaat, E., Kemen, E., McHardy, A.C., Schulze-Lefert, P., O’Connell, R.J., 2016. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat. Commun. 7, 11362.

Harel, M., Aharoni, A., Gaidukov, L., Brumshtein, B., Khersonsky, O., Meged, R., Dvir, H., Ravelli, R.B.G., McCarthy, A., Toker, L., Silman, I., Sussman, J.L., Tawfik, D.S., 2004. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 11, 412–419.

Hartmann, F.E., Sánchez-Vallet, A., McDonald, B.A., Croll, D., 2017. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. ISME J. 11, 1189–1204.

Hatta, R., Ito, K., Hosaki, Y., Tanaka, T., Tanaka, A., Yamamoto, M., Akimitsu, K., Tsuge, T., 2002. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161, 59–70.

He, P., Shan, L., Lin, N.-C., Martin, G.B., Kemmerling, B., Nürnberger, T., Sheen, J., 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563–575.

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.

Hemetsberger, C., Mueller, A.N., 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.

Henty-Ridilla, J.L., Shimono, M., Li, J., Chang, J.H., Day, B., Staiger, C.J., 2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog. 9, e1003290.

Higaki, T., Kutsuna, N., Sano, T., Kondo, N., Hasezawa, S., 2010. Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J. 61, 156–165.

Hiruma, K., Onozawa-Komori, M., Takahashi, F., Asakura, M., Bednarek, P., Okuno, T., Schulze-Lefert, P., Takano, Y., 2010. Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 22, 2429–2443.

Hoff, K.J., Lange, S., Lomsadze, A., Borodovsky, M., Stanke, M., 2016. BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS. Bioinformatics 32,767–769.

Hogenhout, S. a, Van der Hoorn, R. a L., Terauchi, R., Kamoun, S., 2009. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant. Microbe. Interact. 22, 115–122.

Holt, C., Yandell, M., 2011. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12, 491.

Hubert, D.A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K., Dangl, J.L., 2003. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22, 5679–5689.

Islam, M.T., Croll, D., Gladieux, P., Soanes, D.M., Persoons, A., Bhattacharjee, P., Hossain, M.S., Gupta, D.R., Rahman, M.M., Mahboob, M.G., Cook, N., Salam, M.U., Surovy, M.Z., Sancho, V.B., Maciel, J.L.N., NhaniJúnior, A., Castroagudín, V.L., Reges, J.T., Ceresini, P.C., Ravel, S., Kellner, R., Fournier, E., Tharreau, D., Lebrun, M.-H., McDonald, B.A., Stitt, T., Swan, D., Talbot, N.J., Saunders, D.G.O., Win, J., Kamoun, S., 2016. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biol. 14, 84.

Johnson, B.R., 2018. Taxonomically restricted genes are fundamental to biology and evolution. Front. Genet. 9, 407.

Jones, J.D.G., Dangl, J.L., 2006. The plant immune system. Nature 444, 323–329.

Katoh, K., Misawa, K., Kuma, K., Miyata, T., 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066.

Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.

Kistler, H.C., Miao, V.P.W., 1992. New modes of genetic change in filamentous fungi. Annu. Rev. Phytopathol. 30, 131–153.

Kleemann, J., Rincon-Rivera, L.J., Takahara, H., Neumann, U., van Themaat, E.V.L., van der Does, H.C., Hacquard, S., Stüber, K., Will, I., Schmalenbach, W., Schmelzer, E., O’Connell, R.J., 2012. Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog. 8, e1002643.

Korf, I., 2004. Gene finding in novel genomes. BMC Bioinformatics 5, 59.

Krogh, A., Larsson, B., von Heijne, G., Sonnhammer, E.L.., 2001. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. Mol. Biol. 305, 567–580.

Kumakura, N., Ueno, A., Shirasu, K., 2018. Establishment of a selection marker recycling system for sequential transformation of the plant-pathogenic fungus Colletotrichum orbiculare. Mol. Plant Pathol.

Kurtz, S., Phillippy, A., Delcher, A.L., Smoot, M., Shumway, M., Antonescu, C., Salzberg, S.L., 2004. Versatile and open software for comparing large genomes. Genome Biol. 5, R12.

Langmead, B., Salzberg, S.L., 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359.

Lee, A.H.-Y., Hurley, B., Felsensteiner, C., Yea, C., Ckurshumova, W., Bartetzko, V., Wang, P.W., Quach, V., Lewis, J.D., Liu, Y.C., Börnke, F., Angers, S., Wilde, A., Guttman, D.S., Desveaux, D., 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLoS Pathog. 8, e1002523.

Letunic, I., Bork, P., 2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245.

Li, L., Stoeckert, C.J., Roos, D.S., 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–89.

Li, W.F., Costa, L.G., Richter, R.J., Hagen, T., Shih, D.M., Tward, A., Lusis, A.J., Furlong, C.E., 2000. Catalytic efficiency determines the in-vivo efficacy of PON1 for detoxifying organophosphorus compounds. Pharmacogenetics 10, 767–779.

Lingua, G., Fusconi, A., Berta, G., 2001. The nucleus of differentiated root plant cells: modifications induced by arbuscular mycorrhizal fungi. Eur. J. Histochem. 45, 9–20.

Liu, Y., Schiff, M., Marathe, R., Dinesh-Kumar, S.P., 2002. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30, 415–429.

Lomsadze, A., Burns, P.D., Borodovsky, M., 2014. Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Res. 42, 1–8.

Ma, L.-J., van der Does, H.C., Borkovich, K.A., Coleman, J.J., Daboussi, M.-J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P.M., Kang, S., Shim, W.-B., Woloshuk, C., Xie, X., Xu, J.-R., Antoniw, J., Baker, S.E., Bluhm, B.H., Breakspear, A., Brown, D.W., Butchko, R.A.E., Chapman, S., Coulson, R., Coutinho, P.M., Danchin, E.G.J., Diener, A., Gale, L.R., Gardiner, D.M., Goff, S., Hammond-Kosack, K.E., Hilburn, K., Hua-Van, A., Jonkers, W., Kazan, K., Kodira, C.D., Koehrsen, M., Kumar, L., Lee, Y.-H., Li, L., Manners, J.M.,

Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S.-Y., Proctor, R.H., Regev, A., Ruiz-Roldan, M.C., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D.C., Turgeon, B.G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C.A., Kistler, H.C., Rep, M., 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367–373.

Mayor, C., Brudno, M., Schwartz, J.R., Poliakov, A., Rubin, E.M., Frazer, K.A., Pachter, L.S., Dubchak, I., 2000. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16, 1046–1047.

McMullan, M., Rafiqi, M., Kaithakottil, G., Clavijo, B.J., Bilham, L., Orton, E., Percival-Alwyn, L., Ward, B.J., Edwards, A., Saunders, D.G.O., Garcia Accinelli, G., Wright, J., Verweij, W., Koutsovoulos, G., Yoshida, K., Hosoya, T., Williamson, L., Jennings, P., Ioos, R., Husson, C., Hietala, A.M., Vivian-Smith, A., Solheim, H., MaClean, D., Fosker, C., Hall, N., Brown, J.K.M., Swarbreck, D., Blaxter, M., Downie, J.A., Clark, M.D., 2018. The ash dieback invasion of Europe was founded by two genetically divergent individuals. Nat. Ecol. Evol. 2, 1000–1008.

Menat, J., Cabral, A.L., Vijayan, P., Wei, Y., Banniza, S., 2012. Glomerella truncataௗ: another Glomerella species with an atypical mating system. Mycologia 104, 641–649.

Meyer, V., 2008. A small protein that fights fungi: AFP as a new promising antifungal agent of biotechnological value. Appl. Microbiol. Biotechnol. 78, 17-28.

Mikheenko, A., Valin, G., Prjibelski, A., Saveliev, V., Gurevich, A., 2016. Icarus: visualizer for de novo assembly evaluation. Bioinformatics 32, 3321–3323.

Mitchell, A., Chang, H.-Y., Daugherty, L., Fraser, M., Hunter, S., Lopez, R., McAnulla, C., McMenamin, C., Nuka, G., Pesseat, S., Sangrador-Vegas, A., Scheremetjew, M., Rato, C., Yong, S.-Y., Bateman, A., Punta, M., Attwood, T.K., Sigrist, C.J.A., Redaschi, N., Rivoire, C., Xenarios, I., Kahn, D., Guyot, D., Bork, P., Letunic, I., Gough, J., Oates, M., Haft, D., Huang, H., Natale, D.A., Wu, C.H., Orengo, C., Sillitoe, I., Mi, H., Thomas, P.D., Finn, R.D., 2014. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213-221.

Möller, M., Stukenbrock, E.H., 2017. Evolution and genome architecture in fungal plant pathogens. Nat. Rev. Microbiol. 15, 756–771.

Moreno-Hagelsieb, G., Latimer, K., 2008. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 24, 319–324.

Münch, S., Lingner, U., Floss, D.S., Ludwig, N., Sauer, N., Deising, H.B., 2008. The hemibiotrophic lifestyle of Colletotrichum species. J. Plant Physiol. 165, 41–51.

Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., Kimura, T., 2007. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34–41.

Narusaka, M., Iuchi, S., Narusaka, Y., 2017. Analyses of natural variation indicates that the absence of RPS4/RRS1 and amino acid change in RPS4 cause loss of their functions and resistance to pathogens. Plant Signal. Behav. 12, e1293218.

Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., Narusaka, Y., 2009. RRS1 and RPS4 provide a dual Resistance- gene system against fungal and bacterial pathogens. Plant J. 60, 218–226.

Narusaka, Y., Narusaka, M., Park, P., Kubo, Y., Hirayama, T., Seki, M., Shiraishi, T., Ishida, J., Nakashima, M., Enju, A., Sakurai, T., Satou, M., Kobayashi, M., Shinozaki, K., 2004. RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol. Plant-Microbe Interact. 17, 749–762.

Nelson, B.K., Cai, X., Nebenführ, A., 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126–1136.

O’Connell, R., Herbert, C., Sreenivasaprasad, S., Khatib, M., Esquerré-Tugayé, M.-T., Dumas, B., 2004. A novel Arabidopsis-Colletotrichum pathosystem for the molecular dissection of plant-fungal interactions. Mol. Plant. Microbe. Interact. 17, 272–282.

O’Connell, R.J., Thon, M.R., Hacquard, S., Amyotte, S.G., Kleemann, J., Torres, M.F., Damm, U., Buiate, E.A., Epstein, L., Alkan, N., Altmüller, J., Alvarado-Balderrama, L., Bauser, C.A., Becker, C., Birren, B.W., Chen, Z., Choi, J., Crouch, J.A., Duvick, J.P., Farman, M.A., Gan, P., Heiman, D., Henrissat, B., Howard, R.J., Kabbage, M., Koch, C., Kracher, B., Kubo, Y., Law, A.D., Lebrun, M.-H., Lee, Y.-H., Miyara, I., Moore, N., Neumann, U., Nordström, K., Panaccione, D.G., Panstruga, R., Place, M., Proctor, R.H., Prusky, D., Rech, G., Reinhardt, R., Rollins, J.A., Rounsley, S., Schardl, C.L., Schwartz, D.C., Shenoy, N., Shirasu, K., Sikhakolli, U.R., Stüber, K., Sukno, S.A., Sweigard, J.A., Takano, Y., Takahara, H., Trail, F., van der Does, H.C., Voll, L.M., Will, I., Young, S., Zeng, Q., Zhang, J., Zhou, S., Dickman, M.B., Schulze-Lefert, P., Ver Loren van Themaat, E., Ma, L.-J., Vaillancourt, L.J., 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 44, 1060–5.

Parra, G., Bradnam, K., Korf, I., 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061–1067.

Peart, J.R., Cook, G., Feys, B.J., Parker, J.E., Baulcombe, D.C., 2002. An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. Plant J. 29, 569–579.

Petersen, T.N., Brunak, S., Von Heijne, G., Nielsen, H., 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786.

Petre, B., Saunders, D.G.O., Sklenar, J., Lorrain, E., Win, J., Duplessis, E., Kamoun, S., 2015. Candidate effector proteins of the rust pathogen Melampsora larici-populina target diverse plant cell compartments. MPMI 28, 689–700.

Petre, B., Win, J., Menke, F.L.H., Kamoun, S., 2017. Protein–protein interaction assays with effector–GFP fusions in Nicotiana benthamiana. In: Periyannan, S. (Ed.), Wheat Rust Diseases. Methods in Molecular Biology. Humana Press, New York, pp. 85–98.

Plaumann, P.-L., Schmidpeter, J., Dahl, M., Taher, L., Koch, C., 2018. A dispensable chromosome is required for virulence in the hemibiotrophic plant pathogen Colletotrichum higginsianum. Front. Microbiol. 9, 1005.

Price, A.L., Jones, N.C., Pevzner, P.A., 2005. De novo identification of repeat families in large genomes. Bioinformatics 21, i351–i358.

Quinlan, A.R., Hall, I.M., 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842.

Raffaele, S., Farrer, R.A., Cano, L.M., Studholme, D.J., MacLean, D., Thines, M., Jiang, R.H.Y., Zody, M.C., Kunjeti, S.G., Donofrio, N.M., Meyers, B.C., Nusbaum, C., Kamoun, S., 2010. Genome evolution following host jumps in the irish potato famine pathogen lineage. Science. 330, 1540–1543.

Raffaele, S., Kamoun, S., 2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat. Rev. Microbiol. 10, 417–430.

Rao, S., Nandineni, M.R., 2017. Genome sequencing and comparative genomics reveal a repertoire of putative pathogenicity genes in chilli anthracnose fungus Colletotrichum truncatum. PLoS One 12, e0183567.

Rodríguez-Guerra, R., Ramírez-Rueda, M.-T., Cabral-Enciso, M., nica García-Serrano, M., Lira-Maldonado Ramón Gerardo Guevara-González, Z., González-Chavira, M., Simpson, J., 2005. Heterothallic mating observed between Mexican isolates of Glomerella lindemuthiana. Mycologia 97, 793–803.

Rosenblat, M., Aviram, M., 2009. Paraoxonases role in the prevention of cardiovascular diseases. BioFactors. 35, 98-104.

Sainsbury, F., Thuenemann, E.C., Lomonossoff, G.P., 2009. pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol. J. 7, 682–693.

Sánchez-Vallet, A., Fouché, S., Fudal, I., Hartmann, F.E., Soyer, J.L., Tellier, A., Croll, D., 2018. The genome biology of effector gene evolution in filamentous plant pathogens. Annu. Rev. Phytopathol. 56, 21-40.

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. Mol. Plant Pathol. 17, 1048–1062.

Sarris, P.F., Duxbury, Z., Huh, S.U., Ma, Y., Segonzac, C., Sklenar, J., Derbyshire, P., Cevik, V., Rallapalli, G., Saucet, S.B., Wirthmueller, L., Menke, F.L.H., Sohn, K.H., Jones, J.D.G., 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161, 1089–1100.

Sato, T., Moriwaki, J., 2009. Causal fungi of plant anthracnose (1). Microbiol. Cult. Coll. 25, 27–32. Saunders, D.G.O., Win, J., Kamoun, S., Raffaele, S., 2014. Two-dimensional data binning for the analysis of genome architecture in filamentous plant pathogens and other eukaryotes. In: Birch, P., Jones, J., Bos, J. (Eds.), Methods in Molecular Biology (Methods and Protocols). Humana Press, Totowa, pp. 29–51.

Schneider, C.A., Rasband, W.S., Eliceiri, K.W., 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.

Schwessinger, B., Roux, M., Kadota, Y., Ntoukakis, V., Sklenar, J., Jones, A., Zipfel, C., 2011. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046.

Seidl, M.F., Thomma, B.P.H.J., 2014. Sex or no sex: Evolutionary adaptation occurs regardless. BioEssays 36, 335–345.

Shan, X.C., Goodwin, P.H., 2004. Monitoring host nuclear migration and degradation with green fluorescent protein during compatible and incompatible interactions of Nicotiana tabacum with Colletotrichum species. J. Phytopathol. 152, 454–460.

Shimono, M., Lu, Y.-J., Porter, K., Kvitko, B.H., Henty-Ridilla, J., Creason, A., He, Y., Chang, J.H., Staiger, C.J., Day, B., Conducted, B.H.K., Contrib-, C.J.S., 2016. The Pseudomonas syringae type III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection. Plant Physiol. 171, 2239–2255.

Shirasu, K., Lahaye, T., Tan, M.W., Zhou, F., Azevedo, C., Schulze-Lefert, P., 1999. A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99, 355–366.

Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E. V., Zdobnov, E.M., 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212.

Slater, G.S.C., Birney, E., 2005. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31.

Sohn, K.H., Zhang, Y., Jones, J.D.G., 2009. The Pseudomonas syringae effector protein, AvrRPS4, requires in planta processing and the KRVY domain to function. Plant J. 57, 1079–1091.

Spanu, P.D., Panstruga, R., 2017. Editorial: biotrophic plant-microbe interactions. Front. Plant Sci. 8,192.

Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.

Stanke, M., Schöffmann, O., Morgenstern, B., Waack, S., 2006. Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7, 62.

Sullivan, M.J., Petty, N.K., Beatson, S.A., 2011. Easyfig: a genome comparison visualizer. Bioinformatics 27, 1009–1010.

Takahara, H., Hacquard, S., Kombrink, A., Hughes, H.B., Halder, V., Robin, G.P., Hiruma, K., Neumann, U., Shinya, T., Kombrink, E., Shibuya, N., Thomma, B.P.H.J., O’Connell, R.J., 2016. Colletotrichum higginsianum extracellular LysM proteins play dual roles in appressorial function and suppression of chitin-triggered plant immunity. New Phytol. 211, 1323–1337.

Takemoto, D., Jones, D.A., Hardham, A.R., 2006. Re-organization of the cytoskeleton and endoplasmic reticulum in the Arabidopsis pen1-1 mutant inoculated with the non-adapted powdery mildew pathogen, Blumeria graminis f. sp. hordei. Mol. Plant Pathol. 7, 553–563.

Tautz, D., Domazet-Lošo, T., 2011. The evolutionary origin of orphan genes. Nat. Rev. Genet. 12, 692–702.

Treangen, T.J., Salzberg, S.L., 2012. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat. Rev. Genet. 13, 36–46.

Vaillancourt, L.J., Hanau, R.M., 1991. A method for genetic analysis of Glomerella graminicola (Colletotrichum graminicola) from maize. Phytopathology. 81, 530-534.

Wang, J., Li, S., Zhang, Y., Zheng, H., Xu, Z., Ye, J., Yu, J., Wong, G.K.-S., 2003. Vertebrate gene predictions and the problem of large genes. Nat. Rev. Genet. 4, 741–749.

Weir, B.S., Johnston, P.R., Damm, U., 2012. The Colletotrichum gloeosporioides species complex. Stud. Mycol. 73, 115–180.

Westerink, N., Brandwagt, B.F., De Wit, P.J.G.M., Joosten, M.H.A.J., 2004. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol. Microbiol. 54, 533–545.

White, F.F., Yang, B., Johnson, L.B., 2000. Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3, 291–298.

Wickstead, B., Gull, K., 2011. The evolution of the cytoskeleton. J. Cell Biol. 194, 513–25.

Xiang, T., Zong, N., Zou, Y., Wu, Y., Zhang, J., Xing, W., Li, Y., Tang, X., Zhu, L., Chai, J., Zhou, J.-M., 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18, 74–80.

Yoshida, K., Saitoh, H., Fujisawa, S., Kanzaki, H., Matsumura, H., Yoshida, K., Tosa, Y., Chuma, I., Takano, Y., Win, J., Kamoun, S., Terauchi, R., 2009. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21, 1573–1591.

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, 625–36.

Yu, C., Zhang, J., Peterson, T., 2011. Genome rearrangements in maize induced by alternative transposition of reversed Ac/Ds termini. Genetics 188, 59–67.

Zampounis, A., Pigné, S., Dallery, J., Wittenberg, A.H.J., Zhou, S., Schwartz, D.C., Thon, M.R., O’Connell, R.J., 2016. Genome sequence and annotation of Colletotrichum higginsianum, a causal agent of crucifer anthracnose disease. Genome Announc. 4, e00821-16.

Zhang, J., Yu, C., Pulletikurti, V., Lamb, J., Danilova, T., Weber, D.F., Birehler, J., Peterson, T., 2009. Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize. Genes Dev. 23, 755–765.

Zhang, Y., Dorey, S., Swiderski, M., Jones, J.D.G., Centre, J.I., Lane, C., 2004. Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant J. 40, 213–24.

Zhong, Z., Marcel, T.C., Hartmann, F.E., Ma, X., Plissonneau, C., Zala, M., Ducasse, A., Confais, J., Compain, J., Lapalu, N., Amselem, J., McDonald, B.A., Croll, D., Palma-Guerrero, J., 2017. A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol. 214, 619–631.