Host versus nonhost resistance: Distinct wars with similar arsenals

Phytopathology

Volumn 105, Issue 5, 2015, Pages 580-587

  Gill, Upinder S ^a   Lee, Seonghee ^a   Mysore, Kirankumar S ^a  

^a PLANT BIOLOGY DIVISION   (United States)

Author keywords

Gene for gene resistance; Plant disease resistance; R gene resistance

Indexed keywords

BACTERIA (MICROORGANISMS);

BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; DISEASE RESISTANCE; FUNGUS; HOST PATHOGEN INTERACTION; HOST RANGE; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; PLANT; PLANT DISEASE;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; DISEASE RESISTANCE; FUNGI; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANTS;

EID: 84928918559     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-11-14-0298-RVW     Document Type: Review

References (113)

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. USA 95:10306-10311.
2. Anikster, Y. 1984. The formae speciales. Pages 115-130 in: The Cereal Rusts. Vol. I. W. R. Bushnell and A. P. Roelfs, eds. Academic Press, Orlando.
3. Antonovics, J., Boots, M., Ebert, D., Koskella, B., Poss, M., and Sadd, B. M. 2013. The origin of specificity by means of natural selection: Evolved and nonhost resistance in host - pathogen interactions. Evolution 67:1-9.
4. Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. I., Venter, E., Avrova, A. O., Rehmany, A. P., Bohme, U., Brooks, K., Cherevach, I., Hamlin, N., White, B., Fraser, A., Lord, A., Quail, M. A., Churcher, C., Hall, N., Berriman, M., Huang, S., Kamoun, S., Beynon, J. L., and Birch, P. R. 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. USA 102:7766-7771.
5. Ashfield, T., Keen, N. T., Buzzell, R. I., and Innes, R. W. 1995. Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. Genetics 141:1597-1604.
6. Assaad, F. F., Qiu, J. L., Youngs, H., Ehrhardt, D., Zimmerli, L., Kalde, M., Wanner, G., Peck, S. C., Edwards, H., Ramonell, K., Somerville, C. R., and Thordal-Christensen, H. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15:5118-5129.
7. Ayliffe, M. A., and Lagudah, E. S. 2004. Molecular genetics of disease resistance in cereals. Ann. Bot. (Lond.) 94:765-773.
8. Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., and Schulze-Lefert, P. 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073-2076.
9. Barrett, L. G., Thrall, P. H., Burdon, J. J., Nicotra, A. B., and Linde, C. C. 2008. Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Mol. Ecol. 17:3401-3415.
10. Bent, A. F., and Mackey, D. 2007. Elicitors, effectors, and R genes: The new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399-436.
11. Boller, T., and He, S. Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744.
12. Burdon, J. J., and Roelfs, A. P. 1985. The Effect of Sexual and Asexual Reproduction on the Isozyme Structure of Populations of Puccinia graminis. American Phytopathological Society, St. Paul, MN.
13. Buschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., van Daelen, R., van der Lee, T., Diergaarde, P., Groenendijk, J., Topsch, S., Vos, P., Salamini, F., and Schulze-Lefert, P. 1997. The barley Mlo gene: A novel control element of plant pathogen resistance. Cell 88:695-705.
14. Buttner, D., and He, S. Y. 2009. Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150:1656-1664.
15. Carver, T. W. L., Thomas, B. J., Ingerson-Morris, S. M., and Roderick, H. W. 1990. The role of abaxial leaf surface waxes of Lolium spp. in resistance to Erysiphe graminis. Plant Pathol. 39:573-583.
16. 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.
17. Christopher-Kozjan, R., and Heath, M. C. 2003. Cytological and pharmacological evidence that biotrophic fungi trigger different cell death execution processes in host and nonhost cells during the hypersensitive response. Physiol. Mol. Plant Pathol. 62:265-275.
18. Cohn, J., Sessa, G., and Martin, G. B. 2001. Innate immunity in plants. Curr. Opin. Immunol. 13:55-62.
19. Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J. L., Huckelhoven, R., Stein, M., Freialdenhoven, A., Somerville, S. C., and Schulze-Lefert, P. 2003. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973-977.
20. Couch, B. C., Fudal, I., Lebrun, M. H., Tharreau, D., Valent, B., van Kim, P., Notteghem, J. L., and Kohn, L. M. 2005. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 170:613-630.
21. Dangl, J. L., Horvath, D. M., and Staskawicz, B. J. 2013. Pivoting the plant immune system from dissection to deployment. Science 341:746-751.
22. Dangl, J. L., and Jones, J. D. G. 2001. Plant pathogens and integrated defense responses to infection. Nature 411:826-833.
23. Day, B., Henty, J. L., Porter, K. J., and Staiger, C. J. 2011. The pathogen-actin connection: A platform for defense signaling in plants. Annu. Rev. Phytopathol. 49:483-506.
24. de la Cruz, F., and Davies, J. 2000. Horizontal gene transfer and the origin of species: Lessons from bacteria. Trends Microbiol. 8:128-133.
25. de Vienne, D. M., Refregier, G., Lopez-Villavicencio, M., Tellier, A., Hood, M. E., and Giraud, T. 2013. Cospeciation vs. host-shift speciation: Methods for testing, evidence from natural associations and relation to coevolution. New Phytol. 198:347-385.
26. Dodds, P. N., Lawrence, G. J., Catanzariti, A. M., Teh, T., Wang, C. I. A., Ayliffe, M. A., Kobe, B., and 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. USA 103:8888-8893.
27. Dodds, P. N., and Rathjen, J. P. 2010. Plant immunity: Towards an integrated view of plant - pathogen interactions. Nat. Rev. Genet. 11:539-548.
28. 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., van der Hoorn, R. A., and Kamoun, S. 2014. Effector specialization in a lineage of the Irish potato famine pathogen. Science 343:552-555.
29. Ellis, J., Dodds, P., and Pryor, T. 2000. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3:278-284.
30. Fan, J., Crooks, C., Creissen, G., Hill, L., Fairhurst, S., Doerner, P., and Lamb, C. 2011. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331:1185-1188.
31. Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296.
32. Freytag, S., Arabatzis, N., Hahlbrock, K., and Schmelzer, E. 1994. Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta 194:123-135.
33. Friesen, T. L., Stukenbrock, E. H., Liu, Z., Meinhardt, S., Ling, H., Faris, J. D., Rasmussen, J. B., Solomon, P. S., McDonald, B. A., and Oliver, R. P. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953-956.
34. Fu, Y., Duan, X., Tang, C., Li, X., Voegele, R. T., Wang, X., Wei, G., and Kang, Z. 2014. TaADF7, an actin-depolymerizing factor, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. Plant J. 78:16-30.
35. Glazebrook, J. 2001. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4:301-308.
36. Griffis, A. H., Groves, N. R., Zhou, X., and Meier, I. 2014. Nuclei in motion: Movement and positioning of plant nuclei in development, signaling, symbiosis, and disease. Front. Plant Sci. 5:129.
37. Grünwald, N. J., and Flier, W. G. 2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171-190.
38. Hafner, M. S., and Nadler, S. A. 1988. Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332:258-259.
39. 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. USA 100:8577-8582.
40. Heath, M. C. 2000. Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3:315-319.
41. Hirano, S. S., and Upper, C. D. 1983. Ecology and epidemiology of foliar bacterial plant pathogens. Annu. Rev. Phytopathol. 21:243-270.
42. 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.
43. Hoefle, C., Loehrer, M., Schaffrath, U., Frank, M., Schultheiss, H., and Huckelhoven, R. 2009. Transgenic suppression of cell death limits penetration success of the soybean rust fungus Phakopsora pachyrhizi into epidermal cells of barley. Phytopathology 99:220-226.
44. Hückelhoven, R., Dechert, C., and Kogel, K. H. 2001. Non-host resistance of barley is associated with a hydrogen peroxide burst at sites of attempted penetration by wheat powdery mildew fungus. Mol. Plant Pathol. 2:199-205.
45. Hückelhoven, R., and Kogel, K. H. 2003. Reactive oxygen intermediates in plant-microbe interactions: Who is who in powdery mildew resistance? Planta 216:891-902.
46. Inuma, T., Khodaparast, S. A., and Takamatsu, S. 2007. Multilocus phylogenetic analyses within Blumeria graminis, a powdery mildew fungus of cereals. Mol. Phylogenet. Evol. 44:741-751.
47. Jarosch, B., Kogel, K. H., and Schaffrath, U. 1999. The ambivalence of the barley Mlo locus: Mutations conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol. Plant-Microbe Interact. 12:508-514.
48. Jin, Y., and Steffenson, B. J. 1999. Puccinia coronata var. hordei var. nov.: Morphology and pathogenicity. Mycologia 91:877-884.
49. Johnston, P. A., Niks, R. E., Meiyalaghan, V., Blanchet, E., and Pickering, R. 2013. Rph22: Mapping of a novel leaf rust resistance gene introgressed from the non-host Hordeum bulbosum L. into cultivated barley (Hordeum vulgare L.). Theor. Appl. Genet. 126:1613-1625.
50. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
51. Kang, L., Tang, X., and Mysore, K. S. 2004. Pseudomonas type III effector AvrPto suppresses the programmed cell death induced by two nonhost pathogens in Nicotiana benthamiana and tomato. Mol. Plant-Microbe Interact. 17:1328-1336.
52. Keen, N., Kobayashi, D., Tamaki, S., Shen, H., Stayton, M., Lawrence, D., Sharma, A., Midland, S., Smith, M., and Sims, J. 1991. Avirulence gene D from Pseudomonas Syringae pv. tomato and its interaction with resistance gene Rpg4 in soybean. Pages 37-44 in: Advances in Molecular Genetics of Plant - Microbe Interactions. Vol. 1. H. Hennecke and D. Verma, eds. Springer, The Netherlands.
53. Kim, M. G., Geng, X., Lee, S. Y., and Mackey, D. 2009. The Pseudomonas syringae type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2. Plant J. 57:645-653.
54. Király, L., Kumar, J., Hückelhoven, R., and Kogel, K. H. 2002. mlo5, a resistance gene effective against a biotrophic pathogen (Blumeria graminis f. sp. hordei) confers enhanced susceptibility of barley to the necrotrophic fungus Bipolaris sorokiniana (teleomorph: Cochliobolus sativus). Acta. Biol. Szeged. 46:135-136.
55. Kobayashi, Y., Yamada, M., Kobayashi, I., and Kunoh, H. 1997. Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant Cell Physiol. 38:725-733.
56. Kumar, J., Huckelhoven, R., Beckhove, U., Nagarajan, S., and Kogel, K. H. 2001. A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91:127-133.
57. Kwon, C., Bednarek, P., and Schulze-Lefert, P. 2008. Secretory pathways in plant immune responses. Plant Physiol. 147:1575-1583.
58. Li, X., Lin, H., Zhang, W., Zou, Y., Zhang, J., Tang, X., and Zhou, J. M. 2005. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc. Natl. Acad. Sci. USA 102:12990-12995.
59. Li, W., Xu, Y. P., Zhang, Z. X., Cao, W. Y., Li, F., Zhou, X., Chen, G. Y., and Cai, X. Z. 2012. Identification of genes required for nonhost resistance to Xanthomonas oryzae pv. oryzae reveals novel signaling components. PLoS ONE 7:e42796.
60. Lipka, U., Fuchs, R., and Lipka, V. 2008. Arabidopsis non-host resistance to powdery mildews. Curr. Opin. Plant Biol. 11:404-411.
61. 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.
62. Loehrer, M., Langenbach, C., Goellner, K., Conrath, U., and Schaffrath, U. 2008. Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol. Plant-Microbe Interact. 21:1421-1430.
63. Lu, M., Tang, X., and Zhou, J. M. 2001. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13:437-447.
64. McGrann, G. R. D., Stavrinides, A., Russell, J., Corbitt, M. M., Booth, A., Chartrain, L., Thomas, W. T. B., and Brown, J. K. M. 2014. A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot. J. Exp. Bot. 65:1025-1037.
65. Mishina, T. E., and Zeier, J. 2007. Bacterial non-host resistance: Interactions of Arabidopsis with non-adapted Pseudomonas syringae strains. Physiol. Plant. 131:448-461.
66. Moreau, M., Degrave, A., Vedel, R., Bitton, F., Patrit, O., Renou, J. P., Barny, M. A., and Fagard, M. 2012. EDS1 contributes to nonhost resistance of Arabidopsis thaliana against Erwinia amylovora. Mol. Plant-Microbe Interact. 25:421-430.
67. Moscou, M. J., Lauter, N., Steffenson, B., and Wise, R. P. 2011. Quantitative and qualitative stem rust resistance factors in barley are associated with transcriptional suppression of defense regulons. PLoS Genet. 7:e1002208.
68. Mysore, K. S., and Ryu, C. M. 2004. Nonhost resistance: How much do we know? Trends Plant Sci. 9:97-104.
69. Nakao, M., Nakamura, R., Kita, K., Inukai, R., and Ishikawa, A. 2011. Non-host resistance to penetration and hyphal growth of Magnaporthe oryzae in Arabidopsis. Sci. Rep. 1:171.
70. Niks, R. E., and Marcel, T. C. 2009. Nonhost and basal resistance: How to explain specificity? New Phytol. 182:817-828.
71. Nimchuk, Z., Eulgem, T., Holt, B. F., 3rd, and Dangl, J. L. 2003. Recognition and response in the plant immune system. Annu. Rev. Genet. 37:579-609.
72. Nyadanu, D., Akromah, R., Adomako, B., Kwoseh, C., Dzahini-Obiatey, H., Lowor, S. T., Akrofi, A. Y., and Assuah, M. K. 2012. Host plant resistance to Phytophthora pod rot in cacao (Theobroma cacao L.): The role of epicuticular wax on pod and leaf surfaces. Int. J. Bot. 8:13-21.
73. Parker, J. E., Holub, E. B., Frost, L. N., Falk, A., Gunn, N. D., and Daniels, M. J. 1996. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8:2033-2046.
74. Peart, J. R., Lu, R., Sadanandom, A., Malcuit, I., Moffett, P., Brice, D. C., Schauser, L., Jaggard, D. A. W., Xiao, S., Coleman, M. J., Dow, M., Jones, J. D. G., Shirasu, K., and Baulcombe, D. C. 2002. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99:10865-10869.
75. Pennisi, E. 2010. Armed and dangerous. Science 327:804-805.
76. Pretorius, Z. A., Singh, R. P., Wagoire, W. W., and Payne, T. S. 2001. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis. 84:203.
77. Raffaele, S., Farrer, R. A., Cano, L. M., Studholme, D. J., MacLean, D., Thines, M., Jiang, R. H., Zody, M. C., Kunjeti, S. G., Donofrio, N. M., Meyers, B. C., Nusbaum, C., and Kamoun, S. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330:1540-1543.
78. Riley, R., and Macer, R. C. F. 1966. The chromosomal distribution of the genetic resistance of rye to wheat pathogens. Can. J. Genet. Cytol. 8:640-653.
79. Roelfs, A. P. 1978. Estimated losses caused by rust in small grain cereals in the United States, 1918-76. U.S. Department of Agriculture, Agricultural Research Service, U.S. Govt. Print. Off., Washington.
80. Roelfs, A. P. 1982. Effects of barberry eradication on stem rust in the United States. Plant Dis. 66:177-181.
81. Rojas, C. M., Senthil-Kumar, M., Wang, K., Ryu, C. M., Kaundal, A., and Mysore, K. S. 2012. Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24:336-352.
82. Rosewich, U. L., and Kistler, H. C. 2000. Role of horizontal gene transfer in the evolution of fungi. Annu. Rev. Phytopathol. 38:325-363.
83. 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.
84. Senthil-Kumar, M., and Mysore, K. S. 2012. Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response. Plant Cell Environ. 35:1329-1343.
85. Senthil-Kumar, M., and Mysore, K. S. 2013. Nonhost resistance against bacterial pathogens: Retrospectives and prospects. Annu. Rev. Phytopathol. 51:407-427.
86. Shan, W., Cao, M., Leung, D., and Tyler, B. M. 2004. The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol. Plant-Microbe Interact. 17:394-403.
87. Shibata, Y., Kawakita, K., and Takemoto, D. 2011. SGT1 and HSP90 are essential for age-related resistance of Nicotiana benthamiana against the oomycete pathogen Phytophathora infestans. Physiol. Mol. Plant Pathol. 75:120-128.
88. Singh, R. P., Hodson, D. P., Huerta-Espino, J., Jin, Y., Bhavani, S., Njau, P., Herrera-Foessel, S., Singh, P. K., Singh, S., and Govindan, V. 2011. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49:465-481.
89. Stam, R., Mantelin, S., McLellan, H., and Thilliez, G. 2014. The role of effectors in nonhost resistance to filamentous plant pathogens. Front. Plant Sci. 5:582.
90. Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B. H., Molina, A., Schulze-Lefert, P., Lipka, V., and Somerville, S. 2006. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731-746.
91. Sumit, R. 2013. Investigation of the Arabidopsis nonhost resistance mechanism against the soybean pathogen, Phytophthora sojae. Graduate Thesis and Dissertations, Iowa State University.
92. Sumit, R., Sahu, B. B., Xu, M., Sandhu, D., and Bhattacharyya, M. K. 2012. Arabidopsis nonhost resistance gene PSS1 confers immunity against an oomycete and a fungal pathogen but not a bacterial pathogen that cause diseases in soybean. BMC Plant Biol. 12:87.
93. Tadege, M., Wen, J., He, J., Tu, H., Kwak, Y., Eschstruth, A., Endre, G., Zhao, P. X., Chabaud, M., Ratet, P., and Mysore, K. S. 2008. Large scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 54:335-347.
94. Takemoto, D., Jones, D. A., and Hardham, A. R. 2003. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J. 33:775-792.
95. Thordal-Christensen, H. 2003. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6:351-357.
96. 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.
97. Uppalapati, S. R., Ishiga, Y., Doraiswamy, V., Bedair, M., Mittal, S., Chen, J. H., Nakashima, J., Tang, Y. H., Tadege, M., Ratet, P., Chen, R. J., Schultheiss, H., and Mysore, K. S. 2012. Loss of abaxial leaf epicuticular wax in Medicago truncatula irg1/palm1 mutants results in reduced spore differentiation of anthracnose and nonhost rust pathogens. Plant Cell 24:353-370.
98. van Baarlen, P., van Belkum, A., Summerbell, R. C., Crous, P. W., and Thomma, B. P. 2007. Molecular mechanisms of pathogenicity: How do pathogenic microorganisms develop cross-kingdom host jumps? FEMS Microbiol. Rev. 31:239-277.
99. van der Biezen, E. A., and Jones, J. D. G. 1998. The NB-ARC domain: A novel signaling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8:R226-R228.
100. van der Hoorn, R. A., and Kamoun, S. 2008. From guard to decoy: A new model for perception of plant pathogen effectors. Plant Cell 20:2009-2017.
101. van Wees, S. C., and Glazebrook, J. 2003. Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. Plant J. 33:733-742.
102. Vega-Arreguin, J. C., Jalloh, A., Bos, J. I., and Moffett, P. 2014. Recognition of an Avr3a homologue plays a major role in mediating nonhost resistance to Phytophthora capsici in Nicotiana species. Mol. Plant-Microbe Interact. 27:770-780.
103. Vera Cruz, C. M., Bai, J., Oña, I., Leung, H., Nelson, R. J., Mew, T. W., and Leach, J. E. 2000. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl. Acad. Sci. USA 97:13500-13505.
104. Vleeshouwers, V. G., 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.
105. Wang, K., Senthil-Kumar, M., Ryu, C. M., Kang, L., and Mysore, K. S. 2012. Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiol. 158:1789-1802.
106. Wang, K., Uppalapati, S. R., Zhu, X., Dinesh-Kumar, S. P., and Mysore, K. S. 2010. SGT1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol. Plant Pathol. 11:597-611.
107. Wang, X., Richards, J., Gross, T., Druka, A., Kleinhofs, A., Steffenson, B., Acevedo, M., and Brueggeman, R. 2013. The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol. Plant-Microbe Interact. 26:407-418.
108. Watson, I. A. 1981. Wheat and its rust parasites in Australia. Pages 129-147 in: Wheat Science - Today and Tomorrow. L. T. Evans and W. J. Peacock, eds. Cambridge University Press, Cambridge.
109. Wiermer, M., Feys, B. J., and Parker, J. E. 2005. Plant immunity: The EDS1 regulatory node. Curr. Opin. Plant Biol. 8:383-389.
110. Wulff, B. B. H., Horvath, D. M., and Ward, E. R. 2011. Improving immunity in crops: New tactics in an old game. Curr. Opin. Plant Biol. 14:468-476.
111. Zhao, B., Ardales, E. Y., Raymundo, A., Bai, J., Trick, H. N., Leach, J. E., and Hulbert, S. H. 2004. The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Mol. Plant-Microbe Interact. 17:771-779.
112. Zhao, B., Lin, X., Poland, J., Trick, H., Leach, J., and Hulbert, S. 2005. A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. USA 102:15383-15388.
113. Zipfel, C. 2008. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20:10-16.