Morphological and molecular analyses of host and nonhost interactions involving barley and wheat and the covered smut Pathogen Ustilago hordei

Molecular Plant-Microbe Interactions

Volumn 23, Issue 12, 2010, Pages 1619-1634

  Gaudet, Denis A ^a   Wang, Yuanyuan ^a   Penniket, Carolyn ^a   Lu, Z X ^a   Bakkeren, Guus ^b   Laroche, André ^a  

^a LETHBRIDGE RESEARCH CENTRE   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID; VEGETABLE PROTEIN;

ARTICLE; BARLEY; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PROTEIN MICROARRAY; USTILAGO; WHEAT;

CYCLOPENTANES; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; HORDEUM; HOST-PATHOGEN INTERACTIONS; OXYLIPINS; PLANT DISEASES; PLANT PROTEINS; PROTEIN ARRAY ANALYSIS; SALICYLIC ACID; TRITICUM; USTILAGO;

HORDEUM; TRITICUM AESTIVUM; USTILAGO HORDEI;

EID: 78649463578     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-11-09-0271     Document Type: Article

References (80)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B. J., Daniels, M. J., and Parker, J. E. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 95:10306-10311.
2. Abramovitch, R. B., Anderson, J. C., and Martin, G. B. 2006. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell. Biol. 7:601-611.
3. Anand, A., Schmelz, E. A., and Muthukrishnan, S. 2007. Development of a lesion-mimic phenotype in a transgenic wheat line overexpressing genes for pathogenesis-related (PR) proteins is dependent on salicylic acid concentration. Mol. Plant-Microbe Interact. 16:916-925.
4. Avery, G. S. 1930. Comparative anatomy and morphology of embryos and seedlings of maize, oats, and wheat. Bot. Gaz. 89:1-39.
5. Bai, J., Pennill, L. A., Ning, J., Lee, S. W., Ramalingam, J., Webb, C. A., Zhao, B., Sun, Q., Nelson, J. C., Leach, J. E., and Hulbert, S. H. 2002. Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res. 12:1871-1884.
6. Belkhadir, Y., Subramaniam, R., and Dangl, J. L. 2004. Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7:391-399.
7. Bent, A. F., and Mackey, D. 2007. Elicitors, effectors, and R genes: The new paradigm and a lifetime supply of questions. Ann. Rev. Phytopathol. 45:399-436.
8. Blazejczyk, M., Miron, M., and Nadon, R. 2007. FlexArray: A statistical data analysis software for gene expression microarrays. Genome Quebec, Montreal, Canada..
9. Cai, X. Z., Zhou, X., Xu, Y. P., Joosten, M., and de Wit, P. 2007. Cladosporium fulvum CfHNNI1 induces hypersensitive necrosis, defence gene expression and disease resistance in both host and nonhost plants. Plant Mol. Biol. 64:89-101.
10. Caillaud, M.-C., Dubreuil, G., Quentin, M., Perfus-Barbeoch, L., Lecomte, P., de Almeida Engler, J., Abad, P., Rosso, M.-N., and Favery, B. 2008. Root-knot nematodes manipulate plant cell functions during a compatible interaction. J. Plant Physiol. 165:104-113.
11. Catinot, J., Buchala, A., Abou-Mansour, E., and Métraux, J.-P. 2008. Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS (Fed. Eur. Biochem. Soc.) Lett. 582:473-478.
12. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814.
13. Creelman, R. A., and Mullet, J. E. 1995. Jasmonic acid distribution and action in plants: Regulation during development and response to biotic and abiotic stress. Proc. Natl. Acad. Sci. U.S.A. 92:4114-4119.
14. Doehlemann, G., Wahl, R., Horst, R. J., Voll, L. M., Usadel, B., Poree, F., Stitt, M., Pons-Kühnemann, J., Sonnewald, U., Kahmann, R., and Kämper, J. 2008. Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56:181-195.
15. 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, isrequired for successful invasion of plant cells. Plos Pathogens 5:e1000290.
16. Dong, X. Y., Hong, Z. L., Chatterjee, J., Kim, S. H., and Verma, D. P. S. 2008. Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229:87-98.
17. Durrant, W. E., and Dong, X. 2004. Systemic acquired resistance. Ann. Rev. Phytopathol. 42:185-209.
18. Feys, B. J., Moisan, L. J., Newman, M.-A., and Parker, J. E. 2001. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO (Eur. Mol. Biol. Organ.) J. 20:5400-5411.
19. Fischer, G. W. 1953. Manual of the North American smut fungi. The Ronald Press Co. 343 p.
20. Fischer, G. W., and Holton, C. S. 1957. Biology and control of the smut fungi. The Ronald Press Company, New York. 622 p.
21. Gaudet, D. A., Lu, Z. X., Leggett, F., Puchalski, B., and Laroche, A. 2007. Compatible and incompatible interactions in wheat involving the Bt-10 gene for resistance to Tilletia tritici, the common bunt pathogen. Phytopathology 97:1397-1405.
22. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann. Rev. Phytopathol. 43:205-227.
23. Goates, B. J. 1996. Common bunt and dwarf bunt. Pages 12-25 in: Bunt and Smut Disease of Wheat: Concepts and Methods of Disease Management. R. D. Wilcoxson and E. E. Saari, eds. Centro Internacional de Mejoramiento de Maíz y Trigo, Mexico.
24. Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H., and Ryals, J. 1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629-643.
25. Grewal, T. S., Rossnagel, B. G., Bakkeren, G., and Scoles, G. J. 2008. Identification of resistance genes to barley covered smut and mapping of the Ruh1 gene using Ustilago hordei strains with defined virulence genes. Can. J. Plant Pathol. 30:277-284.
26. Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo, M., Nishimura, M., and Hara-Nishimura, I. 2004. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855-858.
27. Hauck, P., Thilmony, R., and He, S. Y. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. U.S.A. 100:8577-8582.
28. Heath, M. C. 2000. Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3:315-319.
29. Hoch, H. C., Staples, R. C., Whitehead, B., Comeau, J., and Wolf, E. D. 1987. Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235:1659-1662.
30. Hood, M. E., and Shew, H. D. 1996. Applications of KOH-aniline blue fluorescence in the study of plant-fungal interactions. Phytopathology 86:704-708.
31. Hu, G. G., Linning, R., and Bakkeren, G. 2002. Sporidial mating and infection process of the smut fungus, Ustilago hordei, in susceptible barley. Can. J. Bot. 80:1103-1114.
32. Hu, G. G., Linning, R., and Bakkeren, G. 2003. Ultrastructural comparison of a compatible and incompatible interaction triggered by the presence of an avirulence gene during early infection of the smut fungus, Ustilago hordei, in barley. Physiol. Mol. Plant Pathol. 62:155-166.
33. Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., Ausubel, F. M., and Glazebrook, J. 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 96:13583-13588.
34. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
35. Keppler, L. D., Baker, C. J., and Atkinson, M. M. 1989. Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells. Phytopathology 79:974-978.
36. Kozar, F. 1969. The pathway of infection of Ustilago hordei. Can. J. Genet. Cytol. 11:977-986.
37. Krzymowska, M., Konopka-Postupolska, D., Sobczak, M., Macioszek, V., Ellis, B. E., and Hennig, J. 2007. Infection of tobacco with different Pseudomonas syringae pathovars leads to distinct morphotypes of programmed cell death. Plant J. 50:253-264.
38. Kudlicka, K., and Brown, R. M. 1997. Cellulose and callose biosynthesis in higher plants (I. Solubilization and separation of (1->3)- and (1->4)- β-glucan synthase activities from mung bean. Plant Physiol. 115:643-656.
39. Lamb, C., and Dixon, R. A. 1997. The oxidative burst in plant disease resistance Ann. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
40. Laurent, Z., Mónica, S., Volker, L., Paul, S.-L., and Shauna, S. 2004. Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J. 40:633-646.
41. Lee, S. C., and Hwang, B. K. 2005. Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221:790-800.
42. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
43. Linning, R., Lin, D., Lee, N., Abdennadher, M., Gaudet, D., Thomas, P., Mills, D., Kronstad, J. W., and Bakkeren, G. 2004. Marker-based cloning of the region containing the UhAvr1 avirulence gene from the basidiomycete barley pathogen Ustilago hordei. Genetics 166:99-111.
44. Lipka, U., Fuchs, R., and Lipka, V. 2008. Arabidopsis non-host resistance to powdery mildews. Curr. Opin. Plant Biol. 11:404-411.
45. Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., Landtag, J., Brandt, W., Rosahl, S., Scheel, D., Llorente, F., Molina, A., Parker, J., Somerville, S., and Schulze-Lefert, P. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180-1183.
46. Lu, Z.-X., Gaudet, D. A., Frick, M., Puchalski, B., Genswein, B., and Laroche, A. 2005a. Identification and characterization of genes differentially expressed in the resistance reaction in wheat infected with Tilletia tritici, the common bunt pathogen. J. Biochem. Mol. Biol. 38:420-431.
47. Lu, Z.-X., Gaudet, D., Puchalski, B., Despins, T., Frick, M., and Laroche, A. 2005b. Inducers of resistance reduce common bunt infection in wheat seedlings while differentially regulating defence-gene expression. Physiol. Mol. Plant Pathol. 67:138-148.
48. Maher, E., Bate, N., Ni, W., Elkind, Y., Dixon, R. A., and Lamb, C. 1994. Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products 91:7802-7806.
49. Maor, R., and Shirasu, K. 2005. The arms race continues: Battle strategies between plants and fungal pathogens. Curr. Opin. Microbiol. 8:399-404.
50. Molina, A., Gãrlach, J., Volrath, S., and Ryals, J. 1999. Wheat genes encoding two types of PR-1 troteins are pathogen inducible, but do not respond to activators of systemic acquired resistance. Mol. Plant-Microbe Interact. 12:53-58.
51. Mysore, K. S., and Ryu, C.-M. 2004. Nonhost resistance: How much do we know? Trends Plant Sci. 9:97-104.
52. Nicholson, R. L., and Hammerschmidt, R. 2003. Phenolic compounds and their role in disease resistance. Ann. Rev. Phytopathol. 30:369-389.
53. Nishimura, M. T., Stein, M., Hou, B. H., Vogel, J. P., Edwards, H., and Somerville, S. C. 2003. Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969-972.
54. Numberger, T., and Lipka, V. 2005. Non-host resistance in plants: New insights into an old phenomenon. Mol. Plant Pathol. 6:335-345.
55. Nurnberger, T., Brunner, F., Kemmerling, B., and Piater, L. 2004. Innate immunity in plants and animals: Striking similarities and obvious differences. Immunol. Rev. 198:249-266.
56. O'Brien, T. P., and Thimann, K. V. 1965. Histological studies on the coleoptile. I. Tissue and cell types in the coleoptile tip. Am. J. Bot. 52:910-918.
57. Papadopoulou, K., Melton, R. E., Leggett, M., Daniels, M. J., and Osbourn, A. E. 1999. Compromised disease resistance in saponin-deficient plants. Proc. Natl. Acad. Sci. U.S.A. 96:12923-12928.
58. Rep, M. 2005. Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 253:19-27.
59. Rusterucci, C., Aviv, D. H., Holt, B. F., III, Dangl, J. L., and Parker, J. E. 2001. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13:2211-2224.
60. Schweizer, P., Gees, R., and Mosinger, E. 1993. Effect of jasmonic acid on the interaction of barley (Hordeum vulgare L.) with the powdery mildew Erysiphe graminis f.sp. hordei. Plant Physiol. 102:503-511.
61. Shetty, N. P., Jorgensen, H. J. L., Jensen, J. D., Collinge, D. B., and Shetty, H. S. 2008. Roles of reactive oxygen species in interactions between plants and pathogens. Eur. J. Plant Pathol. 121:267-280.
62. Shimada, T., Yamada, K., Kataoka, M., Nakaune, S., Koumoto, Y., Kuroyanagi, M., Tabata, S., Kato, T., Shinozaki, K., Seki, M., Kobayashi, M., Kondo, M., Nishimura, M., and Hara-Nishimura, I. 2003. Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J. Biol. Chem. 278:32292-32299.
63. Sidhu, G., and Person, C. 1971. Genetic control of virulence in Ustilago hordei. II. Segregation for higher levels of virulence. Can. J. Genet. Cytol. 13:173-178.
64. Sidhu, G. S., and Person, C. 1972. Genetic control of virulence in Ustilago hordei. III Identification of genes for host resistance and demonstration of a gene-for-gene relationship. Can. J. Genet. Cytol. 14:209-213.
65. Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Metraux, J. P., and Raskin, I. 1995. Salicylic acid in rice (biosynthesis, conjugation, and possible role). Plant Physiol. 108:633-639.
66. Sun, J.-Y., Gaudet, D. A., Lu, Z.-X., Frick, M., Puchalski, B., and Laroche, A. 2008. Characterization and antifungal properties of wheat nonspecific lipid transfer proteins. Mol. Plant-Microbe Interact. 21:346-360.
67. Tapke, V. F. 1945. New physiologic races of Ustilago hordei. Phytopathology 35:970-976.
68. Tenhaken, R., Levine, A., Brisson, L. F., Dixon, R. A., and Lamb, C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. U.S.A. 92:4158-4163.
69. Thomas, P. L. 1991. Genetics of small-grain smuts. Ann. Rev. Phytopathol. 29:137-148.
70. Thordal-Christensen, H. 2003. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6:351-357.
71. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-1194.
72. Truman, W., Zabala, M. T., and Grant, M. 2006. Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J. 46:14-33.
73. Tsuba, M., Katagiri, C., Takeuchi, Y., Takada, Y., and Yamaoka, N. 2002. Chemical factors of the leaf surface involved in the morphogenesis of Blumeria graminis. Physiol. Mol. Plant Pathol. 60:51-57.
74. Vallélian-Bindschedler, L., Métraux, J.-P., and Schweizer, P. 1998. Salicylic acid accumulation in barley is pathogen specific but not required for defense- gene activation. Mol. Plant-Microbe Interact. 11:702-705.
75. Veronese, P., Ruiz, M. T., Coca, M. A., Hernandez-Lopez, A., Lee, H., Ibeas, J. I., Damsz, B., Pardo, J. M., Hasegawa, P. M., Bressan, R. A., and Narasimhan, M. L. 2003. In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiol. 131:1580-1590.
76. Vleeshouwers, V. G. A. A., van Dooijeweert, W., Govers, F., Kamoun, S., and Colon, L. T. 2000. The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210:853-864.
77. Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wiederhold, D. L., Alexander, D. C., Ahl-Goy, P., Metraux, J. P., and Ryals, J. A. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085-1094.
78. Wiermer, M., Feys, B. J., and Parker, J. E. 2005. Plant immunity: The EDS1 regulatory node. Curr. Opin. Plant Biol. 8:383-389.
79. Woolman, H. M. 1930. Infection phenomena and host reactions caused by Tilletia tritici in susceptible and nonsusceptible varieties of wheat. Phytopathology 20:637-652.
80. Wright, G. W., and Simon, R. M. 2003. A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 19:2448-2455.