A Fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development

Molecular Plant-Microbe Interactions

Volumn 29, Issue 2, 2016, Pages 83-95

  Vargas, Walter A ^a   Sanz Martn, Jose M ^a   Rech, Gabriel E ^a   Armijos Jaramillo, Vinicio D ^a   Rivera, Lina P ^a   Echeverria, Maria Mercedes ^b   Diaz Minguez, Jose M ^a   Thon, Michael R ^a   Sukno, Serenella A ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; FUNGAL PROTEIN; PLANT DNA; PROTEIN BINDING;

ACTIVE TRANSPORT; ADAPTATION; COLLETOTRICHUM; EVOLUTION; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; MAIZE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT GENOME; PLANT LEAF; PLANT ROOT; PLANT STEM;

ACTIVE TRANSPORT, CELL NUCLEUS; ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; COLLETOTRICHUM; DNA, FUNGAL; DNA, PLANT; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENETIC VARIATION; GENOME, PLANT; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PLANT STEMS; PROTEIN BINDING; ZEA MAYS;

EID: 84959211317     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-09-15-0209-R     Document Type: Article

References (95)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Anisimova, M., Bielawski, J. P., and Yang, Z. 2001. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol. Biol. Evol. 18:1585-1592.
3. Arora, R., Agarwal, P., Ray, S., Singh, A. K., Singh, V. P., Tyagi, A. K., and Kapoor, S. 2007. MADS-box gene family in rice: Genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242.
4. Baek, J. M., and Kenerley, C. M. 1998. The arg2 gene of Trichoderma virens: Cloning and development of a homologous transformation system. Fungal Genet. Biol. 23:34-44.
5. Bailey, J. A., and Jeger, M. J., eds. 1992 Colletotrichum: Biology, Pathology and Control. CAB International, Wallingford, U.K.
6. Bellafiore, S., Shen, Z., Rosso, M.-N., Abad, P., Shih, P., and Briggs, S. P. 2008. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog. 4: e1000192.
7. Bergstrom, G. C., and Nicholson, R. L. 1981. Invertase in the spore matrix of Colletotrichum graminicola. J. Phytopathol. 102:139-147.
8. Bergstrom, G. C., and Nicholson, R. L. 1999. The biology of corn anthracnose: Knowledge to exploit for improved management. Plant Dis. 83:596-608.
9. Bierne, H., and Cossart, P. 2012. When bacteria target the nucleus: The emerging family of nucleomodulins. Cell. Microbiol. 14:622-633.
10. Bogdanove, A. J., and Voytas, D. F. 2011. TAL effectors: Customizable proteins for DNA targeting. Science 333:1843-1846.
11. Bolton, M. D., van Esse, H. P., Vossen, J. H., de Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., van den Berg, G. C., Borras-Hidalgo, O., Dekker, H. L., de Koster, C. G., de Wit, P. J., Joosten, M. H., and Thomma, B. P. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119-136.
12. Busch, H. 1965. Histones and Other Nuclear Proteins. Academic Press, New York.
13. Chen, S., Songkumarn, P., Venu, R. C., Gowda, M., Bellizzi, M., Hu, J., Liu, W., Ebbole, D., Meyers, B., Mitchell, T., and Wang, G.-L. 2013. Identification and characterization of in planta-expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice. Mol. Plant-Microbe Interact. 26:191-202.
14. Ciftci-Yilmaz, S., and Mittler, R. 2008. The zinc finger network of plants. Cell. Mol. Life Sci. 65:1150-1160.
15. Crouch, J. A., and Beirn, L. A. 2009. Anthracnose of cereals and grasses. Fungal Divers. 39:19-44.
16. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., and Kahmann, R. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog. 5:e1000290.
17. Edgar, R. C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
18. Fellbrich, G., Romanski, A., Varet, A., Blume, B., Brunner, F., Engelhardt, S., Felix, G., Kemmerling, B., Krzymowska, M., and Nürnberger, T. 2002. NPP1, a Phytophthora-Associated trigger of plant defense in parsley and Arabidopsis. Plant J. 32:375-390.
19. Finn, R. D., Clements, J., and Eddy, S. R. 2011. HMMER web server: Interactive sequence similarity searching. Nucl. Acids Res. 39:W29-W37.
20. Forgery, W., Blanco, M., and Loegering, W. 1978. Differences in pathological capabilities and host specificity of Colletotrichum graminicola on Zea mays (maize). Plant Dis. Rep. 62:573-576.
21. Frandsen, R. J., Andersson, J. A., Kristensen, M. B., and Giese, H. 2008. Efficient four fragment cloning for the construction of vectors for targeted gene replacement in filamentous fungi. BMC Mol. Biol. 9:70.
22. Freeman, B. C.,Beattie, G. A 2008, An overview of plant defenses against pathogens and herbivores. Plant Health Instr doi:10.1094/PHI-I-2008- 0226-01 Published online
23. Gan, P., Ikeda, K., Irieda, H., Narusaka, M., O'Connell, R. J., Narusaka, Y., Takano, Y., Kubo, Y., and Shirasu, K. 2013. Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol. 197:1236-1249.
24. Garcia-Pedrajas, M. D., Nadal, M., Kapa, L. B., Perlin, M. H., Andrews, D. L., and Gold, S. E. 2008. DelsGate, a robust and rapid gene deletion construction method. Fungal Genet. Biol. 45:379-388.
25. Guindon, S., and Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
26. Gutowska-Owsiak, D., and Ogg, G. S. 2012. The epidermis as an adjuvant. J. Invest. Dermatol. 132:940-948.
27. Henty-Ridilla, J. L., Li, J., Day, B., and Staiger, C. J. 2014. ACTIN DEPOLYMERIZING FACTOR4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell 26:340-352.
28. Herbers, K., Conrads-Strauch, J., and Bonas, U. 1992. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356:172-174.
29. Heger, A., and Holm, L. 2000. Rapid automatic detection and alignment of repeats in protein sequences. Proteins 41:224-237.
30. Hof, A., Zechmann, B., Schwammbach, D., Hückelhoven, R., and Doehlemann, G. 2014. Alternative cell death mechanisms determine epidermal resistance in incompatible barley-Ustilago interactions. Mol. Plant-Microbe Interact. 27:403-414.
31. Hogenhout, S. A., Van der Hoorn, R. A. L., Terauchi, R., and Kamoun, S. 2009. Emerging concepts in effector biology of plant-Associated organisms. Mol. Plant-Microbe Interact. 22:115-122.
32. Hood, D. W., Deadman, M. E., Jennings, M. P., Bisercic, M., Fleischmann, R. D., Venter, J. C., andMoxon, E. R. 1996.DNArepeats identify novel virulence genes in Haemophilus influenzae. Proc. Natl. Acad. Sci. U.S.A. 93:11121-11125.
33. Horbach, R., Graf, A., Weihmann, F., Antelo, L., Mathea, S., Liermann, J. C., Opatz, T., Thines, E., Aguirre, J., and Deising, H. B. 2009. Sfp-type 49-phosphopantetheinyl transferase is indispensable for fungal pathogenicity. Plant Cell 21:3379-3396.
34. Horton, P., Park, K.-J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., and Nakai, K. 2007. WoLF PSORT: Protein localization predictor. Nucleic Acids Res. 35:W585-W587.
35. Irieda H., Maeda H., Akiyama K., Hagiwara A., Saitoh H., Uemura A., Terauchi R., Takano Y. 2014. Colletotrichum orbiculare secretes virulence effectors to a biotrophic interface at the primary hyphal neck via exocytosis coupled with SEC22-mediated traffic. Plant Cell 26:2265-2281.
36. Javelle, M., Vernoud, V., Rogowsky, P. M., and Ingram, G. C. 2011. Epidermis: The formation and functions of a fundamental plant tissue. New Phytol. 189:17-39.
37. Jensen, M. K., Hagedorn, P. H., de Torres-Zabala, M., Grant, M. R., Rung, J. H., Collinge, D. B., and Lyngkjaer, M. F. 2008. Transcriptional regulation by an NAC (NAM-ATAF1, 2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J. 56:867-880.
38. Jeon, J., Park, S.-Y., Chi, M.-H., Choi, J., Park, J., Rho, H.-S., Kim, S., Goh, J., Yoo, S., Choi, J., Park, J.-Y., Yi, M., Yang, S., Kwon, M.-J., Han, S.-S., Kim, B. R., Khang, C. H., Park, B., Lim, S.-E., Jung, K., Kong, S., Karunakaran, M., Oh, H.-S., Kim, H., Kim, S., Park, J., Kang, S., Choi, W.-B., Kang, S., and Lee, Y.-H. 2007. Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nat. Genet. 39:561-565.
39. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
40. Kanzaki, H., Yoshida, K., Saitoh, H., Fujisaki, K., Hirabuchi, A., Alaux, L., Fournier, E., Tharreau, D., and Terauchi, R. 2012. Arms race coevolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J. 72:894-907.
41. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066.
42. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., and Drummond, A. 2012. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649.
43. Kemen, E., Kemen, A. C., Rafiqi, M., Hempel, U., Mendgen, K., Hahn, M., and Voegele, R. T. 2005. Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol. Plant-Microbe Interact. 18:1130-1139.
44. Khang, C. H., Berruyer, R., Giraldo, M. C., Kankanala, P., Park, S.-Y., Czymmek, K., Kang, S., and Valent, B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cellto-cell movement. Plant Cell 22:1388-1403.
45. Kleemann, J., Rincon-Rivera, L. J., Takahara, H., Neumann, U., Ver Loren van Themaat, E., van der Does, H. C., Hacquard, S., Stüber, K., Will, I., Schmalenbach, W., Schmelzer, E., and 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.
46. Kleemann, J., Takahara, H., Stuber, K., and O'Connell, R. 2008. Identification of soluble secreted proteins from appressoria of Colletotrichum higginsianum by analysis of expressed sequence tags. Microbiology 154:1204-1217.
47. Kloppholz, S., Kuhn, H., and Requena, N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21: 1204-1209.
48. Knight, R., Maxwell, P., Birmingham, A., Carnes, J., Caporaso, J. G., Easton, B. C., Eaton, M., Hamady, M., Lindsay, H., Liu, Z., Lozupone, C., McDonald, D., Robeson, M., Sammut, R., Smit, S., Wakefield, M. J., Widmann, J., Wikman, S., Wilson, S., Ying, H., and Huttley, G. A. 2007. PyCogent: A toolkit for making sense from sequence. Genome Biol. 8:R171.
49. Koga, H., Dohi, K., Nakayachi, O., and Mori, M. 2004. A novel inoculation method of Magnaporthe grisea for cytological observation of the infection process using intact leaf sheaths of rice plants. Physiol. Mol. Plant Pathol. 64:67-72.
50. Liu, B., Ouyang, Z., Zhang, Y., Li, X., Hong, Y., Huang, L., Liu, S., Zhang, H., Li, D., and Song, F. 2014. Tomato NAC transcription factor SlSRN1 positively regulates defense response against biotic stress but negatively regulates abiotic stress response. PLoS One 9:e102067.
51. Livak, K. J., Flood, S. J., Marmaro, J., Giusti, W., and Deetz, K. 1995. Oligonucleotides with fluorescent dyes at opposite ends provide a quenched probe system useful for detecting PCR product and nucleic acid hybridization. PCR Methods Appl. 4:357-362.
52. Maldonado-Bonilla, L. D., Eschen-Lippold, L., Gago-Zachert, S., Tabassum, N., Bauer, N., Scheel, D., and Lee, J. 2014. The Arabidopsis tandem zinc finger 9 protein binds RNA and mediates pathogenassociated molecular pattern-triggered immune responses. Plant Cell Physiol. 55:412-425.
53. Marcel, S., Sawers, R., Oakeley, E., Angliker, H., and Paszkowski, U. 2010. Tissue-Adapted invasion strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 22:3177-3187.
54. Marian, C. O., Bordoli, S. J., Goltz, M., Santarella, R. A., Jackson, L. P., Danilevskaya, O., Beckstette, M., Meeley, R., and Bass, H.W. 2003. The maize single myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol. 133:1336-1350.
55. Mentlak, T. A., Kombrink, A., Shinya, T., Ryder, L. S., Otomo, I., Saitoh, H., Terauchi, R., Nishizawa, Y., Shibuya, N., Thomma, B. P. H. J., and Talbot, N. J. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322-335.
56. Mesarich, C. H., Bowen, J. K., Hamiaux, C., and Templeton, M. D. 2015. Repeat-containing protein effectors of plant-Associated organisms. Front. Plant Sci. 6:872.
57. Micali, C. O., Neumann, U., Grunewald, D., Panstruga, R., and O'Connell, R. 2011. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell. Microbiol. 13:210-226.
58. Mims, C. W., and Vaillancourt, L. J. 2002. Ultrastructural characterization of infection and colonization of maize leaves by Colletotrichum graminicola, and by a C. graminicola pathogenicity mutant. Phytopathology 92:803-812.
59. Nuruzzaman, M., Sharoni, A. M., and Kikuchi, S. 2013. Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front. Microbiol. 4:248.
60. 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., and Vaillancourt, L. J. 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 44:1060-1065.
61. Pandey, S. P., and Somssich, I. E. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiol. 150:1648-1655.
62. Panstruga, R. 2003. Establishing compatibility between plants and obligate biotrophic pathogens. Curr. Opin. Plant Biol. 6:320-326.
63. Perfect, S. E., and Green, J. R. 2001. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol. Plant Pathol. 2:101-108.
64. Perfect, S. E., Hughes, H. B., O'Connell, R. J., and Green, J. R. 1999. Colletotrichum: A model genus for studies on pathology and fungalplant interactions. Fungal Genet. Biol. 27:186-198.
65. Petre, B., Saunders, D. G., Sklenar, J., Lorrain, C., Win, J., Duplessis, S., and Kamoun, S. 2015. Candidate effector proteins of the rust pathogen Melampsora larici-populina target diverse plant cell compartments. Mol. Plant-Microbe Interact. 28:689-700.
66. Plett, J. M., Kemppainen, M., Kale, S. D., Kohler, A., Legué, V., Brun, A., Tyler, B. M., Pardo, A. G., and Martin, F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21:1197-1203.
67. Politis, D. J., and Wheeler, H. 1972. The perfect stage of Colletotrichum graminicola. Plant Dis. Rep. 56:1026-1027.
68. Pretsch, K., Kemen, A., Kemen, E., Geiger, M., Mendgen, K., and Voegele, R. 2013. The rust transferred proteins-A new family of effector proteins exhibiting protease inhibitor function. Mol. Plant Pathol. 14:96-107.
69. Prusky, D., Freeman, S., and Dickman, M. B., eds. 2000. Colletotrichum: Host Specificity, Pathology, and Host-Pathogen Interaction. APS Press, St. Paul, MN, U.S.A.
70. Redkar, A., Villajuana-Bonequi, M., and Doehlemann, G. Conservation of the Ustilago maydis Effector See1 in related smuts. Plant Signal. Behav. In press.
71. Ricardi, M. M., González, R. M., and Iusem, N. D. 2010. Protocol: Finetuning of a Chromatin Immunoprecipitation (ChIP) protocol in tomato. Plant Methods 6:11.
72. Rich, S. M., and Ayala, F. J. 2000. Population structure and recent evolution of Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 97:6994-7001.
73. Rivas, S., and Genin, S. 2011. A plethora of virulence strategies hidden behind nuclear targeting of microbial effectors. Front. Plant Sci. 2: 104.
74. Ronquist, F., and Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
75. Sakaguchi, A., Miyaji, T., Tsuji, G., and Kubo, Y. 2010. A kelch repeat protein, Cokel1p, associates with microtubules and is involved in appressorium development in Colletotrichum orbiculare. Mol. Plant-Microbe Interact. 23:103-111.
76. Sambrook, J., and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual, 3rd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
77. Schilling, L., Matei, A., Redkar, A., Walbot, V., and Doehlemann, G. 2014. Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors. Mol. Plant Pathol. 15:8.
78. Shan, W., Chen, J., Kuang, J., and Lu, W. 2015. Banana fruit NAC transcription factor MaNAC5 cooperates with MaWRKYs to enhance expressions of pathogenesis-related genes against Colletotrichum musae. Mol. Plant Pathol. doi:10.1111/mpp.12281. Published online.
79. Skibbe, D. S., Doehlemann, G., Fernandes, J., and Walbot, V. 2010. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89-92.
80. Stephenson, S. A., Hatfield, J., Rusu, A. G., Maclean, D. J., and Manners, J. M. 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.
81. Sukno, S. A., García, V. M., Shaw, B. D., and Thon, M. R. 2008. Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl. Environ. Microbiol. 74:823-832.
82. Thomas, J. O., and Travers, A. A. 2001. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem. Sci. 26:167-174.
83. Thon, M. R., Nuckles, E. M., and Vaillancourt, L. J. 2000. Restriction enzyme-mediated integration used to produce pathogenicity mutants of Colletotrichum graminicola. Mol. Plant-Microbe Interact. 13:1356-1365.
84. Torres, G., Frisella, P. D., Yousuf, S. J., Sarwar, S., Baldinger, L., Zakhary, S. M., and Leheste, J. R. 2008. A ChIP-cloning approach linking SIRT1 to transcriptional modificationof DNA targets. Biotechniques 44. doi: 10.2144/000112748. Published online.
85. Tucker, S. L., Besi, M. I., Galhano, R., Franceschetti, M., Goetz, S., Lenhert, S., Osbourn, A., and Sesma, A. 2010. Common genetic pathways regulate organ-specific infection-related development in the rice blast fungus. Plant Cell 22:953-972.
86. Vargas, W. A., Martín, J. M. S., Rech, G. E., Rivera, L. P., Benito, E. P., Díaz-Mínguez, J. M., Thon, M. R., and Sukno, S. A. 2012. Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol. 158:1342-1358.
87. Voitsik, A.-M., Muench, S., Deising, H. B., and Voll, L. M. 2013. Two recently duplicated maize NAC transcription factor paralogs are induced in response to Colletotrichum graminicola infection. BMC Plant Biol. 13:85.
88. Wang, C., Zhang, S., Hou, R., Zhao, Z., Zheng, Q., Xu, Q., Zheng, D., Wang, G., Liu, H., Gao, X., Ma, J.-W., Kistler, H. C., Kang, Z., and Xu, J.-R. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog. 7:e1002460.
89. Warren, H. L. 1976. Relationship of Colletotrichum graminicola to foliar and kernel infection. Plant Dis. 60:1084-1086.
90. Warren, H. L., Nicholson, R. L., and Turner, M. T. 1975. Field reaction of corn inbreds to Colletotrichum graminicola. Plant Dis. 59:767-769.
91. Win, J., Chaparro-Garcia, A., Belhaj, K., Saunders, D. G. O., Yoshida, K., Dong, S., Schornack, S., Zipfel, C., Robatzek, S., Hogenhout, S. A., and Kamoun, S. 2012. Effector biology of plant-Associated organisms: Concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77:235-247.
92. Yang, Z. 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24:1586-1591.
93. Yang, Z., and Bielawski, J. P. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. Amst. 15:496-503.
94. Yang, Z., Wong, W. S. W., and Nielsen, R. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22:1107-1118.
95. Yi, M., and Valent, B. 2013. Communication between filamentous pathogens and plants at the biotrophic interface. Annu. Rev. Phytopathol. 51:587-611.