Pushing the boundaries of resistance: Insights from brachypodium-rust interactions

Frontiers in Plant Science

Volumn 6, Issue JULY, 2015, Pages

  Figueroa, Melania ^a   Castell Miller, Claudia V ^a   Li, Feng ^a   Hulbert, Scot H ^b   Bradeen, James M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Brachypodium; Non host resistance; Plant immunity; Puccinia; Rust fungi

Indexed keywords

BRACHYPODIUM; BRACHYPODIUM DISTACHYON; HORDEUM; LILIOPSIDA; POACEAE; PUCCINIA; TRITICUM AESTIVUM; UREDINALES;

EID: 84938412622     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00558     Document Type: Article

References (127)

1. Al-Kherb, S. M., Roelfs, A., and Groth, J. (1987). Diversity for virulence in a sexually reproducing population of Puccinia coronata. Can. J. Bot. 65, 994–998. doi: 10.1139/b87-137
2. Alves, S. C., Worland, B., Thole, V., Snape, J. W., Bevan, M. W., and Vain, P. (2009). A protocol for Agrobacterium-mediated transformation of Brachypodium distachyon community standard line Bd21. Nat. Protoc. 4, 638–649. doi: 10.1038/nprot.2009.30
3. Anderson, C. L., Bremer, K., and Friis, E. M. (2005). Dating phylogenetically basal eudicots using rbcL sequences and multiple fossil reference points. Am. J. Bot. 92, 1737–1748. doi: 10.3732/ajb.92.10.1737
4. Anikster, Y. (1984). “The formae speciales,” in The Cereals Rusts, Vol 1, eds W. R. Bushnell and A. P. Roelfs (Orlando, FL: Academic Press, Inc.), 124–137.
5. Ayliffe, M., Singh, D., Park, R., Moscou, M. J., and Pryor, T. (2013). The infection of Brachypodium distachyon with selected grass rust pathogens. Mol. Plant Microbe Interact. 26, 946–957. doi: 10.1094/MPMI-01-13-0017-R
6. Ayliffe, M. A., Jin, Y., Kang, Z., Persson, M., Steffenson, B., Wang, S., et al. (2011). Determining the basis of nonhost resistance in rice to cereal rusts. Euphytica 179, 33–40. doi: 10.1007/s10681-010-0280-2
7. Azhaguvel, P., Li, W., Rudd, J. C., Gill, B. S., Michels, G., and Weng, Y. (2009). Aphid feeding response and microsatellite-based genetic diversity among diploid Brachypodium distachyon (L.) Beauv accessions.Plant Gen. Res. 7, 72–79. doi: 10.1017/S1479262108994235
8. Barbieri, M., Marcel, T. C., and Niks, R. E. (2011). Host status of false brome grass to the leaf rust fungus Puccinia brachypodii and the stripe rust fungus P. striiformis. Plant Dis. 95, 1339–1345. doi: 10.1094/PDIS-11-10-0825
9. Barbieri, M., Marcel, T. C., Niks, R. E., Francia, E., Pasquariello, M., Mazzamurro, V., et al. (2012). QTLs for resistance to the false brome rust Puccinia brachypodii in the model grass Brachypodium distachyon L. Genome 55, 152–163. doi: 10.1139/g2012-001
10. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., and Nekrasov, V. (2013). Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9, 39. doi: 10.1186/1746-4811-9-39
11. Bettgenhaeuser, J., Gilbert, B., Ayliffe, M., and Moscou, M. J. (2014). Nonhost resistance to rust pathogens–a continuation of continua.Front. Plant Sci. 5:664. doi: 10.3389/fpls.2014.00664
12. Bewley, J., Bradford, K., Hilhorst, H., and Nonogaki, H. (2012). Seeds: Physiology of Development, Germination and Dormancy. New York: Springer-Verlag.
13. Biffen, R. H. (1907). Studies in the inheritance of disease-resistance. J. Agric. Sci. 2, 109–128. doi: 10.1017/S0021859600001234
14. Bossolini, E., Wicker, T., Knobel, P. A., and Keller, B. (2007). Comparison of orthologous loci from small grass genomes Brachypodiumand rice: implications for wheat genomics and grass genome annotation. Plant J. 49, 704–717. doi: 10.1111/j.1365-313X.2006.02991.x
15. Bragg, J. N., Wu, J., Gordon, S. P., Guttman, M. E., Thilmony, R., Lazo, G. R., et al. (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
16. Brand, A., and Gow, N. A. (2012). “Tropic orientation responses of pathogenic fungi,” in Morphogenesis and Pathogenicity in Fungi, eds J. Pérez-Martín and A. Di Pietro (Heidelberg: Springer), 21–41. doi: 10.1007/978-3-642-22916-9_2
17. Brkljacic, J., Grotewold, E., Scholl, R., Mockler, T., Garvin, D. F., Vain, P., et al. (2011). Brachypodium as a model for the grasses: today and the future. Plant Physiol. 157, 3–13. doi: 10.1104/pp.111.179531
18. Catalán, P., Müller, J., Hasterok, R., Jenkins, G., Mur, L. A., Langdon, T., et al. (2012). Evolution and taxonomic split of the model grassBrachypodium distachyon. Ann. Bot. 109, 385–405. doi: 10.1093/aob/mcr294
19. Catanzariti, A.-M., Dodds, P. N., and Ellis, J. G. (2007). Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol. Lett.269, 181–188. doi: 10.1111/j.1574-6968.2007.00684.x
20. Catanzariti, A. M., Dodds, P. N., Lawrence, G. J., Ayliffe, M. A., and Ellis, J. G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18, 243–256. doi: 10.1105/tpc.105.035980
21. Chapman, G. P. (1996). The Biology of Grasses. Salisbury: CAB International.
22. Chaw, S.-M., Chang, C.-C., Chen, H.-L., and Li, W.-H. (2004). Dating the monocot–dicot divergence and the origin of core eudicots using whole chloroplast genomes. J. Mol. Evol. 58, 424–441. doi: 10.1007/s00239-003-2564-9
23. Chawade, A., Sikora, P., Bräutigam, M., Larsson, M., Vivekanand, V., Nakash, M. A., et al. (2010). Development and characterization of an oat TILLING-population and identification of mutations in lignin and β-glucan biosynthesis genes. BMC Plant Biol. 10:86. doi: 10.1186/1471-2229-10-86
24. Chen, H., He, H., Zhou, F., Yu, H., and Deng, X. W. (2013). Development of genomics-based genotyping platforms and their applications in rice breeding. Curr. Opin. Plant Biol. 16, 247–254. doi: 10.1016/j.pbi.2013.04.002
25. Chen, X., and Ronald, P. C. (2011). Innate immunity in rice. Trends Plant Sci. 16, 451–459. doi: 10.1016/j.tplants.2011.04.003
26. Cummins, G. B. (1971). The Rust Fungi of Cereals, Grasses, and Bamboos. New York, NY: Spinger-Verlag.
27. Dangl, J. L., Horvath, D. M., and Staskawicz, B. J. (2013). Pivoting the plant immune system from dissection to deployment. Science 341, 746–751. doi: 10.1126/science.1236011
28. Dangl, J. L., and Jones, J. D. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826–833. doi: 10.1038/35081161
29. Davies, T. J., Barraclough, T. G., Chase, M. W., Soltis, P. S., Soltis, D. E., and Savolainen, V. (2004). Darwin’s abominable mystery: insights from a supertree of the angiosperms. Proc. Natl. Acad. Sci. U.S.A. 101, 1904–1909. doi: 10.1073/pnas.0308127100
30. Davis, R. H., and Perkins, D. D. (2002). Neurospora: a model of model microbes. Nat. Rev. Genet. 3, 397–403. doi: 10.1038/nrg797
31. Dodds, P. N., and Rathjen, J. P. (2010). Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11, 539–548. doi: 10.1038/nrg2812
32. Douchkov, D., Lueck, S., Johrde, A., Nowara, D., Himmelbach, A., Rajaraman, J., et al. (2014). Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi. Genome Biol. 15, 518. doi: 10.1186/s13059-014-0518-8
33. Draper, J., Mur, L. A. J., Jenkins, G., Ghosh-Biswas, G. C., Bablak, P., Hasterok, R., et al. (2001). Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol. 127, 1539–1555. doi: 10.1104/pp.010196
34. Duplessis, S., Cuomo, C. A., Lin, Y. C., Aerts, A., Tisserant, E., Veneault-Fourrey, C., et al. (2011). Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl. Acad. Sci. U.S.A. 108, 9166–9171. doi: 10.1073/pnas.1019315108
35. Dyck, P., Samborski, D., and Anderson, R. (1966). Inheritance of adult-plant leaf rust resistance derived from the common wheat varieties Exchange and Frontana. Can. J. Genet. Cytol. 8, 665–671. doi: 10.1139/g66-082
36. Ellis, J. (2006). Insights into nonhost disease resistance: can they assist disease control in agriculture? Plant Cell 18, 523–528. doi: 10.1105/tpc.105.040584
37. Ellis, J. G., Lagudah, E. S., Spielmeyer, W., and Dodds, P. N. (2014). The past, present and future of breeding rust resistant wheat. Front. Plant Sci. 5:641. doi: 10.3389/fpls.2014.00641
38. Falter, C., and Voigt, C. A. (2014). Comparative cellular analysis of pathogenic fungi with a disease incidence in Brachypodium distachyonand Miscanthus × giganteus. Bioenergy Res. 7, 958–973. doi: 10.1007/s12155-014-9439-3
39. Febrer, M., Goicoechea, J. L., Wright, J., Mckenzie, N., Song, X., Lin, J., et al. (2010). An integrated physical, genetic and cytogenetic map of Brachypodium distachyon, a model system for grass research. PLoS ONE 5:e13461. doi: 10.1371/journal.pone.0013461
40. Ferreira, S., Pitz, K., Manshardt, R., Zee, F., Fitch, M., and Gonsalves, D. (2002). Virus coat protein transgenic papaya provides practical control of papaya ringspot virus in Hawaii. Plant Dis. 86, 101–105. doi: 10.1094/PDIS.2002.86.2.101
41. Figueroa, M., Alderman, S., Garvin, D. F., and Pfender, W. F. (2013). Infection of Brachypodium distachyon by formae speciales ofPuccinia graminis: early infection events and host-pathogen incompatibility. PLoS ONE 8:e56857. doi: 10.1371/journal.pone.0056857
42. Fitzgerald, T. L., Powell, J. J., Schneebeli, K., Hsia, M. M., Gardiner, D. M., Bragg, J. N., et al. (2015). Brachypodium as an emerging model for cereal–pathogen interactions. Ann. Bot. 115, 717–731. doi: 10.1093/aob/mcv010
43. Flor, H. (1971). Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275–296. doi: 10.1146/annurev.py.09.090171.001423
44. Fu, Z. Q., and Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839–863. doi: 10.1146/annurev-arplant-042811-105606
45. Gale, M., and Devos, K. (1998). Plant comparative genetics after 10 years. Science 282, 656–659. doi: 10.1126/science.282.5389.656
46. Garnica, D. P., Nemri, A., Upadhyaya, N. M., Rathjen, J. P., and Dodds, P. N. (2014). The ins and outs of rust haustoria. PLoS Pathog.10:e1004329. doi: 10.1371/journal.ppat.1004329
47. Garvin, D. F. (2011). “Investigating rust resistance with the model grass Brachypodium,” in Proceedings of the 2011 Borlaug Global Rust Initiative Technical Workshop, June 13–19, ed. R. McIntosh (St. Paul, MN), 89–91.
48. Garvin, D. F., Mckenzie, N., Vogel, J. P., Mockler, T. C., Blankenheim, Z. J., Wright, J., et al. (2010). An SSR-based genetic linkage map of the model grass Brachypodium distachyon. Genome 53, 1–13. doi: 10.1139/G09-079
49. Gill, U. S., Uppalapati, S. R., Nakashima, J., and Mysore, K. S. (2015). Characterization of Brachypodium distachyon as a nonhost model against switchgrass rust pathogen Puccinia emaculata. BMC Plant Biol. 15:113. doi: 10.1186/s12870-015-0502-9
50. Goff, S. A., Ricke, D., Lan, T.-H., Presting, G., Wang, R., Dunn, M., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp.japonica). Science 296, 92–100. doi: 10.1126/science.1068275
51. Gordon, S., Priest, H., Des Marais, D., Schackwitz, W., Figueroa, M., Martin, J., et al. (2013). Genome diversity in Brachypodium distachyon: deep sequencing of highly diverse inbred lines Plant J. 79, 361–374. doi: 10.1111/tpj.12569
52. Guarente, L., and Kenyon, C. (2000). Genetic pathways that regulate ageing in model organisms. Nature 408, 255–262. doi: 10.1038/35041700
53. Gutierrez-Gonzalez, J. J., Tu, Z. J., and Garvin, D. F. (2013). Analysis and annotation of the hexaploid oat seed transcriptome. BMC Genomics 14:471. doi: 10.1186/1471-2164-14-471
54. Harder, D. (1984). “Developmental ultrastructure of hyphae and spores,” in The Cereal Rusts, Vol 1. eds W. R. Bushnell and A. P. Roelfs (Orlando, FL: Academic Press, Inc.) 333–373.
55. Harder, D. E., and Chong, J. (1984). “Structure and Physiology of Haustoria,” in The Cereal Rusts, Vol 1, W. R. Bushnell and A. P. Roelfs (Orlando, FL: Academic Press, Inc.), 416–460. doi: 10.1016/b978-0-12-148401-9.50020-0
56. Heath, M. C. (1981). A generalized concept of host-parasite specificity. Phytopathology 71, 1121–1123. doi: 10.1094/Phyto-71-1121
57. Heath, M. C. (1997). Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann. Bot. 80, 713–720. doi: 10.1006/anbo.1997.0507
58. Heath, M. C. (2000). Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3, 315–319. doi: 10.1016/S1369-5266(00)00087-X
59. 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. doi: 10.1126/science.235.4796.1659
60. Hogenhout, S. A., Van Der Hoorn, R. A., Terauchi, R., and Kamoun, S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 22, 115–122. doi: 10.1094/MPMI-22-2-0115
61. Huitema, E., Vleeshouwers, V. G., Francis, D. M., and Kamoun, S. (2003). Active defence responses associated with non-host resistance ofArabidopsis thaliana to the oomycete pathogen Phytophthora infestans. Mol. Plant Pathol 4, 487–500. doi: 10.1046/j.1364-3703.2003.00195.x
62. Huo, N., Lazo, G. R., Vogel, J. P., You, F. M., Ma, Y., Hayden, D. M., et al. (2008). The nuclear genome of Brachypodium distachyon: analysis of BAC end sequences. Funct. Integr. Genomics 8, 135–147. doi: 10.1007/s10142-007-0062-7
63. International Barley Genome Sequencing Consortium, Mayer, K. F., Waugh, R., Brown, J. W., Schulman, A., Langridge, P., et al. (2012). A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–716. doi: 10.1038/nature11543
64. International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463, 763–768. doi: 10.1038/nature08747
65. Jenkins, G., Hasterok, R., and Draper, J. (2003). “Building the molecular cytogenetic infrastructure of a new model grass,” in Application of Novel Cytogenetic and Molecular Techniques in Genetics and Breeding of the Grasses, eds Z. Zwierzykowski, M. Surma, and P. Kachlicki (Poznan: Polish Academy of Sciences), 77–84.
66. Jin, Y., Szabo, L. J., and Carson, M. (2010). Century-old mystery of Puccinia striiformis life history solved with the identification ofBerberis as an alternate host. Phytopathology 100, 432–435. doi: 10.1094/PHYTO-100-5-0432
67. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286
68. Khatib, M., Lafitte, C., Esquerré-Tugayé, M. T., Bottin, A., and Rickauer, M. (2004). The CBEL elicitor of Phytophthora parasitica var.nicotianae activates defence in Arabidopsis thaliana via three different signalling pathways. New Phytol. 162, 501–510. doi: 10.1111/j.1469-8137.2004.01043.x
69. Koeck, M., Hardham, A. R., and Dodds, P. N. (2011). The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell. Microbiol. 13, 1849–1857. doi: 10.1111/j.1462-5822.2011.01665.x
70. Krattinger, S. G., Lagudah, E. S., Spielmeyer, W., Singh, R. P., Huerta-Espino, J., Mcfadden, H., et al. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360–1363. doi: 10.1126/science.1166453
71. Lawrence, G. J., Dodds, P. N., and Ellis, J. G. (2007). Rust of flax and linseed caused by Melampsora lini. Mol. Plant Pathol. 8, 349–364. doi: 10.1111/j.1364-3703.2007.00405.x
72. Lee, H. A., Kim, S. Y., Oh, S. K., Yeom, S. I., Kim, S. B., Kim, M. S., et al. (2014). Multiple recognition of RXLR effectors is associated with nonhost resistance of pepper against Phytophthora infestans. New Phytol. 203, 926–938. doi: 10.1111/nph.12861
73. Leonard, K., and Martinelli, J. (2005). Virulence of oat crown rust in Brazil and Uruguay. Plant Dis. 89, 802–808. doi: 10.1094/PD-89-0802
74. Leonard, K. J., and Szabo, L. J. (2005). Pathogen profile. Stem rust of small grains and grasses caused by Puccinia graminis. Mol. Plant Pathol. 6, 489–489. doi: 10.1111/j.1364-3703.2005.00299.x
75. Lipka, U., Fuchs, R., Kuhns, C., Petutschnig, E., and Lipka, V. (2010). Live and let die–Arabidopsis nonhost resistance to powdery mildews. Eur. J. Cell Biol. 89, 194–199. doi: 10.1016/j.ejcb.2009.11.011
76. Lius, S., Manshardt, R. M., Fitch, M. M., Slightom, J. L., Sanford, J. C., and Gonsalves, D. (1997). Pathogen-derived resistance provides papaya with effective protection against papaya ringspot virus. Mol. Breed. 3, 161–168. doi: 10.1023/A:1009614508659
77. López-Alvarez, D., López-Herranz, M. L., Betekhtin, A., and Catalán, P. (2012). A DNA barcoding method to discriminate between the model plant Brachypodium distachyon and its close relatives B. stacei and B. hybridum (Poaceae). PloS ONE 7:e51058. doi: 10.1371/journal.pone.0051058
78. Maier, W., Begerow, D., Weiß, M., and Oberwinkler, F. (2003). Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Can. J. Bot. 81, 12–23. doi: 10.1139/b02-113
79. Mayer, K. F., Rogers, J., Doležel, J., Pozniak, C., Eversole, K., Feuillet, C., et al. (2014). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 1251788. doi: 10.1126/science.1251788
80. Miklos, G. L. G., and Rubin, G. M. (1996). The role of the genome project in determining gene function: insights from model organisms. Cell 86, 521–529. doi: 10.1016/S0092-8674(00)80126-9
81. Monaghan, J., and Zipfel, C. (2012). Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349–357. doi: 10.1016/j.pbi.2012.05.006
82. Mur, L. A., Allainguillaume, J., Catalan, P., Hasterok, R., Jenkins, G., Lesniewska, K., et al. (2011). Exploiting the Brachypodium tool box in cereal and grass research. New Phytol. 191, 334–347. doi: 10.1111/j.1469-8137.2011.03748.x
83. Mysore, K. S., and Ryu, C. M. (2004). Nonhost resistance: how much do we know? Trends Plant Sci. 9, 97–104. doi: 10.1016/j.tplants.2003.12.005
84. Nirmala, J., Drader, T., Chen, X., Steffenson, B., and Kleinhofs, A. (2010). Stem rust spores elicit rapid RPG1 phosphorylation. Mol. Plant Microbe Interact. 23, 1635–1642. doi: 10.1094/MPMI-06-10-0136
85. Nirmala, J., Drader, T., Lawrence, P. K., Yin, C., Hulbert, S., Steber, C. M., et al. (2011). Concerted action of two avirulent spore effectors activates Reaction to Puccinia graminis 1 (Rpg1)-mediated cereal stem rust resistance. Proc. Natl. Acad. Sci. U.S.A. 108, 14676–14681. doi: 10.1073/pnas.1111771108
86. O’Driscoll, A., Doohan, F., and Mullins, E. (2015). Exploring the utility of Brachypodium distachyon as a model pathosystem for the wheat pathogen Zymoseptoria tritici. BMC Res. Notes 8:132. doi: 10.1186/s13104-015-1097-9
87. Oerke, E.-C. (2006). Crop losses to pests. J. Agric. Sci. 144, 31–43. doi: 10.1017/S0021859605005708
88. Panstruga, R., and Dodds, P. N. (2009). Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324, 748–750. doi: 10.1126/science.1171652
89. Panwar, V., Mccallum, B., and Bakkeren, G. (2013). Endogenous silencing of Puccinia triticina pathogenicity genes through in planta-expressed sequences leads to the suppression of rust diseases on wheat. Plant J. 73, 521–532. doi: 10.1111/tpj.12047
90. Park, R. (2008). Breeding cereals for rust resistance in Australia. Plant Pathol. 57, 591–602. doi: 10.1111/j.1365-3059.2008.01836.x
91. Pennisi, E. (2010). Armed and dangerous. Science 327, 804–805. doi: 10.1126/science.327.5967.804
92. 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, 100–114. doi: 10.1186/1471-2229-11-100
93. Phillips, R. L., and Freeling, M. (1998). Plant genomics and our food supply: an introduction. Proc. Natl. Acad. Sci. U.S.A. 95, 1969–1970. doi: 10.1073/pnas.95.5.1969
94. Piquerez, S. J. M., Harvey, S. E., Beynon, J. L., and Ntoukakis, V. (2014). Improving crop disease resistance: lessons from research onArabidopsis and tomato. Front. Plant Sci. 5:671. doi: 10.3389/fpls.2014.00671
95. Popp, J., and Hantos, K. (2011). The impact of crop protection on agricultural production. Stud. Agric. Econ. 113, 47–66. doi: 10.7896/j.1003
96. Pretorius, Z. A., Singh, R. P., Wagoire, W. W., and Payne, T. S. (2000). Detection of virulence to wheat stem rust resistance gene Sr31 inPuccinia graminis. f. sp. tritici in Uganda. Plant Dis. 84, 203. doi: 10.1094/PDIS.2000.84.2.203B
97. Project, I. R. G. S. (2005). The map-based sequence of the rice genome. Nature 436, 793–800. doi: 10.1038/nature03895
98. Ray, D. K., Mueller, N. D., West, P. C., and Foley, J. A. (2013). Yield trends are insufficient to double global crop production by 2050.PLoS ONE 8:e66428. doi: 10.1371/journal.pone.0066428
99. Replansky, T., Koufopanou, V., Greig, D., and Bell, G. (2008). Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol. Evol. 23, 494–501. doi: 10.1016/j.tree.2008.05.005
100. Risk, J. M., Selter, L. L., Chauhan, H., Krattinger, S. G., Kumlehn, J., Hensel, G., et al. (2013). The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotech. J. 11, 847–854. doi: 10.1111/pbi.12077
101. Roelfs, A. P., Singh, R. P., and Saari, E. E. (eds). (1992). Rust Diseases of Wheat: Concepts and Methods of Disease Management. Mexico, DF: CIMMYT.
102. Routledge, A. P., Shelley, G., Smith, J. V., Talbot, N. J., Draper, J., and Mur, L. A. (2004). Magnaporthe grisea interactions with the model grass Brachypodium distachyon closely resemble those with rice (Oryza sativa). Mol. Plant Pathol. 5, 253–265. doi: 10.1111/j.1364-3703.2004.00224.x
103. Sandoya, G. V., and de Oliveira Buanafina, M. M. (2014). Differential responses of Brachypodium distachyon genotypes to insect and fungal pathogens. Physiol. Mol. Plant Pathol. 85, 53–64. doi: 10.1016/j.pmpp.2014.01.001
104. Schneebeli, K., Mathesius, U., and Watt, M. (2014). Brachypodium distachyon is a pathosystem model for the study of the wheat disease rhizoctonia root rot. Plant Pathol. 64, 91–100. doi: 10.1111/ppa.12227
105. Schulze-Lefert, P., and Panstruga, R. (2011). A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16, 117–125. doi: 10.1016/j.tplants.2011.01.001
106. Schumann, G. L. (1991). Plant Diseases: Their Biology and Social Impact. St. Paul, MN: APS Press.
107. Scoles, G., Filiz, E., Ozdemir, B., Budak, F., Vogel, J., Tuna, M., et al. (2009). Molecular, morphological, and cytological analysis of diverseBrachypodium distachyon inbred lines. Genome 52, 876–890. doi: 10.1139/G09-062
108. Shukla, K., and Srivastava, S. (2014). Evaluation of finger millet incorporated noodles for nutritive value and glycemic index. J. Food Sci. Technol. 51, 527–534. doi: 10.1007/s13197-011-0530-x
109. Singh, R. (1993). Genetic association of gene Bdv1 for tolerance to barley yellow dwarf virus with genes Lr 34 and Yr18 for adult plant resistance to rusts in bread wheat. Plant Dis. 77, 1103–1106. doi: 10.1094/PD-77-1103
110. Singh, R. P., Hodson, D. P., Jin, Y., Huerta-Espino, J., Kinyua, M., Wanyera, R., et al. (2006). Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Rev. 1, 54. doi: 10.1079/PAVSNNR20061054
111. Somerville, C. (2007). Biofuels. Curr. Biol. 17, R115–R119. doi: 10.1016/j.cub.2007.01.010
112. Staples, R. C., and Macko, V. (2004). “Germination of urediniospores and differentiation of infection structures,” in The Cereal Rusts, Vol. 1, eds W. R. Bushell and A. P. Roelfs (Academic Press, Inc.), 250–282.
113. Stotz, H. U., Mitrousia, G. K., De Wit, P. J., and Fitt, B. D. (2014). Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci. 19, 491–500. doi: 10.1016/j.tplants.2014.04.009
114. 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. doi: 10.1093/jxb/err333
115. Tilman, D., Balzer, C., Hill, J., and Befort, B. L. (2011). Global food demand and the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. U.S.A. 108, 20260–20264. doi: 10.1073/pnas.1116437108
116. Tricoll, D. M., Carney, K. J., Russell, P. F., Mcmaster, J. R., Groff, D. W., Hadden, K. C., et al. (1995). Field evaluation of transgenic squash containing single or multiple virus coat protein gene constructs for resistance to cucumber mosaic virus, watermelon mosaic virus 2, and zucchini yellow mosaic virus. Nat. Biotechnol. 13, 1458–1465. doi: 10.1038/nbt1295-1458
117. Upadhyaya, N. M., Garnica, D. P., Karaoglu, H., Sperschneider, J., Nemri, A., Xu, B., et al. (2015). Comparative genomics of Australian isolates of the wheat stem rust pathogen Puccinia graminis f. sp. tritici reveals extensive polymorphism in candidate effector genes.Front. Plant Sci. 5:759. doi: 10.3389/fpls.2014.00759
118. US Census Bureau. (2015). International Data Base. Available at:http://www.census.gov/population/international/data/worldpop/table_population.php
119. Vogel, J., and Bragg, J. (2009). “Brachypodium distachyon, a new model for the Triticeae,” in Genetics and Genomics of the Triticeae, eds C. Feuillet and G. J. Muehlbauer (New York: Springer), 427–449. doi: 10.1007/978-0-387-77489-3_16
120. Vogel, J., and Hill, T. (2008). High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep. 27, 471–478. doi: 10.1007/s00299-007-0472-y
121. Vogel, J. P., Garvin, D. F., Leong, O. M., and Hayden, D. M. (2006a). Agrobacterium-mediated transformation and inbred line development in the model grass Brachypodium distachyon. Plant Cell Tissue Organ. Cult. 84, 199–211. doi: 10.1007/s11240-005-9023-9
122. Vogel, J. P., Gu, Y. Q., Twigg, P., Lazo, G. R., Laudencia-Chingcuanco, D., Hayden, D. M., et al. (2006b). EST sequencing and phylogenetic analysis of the model grass Brachypodium distachyon. Theor. Appl. Genet. 113, 186–195. doi: 10.1007/s00122-006-0285-3
123. Vogel, J. P., Tuna, M., Budak, H., Huo, N., Gu, Y. Q., and Steinwand, M. A. (2009). Development of SSR markers and analysis of diversity in Turkish populations of Brachypodium distachyon. BMC Plant Biol. 9:88. doi: 10.1186/1471-2229-9-88
124. Wahl, I., Anikster, Y., Manisterski, J., and Segal, A. (1984). “Evolution at the center of origin,” in The Cereal Rusts, Vol. 1, Origins, Specificity, Structure, and Physiology, eds W. R. Bushnell and A. P. Roelfs (Orlando: Academic Press, Inc), 39–77.
125. Woodham-Smith, C. (1991). The Great Hunger: Ireland 1845–1849. London: Penguin books.
126. Yin, C., Park, J.-J., Gang, D. R., and Hulbert, S. H. (2014). Characterization of a tryptophan 2-monooxygenase gene from Puccinia graminis f. sp. tritici involved in auxin biosynthesis and rust pathogenicity. Mol. Plant Microbe Interact. 27, 227–235. doi: 10.1094/MPMI-09-13-0289-FI
127. Zhong, S., Ali, S., Leng, Y., Wang, R., and Garvin, D. F. (2014). Brachypodium distachyon–Cochliobolus sativus pathosystem is a new model for studying plant–fungal interactions in cereal crops. Phytopathology 105, 482–489. doi: 10.1094/PHYTO-08-14-0214-R