Innate immune memory in plants

Seminars in Immunology

Volumn 28, Issue 4, 2016, Pages 319-327

  Reimer Michalski, Eva Maria ^a   Conrath, Uwe ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Defense priming; Epigenetic memory; Plant innate immunity; Systemic plant immunity

Indexed keywords

PATTERN RECOGNITION RECEPTOR; ARABIDOPSIS PROTEIN; CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; NPR1 PROTEIN, ARABIDOPSIS; OXYLIPIN; PIPECOLIC ACID; PIPECOLIC ACID DERIVATIVE; SALICYLIC ACID;

CHROMATIN; CONVERGENT EVOLUTION; ENZYME ACTIVITY; HOST RESISTANCE; IMMUNOLOGICAL MEMORY; INHERITANCE; MOLECULAR DYNAMICS; NONHUMAN; PLANT DEFENSE; PLANT IMMUNITY; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC ACQUIRED RESISTANCE; VERTEBRATE; ANIMAL; BACTERIAL INFECTION; DNA METHYLATION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PLANT; PLANT ROOT;

ANIMALS; ARABIDOPSIS PROTEINS; BACTERIAL INFECTIONS; CYCLOPENTANES; DNA METHYLATION; ETHYLENES; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; OXYLIPINS; PIPECOLIC ACIDS; PLANT IMMUNITY; PLANT ROOTS; PLANTS; RECEPTORS, PATTERN RECOGNITION; SALICYLIC ACID; SIGNAL TRANSDUCTION;

EID: 84976482170     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2016.05.006     Document Type: Review

References (194)

1. [1] Heath, M.C., Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3 (2000), 315–319.
2. [2] Lipka, U., Fuchs, R., Kuhns, C., Petutschnig, E., Lipka, V., Live and let die-Arabidopsis nonhost resistance to powdery mildews. Eur. J. Cell Biol. 89 (2010), 194–199.
3. [3] Thordal-Christensen, H., Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6 (2003), 351–357.
4. [4] Mysore, K.S., Ryu, C., Nonhost resistance: how much do we know?. Trends Plant Sci. 9 (2004), 97–104.
5. [5] Ahuja, I., Kissen, R., Bones, A.M., Phytoalexins in defense against pathogens. Trends Plant Sci. 17 (2012), 73–90.
6. [6] Jones, J.D.G., Dangl, J.L., The plant immune system. Nature 444 (2006), 323–329.
7. [7] Takeuchi, O., Akira, S., Pattern recognition receptors and inflammation. Cell 140 (2010), 805–820.
8. [8] Macho, A.P., Zipfel, C., Plant PRRs and the activation of innate immune signaling. Mol. Cell 54 (2014), 263–272.
9. [9] Ham, J.H., Kim, M.G., Lee, S.Y., Mackey, D., Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv phaseolicola. Plant J. 51 (2007), 604–616.
10. [10] Senthil-Kumar, M., Mysore, K.S., Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu. Rev. Phytopathol. 51 (2013), 407–427.
11. [11] Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., et al. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310 (2005), 1180–1183.
12. [12] Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B., Molina, A., Schulze-Lefert, P., et al. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18 (2006), 731–746.
13. [13] Bednarek, P., Pislewska-Bednarek, M., Svatos, A., Schneider, B., Doubsky, J., Mansurova, M., et al. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323 (2009), 101–106.
14. [14] Kobae, Y., Sekino, T., Yoshioka, H., Nakagawa, T., Martinoia, E., Maeshima, M., Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol. 47 (2006), 309–318.
15. [15] Loehrer, M., Langenbach, C., Goellner, K., Conrath, U., Schaffrath, U., Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol. Plant Microbe Interact. 21 (2008), 1421–1430.
16. [16] Xin, X., Nomura, K., Underwood, W., He, S.Y., Induction and suppression of PEN3 focal accumulation during Pseudomonas syringae pv tomato DC3000 infection of Arabidopsis. Mol. Plant Microbe Interact. 26 (2013), 861–867.
17. [17] Johansson, O.N., Fantozzi, E., Fahlberg, P., Nilsson, A.K., Buhot, N., Tor, M., et al. Role of the penetration-resistance genes PEN1, PEN2 and PEN3 in the hypersensitive response and race-specific resistance in Arabidopsis thaliana. Plant J. 79 (2014), 466–476.
18. [18] Meyer, D., Pajonk, S., Micali, C., O'Connell, R., Schulze-Lefert, P., Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. 57 (2009), 986–999.
19. [19] Underwood, W., Somerville, S.C., Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 12492–12497.
20. [20] Benschop, J.J., Mohammed, S., O'Flaherty, M., Heck, A.J.R., Slijper, M., Menke, F.L.H., Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell. Proteomics 6 (2007), 1198–1214.
21. [21] Haruta, M., Sabat, G., Stecker, K., Minkoff, B.B., Sussman, M.R., A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343 (2014), 408–411.
22. [22] Curran, A., Chang, I., Chang, C., Garg, S., Miguel, R.M., Barron, Y.D., et al. Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Front. Plant Sci., 2, 2011, 36.
23. [23] Campe, R., Langenbach, C., Leissing, F., Popescu, G.V., Popescu, S.C., Goellner, K., et al. ABC transporter PEN3/PDR8/ABCG36 interacts with calmodulin that, like PEN3, is required for Arabidopsis nonhost resistance. New Phytol. 209 (2016), 294–306.
24. [24] Felix, G., Duran, J.D., Volko, S., Boller, T., Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18 (1999), 265–276.
25. [25] Nürnberger, T., Kemmerling, B., Receptor protein kinases-pattern recognition receptors in plant immunity. Trends Plant Sci. 11 (2006), 519–522.
26. [26] Zipfel, C., Plant pattern-recognition receptors. Trends Immunol. 35 (2014), 345–351.
27. [27] Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D.G., Boller, T., et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125 (2006), 749–760.
28. [28] Akira, S., Uematsu, S., Takeuchi, O., Pathogen recognition and innate immunity. Cell 124 (2006), 783–801.
29. [29] Uma, B., Rani, T.S., Podile, A.R., Warriors at the gate that never sleep: non-host resistance in plants. J. Plant Physiol. 168 (2011), 2141–2152.
30. [30] Segonzac, C., Zipfel, C., Activation of plant pattern-recognition receptors by bacteria. Curr. Opin. Microbiol. 14 (2011), 54–61.
31. [31] Muthamilarasan, M., Prasad, M., Plant innate immunity: an updated insight into defense mechanism. J. Biosci. 38 (2013), 433–449.
32. [32] Bigeard, J., Colcombet, J., Hirt, H., Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant 8 (2015), 521–539.
33. [33] Lewis, L.A., Polanski, K., de Torres-Zabala, M., Jayaraman, S., Bowden, L., Moore, J., et al. Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with Pseudomonas syringae pv tomato DC3000. Plant Cell 27 (2015), 3038–3064.
34. [34] Huffaker, A., Ryan, C.A., Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 10732–10736.
35. [35] Yamaguchi, Y., Huffaker, A., Endogenous peptide elicitors in higher plants. Curr. Opin. Plant Biol. 14 (2011), 351–357.
36. [36] Tintor, N., Ross, A., Kanehara, K., Yamada, K., Fan, L., Kemmerling, B., et al. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 6211–6216.
37. [37] Ross, A., Yamada, K., Hiruma, K., Yamashita-Yamada, M., Lu, X., Takano, Y., et al. The Arabidopsis PEPR pathway couples local and systemic plant immunity. EMBO J. 33 (2014), 62–75.
38. [38] Bartels, S., Boller, T., Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. J. Exp. Bot. 66 (2015), 5183–5193.
39. [39] Li, H., Xu, H., Zhou, Y., Zhang, J., Long, C., Li, S., et al. The phosphothreonine lyase activity of a bacterial type III effector family. Science 315 (2007), 1000–1003.
40. [40] Zhang, J., Shao, F., Li, Y., Cui, H., Chen, L., Li, H., et al. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1 (2007), 175–185.
41. [41] Asai, S., Shirasu, K., Plant cells under siege: plant immune system versus pathogen effectors. Curr. Opin. Plant Biol. 28 (2015), 1–8.
42. [42] Lindeberg, M., Cunnac, S., Collmer, A., The evolution of Pseudomonas syringae host specificity and type III effector repertoires. Mol. Plant Pathol. 10 (2009), 767–775.
43. [43] Cunnac, S., Lindeberg, M., Collmer, A., Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol 12 (2009), 53–60.
44. [44] Deslandes, L., Rivas, S., Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17 (2012), 644–655.
45. [45] Feng, F., Zhou, J., Plant-bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15 (2012), 469–476.
46. [46] Macho, A.P., Zipfel, C., Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23 (2015), 14–22.
47. [47] Panstruga, R., Dodds, P.N., Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324 (2009), 748–750.
48. [48] Hückelhoven, R., Panstruga, R., Cell biology of the plant-powdery mildew interaction. Curr. Opin. Plant Biol. 14 (2011), 738–746.
49. [49] Dou, D., Zhou, J., Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12 (2012), 484–495.
50. [50] Flor, H.H., Inheritance of pathogenicity in Melampsora lini. Phytopathology 32 (1942), 653–669.
51. [51] Flor, H.H., Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9 (1971), 275–296.
52. [52] Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R., Dangl, J.L., Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112 (2003), 379–389.
53. [53] Dodds, P.N., Rathjen, J.P., Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11 (2010), 539–548.
54. [54] Henry, E., Yadeta, K.A., Coaker, G., Recognition of bacterial plant pathogens: local, systemic and transgenerational immunity. New Phytol. 199 (2013), 908–915.
55. [55] Khan, M., Subramaniam, R., Desveaux, D., Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr. Opin. Microbiol. 29 (2015), 49–55.
56. [56] Mackey, D., Holt, B.F., Wiig, A., Dangl, J.L., RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108 (2002), 743–754.
57. [57] Coll, N.S., Epple, P., Dangl, J.L., Programmed cell death in the plant immune system. Cell Death Differ. 18 (2011), 1247–1256.
58. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79 (1994), 583–593.
59. [59] Heidrich, K., Wirthmueller, L., Tasset, C., Pouzet, C., Deslandes, L., Parker, J.E., Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334 (2011), 1401–1404.
60. [60] Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T., et al. The transcriptional innate immune response to flg22: interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135 (2004), 1113–1128.
61. [61] Tsuda, K., Somssich, I.E., Transcriptional networks in plant immunity. New Phytol. 206 (2015), 932–947.
62. [62] Tsuda, K., Katagiri, F., Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13 (2010), 459–465.
63. [63] Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H., Han, B., et al. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15 (2003), 317–330.
64. [64] Caldo, R.A., Nettleton, D., Wise, R.P., Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16 (2004), 2514–2528.
65. [65] Gómez-Gómez, L., Felix, G., Boller, T., A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18 (1999), 277–284.
66. [66] Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., et al. The innate immune response to bacterial flagellin is mediated by toll-like receptor 5. Nature 410 (2001), 1099–1103.
67. [67] Ausubel, F.M., Are innate immune signaling pathways in plants and animals conserved?. Nat. Immunol. 6 (2005), 973–979.
68. [68] Diacovich, L., Gorvel, J., Bacterial manipulation of innate immunity to promote infection. Nat. Rev. Microbiol. 8 (2010), 117–128.
69. [69] Kumar, S., Ingle, H., Prasad, D.V.R., Kumar, H., Recognition of bacterial infection by innate immune sensors. Crit Rev. Microbiol. 39 (2013), 229–246.
70. [70] Stuart, L.M., Paquette, N., Boyer, L., Effector-triggered versus pattern-triggered immunity: how animals sense pathogens. Nat. Rev. Immunol. 13 (2013), 199–206.
71. [71] Spoel, S.H., Dong, X., How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12 (2012), 89–100.
72. [72] Fu, Z.Q., Dong, X., Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64 (2013), 839–863.
73. [73] Dempsey, D.A., Klessig, D.F., SOS-too many signals for systemic acquired resistance?. Trends Plant Sci. 17 (2012), 538–545.
74. [74] Chester, K.S., The problem of acquired physiological immunity in plants. Quart. Rev. Biol. 8 (1933), 275–324.
75. [75] Ross, A., Systemic acquired resistance induced by localized virus infections in plants. Virology 14 (1961), 340–358.
76. [76] Malamy, J., Carr, J.P., Klessig, D.F., Raskin, I., Salicyclic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250 (1990), 1002–1004.
77. [77] Métraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., et al. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250 (1990), 1004–1006.
78. [78] Ryals, J., Uknes, S., Ward, E., Systemic acquired resistance. Plant Physiol. 104 (1994), 1109–1112.
79. [79] Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., et al. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261 (1993), 754–756.
80. [80] Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., et al. A central role of salicylic acid in plant disease resistance. Science 266 (1994), 1247–1250.
81. [81] Navarova, H., Bernsdorff, F., Doring, A., Zeier, J., Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24 (2012), 5123–5141.
82. [82] Bernsdorff, F., Döring, A., Gruner, K., Schuck, S., Bräutigam, A., Zeier, J., Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and -independent pathways. Plant Cell 28 (2016), 102–129.
83. [83] Shah, J., Zeier, J., Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci., 4, 2013, 30.
84. [84] Gao, Q., Zhu, S., Kachroo, P., Kachroo, A., Signal regulators of systemic acquired resistance. Front. Plant Sci., 6, 2015, 228.
85. [85] Shah, J., Chaturvedi, R., Chowdhury, Z., Venables, B., Petros, R.A., Signaling by small metabolites in systemic acquired resistance. Plant J. 79 (2014), 645–658.
86. [86] Yu, K., Soares, J.M., Mandal, M.K., Wang, C., Chanda, B., Gifford, A.N., et al. A feedback regulatory loop between G3 P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep. 3 (2013), 1266–1278.
87. [87] Bai, Y., Muller, D.B., Srinivas, G., Garrido-Oter, R., Potthoff, E., Rott, M., et al. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528 (2015), 364–369.
88. [88] Bakker Peter, A.H.M., Pieterse, C.M.J., van Loon, L.C., Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97 (2007), 239–243.
89. [89] Pieterse, C.M.J., Poelman, E.H., Van Wees Saskia, C.M., Dicke, M., Induced plant responses to microbes and insects. Front. Plant Sci., 4, 2013, 475.
90. [90] Segarra, G., van der Ent, S., Trillas, I., Pieterse, C.M.J., MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol. 11 (2009), 90–96.
91. [91] Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 13386–13391.
92. [92] Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., Van Wees Saskia, C.M., Bakker Peter, A.H.M., Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52 (2014), 347–375.
93. [93] van Wees, S.C., de Swart, E.A., van Pelt, J.A., van Loon, L.C., Pieterse, C.M., Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 8711–8716.
94. [94] Caarls, L., Pieterse, C.M.J., Van Wees Saskia, C.M., How salicylic acid takes transcriptional control over jasmonic acid signaling. Front. Plant Sci., 6, 2015, 170.
95. [95] Pieterse, C.M.J., Leon-Reyes, A., van der Ent, S., Van Wees Saskia, C.M., Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5 (2009), 308–316.
96. [96] Pieterse, C.M.J., van der Does, D., Zamioudis, C., Leon-Reyes, A., Van Wees Saskia, C.M., Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28 (2012), 489–521.
97. [97] Hilfiker, O., Groux, R., Bruessow, F., Kiefer, K., Zeier, J., Reymond, P., Insect eggs induce a systemic acquired resistance in Arabidopsis. Plant J. 80 (2014), 1085–1094.
98. [98] Gatehouse, J.A., Plant resistance towards insect herbivores: a dynamic interaction. New Phytol. 156 (2002), 145–169.
99. [99] Benikhlef, L., L'Haridon, F., Abou-Mansour, E., Serrano, M., Binda, M., Costa, A., et al. Perception of soft mechanical stress in Arabidopsis leaves activates disease resistance. BMC Plant Biol., 13, 2013, 133.
100. [100] Green, T.R., Ryan, C.A., Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175 (1972), 776–777.
101. [101] Ryan, C.A., Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28 (1990), 425–449.
102. [102] Howe, G.A., Jasmonates as signals in the wound response. J. Plant Growth Regul. 23 (2004), 223–237.
103. [103] Reymond, P., Weber, H., Damond, M., Farmer, E.E., Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12 (2000), 707–719.
104. [104] Beckers, G.J.M., Conrath, U., Priming for stress resistance: from the lab to the field. Curr. Opin. Plant Biol., 10, 2007, 425.
105. [105] Kuć, J., Concepts and direction of induced systemic resistance in plants and its application. Eur. J. Plant Pathol. 107 (2001), 7–12.
106. [106] Baccelli, I., Mauch-Mani, B., β-aminobutyric acid priming of plant defense: the role of ABA and other hormones. Plant Mol. Biol. 53 (2015), 97–119.
107. [107] Lawton, K.A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., et al. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10 (1996), 71–82.
108. [108] Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K.H., et al. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8 (1996), 629–643.
109. [109] Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Rella, M.G., et al. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 10 (1996), 61–70.
110. [110] Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.Y., Hunt, M.D., Systemic acquired resistance. Plant Cell 8 (1996), 1809–1819.
111. [111] Ruess, W., Mueller, K., Knauf-Beiter, G., Kunz, W., Staub, T., Plant activator CGA 245704: an innovative approach for disease control in cereals and tobacco. Proc Brighton Crop Prot Conf Pests and Dis, Brighton, UK Novem 18–21, 1996, 53–60.
112. [112] Conrath, U., Beckers, G.J.M., Langenbach, C.J.G., Jaskiewicz, M.R., Priming for enhanced defense. Annu. Rev. Phytopathol. 53 (2015), 97–119.
113. [113] Horsfall, J.G., Dimond, A.E., Interactions of tissue sugar, growth substances, and disease susceptibility. ZZ Pflanzenkr Pflanzenschutz 64 (1957), 415–421.
114. [114] Herbers, K., Meuwly, P., Metraux, J.P., Sonnewald, U., Salicylic acid-independent induction of pathogenesis-related protein transcripts by sugars is dependent on leaf developmental stage. FEBS Lett. 397 (1996), 239–244.
115. [115] Herbers, K., Meuwly, P., Frommer, W.B., Metraux, J.P., Sonnewald, U., Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8 (1996), 793–803.
116. [116] Johnson, R., Ryan, C.A., Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol. Biol. 14 (1990), 527–536.
117. [117] Geigenberger, P., Stamme, C., Tjaden, J., Schulz, A., Quick, P.W., Betsche, T., et al. Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiol. 125 (2001), 1667–1678.
118. [118] Tjaden, J., Möhlmann, T., Kampfenkel, K., Neuhaus, G.H., Ekkehard, H., Altered plastidic ATP/ADP-transporter activity influences potato (Solanum tuberosum L.) tuber morphology, yield and composition of tuber starch. Plant J., 16, 1998, 540.
119. [119] Linke, C., Conrath, U., Jeblick, W., Betsche, T., Mahn, A., During, K., et al. Inhibition of the plastidic ATP/ADP transporter protein primes potato tubers for augmented elicitation of defense responses and enhances their resistance against Erwinia carotovora. Plant Physiol. 129 (2002), 1607–1615.
120. [120] Conrath, U., Linke, C., Jeblick, W., Geigenberger, P., Quick, W.P., Neuhaus, H.E., Enhanced resistance to Phytophthora infestans and Alternaria solani in leaves and tubers, respectively, of potato plants with decreased activity of the plastidic ATP/ADP transporter. Planta 217 (2003), 75–83.
121. [121] Kúc, J., Translocated signals for plant immunization. Ann. N. Y. Acad. Sci. 494 (1987), 221–223.
122. [122] van der Meer Jos, W.M., Joosten, L.A.B., Riksen, N., Netea, M.G., Trained immunity: a smart way to enhance innate immune defence. Mol. Immunol. 68 (2015), 40–44.
123. [123] Ding, Y., Fromm, M., Avramova, Z., Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat. Commun., 3, 2012, 740.
124. [124] Kuć, J., Induced immunity to plant disease. BioScience 32 (1982), 854–860.
125. [125] Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J., Greenberg, J.T., Priming in systemic plant immunity. Science 324 (2009), 89–91.
126. [126] Kohler, A., Schwindling, S., Conrath, U., Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol. 128 (2002), 1046–1056.
127. [127] Conrath, U., Priming of induced plant defense responses. Advances in Botanical Research Advances in Botanical Research, 2009, Academic Press, 361–395.
128. [128] Beckers, G.J.M., Jaskiewicz, M., Liu, Y., Underwood, W.R., He, S.Y., Zhang, S., et al. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21 (2009), 944–953.
129. [129] Pick, T., Jaskiewicz, M., Peterhänsel, C., Conrath, U., Heat shock factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiol. 159 (2012), 52–55.
130. [130] Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F., Dong, X., The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9 (1997), 1573–1584.
131. [131] van Hulten, M., Pelser, M., van Loon, L.C., Pieterse, C.M.J., Ton, J., Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 5602–5607.
132. [132] Alcázar, R., Reymond, M., Schmitz, G., de Meaux, J., Genetic and evolutionary perspectives on the interplay between plant immunity and development. Curr. Opin. Plant Biol. 14 (2011), 378–384.
133. [133] Huot, B., Yao, J., Montgomery, B.L., He, S.Y., Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7 (2014), 1267–1287.
134. [134] Walters, D.R., Ratsep, J., Havis, N.D., Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64 (2013), 1263–1280.
135. [135] Walters, D.R., Are plants in the field already induced? Implications for practical disease control. Crop Prot. 28 (2009), 459–465.
136. [136] Walters, D., Heil, M., Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant P 71 (2007), 3–17.
137. [137] Heil, M., Ploss, K., Induced resistance enzymes in wild plants – do ‘early birds’ escape from pathogen attack?. Naturwissenschaften 93 (2006), 455–460.
138. [138] Heil, M., Ecological costs of induced resistance. Curr. Opin. Plant Biol. 5 (2002), 345–350.
139. [139] Tateda, C., Zhang, Z., Shrestha, J., Jelenska, J., Chinchilla, D., Greenberg, J.T., Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26 (2014), 4171–4187.
140. [140] Robatzek, S., Wirthmueller, L., Mapping FLS2 function to structure: lRRs, kinase and its working bits. Protoplasma 250 (2013), 671–681.
141. [141] Bruce, T.J., Matthes, M.C., Napier, J.A., Stressful, Pickett J.A., memories of plants: evidence and possible mechanisms. Plant Sci. 173 (2007), 603–608.
142. [142] Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W., Gomez-Gomez, L., et al. MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415 (2002), 977–983.
143. [143] Lee, J., Eschen-Lippold, L., Lassowskat, I., Bottcher, C., Scheel, D., Cellular reprogramming through mitogen-activated protein kinases. Front. Plant Sci., 6, 2015, 940.
144. [144] Yi, S.Y., Min, S.R., Kwon, S., NPR1 is instrumental in priming for the enhanced flg22-induced MPK3 and MPK6 activation. Plant Pathol. J. 31 (2015), 192–194.
145. [145] Nakagami, H., Pitzschke, A., Hirt, H., Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci. 10 (2005), 339–346.
146. [146] Meng, X., Zhang, S., MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51 (2013), 245–266.
147. [147] Dong, X., NPR1, all things considered. Curr. Opin. Plant Biol. 7 (2004), 547–552.
148. [148] Cao, H., Bowling, S.A., Gordon, A.S., Dong, X., Characterization of an Arabidopsis mutant thatis nonresponsive to inducers of systemic acquired resistance. Plant Cell 6 (1994), 1583–1592.
149. [149] Mou, Z., Fan, W., Dong, X., Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113 (2003), 935–944.
150. [150] Cao, H., Glazebrook, J., Clarke, J.D., Volko, S., Dong, X., The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88 (1997), 57–63.
151. [151] van der Ent, S., van Hulten, M., Pozo, M.J., Czechowski, T., Udvardi, M.K., Pieterse, C.M.J., et al. Priming of plant innate immunity by rhizobacteria and β-aminobutyric acid: differences and similarities in regulation. New Phytol. 183 (2009), 419–431.
152. [152] Peterson, C.L., Laniel, M., Histones and histone modifications. Curr. Biol. 14 (2004), 546–551.
153. [153] Gentry, M., Hennig, L., Remodelling chromatin to shape development of plants. Exp. Cell Res. 321 (2014), 40–46.
154. [154] Henikoff, S., Shilatifard, A., Histone modification: cause or cog?. Trends Genet. 27 (2011), 389–396.
155. [155] Berr, A., Shafiq, S., Shen, W., Histone modifications in transcriptional activation during plant development. Biochim. Biophys. Acta 1809 (2011), 567–576.
156. [156] Badeaux, A.I., Shi, Y., Emerging roles for chromatin as a signal integration and storage platform. Nat. Rev. Mol. Cell Biol. 14 (2013), 211–224.
157. [157] Zhang, Y., Reinberg, D., Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Gene Dev. 15 (2001), 2343–2360.
158. [158] Berr, A., Menard, R., Heitz, T., Shen, W., Chromatin modification and remodeling: a regulatory landscape for the control of Arabidopsis defense responses upon pathogen attack. Cell. Microbiol. 14 (2012), 829–839.
159. [159] Bird, A., DNA methylation patterns and epigenetic memory. Genes Dev. 16 (2002), 6–21.
160. [160] Kim, M.Y., Zilberman, D., DNA methylation as a system of plant genomic immunity. Trends Plant Sci. 19 (2014), 320–326.
161. [161] Roudier, F., Teixeira, F.K., Colot, V., Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet. 25 (2009), 511–517.
162. [162] Roudier, F., Ahmed, I., Berard, C., Sarazin, A., Mary-Huard, T., Cortijo, S., et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30 (2011), 1928–1938.
163. [163] Schwämmle, V., Aspalter, C., Sidoli, S., Jensen, O.N., Large scale analysis of co-existing post-translational modifications in histone tails reveals global fine structure of cross-talk. Mol. Cell Proteomics 13 (2014), 1855–1865.
164. [164] Eberharter, A., Becker, P.B., Histone acetylation: a switch between repressive and permissive chromatin. EMBO Rep. 3 (2002), 224–229.
165. [165] Kanno, T., Kanno, Y., Siegel, R.M., Jang, M.K., Lenardo, M.J., Ozato, K., Selective recognition of acetylated histones by bromodomain proteins visualized in living cells. Mol. Cell 13:1 (2004), 33–43.
166. [166] Ng, M.K., Cheung, P., A brief histone in time: understanding the combinatorial functions of histone PTMs in the nucleosome context. Biochem. Cell Biol., 2015, 1–10.
167. [167] Zhang, X., The epigenetic landscape of plants. Science 320 (2008), 489–492.
168. [168] He, G., Elling, A.A., Deng, X.W., The epigenome and plant development. Annu. Rev. Plant Biol. 62 (2011), 411–435.
169. [169] Avramova, Z., Evolution and pleiotropy of TRITHORAX function in Arabidopsis. Int. J. Dev. Biol. 53 (2009), 371–381.
170. [170] Alvarez-Venegas, R., Abdallat, A.A., Guo, M., Alfano, J.R., Avramova, Z., Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2 (2007), 106–113.
171. [171] Jaskiewicz, M., Conrath, U., Peterhänsel, C., Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12 (2011), 50–55.
172. [172] Pokholok, D.K., Harbison, C.T., Levine, S., Cole, M., Hannett, N.M., Lee, T.I., et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122 (2005), 517–527.
173. [173] de La Cruz, X., Lois, S., Sanchez-Molina, S., Martinez-Balbas, M.A., Do protein motifs read the histone code?. Bioessays 27 (2005), 164–175.
174. [174] Feng, S., Jacobsen, S.E., Reik, W., Epigenetic reprogramming in plant and animal development. Science 330 (2010), 622–627.
175. [175] Vermeulen, M., Mulder, K.W., Denissov, S., Pijnappel, W.W.M., Pim, M.A., van Schaik, Frederik, M.A., Varier, R.A., et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131 (2007), 58–69.
176. [176] Singh, P., Yekondi, S., Chen, P., Tsai, C., Yu, C., Wu, K., et al. Environmental history modulates Arabidopsis pattern-triggered immunity in a histone acetyltransferase1-dependent manner. Plant Cell 26 (2014), 2676–2688.
177. [177] Lamarck, J.B., Philosophie zoologique, ou exposition des considérations relatives à l'histoire naturelle des animaux. Philosophie Zoologique Ou Exposition des Consid́erations Relatives a L'histoire Naturelle des Animaux, 1809, Macmillan, London.
178. [178] Luna, E., Bruce, T.J.A., Roberts, M.R., Flors, V., Ton, J., Next-generation systemic acquired resistance. Plant Physiol. 158 (2012), 844–853.
179. [179] Luna, E., Ton, J., The epigenetic machinery controlling transgenerational systemic acquired resistance. Plant Signal. Behav. 7 (2012), 615–618.
180. [180] Ptashne, M., Faddish stuff: epigenetics and the inheritance of acquired characteristics. FASEB J. 27 (2013), 1–2.
181. [181] Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., Mauch-Mani, B., Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158 (2012), 835–843.
182. [182] Mackaness, G.B., The immunological basis of acquired cellular resistance. J. Exp. Med. 120 (1964), 105–120.
183. [183] Mackaness, G.B., The influence of immunologically committed lymphoid cells on macrophage activity in vivo. J. Exp. Med. 129 (1969), 973–992.
184. [184] Netea, M.G., Quintin, J., van der Meer, J.W., Trained immunity: a memory for innate host defense. Cell Host Microbe 9 (2011), 355–361.
185. [185] Hayes, M.P., Freeman, S.L., Donnelly, R.P., IFN-γ priming of monocytes enhances LPS-induced TNF production by augmenting both transcription and mRNA stability. Cytokine 7 (1995), 427–435.
186. [186] Hayes, M.P., Wang, J., Norcross, M.A., Regulation of interleukin-12 expression in human monocytes: selective priming by interferon-gamma of lipopolysaccharide-inducible p35 and p40 genes. Blood 86 (1995), 646–650.
187. [187] Isaacs, A., Burke, D.C., Mode of action of interferon. Nature 182 (1958), 1073–1074.
188. [188] Stewart, W.E., Gosser, L.B., Lockart, R.Z. Jr., Priming: a nonantiviral function of interferon. J. Virol. 7 (1971), 792–801.
189. [189] Sun, J.C., Beilke, J.N., Lanier, L.L., Adaptive immune features of natural killer cells. Nature 457 (2009), 557–561.
190. [190] Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L.A.B., Ifrim, D.C., Saeed, S., et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 17537–17542.
191. [191] Quintin, J., Saeed, S., Martens, J.H.A., Giamarellos-Bourboulis, E.J., Ifrim, D.C., Logie, C., et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12 (2012), 223–232.
192. [192] Schroder, K., Sweet, M.J., Hume, D.A., Signal integration between IFNγ and TLR signaling pathways in macrophages. Immunobiology 211 (2006), 511–524.
193. [193] Hon, G.C., Rajagopal, N., Shen, Y., McCleary, D.F., Yue, F., Dang, M.D., et al. Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat. Genet. 45 (2013), 1198–1206.
194. [194] Quintin, J., Cheng, S.-C., van der Meer Jos, W.M., Netea, M.G., Innate immune memory: towards a better understanding of host defense mechanisms. Curr. Opin. Immunol. 29 (2014), 1–7.