Bitki-Patojen İnteraksiyonlarının Yeni Paradigması: Bitki İmmünolojisi; Temel Kavramlar

Öz

İnsan ve hayvan hastalıklarından doğal korunma ile ilgili çalışmalar bir kaç asır öncelere kadar uzanmaktadır. Bu yöndeki ilk adım, İngiliz Edward Jenner (1749-1823) tarafından atılmıştır. Çok uzun yıllardan beri, bitkilerin mikrobiyel elisitörleri algılama sistemlerine sahip olduğu bilinse de, immünoloji terimi adı altında bitkilere ait bağışıklık ile ilgili çalışmalar yaklaşık son 15-20 yıldan beri tasnif edilmiş olup konu ile ilgili özellikle Türkçe kaynak ve ülkemizde deneysel araştırma çalışması yeterli düzeyde bulunmamaktadır. İmmünite (rezistanslık-dayanıklılık); infektiyöz hastalıklardan bireyleri koruyan, doğal olarak meydana gelen savunma mekanizmasının tamamıdır. Belirli bir mikroorganizmaya karşı vücudun direncidir şeklinde de ifade edilebilir. Bitkiler; bakteri, fungus, protista, böcek, vertebra gibi birçok organizmalar için zengin bir besin kaynağıdır. Hayvanlara benzer immün sistemleri olmasa da, bitkiler yapısal, kimyasal ve istila eden organizmaları tanımak amacıyla protein yapıda bir dizi mekanizmalar sistemine sahiptirler, böylece yıkıcı bir zarardan korunmak için zararlıları durdurabilirler. Karmaşık bir yapıya sahip olan bitki immün sistemini harekete geçirmek için önce patojen tehdidinin bitki tarafından algılanması gerekir. Bitkinin bu algılama olaylarını anlamak için öncelikle savunmada rol oynayan ve patojenden türeyen aracı moleküller ile bitki immün mekanizmasının fazlarının bilinmesi gerekir. Özellikle bitki immün sisteminin çalışma modelini kavrayabilmek için, bitki immünitesinin farklı aşamalarını ilgilendiren ve elisitör molekülleri olan MAMPs, PAMPs, MIMPs, MAMP reseptörü, efektör, dayanıklılık (R) proteinleri, PRR, ETI, PTI vb terimleri yakından tanımak ve aralarındaki farkları ortaya koymak amacıyla bu çalışma derlenmiştir. 

Anahtar Kelimeler

• Bitki immünoloji,Efektör,Rreseptör,Savunma mekanizması

Novel Paradigm of Plant-Pathogen Interactions: Plant Immunity; Basic Concept

Abstract

Research on natural protection of infectious human and plant diseases extend for a few centuries. British Edward Jenner (1749-1823) is the pionner in immunology. Although it is known, sight on microbial elicitors perception of plants, plant immunology concept is classified for 15-20 years, turkish data and experimental studies related with is insufficient with regret.  Immunity is total defense mechanism to infectious diseases to protect body. It can be also defined as is body resistance to the spesific microorganism. Plants are rich food source for several organisms such as bacteria, fungi, protist, insect, vertebrate. Even though there are no animal-like immunity mechanism, plants have a series of mechanisms encompassing constitutional, chemical and proteinaceous compounds to detect invading organisms, thus they can cease devastating damage by pests. Foremost, presence of pathogen has to be perceived by plants, for acitvation of sophisticated plant immune system. So understanding sensing cases, intermediate molecules form microorganisms to discriminate self and/or non-self for plants and phases of immune mechanism is unraveled. In particular, the present review purposes to identify similarity and differences immune elicitor molecules such as MAMPs, PAMPs, MIMPs related to distinct phases of plant immunity and to elucidate events linking MAMP receptor, effector, resistance (R) proteins, PRR, ETI, PTI etc terms.  

Keywords

• Plant immunology,Effector,Receptor,Defense mechanism

References

1. Alfano JR, Collmer A. 2004. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol, 42:385–414.
2. Alfano JR, A Collmer. 1996. Bacterial Pathogens in Plants: Life up against the Wall. Plant Cell, 8/10:1683–1698.
3. Alfano JR, Kim HS, Delanye TP, Collmer A. 1997. Evidence that the Pseudomonas syringae pv syringae hrp-linked hrpA gene encodes an Avr-like protein that acts in an hrp-dependent manner within tobacco cells. Mol Plant Microbe Interact, 10:580-588.
4. Angelova Z, Georgiev S, Roos W. 2006. Elicitation of plants. Biotechnol Biotechnol Eq, 20:72-83.
5. Ausubel FM. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol, 6:973–79.
6. Belkhadir Y, Nimchuk Z, Hubert DA, Mackey D, Dangl JL. 2004. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell, 16/10:2822-35.
7. Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol, 7/4:391-9.
8. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ. 1994. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science, 265:1856–1860.

9. Bent AF, Mackey D. 2007. Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions. Annu. Rev. Phytopathol, 45:399–436. doi:10.1146/annurev.phyto.45.062806.094427.
10. Boller T. 1995. “Chemoperception of microbial signals in plant cells,” Annual Review of Plant Physiology and Plant Molecular Biology, 46:189–214.
11. Boller T, He SY. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 324/5928:742–744. doi: 10.1126/science.1171647.
12. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology, 60:379-406.
13. Böhm H, Albert I, Fan L, Reinhard A, Nürnberger T, 2014. Immune receptor complexes at the plant cell surface. Curr. Opin. Plant Biol, 20:47–54. doi.org/10.1016/j.pbi.2014.04.007.
14. Brown J, Guest D. 1980. Plant defences against pathogens. Australian Vice-Chancellors' Committee, Canberra. pp. 263-285.
15. Brun H, Chèvre AM, Fitt BD, Powers S, Bernard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard M, Andrivon D. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol, 185/1:285-99. doi: 10.1111/j.1469-8137.2009.03049.x
16. Buonaurio R. 2008. Infection and plant defense responses during plant-bacterial interaction. In: Barka EA. Clément C (eds). Plant-Microbe Interactions pp. 169-197.
17. Casadevall A, Pirofski L. 1999. Host–pathogen interactions:redefining the basic concepts of virulence and pathogenicity. Infection and Immunity, 67:3703–3713.
18. Casadevall A, Pirofski L. 2009. Virulence factors and their mechanisms of action: the view from damage–response framework. Journal of Water and Health 7/1:2–18.
19. Chaudhari P, Ahmed B, Joly DL, Germain H. 2014. Effector biology during biotrophic invasion of plant cells. Virulence, 5/7:703-709. doi:10.4161/viru.29652.
20. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: Shaping the evolution of the plant immun response. Cell, 124:803-814.
21. Coll N, Epple P, Dangl J. 2011. Programmed cell death in the plant immune system. Cell Death Differ, 18:1247–1256.
22. Dahal D, Heintz D, Van Dorssealaer A, Braun HP, Wydra K. 2009. Pathogenesis and Stress Related, as well as Metabolic Proteins are Regulated in Tomato Stems Infected with Ralstonia solanacearum. Plant Physiolog Biochem, 47:838-846.
23. Dangl, JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112:379–389.
24. Dangl JL. 2013. Pivoting the plant immune system from dissection to deployment. Science. 341:746–751.
25. Datnoff LE, Elmer WH, Huber DM. 2007. Mineral nutrition and plant disease. APS Press, St Paul.
26. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, Cervone F. 2003. The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci USA,100/17:10124-10128; DOI:10.1073/pnas.1733690100.
27. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet, 11:539–548.
28. Dou D, Zhou JM. 2012. Phytopathogen effectors subverting host immunity:different foes, similar battleground. Cell Host Microbe, 12:484-495.
29. Doughari, JH. 2015. An Overview of Plant Immunity. J Plant Pathol Microbiol, 6:11. http://dx.doi.org/10.4172/2157-7471.1000322.
30. Ebel J, Cosio EG. 1994. “Elicitors of plant defense responses,” International Review of Cytology, 148:1–36.
31. Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR. 2007. The Role of Plant Defence Proteins in Fungal Pathogenesis. Mol Plant Patholog, 8:677-700. DOI: 10.111/j.1364-3703-2007.00419.x.
32. Flor HH. 1942. Inheritance of pathogenicity in Melampsora lini. Phytopathology, 32: 653-669.
33. Freeman BC, Beattite GA. 2008. An Overwiev of Plant Defenses against Pathpgens and Herbivores. The Plant Health Instructor, DOI: 10.1094/PHI-I-2008-0226-01.
34. Gebrie SA. 2016. Biotrophic Fungi Infection and Plant Defense Mechanism. J Plant Pathol Microbiol, 7:378. doi: 10.4172/2157-7471.1000378.
35. Gill US, Lee S, Mysore KS. 2015. Host versus nonhost resistance: distinct wars with similar arsenals. Phytopathology, 105/5: 580-7. doi: 10.1094/PHYTO-11-14-0298-RVW.
36. Glazebrook J. 2005. CONTRASTING MECHANISMS OF DEFENSE AGAINST BIOTROPHIC AND NECROTROPHIC PATHOGENS. Annu. Rev. Phytopathol, 43:205–27.
37. Gopalan S, Bauer DW, Alfano JR, Loniello AO, He SY, Collmer A. 1996. Expression of the Pseudomonas syringae avirulence protein Avrb in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell, 8:1095–1105
38. Gómez-Gómez L, Boller T. 2000. FLS2: An LRR receptor-like kinase involved in the perception bacterial elicitor flagellin in Arabidopsis. Mol. Cell, 5:1003-1011.
39. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangle JL. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science, 11/269(5225):843-846.
40. Guttman DS, McHardy AC, Schulze-Lefert P. 2014. Microbial genome-enabled insights into plant-microorganism interactions. Nat Rev Genet, 15:797-813.
41. Hahn, MG.1996. “Microbial elicitors and their receptors in plants,” Annual Review of Phytopathology, 34:387–412.
42. Hammond-Kosack KE, Paerker JE. 2003. Deciphering plant-pathogen communication: fresh perpectives for molecular resistance breeding. Curr Opin Biotechnol, 14/2:177-93. PMID: 12732319.
43. Hauck P, Thilmony R, He SY. 2003. A Pseudomonas syringae type III effector supresses cell Wall-based extracellular defense in susceptible Arabidopsis plant. Proc. Natl. Acad. Sci. USA, 100:8577-8582.
44. Heath MC. 1997. Evolution of plant resistance and susceptibility to fungal parasites. In: Carroll GC, Tudzynski P, eds. The Mycota V, Part B. Plant relationships. Berlin-
45. Heidelberg, Germany: Springer Verlag, 258–276.
46. Heath, MC. 2000. Nonhost resistance and non specific plant defenses. Curr. Opin. Plant Biol, 3:315-319. https://doi.org/10.1016/S1369-5266(00)00087-X.
47. Henry G, Thonart P, Ongena M. 2012. PAMPs, MAMPs, DAMPs and others: an update on the diversity of plant immunity elicitors. Biotechnol. Agron. Soc. Environ, 16/2:257-268.
48. Hou S, Yang Y, Wu D, Zhang C. 2011. Plant immunity: evolutionary insights from PBS1, Pto, and RIN4. Plant Signal Behav, 6/6:794-9. PMID: 21494098.
49. Huang HC, Hutcheson SW, Collmer A. 1991. Characterization of the hrp clustur from Pseudomonas syringae pv syringae 61 and TnphoA tagging of genes encoding exported or membrane-spaning Hrp proteins. Mol Plant Microbe Interact, 4:469-476.
50. Jones JDG, Dangl JL. 2006. The plant immune system. Nature, 444:323–9. doi: 10.1038/nature05286.
51. Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol, 44:41-60. DOI:10.1146/annurev.phyto.44.070505.143436.
52. Kemen E, Jones JD. 2012. Obligate biotroph parasitism: can we link genomes to lifestyle? Trends Plant Sci, 17:448-457.
53. Kim MG, Cunha L, McFall AJ, Belkhadir Y, DebRoy, S, Dangl JL, David M. 2005. Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis. 121/5:749-759. DOI: http://dx.doi.org/10.1016/j.cell.2005.03.025.
54. Kim J, Lim CJ, Lee BW, Choi JP, Oh SK, Ahmad R, Kwon SY, Ahn J, Hur CG. 2012. A genome-wide comparison of NB-LRR type of resistance gene analogs (RGA) in the plant kingdom. Mol Cells, 33/4:385-92. doi: 10.1007/s10059-012-0003-8.
55. Kiraly L, Barnaz B, Kiraly Z. 2007. Plant Resistance to Pathogen Infection: Forms and Mechanisms of Innate and Acquired Resistance. Journal of Phytopathol, 155:385-396. DOI: 10.111/j.1439-0434.2007.01264.x.
56. Kushalappa AC, Yogendra K, Karre S. 2016. Plant Innate Immune Response: Qualitative and Quantitative Resistance. Crit Rev Plant Sci, 35/1:38–55, http://dx.doi.org/10.1080/07352689.2016.1148980.
57. Laluk K, Mengiste T. 2010. Necrotroph Attacks on Plants: Wanton Destruction or Covert Extortion? The Arabidopsis Book by American Society of Plant Biologists, 8:e0136. doi:10.1199/tab.0136.
58. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G. 2009. RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol, 30/7(6):e1000139. doi: 10.1371/journal.pbio.1000139.
59. Li B, Meng X, Shan L, He P. 2016. Transcriptional regulation of pattern-triggered immunity in plants. Cell host & microbe, 19/5:641-650. doi:10.1016/j.chom.2016.04.011.
60. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME,Liang X, Tor M, Billiar T. 2007. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev, 220:60-81.
61. Luderer R, Joosten MH. 2001. Avirulence proteins of plant pathogens: determinants of victory and defeat. Mol. Plant Pathol, 2:355–64.
62. Macho, A.P, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Mol. Cell, 54:263–272. DOI:10.1016/j.molcel.2014.03.028.
63. Macho AP, Zipfel C. 2015. Targeting of plant pattern recognition receptor triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol, 23:14–22. DOI:10.1016/j.mib.2014.10.009.
64. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112:379–389.
65. Mackey D, McFall J. 2006. MAMPs and MIMIPs; Proposed Classification for Inducers of Innate Immunity. Mol Microbiol, 61/6:1365–1371. doi:10.1111/j.1365-2958.2006.05311.x.
66. Maffei ME, Arimura G, Mithöfer A. 2012. Natural elicitors, effectors and modulators of plant responses. Nat Prod Rep. 29(11):1288-303. doi: 10.1039/c2np20053h. Nat. Prod. Rep, 29:1288–1303. DOI: 10.1039/c2np20053h.
67. Martin, G.B., Bogdanove, A.J., Sessa, G. 2003. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol, 54:23-61.
68. Meehan F, Murphy HC. 1947. Differential phytotoxicity of metabolic byproducts of Helminthosporium victoriae. Science, 106:270–71.
69. Mendgen K, Hahn M. 2002. Plant infection and the establishment of fungal biotrophy. Trends Plant Sci, 7/8:352-6.
70. Mengiste, T. 2012. Plant Immunity to Necrotrophs. Annu. Rev. Phytopathol, 50:267–94.
71. Mindrinos M, Katagiri F, Yu GL, Ausubel FM. 1994. The A.thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell, 78:1089–1099.
72. Monaghan J, Zipfel C. 2012. Plant Pattern Recognition Receptor Complexes at the Plasma Membrane. CURR OPIN PLANT BIOL Curr Opin Plant Biol, 15/4:349-357. DOI: 10.1016/j.pbi.2012.05.006S.
73. Montesano M, Brader G. Palva ET. 2003. Pathogen derived elicitors: searching for receptors in plants. Mol. Plant Pathol, 4:73-79.
74. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot, 59:501–520.
75. Mysore, K. S, Ryu, CM. 2004. Nonhost resistance: How much do we know? Trends Plant Sci, 9:97-104. https://doi.org/10.1016/j.tplants.2003.12.005
76. Newman M-A, Sundelin T, Nielsen JT, Erbs G. 2013. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci, 4:139.
77. Nürnberger T. 1999. “Signal perception in plant pathogen defense,” Cellular and Molecular Life Science, 55:167–182.
78. Nürnberger, T, Brunner F, Kemmerling B, Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev, 198:249–266.
79. Oliver RP, Ipcho SV. 2004. Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol Plant Pathol, 1/5(4):347-52. doi: 10.1111/j.1364-3703.2004.00228.x.
80. Oliver RP, Solomon PS. 2010. New developments in pathogenicity and virulence of necrotrophs. Curr. Opin. Plant Biol, 13:415–19.
81. Onaga G, Wydra K. 2016. Advances in Plant Tolerance to Biotic Stresses. In: Plant Genomics, Edited by Ibrokhim Y.Abdurakhmonov. DOI: 10.5772/60746.
82. Pedley KF, Martin GB. 2005. Role of mitogen-activated protein kinases in plant immunity. Curr Opin Plant Biol, 8/5:541-7.
83. Perfect SE, Green JR. 2001. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol, 1/2(2):101-108. DOI: 10.1046/j.1364-3703.2001.00055.x.
84. Prell HH, Day P. 2001. Plant-Fungal Pathogen Interaction A Classical and Molecular View. XI, 214 p, ISBN 978-3-540-66727-8. http://www.springer.com/978-3-540-66727-8.
85. Pusztahelyi T, Holb IJ, Pócsi I. 2015. Secondary metabolites in fungus-plant interactions. Front Plant Sci, 6:573.
86. Ritter C, Dangl JL. 1995. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol Plant Microbe Interact, 8/3:444-453.
87. Shimizu R, Taguchi F, Marutani M. 2003. The DeltafliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells. Mol. Genet. Genomics, 269:21-30.
88. Shiu SH, Bleecker AB. 2003. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol, 132/2:530-43. DOI:10.1104/pp.103.021964.
89. Slusarenko AJ, Fraser RSS, Van Loon LC. 2000. Mechanisms of resistance to plant diseases. Kluwer Academic Publishers. Pp, 620. ISBN: 079236418X 9780792364184 1402003994 9781402003998.
90. Spoel, SH, Dong X. 2012. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol, 12:89–100.
91. Staskawicz BJ, Dahlbeck D, Keen NT. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc. Natl. Acad. Sci, 81:6024–28.
92. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD. 1995. Molecular genetics of plant disease resistance. Science, 5/268(5211):661–667.
93. Stone JK. 2001. Necrotroph, In: Encyclopedia of plant pathology, OC Maloy, TD Murray (eds.) 2:81676-81677.
94. Stotz HU, Mitrousia GK, de Wit PJGM, Fitt BDL. 2014. Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci, 19/8:491–500. http://doi.org/10.1016/j.tplants.2014.04.009.
95. Strange NR. 2003. Introduction to Plant Pathology. Pp. 480. John Wiley & Sons Publishers, ISBN: 978-0-470-84973-6.
96. Surico G. 2013. The concepts of plant pathogenicity, virulence/avirulence and effector proteins by a teacher of plant pathology. Phytopathol Mediterr, 52/3:399−417.
97. Tanaka S. 1933. Studies on black spot disease of Japanese pears (Pirus serotina Rehd). Mem. Coll. Agric. Kyoto Imp. Univ, 28:1–31.
98. Thomma BPHJ, Nürnberger T, Joosten MHAJ. 2011. Of PAMPs and Effectors: The Blurred PTI-ETI Dichotomy. The Plant Cell, 23:4-15. DOI: https://doi.org/10.1105/tpc.110.082602.
99. Van der Biezen EA, Jones JD. 1998. Plant disease-resistance proteins and gene-for-gen concept. Trends Biochem Sci, 23:454-456.
100. Van derplank JE. 1960. Analysis of epidemics. In: Plant Pathology III, cds. 1. G. Horsfall, A. E. Dimond. New York: Academic. 229-289.
101. Van Ooijen G, Van den Burg HA, Cornelissen BJ, Takken FL. 2007. Structure and function of resistance proteins in solanaceous plants. Annu. Rev. Phytopathol, 45:43-72. Vleeshouwers GAAV, Oliver RP. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol Plant Microbe Interact, 27/3:196-206. doi: 10.1094/MPMI-10-13-0313-IA.
102. Walton JD. 1996. Host-selective toxins: agents of compatibility. Plant Cell. 8/10:1723-33.
103. Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu CM, Woods-Tör A, Zipfel C, de Wit PJ, Jones JD, Tör M, Thomma BP. 2008. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiology, 147:503–517.
104. Wen L. 2012. Cell Death in Plant Immune Response to Necrotrophs. J Plant Biochem Physiol, 1:e103.
105. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, Schornack S, Zipfel C, RobatzekS, Hogenhout SA, Kamoun S. 2012. Effector Biology of Plant-Associated Organisms: Concepts and Perspectives. Cold Spring Harb Symp Quant Biol, 77:235-247. doi: 10.1101/sqb.2012.77.015933.
106. Wolpert TJ, Dunkle LD, Ciuffetti LM. 2002. Host-selective toxins and avirulence determinants: What's in a name?Annu. Rev. Phytopathol, 40:251–85.
107. Yamaguchi Y, Huffaker A. 2011. Endogenous peptide elicitors in higher plants. Curr Opi Plant Biol, 14/4:351–357. DOI 10.1016/j.pbi.2011.05.001.
108. Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM. 2007. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe, 17/1(3):175-85. DOI:10.1016/j.chom.2007.03.006.
109. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428:764-767.
110. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell, 125:749–760.
111. Zipfel C, Robatzek S. 2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi..? Plant Physiol, 154:551–554.