Nonhost resistance against bacterial pathogens: Retrospectives and prospects

Annual Review of Phytopathology

Volumn 51, Issue , 2013, Pages 407-427

  Senthil Kumar, Muthappa ^a   Mysore, Kirankumar S ^a  

^a PLANT BIOLOGY DIVISION   (United States)

Author keywords

Apoplast; Durable disease resistance; Effectors; Hemibiotrophic bacteria; Hypersensitive response; PAMPs

Indexed keywords

ARTICLE; BACTERIUM; CROP; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PLANT; PLANT DISEASE; PLANT IMMUNITY;

BACTERIA; CROPS, AGRICULTURAL; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT IMMUNITY; PLANTS;

EID: 84881465992     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-082712-102319     Document Type: Article

References (146)

1. Abramovitch RB, Kim Y-J, Chen S, Dickman MB, Martin GB. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22:60-69
2. Ahuja I, Kissen R, Bones AM. 2012. Phytoalexins in defense against pathogens. Trends Plant Sci. 17:73-90
3. Aires A, Mota VR, Saavedra MJ, Monteiro AA, Simoes M, et al. 2009. Initial in vitro evaluations of the antibacterial activities of glucosinolate enzymatic hydrolysis products against plant pathogenic bacteria. J. Appl. Microbiol. 106:2096-105
4. Alfano JR, Collmer A. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683-98
5. Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, et al. 2008. A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 22:52-62
6. An C, Mou Z. 2012. Non-host defense response in a novel Arabidopsis Xanthomonas citri subsp. citri pathosystem. PLoS ONE 7:e31130
7. Anand A, Vaghchhipawala Z, RyuC-M, Kang L, Wang K, et al. 2007. Identification and characterization of plant genes involved in Agrobacterium-mediated plant transformation by virus-induced gene silencing. Mol. Plant-Microbe Interact. 20:41-52
8. Atkinson MM, Baker CJ. 1987. Alteration of plasmalemma sucrose transport in Phaseolus vulgaris by Pseudomonas syringae pv. syringae and its association with K+/H+ exchange. Phytopathology 77:1573-78
9. Baltrus DA, Nishimura MT, Dougherty KM, Biswas S, Mukhtar MS, et al. 2012. The molecular basis of host specialization in bean pathovars of Pseudomonas syringae. Mol. Plant-Microbe Interact. 25:877-88
10. Baskar V, Gururani M, Yu J, Park S. 2012. Engineering glucosinolates in plants: current knowledge and potential uses. Appl. Biochem. Biotechnol. 168:1694-717
11. Bednarek P. 2012. Chemical warfare or modulators of defence responses: the function of secondary metabolites in plant immunity. Curr. Opin. Plant Biol. 15:407-14
12. Bednarek P. 2012. Sulfur-containing secondary metabolites from Arabidopsis thaliana and other Brassicaceae with function in plant immunity. ChemBioChem 13:1846-59
13. Bednarek P, Osbourn A. 2009. Plant-microbe interactions: chemical diversity in plant defense. Science 324:746-48
14. Bestwick CS, Bennett MH, Mansfield JW. 1995. Hrp mutant of Pseudomonas syringae pv phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol. 108:503-16
15. Bestwick CS, Brown IR, Bennett M, Mansfield JW. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9:209-21
16. Bestwick CS, Brown IR, Mansfield JW. 1998. Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiol. 118:1067-78
17. Bhattacharjee S, Halane MK, Kim SH, Gassmann W. 2011. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334:1405-8
18. Block A, Li G, Fu ZQ, Alfano Jr. 2008. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11:396-403
19. Botti MG, Taylor MG, Botting NP. 1995. Studies on the mechanism of myrosinase: investigation of the effect of glycosyl acceptors on enzyme activity. J. Biol. Chem. 270:20530-35
20. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100:10181-86
21. Cecchini NM, Monteoliva MI, Alvarez ME. 2011. Proline dehydrogenase contributes to pathogen defense in Arabidopsis. Plant Physiol. 155:1947-59
22. Che Y-Z, Li Y-R, Zou H-S, Zou L-F, Zhang B, Chen G-Y. 2011. A novel antimicrobial protein for plant protection consisting of a Xanthomonas oryzae harpin and active domains of cecropin A andmelittin. Microb. Biotechnol. 4:777-93
23. Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527-32
24. Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, et al. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207-11
25. Chen S, Lin XH, Xu CG, Zhang Q. 2000. Improvement of bacterial blight resistance of "Minghui 63, " an elite restorer line of hybrid rice, by molecular marker-assisted selection. Crop Sci. 40:239-44
26. Coemans B, Takahashi Y, Berberich T, Ito A, Kanzaki H, et al. 2008. High-throughput in planta expression screening identifies an ADP-ribosylation factor (ARF1) involved in non-host resistance and R gene-mediated resistance. Mol. Plant Pathol. 9:25-36
27. Cowan MM. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12:564-82
28. Daurelio LD, Petrocelli S, Blanco F, Holuigue L, Ottado J, Orellano EG. 2011. Transcriptome analysis reveals novel genes involved in nonhost response to bacterial infection in tobacco. J. Plant Physiol. 168:382-91
29. Deslandes L, Rivas S. 2012. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17:644-55
30. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ. 2002. The phenylpropanoid pathway and plant defence: a genomics perspective. Mol. Plant Pathol. 3:371-90
31. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-48
32. Ellis J. 2006. Insights into nonhost disease resistance: Can they assist disease control in agriculturé Plant Cell 18:523-28
33. Fan J, Crooks C, Creissen G, Hill L, Fairhurst S, et al. 2011. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331:1185-88
34. Fan J, Doerner P. 2012. Genetic and molecular basis of nonhost disease resistance: complex, yes; silver bullet, no. Curr. Opin. Plant Biol. 15:400-6
35. Ferrante P, Clarke CR, Cavanaugh KA, Michelmore RW, Buonaurio R, Vinatzer BA. 2009. Contributions of the effector gene hopQ1-1 to differences in host range between Pseudomonas syringae pv. phaseolicola and P. syringae pv. tabaci. Mol. Plant Pathol. 10:837-42
36. Filippone MP, Diaz Ricci J, Mamaní de Marchese A, Farías RN, Castagnaro A. 1999. Isolation and purification of a 316 Da preformed compound from strawberry (Fragaria ananassa) leaves active against plant pathogens. FEBS Lett. 459:115-18
37. Forsyth A, Mansfield JW, Grabov N, de Torres M, Sinapidou E, Grant MR. 2010. Genetic dissection of basal resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol. Plant-Microbe Interact. 23:1545-52
38. Gleason C, Huang S, Thatcher LF, Foley RC, Anderson CR, et al. 2011. Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. USA 108:10768-73
39. Gottwald TR, Graham JH. 1992. A device for precise and nondisruptive stomatal inoculation of leaf tissue with bacterial pathogens. Phytopathology 82:930-35
40. Grimmer MK, John Foulkes M, Paveley ND. 2012. Foliar pathogenesis and plant water relations: a review. J. Exp. Bot. 63:4321-31
41. Gurr SJ, Rushton PJ. 2005. Engineering plants with increased disease resistance: How are we going to express it? Trends Biotechnol. 23:283-90
42. Ham JH, Kim MG, Lee SY, Mackey D. 2007. Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv. phaseolicola. Plant J. 51:604-16
43. Hann DR, Rathjen JP. 2007. Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J. 49:607-18
44. Hauck P, Thilmony R, He SY. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA 100:8577-82
45. Heath MC. 2000. Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3:315-19
46. Hoefle C, H? uckelhoven R. 2008. Enemy at the gates: traffic at the plant cell pathogen interface. Cell. Microbiol. 10:2400-7
47. Holub EB, Cooper A. 2004. Matrix, reinvention in plants: how genetics is unveiling secrets of non-host disease resistance. Trends Plant Sci. 9:211-14
48. H? uckelhoven R. 2007. Cell wall-associated mechanisms of disease resistance and susceptibility. Annu. Rev. Phytopathol. 45:101-27
49. Ishiga Y, Ishiga T, Uppalapati S, Mysore K. 2011. Arabidopsis seedling flood-inoculation technique: a rapid and reliable assay for studying plant-bacterial interactions. Plant Methods 7:32
50. Jafary H, Albertazzi G, Marcel TC, Niks RE. 2008. High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics 178:2327-39
51. Jeuken MJW, Pelgrom K, Stam P, Lindhout P. 2008. Efficient QTL detection for nonhost resistance in wild lettuce: backcross inbred lines versus F2 population. Theor. Appl. Genet. 116:845-57
52. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323-29
53. Kalde M, N? uhse TS, Findlay K, Peck SC. 2007. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc. Natl. Acad. Sci. USA 104:11850-55
54. Kang L, Li J, Zhao T, Xiao F, Tang X, et al. 2003. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc. Natl. Acad. Sci. USA 100:3519-24
55. Kang L, Tang X, Mysore KS. 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. 17:1328-36
56. Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, et al. 2003. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4:383-91
57. Kobayashi DY, Tamaki SJ, Keen NT. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. USA 86:157-61
58. Kwon C, Bednarek P, Schulze-Lefert P. 2008. Secretory pathways in plant immune responses. Plant Physiol. 147:1575-83
59. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365-69
60. Lee J, Klessig DF, N? urnberger T. 2001. A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13:1079-93
61. Lee S, Ishiga Y, Clermont K, Mysore KS. 2013. Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by nonhost bacterial pathogens. PeerJ 1:e34
62. Lee SC, Hwang IS, Choi HW, Hwang BK. 2008. Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol. 148:1004-20
63. Li W, Xu Y-P, Zhang Z-X, Cao W-Y, Li F, et al. 2012. Identification of genes required for nonhost resistance to Xanthomonas oryzae pv. oryzae reveals novel signaling components. PLoS ONE 7:e42796
64. Li X, Lin H, Zhang W, Zou Y, Zhang J, et al. 2005. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc. Natl. Acad. Sci. USA 102:12990-95
65. Lin N-C, Martin GB. 2007. Pto-and Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Mol. Plant-Microbe Interact. 20:806-15
66. Lindeberg M, Cartinhour S, Myers CR, Schechter LM, Schneider DJ, Collmer A. 2006. Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol. Plant-Microbe Interact. 19:1151-58
67. Lindeberg M, Cunnac S, Collmer A. 2012. Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol. 20:199-208
68. Lu M, Tang X, Zhou J-M. 2001. ArabidopsisNHO1is required for general resistance against Pseudomonas bacteria. Plant Cell 13:437-47
69. Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A. 2010. S-glycoprotein-like protein regulates defense responses in Nicotiana plants against Ralstonia solanacearum. Plant Physiol. 152:2023-35
70. McDowell JM, Woffenden BJ. 2003. Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol. 21:178-83
71. McHale L, Truco M, Kozik A, Wroblewski T, Ochoa O, et al. 2009. The genomic architecture of disease resistance in lettuce. Theor. Appl. Genet. 118:565-80
72. Melotto M, Underwood W, He SY. 2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol. 46:101-22
73. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-80
74. Mishina TE, Zeier J. 2007. Bacterial non-host resistance: interactions of Arabidopsis with nonadapted Pseudomonas syringae strains. Physiol. Plant. 131:448-61
75. Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349-57
76. Moreau M, Degrave A, Vedel R, Bitton F, Patrit O, et al. 2012. EDS1 contributes to nonhost resistance of Arabidopsis thaliana against Erwinia amylovora. Mol. Plant-Microbe Interact. 25:421-30
77. Mysore KS, Ryu C-M. 2004. Nonhost resistance: how much do we know? Trends Plant Sci. 9:97-104
78. Naoumkina MA, Zhao Q, Gallego-Giraldo L, Dai X, Zhao PX, Dixon RA. 2010. Genome-wide analysis of phenylpropanoid defence pathways. Mol. Plant Pathol. 11:829-46
79. Nasir KHB, Takahashi Y, Ito A, Saitoh H, Matsumura H, et al. 2005. High-throughput in planta expression screening identifies a class II ethylene-responsive element binding factor-like protein that regulates plant cell death and non-host resistance. Plant J. 43:491-505
80. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, et al. 2004. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135:1113-28
81. Nicaise V, Roux M, Zipfel C. 2009. Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol. 150:1638-47
82. Nissan G, Manulis-Sasson S, Chalupowicz L, Teper D, Yeheskel A, et al. 2011. The type III effector HsvG of the gall-forming Pantoea agglomerans mediates expression of the host gene HSVGT. Mol. Plant-Microbe Interact. 25:231-40
83. Nissan G, Manulis-Sasson S, Weinthal D, Mor H, Sessa G, Barash I. 2006. The type III effectors HsvG and HsvB of gall-forming Pantoea agglomerans determine host specificity and function as transcriptional activators. Mol. Microbiol. 61:1118-31
84. N? urnberger T, Lipka V. 2005. Non-host resistance in plants: new insights into an old phenomenon. Mol. Plant Pathol. 6:335-45
85. N? urnberger T, Scheel D. 2001. Signal transmission in the plant immune response. Trends Plant Sci. 6:372-79
86. Oh S-K, Lee S, Chung E, Park J, Yu S, et al. 2006. Insight into types I and II nonhost resistance using expression patterns of defense-related genes in tobacco. Planta 223:1101-7
87. Oldroyd GED, Staskawicz BJ. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl. Acad. Sci. USA 95:10300-5
88. Peart JR, Lu R, Sadanandom A, Malcuit I, Moffett P, et al. 2002. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99:10865-69
89. Pedley KF, Martin GB. 2003. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41:215-43
90. Ramos LJ, Narayanan KR, McMillan RT. 1992. Association of stomatal frequency and morphology in Lycopersicon species with resistance to Xanthomonas campestris pv. vesicatoria. Plant Pathol. 41:157-64
91. Ramos LJ, Volin RB. 1987. Role of stomatal opening and frequency on infection of Lycopersicon spp. by Xanthomonas campestris pv. vesicatoria. Phytopathology 77:1311-17
92. Rico A, Preston GM. 2008. Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplastinduced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol. Plant-Microbe Interact. 21:269-82
93. Rogers EE, Glazebrook J, Ausebel FM. 1996. Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol. Plant-Microbe Interact. 9:748-57
94. Rojas CM, Mysore KS. 2012. Glycolate oxidase is an alternative source forH2O2 production during plant defense responses and functions independently from NADPH oxidase. Plant Signal. Behav. 7:752-55
95. Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A, Mysore KS. 2012. Glycolate oxidase plays a major role during nonhost resistance responses by modulating reactive oxygen species-mediated signal transduction pathways. Plant Cell 24:336-52
96. Ryan RP, Vorholter F-J, Potnis N, Jones JB, Van SluysM-A, et al. 2011. Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat. Rev. Microbiol. 9:344-55
97. Sagi M, Fluhr R. 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141:336-40
98. Sattelmacher B. 2001. The apoplast and its significance for plant mineral nutrition. New Phytol. 149: 167-92
99. Schwessinger B, Zipfel C. 2008. News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11:389-95
100. Send́n LN, Filippone MP, Orce IG, Rigano L, Enrique R, et al. 2012. Transient expression of pepper Bs2 gene in Citrus limon as an approach to evaluate its utility for management of citrus canker disease. Plant Pathol. 61:648-57
101. Senthil-Kumar M, Mysore KS. 2012. Ornithine-β-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. 35:1329-43
102. Shan L, He P, Sheen J. 2007. Endless hide-and-seek: dynamic co-evolution in plant-bacterium warfare. J. Integr. Plant Biol. 49:105-11
103. Sharma PC, Ito A, Shimizu T, Terauchi R, Kamoun S, Saitoh H. 2003. Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana. Mol. Genet. Genomics 269:583-91
104. Sohn KH, Saucet SB, Clarke CR, Vinatzer BA, O'Brien HE, et al. 2012. HopAS1 recognition significantly contributes to Arabidopsis nonhost resistance to Pseudomonas syringae pathogens. New Phytol. 193:58-66
105. Stall RE, Jones JB, Minsavage GV. 2009. Durability of resistance in tomato and pepper toXanthomonads causing bacterial spot. Annu. Rev. Phytopathol. 47:265-84
106. Szabo E, Szatmari A, Hunyadi-Gulyas E, Besenyei E, Zsiros LR, et al. 2012. Changes in apoplast protein pattern suggest an early role of cell wall structure remodelling in flagellin-triggered basal immunity. Biol. Plantarum 56:551-59
107. Szczesny R, B? uttner D, Escolar L, Schulze S, Seiferth A, Bonas U. 2010. Suppression of the AvrBs1-specific hypersensitive response by the YopJ effector homolog AvrBsT from Xanthomonas depends on a SNF1-related kinase. New Phytol. 187:1058-74
108. Taguchi F, Ichinose Y. 2011. Role of type IV pili in virulence of Pseudomonas syringae pv. tabaci 6605: correlation of motility, multidrug resistance, and HR-inducing activity on a nonhost plant. Mol. Plant-Microbe Interact. 24:1001-11
109. Taguchi F, Ichinose Y. 2012. Virulence factor regulator (Vfr) controls virulence-associated phenotypes in Pseudomonas syringae pv. tabaci 6605 by a quorum sensing-independent mechanism. Mol. Plant Pathol. 14:279-92
110. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, et al. 1999. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl. Acad. Sci. USA 96:14153-58
111. Takahashi Y, Nasir KHB, Ito A, Kanzaki H, Matsumura H, et al. 2007. A high-throughput screen of celldeath-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii. Plant J. 49:1030-40
112. Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S, et al. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317-30
113. Tek A, Stevenson W, Helgeson J, Jiang J. 2004. Transfer of tuber soft rot and early blight resistances from Solanum brevidens into cultivated potato. Theor. Appl. Genet. 109:249-54
114. Thordal-Christensen H. 2003. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6:351-57
115. Torres MA, Jones JDG, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-78
116. Tsuji J, Jackson EP, Gage DA, Hammerschmidt R, Somerville SC. 1992. Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae. Plant Physiol. 98:1304-09
117. Van Wees SCM, 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. 33:733-42
118. VanEtten HD, Mansfield JW, Bailey JA, Farmer EE. 1994. Two classes of plant antibiotics: phytoalexins versus "phytoanticipins. " Plant Cell 6:1191-92
119. Venugopal SC, Jeong R-D, Mandal MK, Zhu S, Chandra-Shekara AC, et al. 2009. Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLoS Genet. 5:e1000545
120. Vera Cruz CM, Bai J, O? na I, Leung H, Nelson RJ, et al. 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 97:13500-5
121. Wang K, Kang L, Anand A, Lazarovits G, Mysore KS. 2007. Monitoring in planta bacterial infection at both cellular and whole-plant levels using the green fluorescent protein variant GFPuv. New Phytol. 174:212-23
122. Wang K, Senthil-Kumar M, Ryu C-M, Kang L, Mysore KS. 2012. Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiol. 158:1789-802
123. Wang K, Uppalapati SR, Zhu X, Dinesh-Kumar SP, Mysore KS. 2010. SGT1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol. Plant Pathol. 11:597-611
124. Wei C-F, Kvitko BH, Shimizu R, Crabill E, Alfano JR, et al. 2007. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J. 51:32-46
125. Whalen MC, Stall RE, Staskawicz BJ. 1988. Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc. Natl. Acad. Sci. USA 85:6743-47
126. Wiermer M, Feys BJ, Parker JE. 2005. Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8:383-89
127. Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA, Xu H, et al. 2009. Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 150:1733-49
128. Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, et al. 2004. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 23:2903-13
129. Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H. 2009. Polyamines as a common source of hydrogen peroxide in host-and nonhost hypersensitive response during pathogen infection. Plant Mol. Biol. 70:103-12
130. Yu X, Lund SP, Scott RA, Greenwald JW, Records AH, et al. 2013. Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites. Proc. Natl. Acad. Sci. USA 110:E425-34
131. Zeng W, Brutus A, Kremer JM, Withers JC, Gao X, et al. 2011. A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. tomato DC3000. PLoS Pathog. 7:e1002291
132. Zhang NW, Lindhout P, Niks RE, Jeuken MJW. 2009. Genetic dissection of Lactuca saligna nonhost resistance to downy mildew at various lettuce developmental stages. Plant Pathol. 58:923-32
133. Zhao B, Ardales EY, Raymundo A, Bai J, Trick HN, 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. 17:771-79
134. Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S. 2005. A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. USA 102:15383-88
135. Zhao BY, Ardales E, Brasset E, Claflin LE, Leach JE, Hulbert SH. 2004. The Rxo1/Rba1 locus of maize controls resistance reactions to pathogenic and non-host bacteria. Theor. Appl. Genet. 109:71-79
136. Zhou Y-L, Xu J-L, Zhou S-C, Yu J, Xie X-W, et al. 2009. Pyramiding Xa23 and Rxo1 for resistance to two bacterial diseases into an elite indica rice variety using molecular approaches. Mol. Breed. 23:279-87
137. Zipfel C, Robatzek S. 2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi⋯ ? Plant Physiol. 154:551-54
138. Zurbriggen MD, Carrillo N, Tognetti VB, Melzer M, Peisker M, et al. 2009. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J. 60:962-73
139. Dixon RA. 2001. Natural products and plant disease resistance. Nature 411:843-47
140. Dubery IA, Sanabria NM, Huang J-C. 2012. Nonself perception in plant innate immunity. Adv. Exp. Med. Biol. 738:79-107
141. Heath MC. 2009. Look before you leap: memoirs of a "cell biological" plant pathologist. Annu. Rev. Phytopathol. 47:1-13
142. Loake G, Grant M. 2007. Salicylic acid in plant defense: the players and protagonists. Curr. Opin. Plant Biol. 10:466-72
143. Niks RE, Marcel TC. 2009. Nonhost and basal resistance: how to explain specificity? New Phytol. 182:817-28
144. PPI. 2012. Pseudomonas syringae genome resources home page. Pseudomonas-Plant Interaction http://www. pseudomonas-syringae. org/
145. Sattelmacher B, Horst WJ, eds. 2007. The Apoplast of Higher Plants: Compartment of Storage, Transport and Reactions. London: Springer
146. Spoel SH, Dong X. 2012. How do plants achieve immunity? Defense without specialized immune cells. Nat. Rev. Immunol. 12:89-100