Enhanced disease resistance caused by BRI1 mutation is conserved between Brachypodium distachyon and barley (Hordeum vulgare)

Molecular Plant-Microbe Interactions

Volumn 27, Issue 10, 2014, Pages 1095-1106

  Goddard, R ^a   Peraldi, A ^a   Ridout, C ^a   Nicholson, P ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRACHYPODIUM DISTACHYON; HORDEUM; HORDEUM VULGARE;

VEGETABLE PROTEIN;

ARTICLE; ASCOMYCETES; BRACHYPODIUM; DISEASE RESISTANCE; FLOWER; FUSARIUM; GENETICS; HORDEUM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PLANT CHROMOSOME; PLANT DISEASE; PLANT LEAF; PLANT ROOT; SEEDLING;

ASCOMYCOTA; BRACHYPODIUM; CHROMOSOMES, PLANT; DISEASE RESISTANCE; FLOWERS; FUSARIUM; HORDEUM; MUTATION; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; SEEDLING;

EID: 84907214374     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-03-14-0069-R     Document Type: Article

References (76)

1. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.
2. Achard, P., and Genschik, P. 2009. Releasing the brakes of plant growth: How GAs shutdown DELLA proteins. J. Exp. Bot. 60:1085-1092.
3. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van der Straeten, D., Peng, J. R., and Harberd, N. P. 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91-94.
4. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., and Genschik, P. 2008. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117-2129.
5. Albrecht, C., Boutrot, F., Segonzac, C., Schwessinger, B., Gimenez-Ibanez, S., Chinchilla, D., Rathjen, J. P., De Vries, S. C., and Zipfel, C. 2012. Brassinosteroids inhibit pathogen-associated molecular patterntriggered immune signalling independent of the receptor kinase BAK1. Proc. Natl. Acad. Sci. U.S.A. 109:303-308.
6. Ali, S. S., Kumar, G. B. S, Khan, M., and Doohan, F. M. 2013. Brassinosteroid enhances resistance to Fusarium diseases. Phytopathology 103:1260-1267.
7. Bai G. H., and Shaner, G. 2004. Management and resistance in wheat and barley to Fusarium head blight. Annu. Rev. Phytopathol. 42:135-161.
8. Barbieri, M., Marcel, T. C., Niks, R. E., Francia, E., Pasquariello, M., Mazzamurro, V., Garvin, D. F., and Pecchioni, N. 2012. QTLs for resistance to the false brome rust Puccinia brachypodii in the model grass Brachypodium distachyon L. Genome 55:152-163.
9. Bari, R., and Jones, D. G. J. 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69:473-488.
10. Beccari, G., Covarelli, L., and Nicholson, P. 2011. Infection processes and soft wheat response to root rot and crown rot caused by Fusarium culmorum. Plant Pathol. 60:671-684.
11. Belkhadir, Y., Jailais, Y., Epple, P., Balsemão-Pires, E., Dangl, J. L., and Chory, J. 2012. Brassinosteroids modulate the efficiency of plant immune response to microbe-associated molecular patterns. Proc. Natl. Acad. Sci. U.S.A. 109:297-302.
12. Blein, M., Levrel, A., Lemoine, J., Gautier, V., Chevalier, M., and Barloy, D. 2009. Oculimacula yallundae lifestyle revisited: Relationships between the timing of eyespot symptom appearance, the development of the pathogen and the responses of infected partially resistant wheat plants. Plant Pathol. 58:1-11.
13. Both, M., Csukai, M., Stumpf, M. P. H., and Spanu, P. D. 2005. Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell 17:2107-2122.
14. Bottalico, A., and Perrone, G. 2002. Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur. J. Plant Pathol. 108:611-624.
15. Boyd, L. A., Smith, P. H., Green, R. M., and Brown, J. K. M. 1994. The relationship between the expression of defense-related genes and mildew development in barley. Mol. Plant-Microbe Interact. 7:401-410.
16. Bragg, J. N., Wu, J., Gordon, S. P., Guttman, M. E., Thilmony, R., Lazo, G. R., Gu, Y. Q., and Vogel, J. P. 2012. Generation and characterization of the Western Regional Research Center Brachypodium T-DNA insertional mutant collection. PLoS One 7:e41916. doi:10.1371/journal.pone.0041916. Published online.
17. Brown, J. K. M., and Wolfe, M. S. 1990. Structure and evolution of a population of Erysiphe-graminis f. sp. hordei. Plant Pathol. 39:376-390.
18. Brown, N. A., Urban, M., Van de Meene, A. M. L., and Hammond-Kosack, K. E. 2010. The infection biology of Fusarium graminearum: Defining the pathways of spikelet to spikelet colonisation in wheat ears. Fungal Biol. 114:555-571.
19. Burt, C., Hollins, T. W., Powell., N, and Nicholson, P. 2010. Differential seedling resistance to the eyespot pathogens Oculimacula yallundae and Oculimacula acuformis, conferred by Pch2 in wheat and among accessions of Triticum monococcum. Plant Pathol. 59:819-828.
20. Chandler, P. M., Marion-Poll, A., Ellis, M., and Gubler, F. 2002. Mutants at the Slender1 locus of barley cv. Himalaya. Molecular and physiological characterization. Plant Physiol. 129: 181-190.
21. Chapman, N. H., Burt, C., Dong, H., and Nicholson, P. 2008. The development of PCR based markers for the selection of eyespot resistance genes Pch1 and Pch2. Theor. Appl. Genet. 117:425-433.
22. Chen, G. D., Liu, Y. X., Wei, Y. M., McIntyre, C. L., Zhou, M. X., Zheng, Y. L., and Liu, C. J. 2013. Major QTL for Fusarium crown rot resistance in a barley landrace. Theor. Appl. Genet. 126:2511-2520.
23. Chen, G. D., Yan, W., Liu, Y., Wei, Y. M., Zhou, M. X., Zheng, Y. L., Manners, J. M., and Liu, C. J. 2014. The non-gibberellic acid-responsive semi-dwarfing gene uzu affects Fusarium crown rot resistance in barley. BMC Plant Biol. 14:22. doi:10.1186/1471-2229-14-22. Published online.
24. Chen, X., Steed, A., Travella, S., Keller, B., and Nicholson, P. 2009. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol. 182:975-983.
25. Chono, M., Honda, I., Zeniya, H., Yoneyama, K., Saisho, D., Takeda, K., Takatsuto, S., Hoshino, T., and Watanabe, Y. 2003. A semi dwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol. 133:1209-1219.
26. Clouse S. D., Langford, M., and McMorris, T. C. 1996. A brassinosteroid insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111:671-678.
27. Dalmais, M., Antelme, S., Ho-Yue-Kuang, S., Wang, Y., Darracq, O., Bouvier d'Yvoire, M., Cézard, L., Légée, F., Blondet, E., Oria, N., Troadec, C., Brunaud, V., Jouanin, L., Höfte, H., Bendahmane, A., Lapierre, C., and Sibout, R. 2013. A TILLING Platform for Functional Genomics in Brachypodium distachyon. PLoS One 8:e65503. doi: 10.1371/journal.pone.0065503. Published online.
28. De Vleesschauwer, D., Van Buyten, E., Satoh, K., Balidion, J., Mauleon, R., Choi, I. R., Vera-Cruz, C., Kikuchi, S., and Höfte, M. 2012. Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol. 158:1833-1846.
29. De Vleesschauwer, D., Gheysen, G., and Hofte, M. 2013. Hormone defense networking in rice: Tales from a different world. Trends Plant Sci. 18:555-565.
30. Draper, J., Mur, L. A. J., Jenkins, G., Ghosh-Biswas, G. C., Bablak, P., Hasterok, R., and Routledge, A. P. M. 2001. Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol. 127:1539-1555.
31. Fan, M., Bai, M. Y., Kim, J. G., Wang, T., Oh, E., Chen, L., Park, C. H., Son, S. H., Kim, S. K., Mudgett, M. B., and Wang, Z. Y. 2014. The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26:828-841.
32. Freeman, J., and Ward, E. 2004. Gaeumannomyces graminis, the take-all fungus and its relatives. Mol. Plant Pathol. 5: 235-252.
33. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-227.
34. Honda, I., Zeniya, H., Yoneyama, K., Chono, M., Kaneko, S., and Watanabe, Y. 2003. Uzu mutation in barley (Hordeum vulgare L.) reduces the leaf unrolling response to brassinolide. Biosci. Biotechnol. Biochem. 67:1194-1197.
35. Huo, N., Vogel, J. P., Lazo, G. R., You, F. M., Ma, Y., McMahon, S., Dvorak, J., Anderson, O. D., Luo, M. C., and Gu, Y. Q. 2009. Structural characterization of Brachypodium genome and its syntenic relationship with rice and wheat. Plant Mol. Biol. 70:47-61.
36. International Brachypodium Initiative. 2010. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763-768.
37. Jarosch, B., Jansen, M., and Schaffrath, U. 2003. Acquired resistance functions in mlo barley, which is hypersusceptible to Magnaporthe grisea. Mol. Plant-Microbe Interact. 16:107-114.
38. Kim, T. W., and Wang, Z. Y. 2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61:681-704.
39. Kliebenstein, D. J., and Rowe, H. C. 2008. Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction. Plant Sci. 174:551-556.
40. Knight, N. L., and Sutherland, M. W. 2013. Histopathological assessment of wheat seedling tissues infected by Fusarium pseudograminearum. Plant Pathol. 62:679-687.
41. Koh, S., Lee, S. C., Kim, M. H., Koh, J. H., Lee, S., An, G., Choe, S., and Kim, S. R. 2007. T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol. Biol. 65:453-466.
42. León, J., Rojo, E., and Sánchez-Serrano, J. J. 2001. Wound signalling in plants. J. Exp. Bot. 52:1-9.
43. Lozano-Durán, R., Macho, A. P., Boutrot, F., Segonzac, C., Somssich, I. E., and Zipfel, C. 2013. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. Elife 2:e00983.doi:10.7554/eLife.00983. Published online.
44. Makandar, R., Nalam, V., Chaturvedi, R., Jeannotte, R., Sparks, A. A., and Shah, J. 2010. Involvement of salicylate and jasmonate signalling pathways in Arabidopsis interaction with Fusarium graminearum. Mol. Plant-Microbe Interact. 23:961-970.
45. Makepeace, J. C., Havis, N. D., Burke, J. I., Oxley, S. J. P., and Brown, J. K. M. 2008. A method of inoculating barley seedlings with Ramularia collo-cygni. Plant Pathol. 57:991-999.
46. Malinovsky, F. G., Batoux, M., Schwessinger, B., Youn, J. H., Stransfeld, L., Win, J., Kim, S. K., and Zipfel, C. 2014. Antagonistic regulation of growth and immunity by the Arabidopsis basic helix-loop-helix transcription factor homolog of brassinosteroid enhanced expression 2 interacting with increased leaf inclination binding bHLH1. Plant Physiol. 164:1443-1455.
47. Miedaner, T. 1997. Breeding wheat and rye for resistance to Fusarium diseases. Plant Breed. 116:201-220.
48. Moseman, J. G., Macer, R. C. F., and Greeley, L. W. 1965. Genetic studies with cultures of Erysiphe graminis f. sp. hordei virulent on Hordeum spontaneum. Trans. Br. Mycol. Soc. 48:479-489.
49. Nahar, K., Kyndt, T., Hause, B., Höfte, M., and Gheysen, G. 2013. Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with jasmonate pathway. Mol. Plant-Microbe Interact. 26:106-115.
50. Nakashita, H., Yasuda, M., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., Takatsuto, S., Yamaguchi, I., and Yoshida, S. 2003. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33:887-898.
51. Nam, K. H., and Li, J. 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signalling. Cell 110:203-212.
52. Navarro, L., Bari, R., Achard, P., Lison, P., Memri, A., Harberd, N. P., and Jones, J. D. G. 2008. DELLAs control plant immune responses by modulating the balance and salicylic acid signalling. Curr. Biol. 18:650-655.
53. O'Donnell, P. J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., and Bowles, D. J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914-1917.
54. Parker, D., Beckmann, M., Enot, D. P., Overy, D. P., Rios, Z. C., Gilbert, M., Talbot, N., and Draper, J. 2008. Rice blast infection of Brachypodium distachyon as a model system to study dynamic host/pathogen interactions. Nat. Protocols 3:435-445.
55. Peng, J. R., Richards, D. E., Hartley, N. M., Murphy, G. P., Devos, K. M., Flintham, J. E., Beales, J., Fish, L. J., Worland, A. J., Pelica, F., Sudhakar, D., Christou, P., Snape, J. W., Gale, M. D., and Harberd, N. P. 1999. 'Green revolution' genes encode mutant gibberellins response modulators. Nature 400:256-261.
56. Peraldi, A., Beccari, G., Steed, A., and Nicholson, P. 2011. Brachypodium distachyon: A new pathosystem to study Fusarium head blight and other Fusarium diseases of wheat. BMC Plant Biol. 11:100.
57. Peraldi, A., Griffe, L. L., Burt, C., McGrann, G. R. D., and Nicholson, P. 2013. Brachypodium distachyon exhibits compatible interactions with Oculimacula spp. and Ramularia collo-cygni, providing the first pathosystem model to study eyespot and Ramularia leaf spot diseases. Plant Pathol. 5:35-41.
58. Robert-Seilaniantz, A., Grant, M., and Jones, J. D. G. 2011. Hormone crosstalk in plant disease and defense: More than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:317-343.
59. Routledge, A. P. M., Shelley, G., Smith, J. V., Talbot, N. J., Draper, J., and Mur, L. A. J. 2004. Magnaporthe grisea interactions with the model grass Brachypodium distachyon closely resemble those with rice (Oryza sativa). Mol. Plant Pathol. 5:253-265.
60. Saisho, D., Tanno, K., Chono, M., Honda, I., Kitano, H., and Takeda, K. 2004. Spontaneous Brassinolide-insensitive barley mutants 'uzu' adapted to East Asia. Breed. Sci. 54:409-416.
61. Saville, R. J., Gosman, N., Burt, C. J., Makepeace, J., Steed, A., Corbitt, M., Chandler, E., Brown, J. K. M., Boulton, M. I., and Nicholson, P. 2012. The 'Green Revolution' dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. J. Exp. Bot. 63:1271-1283.
62. Schroeder, H. W., and Christensen, J. J. 1963. Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53:831-838.
63. Scott, P. R. 1971. The effect of temperature on eyespot (Cercosporella herporichoides) in wheat seedlings. Ann. Appl. Biol. 68:169-175.
64. Simpson, D. R., Rezanoor, H. N., Parry, D. W., and Nicholson, P. 2000. Evidence for differential host preference in Microdochium nivale var. majus and Microdochium nivale var. nivale. Plant Pathol. 49:261-268.
65. Stabentheiner, E., Minihofer, T., and Huss, H. 2009. Infection of barley by Ramularia collo-cygni: Scanning electron microscopic investigations. Mycopathologia 168:135-143.
66. Sun, T. P., and Gubler, F. 2004. Molecular mechanism of gibberellin signalling in plants. Annu. Rev. Phytopathol. 55:197-223.
67. Szekeres, M., Németh, K., Koncz-Kálmán, Z., Mathur, J., Kauschmann, A., Altmann, T., Rédei, G. P., Nagy, F., Schell, J., and Csaba, K. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171-182.
68. Thole, V., Peraldi, A., Worland, B., Nicholson, P., Doonan, J. H., and Vain, P. 2012. T-DNA mutagenesis in Brachypodium distachyon. J. Exp. Bot. 63:567-576.
69. Tufan, H. A., McGrann, G. R. D., Magusin, A., Morel, J. B., Miché, L., and Boyd, L. A. 2009. Wheat blast: Histopathology and transcriptome reprogramming in response to adapted and nonadapted Magnaporthe isolates. New Phytol. 184:473-484.
70. Urashima, A. S., Lavorent, N. A., Goulart, A. C. P., and Mehta, Y. R. 2004. Resistance spectra of wheat cultivars and virulence diversity of Magnaporthe grisea isolates in Brazil. Fitopaol. Bras. 29:511-518.
71. Vain, P. 2011. Brachypodium as a model system for grass research. J. Cereal Sci. 54:1-7.
72. Vain, P., Worland, B., Thole, V., McKenzie, N., Alves, S. C., Opanowicz, M., Fish, L. J., Bevan, M. W., and Snape, J. W. 2008. Agrobacteriummediated transformation of the temperate grass Brachypodium distachyon (genotype Bd21) for T-DNA insertional mutagenesis. Plant Biotechnol. J. 6:941-941.
73. Xu, X. M., Monger, W., Ritieni, A., and Nicholson, P. 2007. Effect of temperature and duration of wetness during initial infection periods on disease development, fungal biomass and mycotoxin concentrations on wheat inoculated with single, or combinations of, Fusarium species. Plant Pathol. 56:943-956.
74. Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H., and Matsuoka, M. 2000. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12:1591-1605.
75. Zhao, J., Zheng, S. H., Fujita, K., and Sakai, K. 2004. Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor signalling pathway leading to beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J. Exp. Bot.55:1003-1012.
76. Zhu, J. Y., Sae-Seaw, J., and Wang, Z. Y. 2013. Brassinosteroid signalling. Development 140:1615-1620.