Improving crop disease resistance: Lessons from research on Arabidopsis and tomato

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages

  Piquerezt, Sophie J M ^a   Harvey, Sarah E ^a   Beynon, Jim L ^a   Ntoukakis, Vardis ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Arabidopsis; Crop engineering; Disease resistance; Food security; Model; Tomato

Indexed keywords

ARABIDOPSIS; LYCOPERSICON ESCULENTUM;

EID: 84914674989     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00671     Document Type: Review

References (226)

1. Afroz, A., Chaudhry, Z., Rashid, U., Ali, G. M., Nazir, F., Iqbal, J., et al. (2010). Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tissue Organ Cult. 104, 227-237. doi: 10.1007/s11240-010-9825-2
2. Aharoni, A., and Vorst, O. (2002). DNA microarrays for functional plant genomics. PlantMol. Biol. 48, 99-118. doi: 10.1023/A:1013734019946
3. Alfano, J. R. (2009). Roadmap for future research on plant pathogen effectors. Mol. PlantPathol. 10, 805-813. doi: 10.1111/j.1364-3703.2009.00588.x
4. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657. doi: 10.1126/science.1086391
5. Andolfo, G., Jupe, F., Witek, K., Etherington, G. J., Ercolano, M. R., and Jones, J. D. G. (2014). Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol. 14:120. doi: 10.1186/1471-222914-120
6. Andolfo, G., Sanseverino, W., Rombauts, S., Van de Peer, Y., Bradeen, J. M., Carputo, D., et al. (2013). Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol. 197, 223-237. doi: 10.1111/j.1469-8137.2012.04380.x
7. Arabidopsis Interactome Mapping Consortium. (2011). Evidence for network evolution in an Arabidopsis interactome map. Science 333, 601-607. doi: 10.1126/science.1203877
8. Arie, T., Takahashi, H., Kodama, M., and Teraoka, T. (2007). Tomato as a model plant for plant-pathogen interactions. Plant Biotechnol. 24, 135-147. doi: 10.5511/plantbiotechnology.24.135
9. Ashfield, T., Danzer, J. R., Held, D., Clayton, K., Keim, P., Saghai Maroof, M. A., et al. (1998). Rpg1, a soybean gene effective against races of bacterial blight, maps to a cluster of previously identified disease resistance genes. Theor. Appl. Genet. 96, 1013-1021. doi: 10.1007/s001220050833
10. 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 closelylinked, at the RPG1 locus. Genetics 141, 1597-1604.
11. Assaad, F. F., Qiu, J.-L., Youngs, H., Ehrhardt, D., Zimmerli, L., Kalde, M., et al. (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. doi: 10.1091/mbc.E04-02-0140
12. Axtell, M. J., and Staskawicz, B. J. (2003). Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369-377. doi: 10.1016/S0092-8674(03)00036-9
13. Ayliffe, M., Singh, R., andLagudah, E. (2008). Durable resistance to wheat stem rust needed. Curr. Opin. Plant Biol. 11, 187-192. doi: 10.1016/j.pbi.2008.02.001
14. Baltrus, D. A., Nishimura, M. T., Romanchuk, A., Chang, J. H., Mukhtar, M. S., Cherkis, K., et al. (2011). Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of19 Pseudomonas syringae isolates. PLoS Pathog. 7:e1002132. doi: 10.1371/journal.ppat.1002132
15. Bancroft, I., Morgan, C., Fraser, F., Higgins, J., Wells, R., Clissold, L., et al. (2011). Dissecting the genome of the polyploid crop oilseed rape by transcriptome sequencing. Nat. Biotechnol. 29, 762-766. doi: 10.1038/nbt.1926
16. Baxter, L., Jironkin, A., Hickman, R., Moore, J., Barrington, C., Krusche, P., et al. (2012). Conserved noncoding sequences highlight shared components of regulatory networks in dicotyledonous plants. Plant Cell 24, 3949-3965. doi: 10.1105/tpc.112.103010
17. Bebber, D. P., Ramotowski, M. A. T., and Gurr, S. J. (2013). Crop pests and pathogens move polewards in a warming world. Nat. Clim. Chang. 3, 985-988. doi: 10.1038/nclimate1990
18. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., andNekrasov, V. (2013). Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. PlantMethods 9, 39. doi: 10.1186/1746-4811-9-39
19. Bent, A. F., Kunkel, B. N., Dahlbeck, D., Brown, K. L., Schmidt, R., Giraudat, J., et al. (1994). RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265, 1856-1860. doi: 10.1126/science.8091210
20. Bernoux, M., Ve, T., Williams, S., Warren, C., Hatters, D., Valkov, E., et al. (2011). Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. CellHost Microbe 9, 200-211. doi: 10.1016/j.chom.2011.02.009
21. Biffen, R. H. (1905). Mendel’s laws of inheritance and wheat breeding. J. Agric. Sci. 1, 4-48. doi: 10.1017/S0021859600000137
22. Binder, A., Lambert, J., Morbitzer, R., Popp, C., Ott, T., Lahaye, T., et al. (2014). A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants. PLoS ONE 9:e88218. doi: 10.1371/journal.pone.0088218
23. Birker, D., Heidrich, K., Takahara, H., Narusaka, M., Deslandes, L., Narusaka, Y., et al. (2009). A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsisaccessions. Plant J.60, 602-613. doi: 10.1111/j.1365-313X.2009.03984.x
24. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., et al. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512. doi: 10.1126/science.1178811
25. Bogdanove, A. J., and Voytas, D. F. (2011). TAL effectors: customizable proteins for DNA targeting. Science 333, 1843-1846. doi: 10.1126/science.1204094
26. Bolton, M. D. (2009). Primarymetabolism and plant defense-fuel for the fire. Mol. Plant MicrobeInteract. 22, 487-497. doi: 10.1094/MPMI-22-5-0487
27. Bonardi, V., Cherkis, K., Nishimura, M. T., and Dangl, J. L. (2012). A new eye on NLRproteins: focused on clarity or diffused by complexity? Curr. Opin. Immunol. 24, 41-50. doi: 10.1016/j.coi.2011.12.006
28. Botella, M. A., Parker, J. E., Frost, L. N., Bittner-Eddy, P. D., Beynon, J. L., Daniels, M. J., et al. (1998). Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10, 1847-1860. doi: 10.1105/tpc.10.11.1847
29. Bouwmeester, K., Han, M., Blanco-Portales, R., Song, W., Weide, R., Guo, L.-Y., et al. (2014). The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnol. J. 12, 10-16. doi: 10.1111/pbi.12111
30. Bozkurt, T. O., Schornack, S., Banfield, M. J., and Kamoun, S. (2012). Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 15, 483-492. doi: 10.1016/j.pbi.2012.03.008
31. Brooks, C., Nekrasov, V., Lippman, Z. B., and Van Eck, J. (2014). Efficient gene editing in tomato in the first generation using the CRISPR/Cas9 system. Plant Physiol. 166, 1292-1297. doi: 10.1104/pp.114.247577
32. Brown, P., Baxter, L., Hickman, R., Beynon, J., Moore, J. D., and Ott, S. (2013). MEME-LaB: motif analysis in clusters. Bioinformatics 29, 1696-1697. doi: 10.1093/bioinformatics/btt248
33. Buell, C.R. (1998). Arabidopsis: aweed leading the field of plant-pathogen interactions. PlantPhysiol. Biochem. 36, 177-186. doi: 10.1016/S0981-9428(98)80102-2
34. Butler, D. (2013). Fungus threatens top banana. Nature 504, 195-196. doi: 10.1038/504195a
35. Cao, H., Bowling, S. A., Gordon, A. S., and Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583-1592. doi: 10.1105/tpc.6.11.1583
36. Carmona, M. A., Gally, M. E., and Lopez, S. E. (2005). Asian soybean rust: incidence, severity, and morphological characterization of Phakopsora pachyrhizi (Uredinia and Telia) in Argentina. Plant Dis. 89:109. doi: 10.1094/PD-89-0109B
37. Cesari, S., Thilliez, G., Ribot, C., Chalvon, V., Michel, C., Jauneau, A., et al. (2013). The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25, 1463-1481. doi: 10.1105/tpc.112.107201
38. Childers, R., Danies, G., Myers, K. L., Fei, Z., Small, I. M., and Fry, W. (2014). Acquired resistance to mefenoxam in sensitive isolates of Phytophthora infestans. Phytopathology doi: 10.1094/PHYT0-05-14-0148-R [Epub ahead of print].
39. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nurnberger, T., Jones, J. D. G., et al. (2007). A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497-500. doi: 10.1038/nature05999
40. Christian, M., Cermak, T., Doyle, E. L., Schmidt, C., Zhang, F., Hummel, A., et al. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757-761. doi: 10.1534/genetics.110.120717
41. Coates, M. E., and Beynon, J. L. (2010). Hyaloperonospora arabidopsidis as a pathogen model. Annu. Rev. Phytopathol. 48, 329-345. doi: 10.1146/annurev-phyto-080508-094422
42. Collier, S. M., and Moffett, P. (2009). NB-LRRs work a “bait and switch” on pathogens. Trends PlantSci. 14, 521-529. doi: 10.1016/j.tplants.2009.08.001
43. Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.-L., et al. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature425, 973-977. doi: 10.1038/nature02076
44. Collmer, A., Badel, J. L., Charkowski, A. O., Deng, W. L., Fouts, D. E., Ramos, A. R., et al. (2000). Pseudomonas syringae Hrp type III secretion system and effector proteins. Proc. Natl. Acad. Sci. U.S.A. 97, 8770-8777. doi: 10.1073/pnas.97.16.8770
45. Conrath, U., Gollner, K., Langenbach, C., Schultheiss, H., and Tresch, N. (2013). Genes to Enhance the Disease Resistance in Crops. Patent number WO/2013/093738.
46. Cooper, A. J., Latunde-Dada, A. O., Woods-Tor, A., Lynn, J., Lucas, J. A., Crute, I. R., et al. (2008). Basic compatibility of Albugo candida in Arabidopsis thaliana and Brassicajuncea causes broad-spectrum suppression of innate immunity. Mol. PlantMicrobe Interact. 21, 745-756. doi: 10.1094/MPMI-21-6-0745
47. Crute, I., Beynon, J., Dangl, J., Holub, E., Mauch-Mani, B., Slusarenko, A., et al. (1994). “Microbial pathogenesis of Arabidopsis, ” in Arabidopsis, eds E. M. Meyerowitz and C. R. Somerville (Newyork, NY: Cold Spring Harbor Laboratory Press), 705-747.
48. 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
49. Dangl, J. L., andJones, J. D. (2001). Plantpathogensandintegrateddefence responses to infection. Nature 411, 826-833. doi: 10.1038/35081161
50. Deslandes, L., Olivier, J., Peeters, N., Feng, D. X., Khounlotham, M., Boucher, C., et al. (2003). Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. U.S.A. 100, 8024-8029. doi: 10.1073/pnas.1230660100
51. Dixon, M. S., Jones, D. A., Keddie, J. S., Thomas, C. M., Harrison, K., and Jones, J. D. (1996). The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84, 451-459. doi: 10.1016/S0092-8674(00)81290-8
52. Dodds, P. N., Lawrence, G. J., Catanzariti, A.-M., Teh, T., Wang, C.-I. A., Ayliffe, M. A., et al. (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. U.S.A. 103, 8888-8893. doi: 10.1073/pnas.0602577103
53. Eitas, T. K., and Dangl, J. L. (2010). NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 13, 472-477. doi: 10.1016/j.pbi.2010.04.007
54. El Oirdi, M., El Rahman, T. A., Rigano, L., El Hadrami, A., Rodriguez, M. C., Daayf, F., et al. (2011). Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23, 2405-2421. doi: 10.1105/tpc.111.083394
55. Engler, C., Kandzia, R., and Marillonnet, S. (2008). A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3:e3647. doi: 10.1371/journal.pone.0003647
56. Engler, C., Youles, M., Gruetzner, R., Ehnert, T.-M., Werner, S., Jones, J. D. G., et al. (2014).A golden gate modular cloning toolbox for plants. ACS Synth. Biol. doi: 10.1021/sb4001504
57. Escobar, M. A., Civerolo, E. L., Summerfelt, K. R., and Dandekar, A. M. (2001). RNAi-mediated oncogene silencing confers resistance to crown gall tumorigene- sis. Proc. Natl. Acad. Sci. U.S.A 98, 13437-13442. doi: 10.1073/pnas.241276898
58. FAOSTAT. (2012). Food and Agriculture Organization ofthe United Nations. Available at: http://faostat.fao.org (accessed September 11, 2014).
59. Farnham, G., and Baulcombe, D. C. (2006).Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. Proc. Natl. Acad. Sci. U.S.A. 103, 18828-18833. doi: 10.1073/pnas.0605777103
60. Finkelstein, R. R. (1994). Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J. 5, 765-771. doi: 10.1046/j.1365-313X.1994.5060765.x
61. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194. doi: 10.1038/nature10947
62. Flor, H. H. (1955). Host-parasite interaction in flax rust - its genetics and other implications. Phytopathology 45, 680-685.
63. Flor, H. H. (1971). Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275-296. doi: 10.1146/annurev.py.09.090171.001423
64. Fradin, E. F., Abd-El-Haliem, A., Masini, L., van den Berg, G. C. M., Joosten, M. H., and Thomma, B. P. (2011). Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 156, 2255-2265. doi: 10.1104/pp.111.180067
65. Fradin, E. F., Zhang, Z., Juarez Ayala, J. C., Castroverde, C. D. M., Nazar, R. N., Robb, J., et al. (2009). Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. PlantPhysiol. 150, 320-332. doi: 10.1104/pp.109.136762
66. Fritz-Laylin, L. K., Krishnamurthy, N., Tor, M., Sjolander, K. V., and Jones, J. D. G. (2005). Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. PlantPhysiol. 138, 611-623. doi: 10.1104/pp.104.054452
67. Galletta, G. J., and Maas, J. L. (1990). Strawberry genetics. Hort Science 25, 871-879.
68. Geu-Flores, F., Nour-Eldin, H. H., Nielsen, M. T., and Halkier, B. A. (2007). USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCRproducts. NucleicAcids Res. 35:e55. doi: 10.1093/nar/gkm106
69. Gimenez-Ibanez, S., Hann, D. R., Ntoukakis, V., Petutschnig, E., Lipka, V., and Rathjen, J. P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423-429. doi: 10.1016/j.cub.2009.01.054
70. Giovannoni, J. (2001). Molecular biology of fruit maturation and ripening. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 725-749. doi: 10.1146/annurev.arplant.52.1.725
71. Giovannoni, J. (2004). Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl.), S170-S180. doi: 10.1105/tpc.019158
72. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227. doi: 10.1146/annurev.phyto.43.040204.135923
73. Glazebrook, J., Rogers, E. E., and Ausubel, F. M. (1996). Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143, 973-982.
74. Gohre, V., Jones, A. M. E., Sklenar, J., Robatzek, S., and Weber, A. P. M. (2012). Molecular crosstalk between PAMP-triggered immunityand photosynthesis. Mol. Plant MicrobeInteract. 25, 1083-1092. doi: 10.1094/MPMI-11-11-0301
75. Gohre, V., Spallek, T., Haweker, H., Mersmann, S., Mentzel, T., Boller, T., et al. (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824-1832. doi: 10.1016/j.cub.2008.10.063
76. Gomez-Gomez, L., andBoller, T. (2000). FLS2: an LRRreceptor-like kinaseinvolved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011. doi: 10.1016/S1097-2765(00)80265-8
77. Grant, M. R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., et al. (1995). Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269, 843-846. doi: 10.1126/science.7638602
78. Grant, M. R., Kazan, K., and Manners, J. M. (2013). Exploiting pathogens’ tricks of the trade for engineering of plant disease resistance: challenges and opportunities. Microb. Biotechnol. 6, 212-222. doi: 10.1111/1751-7915.12017
79. Greene, E. A., Codomo, C. A., Taylor, N. E., Henikoff, J. G., Till, B. J., Reynolds, S. H., et al. (2003). Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 164, 731-740.
80. Grzeskowiak, L., Stephan, W., and Rose, L. E. (2014). Epistatic selection and coadaptation in the Prf resistance complex of wild tomato. Infect. Genet. Evol. 27, 456-471. doi: 10.1016/j.meegid.2014.06.019
81. Gu, K., Yang, B., Tian, D., Wu, L., Wang, D., Sreekala, C., et al. (2005). R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435, 1122-1125. doi: 10.1038/nature03630
82. Gutierrez, J. R., Balmuth, A. L., Ntoukakis, V., Mucyn, T. S., Gimenez-Ibanez, S., Jones, A. M. E., et al. (2010). Prf immune complexes of tomato are oligomeric and contain multiple Pto-like kinases that diversify effector recognition. Plant J. 61, 507-518. doi: 10.1111/j.1365-313X.2009.04078.x
83. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G., and Greenberg, J. T. (2002). A functional screen for the Type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295, 1722-1726. doi: 10.1126/science.295.5560.1722
84. Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H. Y., Handsaker, R. E., Cano, L. M., et al. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393-398. doi: 10.1038/nature08358
85. Hahn, M. (2014). The rising threat of fungicide resistance in plant pathogenic fungi: Botrytisasacasestudy. J. Chem. Biol. 7, 133-141. doi: 10.1007/s12154-014-0113-1
86. Hao, Y., Wang, X., Li, X., Bassa, C., Mila, I., Audran, C., et al. (2014). Genome-wide identification, phylogenetic analysis, expression profiling, and protein-protein interaction properties of TOPLESS gene family members in tomato. J. Exp. Bot. 65, 1013-1023. doi: 10.1093/jxb/ert440
87. Harris, C. J., Slootweg, E. J., Goverse, A., and Baulcombe, D. C. (2013). Stepwise artificial evolution of a plant disease resistance gene. Proc. Natl. Acad. Sci. U.S.A. 110, 21189-21194. doi: 10.1073/pnas.1311134110
88. Haverkort, A. J., Boonekamp, P. M., Hutten, R., Jacobsen, E., Lotz, L. A. P., Kessel, G.J. T., et al. (2008). Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Res. 51, 47-57. doi: 10.1007/s11540-008-9089-y
89. Heath, M. C. (1981). A generalized concept of host-parasite specificity. Phytopathology 71, 1121-1123. doi: 10.1094/Phyto-71-1121
90. Heese, A., Hann, D. R., Gimenez-Ibanez, S., Jones, A. M. E., He, K., Li, J., et al. (2007). The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. U.S.A. 104, 12217-12222. doi: 10.1073/pnas.0705306104
91. Heidel, A. J., Clarke, J. D., Antonovics, J., and Dong, X. (2004). Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168, 2197-2206. doi: 10.1534/genetics.104.032193
92. Holub, E. B. (2007). Natural variation in innate immunity of a pioneer species. Curr. Opin. PlantBiol. 10, 415-424. doi: 10.1016/j.pbi.2007.05.003
93. Holub, E. B. (2008). Natural history of Arabidopsis thaliana and oomycete symbioses. Eur. J. PlantPathol. 122, 91-109. doi:10.1007/s10658-008-9286-1
94. Holub, E. B., and Beynon, J. L. (1997). Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Adv. Bot. Res. 24, 227-269. doi: 10.1016/S0065-2296(08)60075-0
95. Holub, E. B., Brose, E., Tor, M., Clay, C., Crute, I. R., and Beynon, J. L. (1995). Phenotypic andgenotypicvariation in the interaction between Arabidopsis thaliana and Albugo candida. Mol. Plant Microbe Interact. 8, 916-928. doi: 10.1094/MPMI-8-0916
96. Horvath, D. M., Stall, R. E., Jones, J. B., Pauly, M. H., Vallad, G. E., Dahlbeck, D., et al. (2012). Transgenic resistance confers effective field level control of bacterial spot disease in tomato. PLoS ONE 7:e42036. doi: 10.1371/journal.pone.0042036
97. Hou, L., Chen, L., Wang, J., Xu, D., Dai, L., Zhang, H., et al. (2012). Construction of stress responsive synthetic promoters and analysis of their activity in transgenic Arabidopsis thaliana. Plant Mol. Biol. Rep. 30, 1496-1506. doi: 10.1007/s11105-012-0464-0
98. Hrabak, E. M., Chan, C. W. M., Gribskov, M., Harper, J. F., Choi, J. H., Halford, N., et al. (2003). The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132, 666-680. doi: 10.1104/pp.102.011999
99. Huai, J., Wang, M., He, J., Zheng, J., Dong, Z., Lv, H., et al. (2008). Cloning and characterization of the SnRK2 gene family from Zea mays. Plant Cell Rep. 27, 1861-1868. doi: 10.1007/s00299-008-0608-8
100. Huang, G., Allen, R., Davis, E. L., Baum, T. J., and Hussey, R. S. (2006). Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. U.S.A. 103, 14302-14306. doi: 10.1073/pnas.0604698103
101. Huitema, E., Vleeshouwers, V. G., Francis, D. M., and Kamoun, S. (2003). Active defence responses associated with non-host resistance of Arabidopsis thaliana to the oomycete pathogen Phytophthora infestans. Mol. PlantPathol. 4, 487-500. doi: 10.1046/j.1364-3703.2003.00195.x
102. Innes, R. W., Bisgrove, S. R., Smith, N. M., Bent, A. F., Staskawicz, B. J., and Liu, Y. C. (1993). Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant J. 4, 813-820. doi: 10.1046/j.1365-313X.1993.04050813.x
103. Jakob, K., Goss, E. M., Araki, H., Van, T., Kreitman, M., and Bergel- son, J. (2002). Pseudomonas viridiflava and P. syringae - natural pathogens of Arabidopsis thaliana. Mol. Plant Microbe Interact. 15, 1195-1203. doi: 10.1094/MPMI.2002.15.12.1195
104. Jia, Y., McAdams, S. A., Bryan, G. T., Hershey, H. P., and Valent, B. (2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004-4014. doi: 10.1093/emboj/19.15.4004
105. Jo, K.-R., Kim, C.-J., Kim, S.-J., Kim, T.-Y., Bergervoet, M., Jongsma, M. A., et al. (2014). Development of late blight resistant potatoes by cisgene stacking. BMC Biotechnol. 14:50. doi: 10.1186/1472-6750-14-50
106. Johnson, R., and Allen, D. J. (1975). Induced resistance to rust diseases and its possible rolein the resistance of multilinevarieties. Annu. Appl. Biol. 80, 359-363. doi: 10.1111/j.1744-7348.1975.tb01642.x
107. Jones, D.A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J., and Jones, J. D.(1994).IsolationofthetomatoCf-9geneforresistancetoCladosporiumfulvum bytransposon tagging. Science 266, 789-793. doi: 10.1126/science.7973631
108. Jones, J. B., Jones, J. P., Stall, R. E., and Zitter, T. A. (1991). Compendium of Tomato 1094 Diseases. St Paul, MN: APS Press.
109. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
110. Jones, J. D. G., Witek, K., Verweij, W., Jupe, F., Cooke, D., Dorling, S., et al. (2014). Elevating crop disease resistance with cloned genes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369:20130087. doi: 10.1098/rstb.2013.0087
111. Jupe, F., Witek, K., Verweij, W., Sliwka, J., Pritchard, L., Etherington, G. J., et al. (2013a). Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 76, 530-544. doi: 10.1111/tpj.12307
112. Jupe, J., Stam, R., Howden, A. J. M., Morris, J. A., Zhang, R., Hedley, P. E., et al. (2013b). Phytophthora capsici-tomato interaction features dramatic shifts in gene expressionassociatedwith ahemi-biotrophiclifestyle. GenomeBiol. 14:R63. doi: 10.1186/gb-2013-14-6-r63
113. Kim, H.-J., Lee, H.-R., Jo, K.-R., Mortazavian, S. M. M., Huigen, D. J., Evenhuis, B., et al. (2012). Broad spectrum late blight resistance in potato differential set plants MaR8 and MaR9 is conferred by multiple stacked R genes. Theor. Appl. Genet. 124, 923-935. doi: 10.1007/s00122-011-1757-7
114. Kim, Y. J., Lin, N.-C., and Martin, G. B. (2002). Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109, 589598. doi: 10.1016/S0092-8674(02)00743-2
115. Kobayashi, D.Y., Tamaki, S. J., andKeen, N. T. (1989). Clonedavirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. U.S.A. 86, 157-161. doi: 10.1073/pnas.86.1.157
116. Koch, A., Kumar, N., Weber, L., Keller, H., Imani, J., and Kogel, K.-H. (2013). Host-induced gene silencing of cytochrome P450 lanosterol C14a-demethylase- encoding genes confers strong resistance to Fusarium species. Proc. Natl. Acad. Sci. U.S.A. 110, 19324-19329. doi: 10.1073/pnas.1306373110
117. Kohm, B. A., Goulden, M. G., Gilbert, J. E., Kavanagh, T. A., and Baulcombe, D. C. (1993). A potato virus X resistance gene mediates an induced, nonspecific resistance in protoplasts. Plant Cell 5, 913-920. doi: 10.1105/tpc.5.8.913
118. Koornneef, M., and Meinke, D. (2010). The development of Arabidopsis as amodel plant. PlantJ. 61, 909-921. doi: 10.1111/j.1365-313X.2009.04086.x
119. Koornneef, M., Reuling, G., and Karssen, C. M. (1984). The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol. Plant. 61, 377-383. doi: 10.1111/j.1399-3054.1984.tb06343.x
120. Krasileva, K.V., Dahlbeck, D., and Staskawicz, B. J. (2010).Activation of an Arabidop- sis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. PlantCell 22, 2444-2458. doi: 10.1105/tpc.110.075358
121. Lacombe, S., Rougon-Cardoso, A., Sherwood, E., Peeters, N., Dahlbeck, D., van Esse, H.P., et al. (2010). Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28, 365-369. doi: 10.1038/nbt.1613
122. Langenbach, C., Campe, R., Schaffrath, U., Goellner, K., and Conrath, U. (2013). UDP-glucosyltransferase UGT84A2/BRT1 is required for Arabidopsis nonhost resistance to the Asian soybean rust pathogen Phakopsorapachyrhizi. New Phytol. 198, 536-545. doi: 10.1111/nph.12155
123. Li, J., Wen, J., Lease, K. A., Doke, J. T., Tax, F. E., and Walker, J. C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222. doi: 10.1016/S0092-8674(02)00812-7
124. Li, L.-B., Zhang, Y.-R., Liu, K.-C., Ni, Z.-F., Fang, Z.-J., Sun, Q.-X., et al. (2010). Identification and bioinformatics analysis of SnRK2 and CIPK family genes in sorghum. Agric. Sci. China 9, 19-30. doi: 10.1016/S1671-2927(09)60063-8
125. Lindeberg, M., Cunnac, S., and Collmer, A. (2012). Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol. 20, 199-208. doi: 10.1016/j.tim.2012.01.003
126. Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., et al. (2005). Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310, 1180-1183. doi: 10.1126/science.1119409
127. Liu, Q., Rimmer, S. R., and Scarth, R. (1989). Histopathology of compatibility and incompatibility between oilseed rape and Albugo candida. Plant Pathol. 38, 176-182. doi: 10.1111/j.1365-3059.1989.tb02131.x
128. Loehrer, M., Langenbach, C., Goellner, K., Conrath, U., and Schaffrath, U. (2008). Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol. PlantMicrobeInteract. 21, 1421-1430. doi: 10.1094/MPMI-21-11-1421
129. Long, J. A., Woody, S., Poethig, S., Meyerowitz, E. M., and Barton, M. K. (2002). Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129, 2797-2806.
130. Lozano-Duran, R., Macho, A. P., Boutrot, F., Segonzac, C., Somssich, I. E., and Zipfel, C. (2013). The transcriptional regulator BZR1 mediates trade-offbetween plant innate immunity and growth. Elife 2:e00983. doi: 10.7554/eLife.00983
131. Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V., and Ton, J. (2012). Next- generation systemic acquired resistance. Plant Physiol. 158, 844-853. doi: 10.1104/pp.111.187468
132. Macho, A. P., Schwessinger, B., Ntoukakis, V., Brutus, A., Segonzac, C., Roy, S., et al. (2014). A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343, 1509-1512. doi: 10.1126/science.1248849
133. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R., and Dangl, J. L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379-389. doi: 10.1016/S0092-8674(03)00040-0
134. Mackey, D., Holt, B. F., Wiig, A., and Dangl, J. L. (2002). RIN4 interacts with Pseu- domonassyringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743-754. doi: 10.1016/S0092-8674(02)00661-X
135. Maekawa, T., Cheng, W., Spiridon, L. N., Toller, A., Lukasik, E., Saijo, Y., et al. (2011). Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. CellHostMicrobe 9, 187-199. doi: 10.1016/j.chom.2011.02.008
136. Maekawa, T., Kracher, B., Vernaldi, S., Ver Loren van Themaat, E., and Schulze-Lefert, P. (2012). Conservation of NLR-triggered immunityacross plant lineages. Proc. Natl. Acad. Sci. U.S.A. 109, 20119-20123. doi: 10.1073/pnas.1218059109
137. Marco, G. M., and Stall, R. E. (1983). Control of bacterial spot of pepper initiated by strains of Xanthomonas campestris pv. vesicatoria that differ in sensitivity to copper. PlantDis. 67, 779-781. doi: 10.1094/PD-67-779
138. Martin, G. B., Brommonschenkel, S. H., Chunwongse, J., Frary, A., Ganal, M. W., Spivey, R., et al. (1993). Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262, 1432-1436. doi: 10.1126/science.7902614
139. Marumo, S., Katayama, M., Komori, E., Ozaki, Y., Natsume, M., and Kondo, S. (1982). Microbial production of abscisic acid by Botrytis cinerea. Agric. Biol. Chem. 46, 1967-1968. doi: 10.1271/bbb1961.46.1967
140. Mauch-Mani, B., and Slusarenko, A. J. (1993). Arabidopsis as a model host for studying plant-pathogen interactions. Trends Microbiol. 1, 265-270. doi: 10.1016/0966-842X(93)90049-W
141. McLellan, H., Boevink, P. C., Armstrong, M. R., Pritchard, L., Gomez, S., Morales, J., et al. (2013). An RxLR effector from Phytophthora infestans prevents re-localisation of two Plant NAC transcription factors from the endoplasmic reticulumtothenucleus. PLoSPathog. 9:e1003670. doi:10.1371/journal.ppat.1003670
142. Mendes, B., Cardoso, S. C., Boscariol-Camargo, R. L., Cruz, R. B., Mourao Filho, F., and Bergamin Filho, A. (2010). Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. PlantPathol. 59, 68-75. doi: 10.1111/j.1365-3059.2009.02148.x
143. Mestre, P., and Baulcombe, D. C. (2006). Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18, 491-501. doi: 10.1105/tpc.105.037234
144. Meyers, B. C., Kozik, A., Griego, A., Kuang, H., and Michelmore, R. W. (2003). Genome-wide analysis ofNBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809-834. doi: 10.1105/tpc.009308
145. Mindrinos, M., Katagiri, F., Yu, G. L., andAusubel, F. M. (1994). The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site andleucine-richrepeats. Cell78, 1089-1099.doi: 10.1016/0092-8674(94)90282-8
146. Mucyn, T. S., Clemente, A., Andriotis, V. M. E., Balmuth, A. L., Oldroyd, G. E. D., Staskawicz, B. J., et al. (2006). The tomato NBARC-LRRprotein Prf interactswith Pto kinase in vivo to regulate specific plant immunity. PlantCell 18, 2792-2806. doi: 10.1105/tpc.106.044016
147. Mucyn, T. S., Wu, A. J., Balmuth, A. L., Arasteh, J. M., and Rathjen, J. P. (2009). Regulation of tomato PrfbyPto-Like protein kinases. Mol. PlantMicrobe. Interact. 22, 391-401. doi: 10.1094/MPMI-22-4-0391
148. Mukhtar, M. S., Carvunis, A.-R., Dreze, M., Epple, P., Steinbrenner, J., Moore, J., et al. (2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596-601. doi: 10.1126/science.1203659
149. Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2012). NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 97-103. doi: 10.1016/j.bbagrm.2011.10.005
150. Narusaka, M., Hatakeyama, K., Shirasu, K., and Narusaka, Y. (2014). Arabidopsis dual resistance proteins, both RPS4 and RRS1, are required for resistance to bacterial wilt in transgenic Brassica crops. Plant Signal. Behav. 9:e29130. doi: 10.4161/psb.29130
151. Narusaka, M., Kubo, Y., Hatakeyama, K., Imamura, J., Ezura, H., Nanasato, Y., et al. (2013a). Interfamilytransfer of dual NB-LRRgenes confers resistance to multiple pathogens. PLoS ONE 8:e55954. doi: 10.1371/journal.pone.0055954
152. Narusaka, M., Kubo, Y., Hatakeyama, K., Imamura, J., Ezura, H., Nanasato, Y., et al. (2013b). Breaking restricted taxonomic functionality by dual resistance genes. PlantSignal. Behav. 8:e24244. doi: 10.4161/psb.24244
153. Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., et al. (2009). RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. PlantJ. 60, 218-226. doi: 10.1111/j.1365-313X.2009.03949.x
154. Nicaise, V., Joe, A., Jeong, B.-R., Korneli, C., Boutrot, F., Westedt, I., et al. (2013). Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32, 701-712. doi: 10.1038/emboj.2013.15
155. Ntoukakis, V., Balm uth, A. L., Mucyn, T. S., Gutierrez, J. R., Jones, A. M. E., and Rathjen, J. P. (2013). The tomato Prf complex is a molecular trap for bacterial effectors based on Pto transphosphorylation. PLoS Pathog. 9:e1003123. doi: 10.1371/journal.ppat.1003123
156. Ntoukakis, V., Mucyn, T. S., Gimenez-Ibanez, S., Chapman, H. C., Gutierrez, J. R., Balmuth, A. L., et al. (2009). Host inhibition of a bacterial virulence effector triggers immunity to infection. Science 324, 784-787. doi: 10.1126/science.1169430
157. Ntoukakis, V., Saur, I. M., Conlan, B., and Rathjen, J. P. (2014). The changing of the guard: the Pto/Prf receptor complex of tomato and pathogen recognition. Curr. Opin. PlantBiol. 20, 69-74. doi: 10.1016/j.pbi.2014.04.002
158. O’Brien, H. E., Thakur, S., and Guttman, D. S. (2011). Evolution of plant pathogenesis in Pseudomonas syringae: a genomics perspective. Annu. Rev. Phytopathol. 49, 269-289. doi: 10.1146/annurev-phyto-072910-095242
159. Oerke, E. C. (2006). Crop losses to pests. J. Agric. Sci. 144, 31-43. doi: 10.1017/S0021859605005708
160. Osmont, K. S., and Hardtke, C. S. (2008). The topless plant developmental phenotype explained! GenomeBiol. 9, 219. doi: 10.1186/gb-2008-9-4-219
161. 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. doi: 10.1105/tpc.8.11.2033
162. Pauwels, L., Barbero, G. F., Geerinck, J., Tilleman, S., Grunewald, W., Perez, A. C., et al. (2010). NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464, 788-791. doi: 10.1038/nature08854
163. Penfold, C. A., Buchanan-Wollaston, V., Denby, K. J., and Wild, D. L. (2012). Nonparametric Bayesian inference for perturbed and orthologous gene regulatory networks. Bioinformatics 28, 1233-1241. doi: 10.1093/bioinformatics/bts222
164. Penfold, C. A., andWild, D. L. (2011). Howto infer gene networks from expression profiles, revisited. Interface Focus 1, 857-870. doi: 10.1098/rsfs.2011.0053
165. Pennisi, E. (2010). Armed and dangerous. Science 327, 804-805. doi: 10.1126/sci-ence.327.5967.804
166. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., et al. (2000). Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111-1120. doi: 10.1016/S0092-8674(00)00213-0
167. Petnicki-Ocwieja, T., Schneider, D. J., Tam, V. C., Chancey, S. T., Shan, L., Jamir, Y., et al. (2002). Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 99, 7652-757. doi: 10.1073/pnas.112183899
168. Pivonia, S., Yang, X. B., and Pan, Z. (2005). Assessment of epidemic potential of soybean rust in the United States. Plant Dis. 89, 678-682. doi: 10.1094/PD-89-0678
169. Polanski, K., Rhodes, J., Hill, C., Zhang, P., Jenkins, D. J., Kiddle, S. J., et al. (2014). Wigwams: identifying gene modules co-regulated across multiple biological conditions. Bioinformatics30, 962-970. doi: 10.1093/bioinformatics/btt728
170. Pound, G. S., and Williams, P. H. (1963). Biological races of Albugo candida. Phytopathology 53, 1146-1149.
171. Redman, J. C., Haas, B. J., Tanimoto, G., and Town, C. D. (2004). Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. Plant J. 38, 545-561. doi: 10.1111/j.1365-313X.2004.02061.x
172. Redei, G. P., and Koncz, C. (1992). Classical Mutagenesis. Methods in Arabidopsis Research. Singapore: World Scientific Publishing Co.
173. Rhee, S. Y. (2003). The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 31, 224-228. doi: 10.1093/nar/gkg076
174. Robert-Seilaniantz, A., Grant, M., and Jones, J. D. G. (2011). Hormone crosstalk in plant disease and defense: more thanjustjasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49, 317-343. doi: 10.1146/annurev-phyto-073009-114447
175. Ronald, P. C., Albano, B., Tabien, R., Abenes, L., Wu, K. S., McCouch, S., et al. (1992). Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21. Mol. Gen. Genet. 236, 113-120. doi: 10.1007/BF00279649
176. Salmeron, J. M., Oldroyd, G. E. D., Rommens, C. M. T., Scofield, S. R., Kim, H.-S., Lavelle, D. T., et al. (1996). Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell86, 123-133. doi: 10.1016/S0092-8674(00)80083-5
177. Sarrion-Perdigones, A., Vazquez-Vilar, M., Palaci, J., Castelijns, B., Forment, J., Ziarsolo, P., et al. (2013). GoldenBraid 2.0: a comprehensive DNA assembly framework for plant synthetic biology. Plant Physiol. 162, 1618-1631. doi: 10.1104/pp.113.217661
178. Schornack, S., Moscou, M. J., Ward, E. R., and Horvath, D. M. (2013). Engineering plant disease resistance based on TAL effectors. Annu. Rev. Phytopathol. 51, 383406. doi: 10.1146/annurev-phyto-082712-102255
179. Schulze-Lefert, P., and Panstruga, R. (2011). A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. TrendsPlantSci. 16, 117-125. doi: 10.1016/j.tplants.2011.01.001
180. Scofield, S., Tobias, C., Rathjen, J., Chang, J., Lavelle, D., Michelmore, R., et al. (1996). Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274, 2063-2065. doi: 10.1126/science.274.5295.2063
181. Seifers, D. L., Haber, S., Martin, T. J., and McCallum, B. D. (2014). Heritable, de novo resistance to leaf rust and other novel traits in selfed descendants of wheat responding to inoculation with wheat streak mosaic virus. PLoS ONE 9:e86307. doi: 10.1371/journal.pone.0086307
182. Selote, D., and Kachroo, A. (2010). RIN4-like proteins mediate resistance protein- derived soybean defense against Pseudomonas syringae. Plant Signal. Behav. 5, 1453-1456. doi: 10.1104/pp.110.158147
183. Sijmons, P. C., Grundler, F. M., Mende, N., Burrows, P. R., and Wyss, U. (1991). Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J. 1, 245-254. doi: 10.1111/j.1365-313X.1991.00245.x
184. Singh, A. K., Sharma, V., Pal, A. K., Acharya, V., and Ahuja, P. S. (2013). Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res. 20, 403-423. doi: 10.1093/dnares/dst019
185. Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., and Mauch-Mani, B. (2012). Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158, 835-843. doi: 10.1104/pp.111.191593
186. Somerville, C., and Koornneef, M. (2002). A fortunate choice: the history of Arabidopsis as a model plant. Nat. Rev. Genet. 3, 883-889. doi: 10.1038/nrg927
187. Sprague, S. J., Balesdent, M.-H., Brun, H., Hayden, H. L., Marcroft, S. J., Pinochet, X., et al. (2006). Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur. J. Plant Pathol. 114, 33-40. doi: 10.1007/s10658-005-3683-5
188. Staal, J., Kaliff, M., Bohman, S., and Dixelius, C. (2006). Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J. 46, 218-230. doi: 10.1111/j.1365-313X.2006.02688.x
189. Staskawicz, B. J., Dahlbeck, D., and Keen, N. T. (1984). Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc. Natl. Acad. Sci. U.S.A. 81, 6024-6028. doi: 10.1073/pnas.81.19.6024
190. Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B. H., Molina, A., Schulze- Lefert, P., et al. (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. doi: 10.1105/tpc.105.038372
191. Takahashi, H., Shimizu, A., Arie, T., Rosmalawati, S., Fukushima, S., Kikuchi, M., et al. (2005). Catalog of Micro-Tom tomato responses to common fungal, bacterial, andviralpathogens. J. Gen. PlantPathol. 71, 8-22. doi: 10.1007/s10327-004-0168-x
192. Tang, P., Zhang, Y., Sunc, X., Tian, D., Yang, S., and Ding, J. (2010). Disease resistance signature of the leucine-rich repeat receptor-like kinase genes in four plant species. Plant Sci. 179, 399-406. doi: 10.1016/j.plantsci.2010.06.017
193. Tang, X., Frederick, R., Zhou, J., Halterman, D., Jia, Y., and Martin, G. (1996). Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274, 2060-2063. doi: 10.1126/science.274.5295.2060
194. Thilmony, R., Underwood, W., and He, S. Y. (2006). Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J. 46, 34-53. doi: 10.1111/j.1365-313X.2006.02725.x
195. Thines, M., Choi, Y.-J., Kemen, E., Ploch, S., Holub, E. B., Shin, H.-D., et al. (2009). A new species of Albugo parasitic to Arabidopsis thaliana reveals new evolutionary patterns in white blister rusts (Albuginaceae). Persoonia 22, 123-128. doi: 10.3767/003158509X457931
196. Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M., and Bergelson, J. (2003). Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74-77. doi: 10.1038/nature01588
197. Tomato Genome Consortium. (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641. doi: 10.1038/nature11119
198. Tripathi, J. N., Lorenzen, J., Bahar, O., Ronald, P., andTripathi, L. (2014). Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. PlantBiotechnol. J. 12, 663-673. doi: 10.1111/pbi.12170
199. Tsuji, J. (1992). First report of natural infection of Arabidopsis thaliana by Xanthomonas campestris pv. campestris. Plant Dis. 76, 539. doi: 10.1094/PD-76-0539A
200. Valls, M., Genin, S., and Boucher, C. (2006). Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. PLoS Pathog. 2:e82. doi: 10.1371/journal.ppat.0020082
201. Van Der Biezen, E. A., and Jones, J. D. (1998). Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454-456. doi: 10.1016/S0968-0004(98)01311-5
202. van der Hoorn, R. A. L., and Kamoun, S. (2008). From guard to decoy: a new model for perception of plant pathogen effectors. PlantCell 20, 2009-2017. doi: 10.1105/tpc.108.060194
203. Verma, P. R., Harding, H., Petrie, G. A., and Williams, P. H. (1975). Infection and temporal development of mycelium of Albugo candida in cotyledons of four Brassica species. Can. J. Bot. 53, 1016-1020. doi: 10.1139/b75-119
204. Walawage, S. L., Britton, M. T., Leslie, C. A., and Uratsu, S. L. (2013). Stacking resistance to crown gall and nematodes in walnut rootstocks. BMC Genomics 14:668. doi: 10.1186/1471-2164-14-668
205. Walters, D. R., andPaterson, L. (2012). Parents lendahelping handto their offspring in plant defence. Biol. Lett. 8, 871-873. doi: 10.1098/rsbl.2012.0416
206. Wang, X., Basnayake, B. M. V. S., Zhang, H., Li, G., Li, W., Virk, N., et al. (2009). The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Mol. PlantMicrobe Interact. 22, 1227-1238. doi: 10.1094/MPMI-22-10-1227
207. Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., et al. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32, 947-951. doi: 10.1038/nbt.2969
208. WeCling, R., Epple, P., Altmann, S., He, Y., Yang, L., Henz, S. R., et al. (2014). Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16, 364-375. doi: 10.1016/j.chom.2014.08.004
209. Whalen, M. C., Innes, R. W., Bent, A. F., and Staskawicz, B. J. (1991). Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3, 49-59. doi: 10.1105/tpc.3.1.49
210. Whitham, S., Dinesh-Kumar, S. P., Choi, D., Hehl, R., Corr, C., and Baker, B. (1994). The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78, 1101-1115. doi: 10.1016/0092-8674(94)90283-6
211. Williams, S. J., Sohn, K. H., Wan, L., Bernoux, M., Sarris, P. F., Segonzac, C., et al. (2014). Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344, 299-303. doi: 10.1126/science.1247357
212. Windram, O., Madhou, P., McHattie, S., Hill, C., Hickman, R., Cooke, E., et al. (2012). Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24, 3530-3557. doi: 10.1105/tpc.112.102046
213. Windram, O., Penfold, C. A., and Denby, K. J. (2014). Network modeling to understand plant immunity. Annu. Rev. Phytopathol. 52, 93-111. doi: 10.1146/annurev-phyto-102313-050103
214. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N. J. (2007). An“Electronic Fluorescent Pictograph” browser for exploring and analyzing large- scale biological data sets. PLoS ONE 2:e718. doi: 10.1371/journal.pone.0000718
215. Xie, D.X., Feys, B. F., James, S., Nieto-Rostro, M., and Turner, J. G. (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091-1094. doi: 10.1126/science.280.5366.1091
216. Xin, X.-F., and He, S.Y. (2013). Pseudomonassyringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytopathol. 51, 473-498. doi: 10.1146/annurev-phyto-082712-102321
217. Xing, W., Zou, Y., Liu, Q., Liu, J., Luo, X., Huang, Q., et al. (2007). The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449, 243-247. doi: 10.1038/nature06109
218. Xu, M.-R., Huang, L.-Y., Zhang, F., Zhu, L.-H., Zhou, Y.-L., and Li, Z.-K. (2013). Genome-wide phylogenetic analysis of stress-activated protein kinase genes in rice (OsSAPKs) and expression profiling in response to Xanthomonas oryzae pv. oryzicola infection. Plant Mol. Biol. Rep. 31, 877-885. doi: 10.1007/s11105-013-0559-2
219. Yang, S., Li, J., Zhang, X., Zhang, Q., Huang, J., Chen, J.-Q., et al. (2013a). Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease. Proc. Natl. Acad. Sci. U.S.A. 110, 18572-18577. doi: 10.1073/pnas.1318211110
220. Yang, Y., Jittayasothorn, Y., Chronis, D., Wang, X., Cousins, P., and Zhong, G.-Y. (2013b). Molecular characteristics and efficacy of 16D10 siRNAs in inhibiting root-knot nematode infection in transgenic grape hairy roots. PLoS ONE 8:e69463. doi: 10.1371/journal.pone.0069463
221. Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Aronso, J., et al. (2002). ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 43, 1473-1483. doi: 10.1093/pcp/pcf188
222. Zhang, J., Li, W., Xiang, T., Liu, Z., Laluk, K., Ding, X., et al. (2010). Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted bya Pseudomonassyringae effector. CellHostMicrobe 7, 290-301. doi: 10.1016/j.chom.2010.03.007
223. Zhao, B., Ardales, E. Y., Raymundo, A., Bai, J., Trick, H. N., Leach, J. E., et al. (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. doi: 10.1094/MPMI.2004.17.7.771
224. 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. U.S.A. 102, 15383-15388. doi: 10.1073/pnas.0503023102
225. Zhu, Z., Xu, F., Zhang, Y., Cheng, Y. T., Wiermer, M., Li, X., et al. (2010). Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc. Natl. Acad. Sci. U.S.A. 107, 13960-13965. doi: 10.1073/pnas.1002828107
226. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632. doi: 10.1104/pp.104.046367