1932

Abstract

As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-082718-095959
2019-08-25
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/phyto/57/1/annurev-phyto-082718-095959.html?itemId=/content/journals/10.1146/annurev-phyto-082718-095959&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ade J, DeYoung BJ, Golstein C, Innes RW 2007. Indirect activation of a plant nucleotide binding site–leucine-rich repeat protein by a bacterial protease. PNAS 104:72531–36
    [Google Scholar]
  2. 2. 
    Agrawal AA, Laforsch C, Tollrian R 1999. Transgenerational induction of defences in animals and plants. Nature 401:674860–63
    [Google Scholar]
  3. 3. 
    Ahmad S, Van Hulten M, Martin J, Pieterse CMJ, Van Wees SCM, Ton J 2011. Genetic dissection of basal defence responsiveness in accessions of Arabidopsis thaliana. Plant Cell Environ 34:71191–206
    [Google Scholar]
  4. 4. 
    Anderson JP, Gleason CA, Foley RC, Thrall PH, Burdon JB, Singh KB 2010. Plants versus pathogens: an evolutionary arms race. Funct. Plant Biol. 37:6499–512
    [Google Scholar]
  5. 5. 
    Bakker PAHM, Pieterse CMJ, De Jonge R, Berendsen RL 2018. The soil-borne legacy. Cell 172:61178–80
    [Google Scholar]
  6. 6. 
    Balint-Kurti P, Simmons SJ, Blum JE, Ballaré CL, Stapleton AE 2010. Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol. Plant-Microbe Interact. 23:4473–84
    [Google Scholar]
  7. 7. 
    Basu S, Varsani S, Louis J 2018. Altering plant defenses: herbivore-associated molecular patterns and effector arsenal of chewing herbivores. Mol. Plant-Microbe Interact. 31:113–21
    [Google Scholar]
  8. 8. 
    Bebber DP. 2015. Range-expanding pests and pathogens in a warming world. Annu. Rev. Phytopathol. 53:335–56
    [Google Scholar]
  9. 9. 
    Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY et al. 2009. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:3944–53
    [Google Scholar]
  10. 10. 
    Bender J. 2004. DNA methylation and epigenetics. Annu. Rev. Plant Biol. 55:41–68
    [Google Scholar]
  11. 11. 
    Berendsen RL, Vismans G, Yu K, Song Y, De Jonge R et al. 2018. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:61496–507
    [Google Scholar]
  12. 12. 
    Berg M, Koskella B. 2018. Nutrient- and dose-dependent microbiome-mediated protection against a plant pathogen. Curr. Biol. 28:152487–92
    [Google Scholar]
  13. 13. 
    Bewick AJ, Ji L, Niederhuth CE, Willing E-M, Hofmeister BT et al. 2016. On the origin and evolutionary consequences of gene body DNA methylation. PNAS 113:329111–16
    [Google Scholar]
  14. 14. 
    Bigeard J, Colcombet J, Hirt H 2015. Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant 8:4521–39
    [Google Scholar]
  15. 15. 
    Birch ANE, Wynne Griffiths D, Hopkins RJ, Macfarlane Smith WH, McKinlay RG 1992. Glucosinolate responses of swede, kale, forage and oilseed rape to root damage by turnip root fly (Deliafloralis) larvae. J. Sci. Food Agric. 60:11–9
    [Google Scholar]
  16. 16. 
    Boughton AJ, Hoover K, Felton GW 2005. Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersiconesculentum. J. Chem. Ecol. 31:92211–16
    [Google Scholar]
  17. 17. 
    Boutrot F, Zipfel C. 2017. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 55:257–86
    [Google Scholar]
  18. 18. 
    Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, Kovalchuk I 2007. Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic Acids Res 35:51714–25
    [Google Scholar]
  19. 19. 
    Bozarth RF, Ross AF. 1964. Systemic resistance induced by localized virus infections: extent of changes in uninfected plant parts. Virology 24:3446–55
    [Google Scholar]
  20. 20. 
    Bronstein JL, Alarcón R, Geber M 2006. The evolution of plant-insect mutualisms. New Phytol 172:3412–28
    [Google Scholar]
  21. 21. 
    Bruce TJA, Matthes MC, Napier JA, Pickett JA 2007. Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:6603–8
    [Google Scholar]
  22. 22. 
    Burow M, Halkier BA. 2017. How does a plant orchestrate defense in time and space? Using glucosinolates in Arabidopsis as case study. Curr. Opin. Plant Biol. 38:142–47
    [Google Scholar]
  23. 23. 
    Buswell W, Schwarzenbacher RE, Luna E, Sellwood M, Chen B et al. 2018. Chemical priming of immunity without costs to plant growth. New Phytol 218:31205–16
    [Google Scholar]
  24. 24. 
    Cambiagno DA, Nota F, Zavallo D, Rius S, Casati P et al. 2018. Immune receptor genes and pericentromeric transposons as targets of common epigenetic regulatory elements. Plant J 96:61178–90
    [Google Scholar]
  25. 25. 
    Cameron DD, Neal AL, Van Wees SCM, Ton J 2013. Mycorrhiza-induced resistance: more than the sum of its parts?. Trends Plant Sci 18:10539–45
    [Google Scholar]
  26. 26. 
    Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM 2015. Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol. Plant-Microbe Interact. 28:91049–58
    [Google Scholar]
  27. 27. 
    Clavijo McCormick A, Boeckler GA, Köllner TG, Gershenzon J, Unsicker SB 2014. The timing of herbivore-induced volatile emission in black poplar (Populusnigra) and the influence of herbivore age and identity affect the value of individual volatiles as cues for herbivore enemies. BMC Plant Biol 14:304
    [Google Scholar]
  28. 28. 
    Clavijo McCormick A, Irmisch S, Reinecke A, Boeckler GA, Veit D et al. 2014. Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plant Cell Environ 37:81909–23
    [Google Scholar]
  29. 29. 
    Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B et al. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:7184215–19
    [Google Scholar]
  30. 30. 
    Conrath U. 2011. Molecular aspects of defence priming. Trends Plant Sci 16:10524–31
    [Google Scholar]
  31. 31. 
    Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G et al. 2006. Priming: getting ready for battle. Mol. Plant-Microbe Interact. 19:101062–71
    [Google Scholar]
  32. 32. 
    Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR 2015. Priming for enhanced defense. Annu. Rev. Phytopathol. 53:97–119
    [Google Scholar]
  33. 33. 
    Cook DE, Mesarich CH, Thomma BPHJ 2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63
    [Google Scholar]
  34. 34. 
    Cotton TEA, Pétriacq P, Cameron DD, Al Meselmani M, Schwarzenbacher R et al. 2019. Metabolic regulation of the maize rhizobiome by benzoxazinoids. ISME J 13:1647–58
    [Google Scholar]
  35. 35. 
    Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:9537–52
    [Google Scholar]
  36. 36. 
    Cui H, Tsuda K, Parker JE 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
    [Google Scholar]
  37. 37. 
    Deal RB, Henikoff S. 2011. Histone variants and modifications in plant gene regulation. Curr. Opin. Plant Biol. 14:2116–22
    [Google Scholar]
  38. 38. 
    Deng Y, Zhai K, Xie Z, Yang D, Zhu X et al. 2017. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:6328962–65
    [Google Scholar]
  39. 39. 
    De Román M, Fernández I, Wyatt T, Sahrawy M, Heil M, Pozo MJ 2011. Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J. Ecol. 99:136–45
    [Google Scholar]
  40. 40. 
    De Vries J, Poelman EH, Anten N, Evers JB 2018. Elucidating the interaction between light competition and herbivore feeding patterns using functional-structural plant modelling. Ann. Bot. 121:51019–31
    [Google Scholar]
  41. 41. 
    Dicke M, Sabelis MW. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:2148–65
    [Google Scholar]
  42. 42. 
    Dolatabadian A, Patel DA, Edwards D, Batley J 2017. Copy number variation and disease resistance in plants. Theor. Appl. Genet. 130:122479–90
    [Google Scholar]
  43. 43. 
    Douma JC, Vermeulen PJ, Poelman EH, Dicke M, Anten NPR 2017. When does it pay off to prime for defense? A modeling analysis. New Phytol 216:3782–97
    [Google Scholar]
  44. 44. 
    Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM et al. 2012. Widespread dynamic DNA methylation in response to biotic stress. PNAS 109:32E2183–91
    [Google Scholar]
  45. 45. 
    Dubin MJ, Mittelsten Scheid O, Becker C 2018. Transposons: a blessing curse. Curr. Opin. Plant Biol. 42:23–29
    [Google Scholar]
  46. 46. 
    Dudenhöffer JH, Scheu S, Jousset A 2016. Systemic enrichment of antifungal traits in the rhizosphere microbiome after pathogen attack. J. Ecol. 104:61566–75
    [Google Scholar]
  47. 47. 
    Ellis J, Dodds P, Pryor T 2000. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3:4278–84
    [Google Scholar]
  48. 48. 
    Franceschi VR, Krokene P, Christiansen E, Krekling T 2005. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:2353–76
    [Google Scholar]
  49. 49. 
    Furci L, Jain R, Stassen JHM, Berkowitz O, Whelan J et al. 2019. Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. eLife 8:e40655
    [Google Scholar]
  50. 50. 
    Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27
    [Google Scholar]
  51. 51. 
    Hayashi K, Yoshida H. 2009. Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. Plant J 57:3413–25
    [Google Scholar]
  52. 52. 
    Heil M. 2001. Induced systemic resistance (ISR) against pathogens: a promising field for ecological research. Perspect. Plant Ecol. Evol. Syst. 4:265–79
    [Google Scholar]
  53. 53. 
    Heil M, Land WG. 2014. Danger signals: damaged-self recognition across the tree of life. Front. Plant Sci. 5:578
    [Google Scholar]
  54. 54. 
    Hendriks M, Mommer L, De Caluwe H, Smit-Tiekstra A, Van der Putten WH, De Kroon H 2013. Independent variations of plant and soil mixtures reveal soil feedback effects on plant community overyielding. J. Ecol. 101:2287–97
    [Google Scholar]
  55. 55. 
    Hilker M, Kobs C, Varama M, Schrank K 2002. Insect egg deposition induces Pinussylvestris to attract egg parasitoids. J. Exp. Biol. 205:4455–61
    [Google Scholar]
  56. 56. 
    Holeski LM. 2007. Within and between generation phenotypic plasticity in trichome density of Mimulusguttatus. J. Evol. Biol 20:62092–100
    [Google Scholar]
  57. 57. 
    Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD et al. 2014. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun. 5:5320
    [Google Scholar]
  58. 58. 
    Hu L, Robert CAM, Cadot S, Zhang X, Ye M et al. 2018. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9:12738
    [Google Scholar]
  59. 59. 
    Huang X-F, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM 2014. Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:4267–75
    [Google Scholar]
  60. 60. 
    Innerebner G, Knief C, Vorholt JA 2011. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonassyringae by Sphingomonas strains in a controlled model system. Appl. Environ. Microbiol. 77:103202–10
    [Google Scholar]
  61. 61. 
    Jaskiewicz M, Conrath U, Peterhänsel C 2011. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:150–55
    [Google Scholar]
  62. 62. 
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:7117323–29
    [Google Scholar]
  63. 63. 
    Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT 2009. Priming in systemic plant immunity. Science 324:592389–91
    [Google Scholar]
  64. 64. 
    Kathiria P, Sidler C, Golubov A, Kalischuk M, Kawchuk LM, Kovalchuk I 2010. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol 153:41859–70
    [Google Scholar]
  65. 65. 
    Kawakatsu T, Huang SC, Jupe F, Sasaki E, Schmitz RJ et al. 2016. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:2492–505
    [Google Scholar]
  66. 66. 
    Kellenberger RT, Desurmont GA, Schlüter PM, Schiestl FP 2018. Trans-generational inheritance of herbivory-induced phenotypic changes in Brassicarapa. Sci. Rep 8:13536
    [Google Scholar]
  67. 67. 
    Kliebenstein DJ, Rowe HC. 2008. Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction. Plant Sci 174:6551–56
    [Google Scholar]
  68. 68. 
    Kong HG, Kim BK, Song GC, Lee S, Ryu CM 2016. Aboveground whitefly infestation-mediated reshaping of the root microbiota. Front. Microbiol. 7:1314
    [Google Scholar]
  69. 69. 
    Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J et al. 2003. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423:6941760–62
    [Google Scholar]
  70. 70. 
    Krasileva KV, Dahlbeck D, Staskawicz BJ 2010. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:72444–58
    [Google Scholar]
  71. 71. 
    Kulmatiski A, Beard KH, Stevens JR, Cobbold SM 2008. Plant-soil feedbacks: a meta‐analytical review. Ecol. Lett. 11:9980–92
    [Google Scholar]
  72. 72. 
    Kwak Y-S, Weller DM. 2013. Take-all of wheat and natural disease suppression: a review. Plant Pathol. J. 29:2125–35
    [Google Scholar]
  73. 73. 
    Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J et al. 2015. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:6250860–64
    [Google Scholar]
  74. 74. 
    Lee H, Raskin I. 1998. Glucosylation of salicylic acid in Nicotianatabacum cv. Xanthi-nc. Phytopathology 88:7692–97
    [Google Scholar]
  75. 75. 
    Lemanceau P, Barret M, Mazurier S, Mondy S, Pivato B et al. 2017. Plant communication with associated microbiota in the spermosphere, rhizosphere and phyllosphere. Advances in Botanical Research 82 G Becard 101–33 Cambridge, UK: Academic
    [Google Scholar]
  76. 76. 
    Li X, Clarke JD, Zhang Y, Dong X 2001. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant-Microbe Interact. 14:101131–39
    [Google Scholar]
  77. 77. 
    Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM et al. 2001. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:55242077–80
    [Google Scholar]
  78. 78. 
    Lisch D. 2013. How important are transposons for plant evolution?. Nat. Rev. Genet. 14:149–61
    [Google Scholar]
  79. 79. 
    Liu C, Xin Y, Xu L, Cai Z, Xue Y et al. 2018. Arabidopsis ARGONAUTE 1 binds chromatin to promote gene transcription in response to hormones and stresses. Dev. Cell 44:3348–61
    [Google Scholar]
  80. 80. 
    López A, Ramírez V, García-Andrade J, Flors V, Vera P 2011. The RNA silencing enzyme RNA polymerase V is required for plant immunity. PLOS Genet 7:12e1002434
    [Google Scholar]
  81. 81. 
    López Sánchez A, Stassen JHM, Furci L, Smith LM, Ton J 2016. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J 88:3361–74
    [Google Scholar]
  82. 82. 
    Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M et al. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:6107659–62
    [Google Scholar]
  83. 83. 
    Lucht JM, Mauch-Mani B, Steiner H-Y, Metraux J-P, Ryals J, Hohn B 2002. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat. Genet 30:3311–14
    [Google Scholar]
  84. 84. 
    Luna E, Bruce TJA, Roberts MR, Flors V, Ton J 2012. Next-generation systemic acquired resistance. Plant Physiol 158:2844–53
    [Google Scholar]
  85. 85. 
    Luna E, Ton J. 2012. The epigenetic machinery controlling transgenerational systemic acquired resistance. Plant Signal. Behav. 7:6615–18
    [Google Scholar]
  86. 86. 
    Maag D, Köhler A, Robert CAM, Frey M, Wolfender J-L et al. 2016. Highly localized and persistent induction of Bx1-dependent herbivore resistance factors in maize. Plant J 88:6976–91
    [Google Scholar]
  87. 87. 
    Malinovsky FG, Fangel JU, Willats WGT 2014. The role of the cell wall in plant immunity. Front. Plant Sci. 5:178
    [Google Scholar]
  88. 88. 
    Mallinson L, Russell J, Cameron DD, Ton J, Horton P, Barker ME 2018. Why rational argument fails the genetic modification (GM) debate. Food Secur 10:51145–61
    [Google Scholar]
  89. 89. 
    Martin D, Tholl D, Gershenzon J, Bohlmann J 2002. Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:31003–18
    [Google Scholar]
  90. 90. 
    Martin FM, Uroz S, Barker DG 2017. Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356:6340eaad4501
    [Google Scholar]
  91. 91. 
    Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ et al. 2016. Recognizing plant defense priming. Trends Plant Sci 21:10818–22
    [Google Scholar]
  92. 92. 
    Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:6394–408
    [Google Scholar]
  93. 93. 
    McDowell JM, Dhandaydham M, Long TA, Aarts MGM, Goff S et al. 1998. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10:111861–74
    [Google Scholar]
  94. 94. 
    Molinier J, Ries G, Zipfel C, Hohn B 2006. Transgeneration memory of stress in plants. Nature 442:71061046–49
    [Google Scholar]
  95. 95. 
    Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P et al. 2018. The timescale of early land plant evolution. PNAS 115:10E2274–83
    [Google Scholar]
  96. 96. 
    Mumm R, Dicke M. 2010. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can. J. Zool. 88:7628–67
    [Google Scholar]
  97. 97. 
    Mumm R, Hilker M. 2005. The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem. Senses 30:4337–43
    [Google Scholar]
  98. 98. 
    Mumm R, Schrank K, Wegener R, Schulz S, Hilker M 2003. Chemical analysis of volatiles emitted by Pinussylvestris after induction by insect oviposition. J. Chem. Ecol. 29:51235–52
    [Google Scholar]
  99. 99. 
    Neilson EH, Goodger JQD, Woodrow IE, Møller BL 2013. Plant chemical defense: at what cost?. Trends Plant Sci 18:5250–58
    [Google Scholar]
  100. 100. 
    Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Do Kim K et al. 2016. Widespread natural variation of DNA methylation within angiosperms. Genome Biol 17:194
    [Google Scholar]
  101. 101. 
    Niederhuth CE, Schmitz RJ. 2014. Covering your bases: inheritance of DNA methylation in plant genomes. Mol. Plant 7:3472–80
    [Google Scholar]
  102. 102. 
    Ossowski S, Schneeberger K, Lucas-Lledó JI, Warthmann N, Clark RM et al. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:596192–94
    [Google Scholar]
  103. 103. 
    Panchy N, Lehti-Shiu M, Shiu S-H 2016. Evolution of gene duplication in plants. Plant Physiol 171:42294–316
    [Google Scholar]
  104. 104. 
    Pastor V, Balmer A, Gamir J, Flors V, Mauch-Mani B 2014. Preparing to fight back: generation and storage of priming compounds. Front. Plant Sci. 5:295
    [Google Scholar]
  105. 105. 
    Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V 2013. Primed plants do not forget. Environ. Exp. Bot. 94:46–56
    [Google Scholar]
  106. 106. 
    Pavet V, Quintero C, Cecchini NM, Rosa AL, Alvarez ME 2006. Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonassyringae. Mol. Plant-Microbe Interact 19:6577–87
    [Google Scholar]
  107. 107. 
    Pétriacq P, Williams A, Cotton A, McFarlane AE, Rolfe SA, Ton J 2017. Metabolite profiling of non-sterile rhizosphere soil. Plant J 92:1147–62
    [Google Scholar]
  108. 108. 
    Piasecka A, Jedrzejczak-Rey N, Bednarek P 2015. Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:3948–64
    [Google Scholar]
  109. 109. 
    Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489–521
    [Google Scholar]
  110. 110. 
    Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:1347–75
    [Google Scholar]
  111. 111. 
    Pikaard CS, Mittelsten Scheid O 2014. Epigenetic regulation in plants. Cold Spring Harb. Perspect. Biol. 6:12a019315
    [Google Scholar]
  112. 112. 
    Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA et al. 2016. The Arabidopsis thaliana mobilome and its impact at the species level. eLife 5:e15716
    [Google Scholar]
  113. 113. 
    Quadrana L, Etcheverry M, Gilly A, Caillieux E, Madoui M-A et al. 2018. Transposon accumulation lines uncover histone H2A.Z-driven integration bias towards environmentally responsive genes. bioRxiv 447870 https://doi.org/10.1101/447870
    [Crossref]
  114. 114. 
    Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R et al. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:2854–63
    [Google Scholar]
  115. 115. 
    Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S et al. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:7034732–37
    [Google Scholar]
  116. 116. 
    Reams AB, Roth JR. 2015. Mechanisms of gene duplication and amplification. Cold Spring Harb. Perspect. Biol. 7:2a016592
    [Google Scholar]
  117. 117. 
    Ritpitakphong U, Falquet L, Vimoltust A, Berger A, Métraux JP, L'Haridon F 2016. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol 210:31033–43
    [Google Scholar]
  118. 118. 
    Ross AF. 1961. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:3340–58
    [Google Scholar]
  119. 119. 
    Sasse J, Martinoia E, Northen T 2018. Feed your friends: Do plant exudates shape the root microbiome?. Trends Plant Sci 23:125–41
    [Google Scholar]
  120. 120. 
    Saze H, Mittelsten Scheid O, Paszkowski J 2003. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet. 34:165–69
    [Google Scholar]
  121. 121. 
    Schillheim B, Jansen I, Baum S, Beesley A, Bolm C, Conrath U 2018. Sulforaphane modifies histone H3, unpacks chromatin, and primes defense. Plant Physiol 176:32395–405
    [Google Scholar]
  122. 122. 
    Seidl MF, Thomma BPHJ. 2017. Transposable elements direct the coevolution between plants and microbes. Trends Genet 33:11842–51
    [Google Scholar]
  123. 123. 
    Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B 2012. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:2835–43
    [Google Scholar]
  124. 124. 
    Smith LM. 2015. Mechanisms of transposable element evolution in plants and their effects on gene expression. Nuclear Functions in Plant Transcription and Signaling O Pontes, H Jin 133–64 New York: Springer-Verlag
    [Google Scholar]
  125. 125. 
    Smith SM, Pryor AJ, Hulbert SH 2004. Allelic and haplotypic diversity at the Rp1 rust resistance locus of maize. Genetics 167:41939–47
    [Google Scholar]
  126. 126. 
    Song JT. 2006. Induction of a salicylic acid glucosyltransferase, AtSGT1, is an early disease response in Arabidopsis thaliana. Mol. Cells 22:2233–38
    [Google Scholar]
  127. 127. 
    Spoel SH, Dong X. 2012. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12:289–100
    [Google Scholar]
  128. 128. 
    Stassen JHM, López A, Jain R, Pascual-Pardo D, Luna E et al. 2018. The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis. Sci. Rep 8:114761
    [Google Scholar]
  129. 129. 
    Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T et al. 2007. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:71290–306
    [Google Scholar]
  130. 130. 
    Stokes TL, Kunkel BN, Richards EJ 2002. Epigenetic variation in Arabidopsis disease resistance. Genes Dev 16:2171–82
    [Google Scholar]
  131. 131. 
    Suda W, Nagasaki A, Shishido M 2009. Powdery mildew-infection changes bacterial community composition in the phyllosphere. Microbes Environ 24:3217–23
    [Google Scholar]
  132. 132. 
    Thulke O, Conrath U. 1998. Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant J 14:135–42
    [Google Scholar]
  133. 133. 
    Ton J, D'Alessandro M, Jourdie V, Jakab G, Karlen D et al. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:116–26
    [Google Scholar]
  134. 134. 
    Ton J, Jakab G, Toquin V, Flors V, Iavicoli A et al. 2005. Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:3987–99
    [Google Scholar]
  135. 135. 
    Toruño TY, Stergiopoulos I, Coaker G 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
    [Google Scholar]
  136. 136. 
    Tsuchiya T, Eulgem T. 2013. An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. PNAS 110:37E3535–43
    [Google Scholar]
  137. 137. 
    Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T 2009. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:7262423–26
    [Google Scholar]
  138. 138. 
    Turlings TCJ, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 63:433–52
    [Google Scholar]
  139. 139. 
    Turlings TCJ, Tumlinson JH. 1992. Systemic release of chemical signals by herbivore-injured corn. PNAS 89:178399–402
    [Google Scholar]
  140. 140. 
    Turlings TCJ, Tumlinson JH, Lewis WJ 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:49851251–53
    [Google Scholar]
  141. 141. 
    Van Der Ent S, Van Hulten M, Pozo MJ, Czechowski T, Udvardi MK et al. 2009. Priming of plant innate immunity by rhizobacteria and β-aminobutyric acid: differences and similarities in regulation. New Phytol 183:2419–31
    [Google Scholar]
  142. 142. 
    Van Hulten M, Pelser M, Van Loon LC, Pieterse CMJ, Ton J 2006. Costs and benefits of priming for defense in Arabidopsis. PNAS 103:145602–7
    [Google Scholar]
  143. 143. 
    Van Loon LC, Rep M, Pieterse CMJ 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135–62
    [Google Scholar]
  144. 144. 
    Verhoeven KJF, Van Gurp TP 2012. Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLOS ONE 7:6e38605
    [Google Scholar]
  145. 145. 
    Vorholt JA. 2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10:12828–40
    [Google Scholar]
  146. 146. 
    Waddington C. 1942. The epigenotype. Endeavor 1:18–20
    [Google Scholar]
  147. 147. 
    Walters DR, Paterson L, Walsh DJ, Havis ND 2009. Priming for plant defense in barley provides benefits only under high disease pressure. Physiol. Mol. Plant Pathol. 73:4–595–100
    [Google Scholar]
  148. 148. 
    Walters DR, Ratsep J, Havis ND 2013. Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64:51263–80
    [Google Scholar]
  149. 149. 
    Weber B, Zicola J, Oka R, Stam M 2016. Plant enhancers: a call for discovery. Trends Plant Sci 21:11974–87
    [Google Scholar]
  150. 150. 
    Weiberg A, Wang M, Lin F, Zhao H, Zhang Z et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:6154118–23
    [Google Scholar]
  151. 151. 
    Whipps JM. 2001. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52:487–511
    [Google Scholar]
  152. 152. 
    Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P et al. 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8:12973–82
    [Google Scholar]
  153. 153. 
    Yelina NE, Lambing C, Hardcastle TJ, Zhao X, Santos B, Henderson IR 2015. DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev 29:202183–202
    [Google Scholar]
  154. 154. 
    Yi H, Richards EJ. 2009. Gene duplication and hypermutation of the pathogen resistance gene SNC1 in the Arabidopsis bal variant. Genetics 183:41227–34
    [Google Scholar]
  155. 155. 
    Yu A, Lepère G, Jay F, Wang J, Bapaume L et al. 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS 110:62389–94
    [Google Scholar]
  156. 156. 
    Zemach A, Kim MY, Hsieh P-H, Coleman-Derr D, Eshed-Williams L et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:1193–205
    [Google Scholar]
  157. 157. 
    Zervudacki J, Yu A, Amesefe D, Wang J, Drouaud J et al. 2018. Transcriptional control and exploitation of an immune-responsive family of plant retrotransposons. EMBO J 37:14e98482
    [Google Scholar]
  158. 158. 
    Zhang R, Murat F, Pont C, Langin T, Salse J 2014. Paleo-evolutionary plasticity of plant disease resistance genes. BMC Genom 15:187
    [Google Scholar]
  159. 159. 
    Zhang Y, Goritschnig S, Dong X, Li X 2003. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15:112636–46
    [Google Scholar]
  160. 160. 
    Zhao D, Ferguson AA, Jiang N 2016. What makes up plant genomes: the vanishing line between transposable elements and genes. Biochim. Biophys. Acta 1859:2366–80
    [Google Scholar]
  161. 161. 
    Zipfel C. 2014. Plant pattern-recognition receptors. Trends Immunol 35:7345–51
    [Google Scholar]
  162. 162. 
    Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG et al. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:6984764–67
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-082718-095959
Loading
/content/journals/10.1146/annurev-phyto-082718-095959
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error