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Biological and Molecular Control Tools in Plant Defense

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Plant Defence: Biological Control

Part of the book series: Progress in Biological Control ((PIBC,volume 22))

Abstract

In nature, plants are continuously challenged by biotic stressors such as pathogenic microorganisms and herbivorous pests that often cause important yield reductions in crops. To address global food security issues but also consumer demands for healthier food production, a series of environmentally friendly crop protection strategies need to be employed in modern agriculture. In this chapter, we explore promising opportunities for controlling pests and pathogens of crops on the basis of our current knowledge on molecular, chemical and ecological parameters that determine plant defense. We present evidence about the feasibility of RNA-based molecular tools against a diversity of plant enemies. Moreover, a brief overview of current knowledge on applied aspects of plant defense priming in crop protection is provided in light of our fundamental understanding on mechanisms underlying this phenomenon. We specifically refer to beneficial organisms such as soil microbes and zoophytophagous predators and propose their use as plant vaccination agents, alongside chemicals that could be used to prime plants against future attackers. Endophytic fungi that not only mediate systemic plant resistance against pests or pathogens, but also impact entomopathogenic and plant growth promoting capabilities, are specifically addressed. Finally, we identify knowledge gaps and present future considerations about the use of the proposed biological and molecular control tools in sustainable crop production.

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References

  1. Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439

    Google Scholar 

  2. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43

    Google Scholar 

  3. Jez JM, Lee SG, Sherp AM (2016) The next green movement: plant biology for the environment and sustainability. Science 353:1241–1244

    Google Scholar 

  4. Doughari J (2015) An overview of plant immunity. J Plant Pathol Microbiol 6:322

    Google Scholar 

  5. Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago

    Google Scholar 

  6. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    Google Scholar 

  7. Serrano M, Coluccia F, Torres M, L’Haridon F, Métraux JP (2014) The cuticle and plant defense to pathogens. Front Plant Sci 5:274

    Google Scholar 

  8. Ziv C, Zhao Z, Gao YG, Xia Y (2018) Multifunctional roles of plant cuticle during plant-pathogen interactions. Front Plant Sci 9:1088

    Google Scholar 

  9. Malinovsky FG, Fangel JU, Willats WGT (2014) The role of the cell wall in plant immunity. Front Plant Sci 5:178

    Google Scholar 

  10. Soledade M, Pedras C, Yaya EE (2015) Plant chemical defenses: are all constitutive antimicrobial metabolites phytoanticipins? Nat Prod Commun 10:209–218

    Google Scholar 

  11. Dicke M (2015) Herbivore-induced plant volatiles as a rich source of information for arthropod predators: fundamental and applied aspects. J Indian Inst Sci 95:35–42

    Google Scholar 

  12. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help. Trends Plant Sci 15:167–175

    Google Scholar 

  13. Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24

    Google Scholar 

  14. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    Google Scholar 

  15. Baldwin IT, Callahan P (1993) Autotoxicity and chemical defense: nicotine accumulation and carbon gain in solanaceous plants. Oecologia 94:534–541

    Google Scholar 

  16. Steppuhn A, Baldwin IT (2008) Induced defenses and the cost-benefit paradigm. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, pp 61–83

    Google Scholar 

  17. Maffei ME, Arimura GI, Mithöfer A (2012) Natural elicitors, effectors and modulators of plant responses. Nat Prod Rep 29:1288–1303

    Article  CAS  PubMed  Google Scholar 

  18. Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–272

    Article  CAS  PubMed  Google Scholar 

  19. Noman A, Aqeel M, Lou Y (2019) PRRs and NB-LRRs: from signal perception to activation of plant innate immunity. Int J Mol Sci 20:1882

    Article  CAS  PubMed Central  Google Scholar 

  20. Yu X, Feng B, He P, Shan L (2017) From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu Rev Phytopathol 55:109–137

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Schellenberger R, Touchard M, Clément C, Baillieul F, Cordelier S, Crouzet J, Dorey S (2019) Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline. Mol Plant Pathol 20:1602–1616

    PubMed  PubMed Central  Google Scholar 

  22. Bhat A, Ryu CM (2016) Plant perceptions of extracellular DNA and RNA. Mol Plant 9:956–958

    CAS  PubMed  Google Scholar 

  23. Hou S, Liu Z, Shen H, Wu D (2019) Damage-associated molecular pattern-triggered immunity in plants. Front Plant Sci 10:646

    PubMed  PubMed Central  Google Scholar 

  24. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539

    CAS  PubMed  Google Scholar 

  26. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Google Scholar 

  27. Chaudhari P, Ahmed B, Joly DL, Germain H (2014) Effector biology during biotrophic invasion of plant cells. Virulence 5:703–709

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511

    CAS  PubMed  Google Scholar 

  30. Gao QM, Zhu S, Kachroo P, Kachroo A (2015) Signal regulators of systemic acquired resistance. Front Plant Sci 6:228

    PubMed  PubMed Central  Google Scholar 

  31. Felton GW, Tumlinson JH (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11:457–463

    Article  CAS  PubMed  Google Scholar 

  32. Uemura T, Arimura GI (2019) Current opinions about herbivore-associated molecular patterns and plant intracellular signaling. Plant Signal Behav 14:e1633887

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Annu Rev Entomol 60:493–515

    Article  CAS  PubMed  Google Scholar 

  34. Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J, Schimmel BCJ, Villarroel CA, Ataide LMS, Dermauw W, Glas JJ, Egas M, Janssen A, Van Leeuwen T, Schuurink RC, Sabelis MW, Alba JM (2015) Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann Bot 115:1015–1051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Walling LL (2009) Chapter 13 adaptive defense responses to pathogens and insects. Adv Bot Res 51:551–612

    Article  CAS  Google Scholar 

  36. Blaazer CJH, Villacis-Perez EA, Chafi R, Van Leeuwen T, Kant MR, Schimmel BCJ (2018) Why do herbivorous mites suppress plant defenses? Front Plant Sci 9:1057

    Article  PubMed  PubMed Central  Google Scholar 

  37. Santamaria ME, Arnaiz A, Gonzalez-Melendi P, Martinez M, Diaz I (2018) Plant perception and short-term responses to phytophagous insects and mites. Int J Mol Sci 19:1356

    Article  PubMed Central  CAS  Google Scholar 

  38. Munnik T, Nielsen E (2011) Green light for polyphosphoinositide signals in plants. Curr Opin Plant Biol 14:489–497

    Article  CAS  PubMed  Google Scholar 

  39. Zebelo SA, Maffei ME (2015) Role of early signalling events in plant-insect interactions. J Exp Bot 66:435–448

    Article  CAS  PubMed  Google Scholar 

  40. Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bruce TJ, Pickett JA (2007) Plant defence signalling induced by biotic attacks. Curr Opin Plant Biol 10:387–392

    Article  CAS  PubMed  Google Scholar 

  42. Thaler JS, Fidantsef AL, Bostock RM (2002) Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore. and pathogen performance in tomato. J Chem Ecol 28:1131–1159

    Article  CAS  PubMed  Google Scholar 

  43. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Inbar M, Gerling D (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annu Rev Entomol 53:431–448

    Article  CAS  PubMed  Google Scholar 

  45. Pastor V, Luna E, Ton J, Cerezo M, García-Agustín P, Flors V (2013) Fine tuning of reactive oxygen species homeostasis regulates primed immune responses in arabidopsis. Mol Plant-Microbe Interact 26:1334–1344

    Article  CAS  PubMed  Google Scholar 

  46. Mauch-Mani B, Baccelli I, Luna E, Priming FVD (2017) An adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512

    Article  CAS  PubMed  Google Scholar 

  47. Agut B, Gamir J, Jacas JA, Hurtado M, Flors V (2014) Different metabolic and genetic responses in citrus may explain relative susceptibility to Tetranychus urticae. Pest Manag Sci 70:1728–1741

    Google Scholar 

  48. Camañes G, Pastor V, Cerezo M, García-Andrade J, Vicedo B, García-Agustín P, Flors V (2012) A deletion in NRT2.1 attenuates pseudomonas syringae-induced hormonal perturbation, resulting in primed plant defenses. Plant Physiol 158:1054–1066

    Article  PubMed  CAS  Google Scholar 

  49. Van Hulten M, Pelser M, Van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103:5602–5607

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531

    Article  CAS  PubMed  Google Scholar 

  51. Coego A, Ramirez V, Gil MJ, Flors V, Mauch-Mani B, Vera P (2005) An arabidopsis homeodomain transcription factor, overexpressor of cationic peroxidase 3, mediates resistance to infection by necrotrophic pathogens. Plant Cell 17:2123–2137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. García-Andrade J, Ramírez V, Flors V, Vera P (2011) Arabidopsis ocp3 mutant reveals a mechanism linking ABA and JA to pathogen-induced callose deposition. Plant J 67:783–794

    Article  PubMed  CAS  Google Scholar 

  53. Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi N, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid. and the NPR1 gene. Mol Plant-Microbe Interact 23:340–351

    Google Scholar 

  54. Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ, Pozo MJ, Ton J, van Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21:818–822

    Article  CAS  PubMed  Google Scholar 

  55. Boachon B, Gamir J, Pastor V, Erb M, Dean JV, Flors V, Mauch-Mani B (2014) Role of two UDP-Glycosyltransferases from the L group of Arabidopsis in resistance against Pseudomonas syringae. Eur J Plant Pathol 139:707–720

    Google Scholar 

  56. Bednarek P (2012) Chemical warfare or modulators of defence responses – the function of secondary metabolites in plant immunity. Curr Opin Plant Biol 15:407–414

    Article  CAS  PubMed  Google Scholar 

  57. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  CAS  PubMed  Google Scholar 

  58. Fester T, Fetzer I, Buchert S, Lucas R, Rillig MC, Härtig C (2011) Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction. Oecologia 167:913–924

    Article  PubMed  Google Scholar 

  59. Sanchez-Bel P, Troncho P, Gamir J, Pozo MJ, Camañes G, Cerezo M, Flors V (2016) The nitrogen availability interferes with mycorrhiza-induced resistance against Botrytis cinerea in tomato. Front Microbiol 7:1598

    Google Scholar 

  60. Gamir J, Pastor V, Sánchez-Bel P, Agut B, Mateu D, García-Andrade J, Flors V (2018) Starch degradation, abscisic acid and vesicular trafficking are important elements in callose priming by indole-3-carboxylic acid in response to Plectosphaerella cucumerina infection. Plant J 96:518–531

    Google Scholar 

  61. Yu K, Soares J, Mandal M, Wang C, Chanda B, Gifford A, Fowler J, Navarre D, Kachroo A, Kachroo P, Feedback Regulatory A (2013) Loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep 3:1266–1278

    Article  CAS  PubMed  Google Scholar 

  62. 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

    PubMed  PubMed Central  Google Scholar 

  63. Wilkinson SW, Mageroslashy MH, Lopez Sanchez A, Smith LM, Furci L, Cotton TEA, Krokene P, Ton J (2019) Surviving in a hostile world: plant strategies to resist pests and diseases. Annu Rev Phytopathol 57:505–529

    Article  CAS  PubMed  Google Scholar 

  64. Stassen JHM, López A, Jain R, Pascual-Pardo D, Luna E, Smith LM, Ton J (2018) The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis. Sci Rep 8:14761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Schillheim B, Jansen I, Baum S, Beesley A, Bolm C, Conrath U (2018) Sulforaphane modifies histone H3, unpacks chromatin. and primes defense. Plant Physiol 176:2395–2405

    Article  CAS  PubMed  Google Scholar 

  66. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  PubMed  Google Scholar 

  67. Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452

    Article  CAS  PubMed  Google Scholar 

  68. Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, De Hollander M, Ruiz-Buck D, Mendes LW, van Ijcken WFJ, Gomez-Exposito R, Elsayed SS, Mohanraju P, Arifah A, van der Oost J, Paulson JN, Mendes R, van Wezel GP, Medema MH, Raaijmakers JM (2019) Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366:606–612

    Article  PubMed  CAS  Google Scholar 

  69. Bakker PAHM, Pieterse CMJ, de Jonge R, Berendsen RL (2018) The soil-borne legacy. Cell 172:1178–1180

    Article  CAS  PubMed  Google Scholar 

  70. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840

    Article  CAS  PubMed  Google Scholar 

  71. Chandrashekara C, Bhatt JC, Kumar R, Chandrashekara KN (2012) Supressive soils in plant disease management. Eco-Friendly Innov Approach Plant. Dis Manag:241–256

    Google Scholar 

  72. Durán P, Jorquera M, Viscardi S, Carrion VJ, Mora ML, Pozo MJ (2017) Screening and characterization of potentially suppressive soils against Gaeumannomyces graminis under extensive wheat cropping by Chilean indigenous communities. Front Microbiol 8:1552

    Google Scholar 

  73. Ton J, Mauch-Mani B (2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130

    Article  CAS  PubMed  Google Scholar 

  74. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environ Exp Bot 94:46–56

    Article  CAS  Google Scholar 

  75. Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953

    Google Scholar 

  76. Gamir J, Sánchez-Bel P, Flors V (2014) Molecular and physiological stages of priming: how plants prepare for environmental challenges. Plant Cell Rep 33:1935–1949

    Article  CAS  PubMed  Google Scholar 

  77. Jaskiewicz M, Conrath U, Peterhälnsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55

    Article  CAS  PubMed  Google Scholar 

  78. Pikaard CS, Scheid OM (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol 6:a019315

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. 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:e1002434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. 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 158:835–843

    Article  CAS  PubMed  Google Scholar 

  81. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J (2012) Next-generation systemic acquired resistance. Plant Physiol 158:844–853

    Article  CAS  PubMed  Google Scholar 

  82. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:854–863

    Article  CAS  PubMed  Google Scholar 

  83. Bouagga S, Urbaneja A, Rambla JL, Flors V, Granell A, Jaques JA, Pérez-Hedo M (2018) Zoophytophagous mirids provide pest control by inducing direct defences, antixenosis and attraction to parasitoids in sweet pepper plants. Pest Manag Sci 74:1286–1296

    Article  CAS  PubMed  Google Scholar 

  84. Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26

    Article  CAS  PubMed  Google Scholar 

  85. Agut B, Gamir J, Jaques JA, Flors V (2015) Tetranychus urticae-triggered responses promote genotype-dependent conspecific repellence or attractiveness in citrus. New Phytol 207:790–804

    Google Scholar 

  86. Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Agut B, Pastor V, Jaques JA, Flors V (2018) Can plant defence mechanisms provide new approaches for the sustainable control of the two-spotted spider mite Tetranychus urticae? Int J Mol Sci 19:614

    Google Scholar 

  88. Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, Van Der Heijden MGA, Schlaeppi K, Erb M (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:2738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Google Scholar 

  90. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    CAS  PubMed  Google Scholar 

  91. Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Castel SE, Martienssen RA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14:100–112

    CAS  PubMed  Google Scholar 

  93. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    CAS  PubMed  Google Scholar 

  94. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    CAS  PubMed  Google Scholar 

  95. Voinnet O (2009) Origin, biogenesis. and activity of plant microRNAs. Cell 136:669–687

    CAS  PubMed  Google Scholar 

  96. Wassenegger M (2005) The role of the RNAi machinery in heterochromatin formation. Cell 122:13–16

    Article  CAS  PubMed  Google Scholar 

  97. Pooggin MM (2013) How can plant DNA viruses evade siRNA-directed DNA methylation and silencing? Int J Mol Sci 14:15233–15259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Pooggin MM (2017) RNAi-mediated resistance to viruses: a critical assessment of methodologies. Curr Opin Virol 26:28–35

    Article  CAS  PubMed  Google Scholar 

  99. Baulcombe DC (2019) How virus resistance provided a mechanistic foundation for RNA silencing. Plant Cell 31:1395–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Cai Q, He B, Kogel KH, Jin H (2018) Cross-kingdom RNA trafficking and environmental RNAi-nature’s blueprint for modern crop protection strategies. Curr Opin Microbiol 46:58–64

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Huang CY, Wang H, Hu P, Hamby R, Jin H (2019) Small RNAs – Big players in plant-microbe interactions. Cell Host Microbe 26:173–182

    CAS  PubMed  Google Scholar 

  102. Zhang T, Zhao YL, Zhao JH, Wang S, Jin Y, Chen ZQ, Fang YY, Hua CL, Ding SW, Guo HS (2016) Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat Plants 2:16153

    CAS  PubMed  Google Scholar 

  103. Eamens A, Wang MB, Smith NA, Waterhouse PM (2008) RNA silencing in plants: yesterday, today. and tomorrow. Plant Physiol 147:456–468

    CAS  PubMed  Google Scholar 

  104. Koch A, Kogel KH (2014) New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing. Plant Biotechnol J 12:821–831

    CAS  PubMed  Google Scholar 

  105. Rosa C, Kuo YW, Wuriyanghan H, Falk BW (2018) RNA interference mechanisms and applications in plant pathology. Annu Rev Phytopathol 56:581–610

    CAS  PubMed  Google Scholar 

  106. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    CAS  PubMed  Google Scholar 

  107. Sherman JH, Munyikwa T, Chan SY, Petrick JS, Witwer KW, Choudhuri S (2015) RNAi technologies in agricultural biotechnology: the toxicology forum 40th annual summer meeting. Regul Toxicol Pharmacol 73:671–680

    PubMed  Google Scholar 

  108. Szittya G, Burgyan J (2013) RNA interference-mediated intrinsic antiviral immunity in plants. Curr Top Microbiol Immunol 371:153–181

    CAS  PubMed  Google Scholar 

  109. Dalakouras A, Jarausch W, Buchholz G, Bassler A, Braun M, Manthey T, Krczal G, Wassenegger M (2018) Delivery of hairpin RNAs and small RNAs into woody and herbaceous plants by trunk injection and petiole absorption. Front Plant Sci 9:1253

    PubMed  PubMed Central  Google Scholar 

  110. Dalakouras A, Wassenegger M, Dadami E, Ganopoulos I, Pappas ML, Papadopoulou KK (2019) Genetically modified organism-free RNA interference: exogenous application of RNA molecules in plants. Plant Physiol 182:1–13

    Google Scholar 

  111. Dalakouras A, Wassenegger M, McMillan JN, Cardoza V, Maegele I, Dadami E, Runne M, Krczal G, Wassenegger M (2016) Induction of silencing in plants by high-pressure spraying of in vitro-synthesized small RNAs. Front Plant Sci 7:1327

    Article  PubMed  PubMed Central  Google Scholar 

  112. Cagliari D, Dias NP, Galdeano DM, Dos Santos EA, Smagghe G, Zotti MJ (2019) Management of pest insects and plant diseases by non-transformative RNAi. Front Plant Sci 10:1319

    Article  PubMed  PubMed Central  Google Scholar 

  113. Taning CNT, Arpaia S, Christiaens O, Dietz-Pfeilstetter A, Jones H, Mezzetti B, Sabbadini S, Sorteberg HG, Sweet J, Ventura V, Smagghe G (2019) RNA-based biocontrol compounds: current status and perspectives to reach the market. Pest Manag Sci 76:841–845

    Article  PubMed  CAS  Google Scholar 

  114. Nicaise V (2014) Crop immunity against viruses: outcomes and future challenges. Front Plant Sci 5:660

    Article  PubMed  PubMed Central  Google Scholar 

  115. Gan D, Zhang J, Jiang H, Jiang T, Zhu S, Cheng B (2010) Bacterially expressed dsRNA protects maize against SCMV infection. Plant Cell Rep 29:1261–1268

    Article  CAS  PubMed  Google Scholar 

  116. Kaldis A, Berbati M, Melita O, Reppa C, Holeva M, Otten P, Voloudakis A (2018) Exogenously applied dsRNA molecules deriving from the Zucchini yellow mosaic virus (ZYMV) genome move systemically and protect cucurbits against ZYMV. Mol Plant Pathol 19:883–895

    Article  CAS  PubMed  Google Scholar 

  117. Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ (2017) Lu GQ and Xu ZP, Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat Plants 3:16207

    Article  CAS  PubMed  Google Scholar 

  118. Niehl A, Soininen M, Poranen MM, Heinlein M (2018) Synthetic biology approach for plant protection using dsRNA. Plant Biotechnol J 16:1679–1687

    Article  CAS  PubMed Central  Google Scholar 

  119. Safarova D, Brazda P, Navratil M (2014) Effect of artificial dsRNA on infection of pea plants by pea seed-borne mosaic virus. Czech J Genet Plant Breed 50:105–108

    Article  Google Scholar 

  120. Shen W, Yang G, Chen Y, Yan P, Tuo D, Li X, Zhou P (2014) Resistance of non-transgenic papaya plants to papaya ringspot virus (PRSV) mediated by intron-containing hairpin dsRNAs expressed in bacteria. Acta Virol 58:261–266

    Article  CAS  PubMed  Google Scholar 

  121. Tenllado F, Diaz-Ruiz JR (2001) Double-stranded RNA-mediated interference with plant virus infection. J Virol 75:12288–12297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Worrall EA, Bravo-Cazar A, Nilon AT, Fletcher SJ, Robinson KE, Carr JP, Mitter N (2019) Exogenous application of RNAi-inducing double-stranded RNA inhibits aphid-mediated transmission of a plant virus. Front Plant Sci 10:265

    Article  PubMed  PubMed Central  Google Scholar 

  123. Yin G, Sun Z, Liu N, Zhang L, Song Y, Zhu C, Wen F (2009) Production of double-stranded RNA for interference with TMV infection utilizing a bacterial prokaryotic expression system. Appl Microbiol Biotechnol 84:323–333

    Article  CAS  PubMed  Google Scholar 

  124. Yin GH, Sun ZN, Song YZ, An HL, Zhu CX, Wen FJ (2010) Bacterially expressed double-stranded RNAs against hot-spot sequences of tobacco mosaic virus or potato virus Y genome have different ability to protect tobacco from viral infection. Appl Biochem Biotechnol 162:1901–1914

    Article  PubMed  CAS  Google Scholar 

  125. Tabler M, Tsagris M (2004) Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci 9:339–348

    Article  CAS  PubMed  Google Scholar 

  126. Carbonell A, Martinez de Alba A, Flores R, Gago S (2008) Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology 371:44–53

    Article  CAS  PubMed  Google Scholar 

  127. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  PubMed  PubMed Central  Google Scholar 

  128. Laurie JD, Linning R, Bakkeren G (2008) Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr Genet 53:49–58

    Google Scholar 

  129. Koch A, Biedenkopf D, Furch A, Weber L, Rossbach O, Abdellatef E, Linicus L, Johannsmeier J, Jelonek L, Goesmann A, Cardoza V, McMillan J, Mentzel T, Kogel KH (2016) An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLoS Pathog 12:e1005901

    Google Scholar 

  130. McLoughlin AG, Wytinck N, Walker PL, Girard IJ, Rashid KY, de Kievit T, Fernando WGD, Whyard S, Belmonte MF (2018) Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea. Sci Rep 8:7320

    Google Scholar 

  131. Song XS, Gu KX, Duan XX, Xiao XM, Hou YP, Duan YB, Wang JX (2018) Yu N and Zhou MG, Secondary amplification of siRNA machinery limits the application of spray-induced gene silencing. Mol Plant Pathol 19:2543–2560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Wang M, Weiberg A, Lin FM, Thomma BP, Huang HD, Jin H (2016) Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat Plants 2:16151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Hunter W, Glick E, Paldi N, Bextine B (2012) Advances in RNA interference: dsRNA treatment in trees and grapevines for insect pest suppression. Southwest Entomol 37:85–87

    Article  Google Scholar 

  134. Gong L, Chen Y (2013) Hu Z and Hu M, Testing insecticidal activity of novel chemically synthesized siRNA against Plutella xylostella under laboratory and field conditions. PLoS One 8:e62990

    Google Scholar 

  135. Ivashuta S, Zhang Y, Wiggins BE, Ramaseshadri P, Segers GC, Johnson S, Meyer SE, Kerstetter RA, McNulty BC, Bolognesi R, Heck GR (2015) Environmental RNAi in herbivorous insects. RNA 21:840–850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Li H, Guan R, Guo H, Miao X (2015) New insights into an RNAi approach for plant defence against piercing-sucking and stem-borer insect pests. Plant Cell Environ 38:2277–2285

    Article  CAS  PubMed  Google Scholar 

  137. San Miguel K, Scott J (2016) The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide. Pest Manag Sci 72:801–809

    Article  CAS  PubMed  Google Scholar 

  138. Shukla JN, Kalsi M, Sethi A, Narva KE, Fishilevich E, Singh S, Mogilicherla K, Palli SR (2016) Reduced stability and intracellular transport of dsRNA contribute to poor RNAi response in lepidopteran insects. RNA Biol 13:656–669

    Article  PubMed  PubMed Central  Google Scholar 

  139. Joga MR, Zotti MJ, Smagghe G, Christiaens O (2016) RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front Physiol 7:553

    Article  PubMed  PubMed Central  Google Scholar 

  140. Zotti MJ, Smagghe G (2015) RNAi technology for insect management and protection of beneficial insects from diseases: lessons, challenges and risk assessments. Neotrop Entomol 44:197–213

    Article  CAS  PubMed  Google Scholar 

  141. Baum S, Reimer-Michalski EM, Bolger A, Mantai AJ, Benes V, Usadel B, Conrath U (2019) Isolation of open chromatin identifies regulators of systemic acquired resistance. Plant Physiol 181:817–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Schoenherr AP, Rizzo E, Jackson N, Manosalva P, Gomez SK (2019) Mycorrhiza-induced resistance in potato involves priming of defense responses against cabbage looper (Noctuidae: Lepidoptera). Environ Entomol 48:370–381

    Article  CAS  PubMed  Google Scholar 

  143. Hussain A, Rizwan M, Ali Q, Ali S (2019) Seed priming with silicon nanoparticles improved the biomass and yield while reduced the oxidative stress and cadmium concentration in wheat grains. Environ Sci Pollut Res 26:7579–7588

    Article  CAS  Google Scholar 

  144. Walters DR, Paterson L, Walsh DJ, Havis ND (2008) Priming for plant defense in barley provides benefits only under high disease pressure. Physiol Mol Plant Pathol 73:95–100

    Article  CAS  Google Scholar 

  145. Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: Interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20

    Article  CAS  Google Scholar 

  146. Cruz-Miralles J, Cabedo-López M, Pérez-Hedo M, Flors V, Jaques JA (2019) Zoophytophagous mites can trigger plant-genotype specific defensive responses affecting potential prey beyond predation: the case of Euseius stipulatus and Tetranychus urticae in citrus. Pest Manag Sci 75:1962–1970

    Google Scholar 

  147. Sukegawa S, Shiojiri K, Higami T, Suzuki S, Arimura GI (2018) Pest management using mint volatiles to elicit resistance in soy: mechanism and application potential. Plant J 96:910–920

    Article  CAS  PubMed  Google Scholar 

  148. Luna-Diez E (2016) Using green vaccination to brighten the agronomic future. Outlooks Pest Manag 27:136–140

    Article  Google Scholar 

  149. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    Article  CAS  PubMed  Google Scholar 

  150. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514

    Article  CAS  PubMed  Google Scholar 

  151. Shikano I, Rosa C, Tan CW, Interactions FGWT (2017) Microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:313–331

    Article  CAS  PubMed  Google Scholar 

  152. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Dangl JL, Tringe SG (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90

    Google Scholar 

  153. Pérez-Montaño F, Alías-Villegas C, Bellogín RA, Del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336

    Article  PubMed  Google Scholar 

  154. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    Article  CAS  PubMed  Google Scholar 

  155. Ramakrishna W, Yadav R, Li K (2019) Plant growth promoting bacteria in agriculture: two sides of a coin. Appl Soil Ecol 138:10–18

    Article  Google Scholar 

  156. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM (2013) Trichoderma research in the genome era. Annu Rev Phytopathol 51:105–129

    Google Scholar 

  157. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  158. Rivero J, Gamir J, Aroca R, Pozo MJ, Flors V (2015) Metabolic transition in mycorrhizal tomato roots. Front Microbiol 6:598

    Article  PubMed  PubMed Central  Google Scholar 

  159. Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436

    Article  CAS  PubMed  Google Scholar 

  160. Adnan M, Islam W, Shabbir A, Khan KA, Ghramh HA, Huang Z, Chen HYH, Lu GD (2019) Plant defense against fungal pathogens by antagonistic fungi with Trichoderma in focus. Microb Pathog 129:7–18

    Google Scholar 

  161. Martínez-Medina A, Van Wees SCM, Pieterse CMJ (2017) Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ 40:2691–2705

    Google Scholar 

  162. Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588

    Article  PubMed  CAS  Google Scholar 

  163. Pozo MJ, Van Der Ent S, Van Loon LC, Pieterse CMJ (2008) Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol 180:511–523

    Google Scholar 

  164. Kavroulakis N, Ntougias S, Zervakis GI, Ehaliotis C, Haralampidis K, Papadopoulou KK (2007) Role of ethylene in the protection of tomato plants against soil-borne fungal pathogens conferred by an endophytic Fusarium solani strain. J Exp Bot 58:3853–3864

    Google Scholar 

  165. Garantonakis N, Pappas ML, Varikou K, Skiada V, Broufas GD, Kavroulakis N, Papadopoulou KK (2018) Tomato inoculation with the endophytic strain Fusarium solani K results in reduced feeding damage by the zoophytophagous predator Nesidiocoris tenuis. Front Ecol Evol 6

    Google Scholar 

  166. Pappas ML, Liapoura M, Papantoniou D, Avramidou M, Kavroulakis N, Weinhold A, Broufas GD, Papadopoulou KK (2018) The beneficial endophytic fungus Fusarium solani strain K alters tomato responses against spider mites to the benefit of the plant. Front Plant Sci 9:1603

    Google Scholar 

  167. Angelopoulou DJ, Naska EJ, Paplomatas EJ, Tjamos SE (2014) Biological control agents (BCAs) of verticillium wilt: influence of application rates and delivery method on plant protection, triggering of host defence mechanisms and rhizosphere populations of BCAs. Plant Pathol 63:1062–1069

    Article  Google Scholar 

  168. Veloso J, Díaz J (2012) Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici, and induces the expression of defence genes. Plant Pathol 61:281–288

    Google Scholar 

  169. Varo A, Raya-Ortega MC, Trapero A (2016) Selection and evaluation of micro-organisms for biocontrol of Verticillium dahliae in olive. J Appl Microbiol 121:767–777

    Google Scholar 

  170. Deketelaere S, Tyvaert L, França SC, Hofte M (2017) Desirable traits of a good biocontrol agent against Verticillium wilt. Front Microbiol 8:1186

    Article  PubMed  PubMed Central  Google Scholar 

  171. Kumar H, Dubey RC, Maheshwari DK (2011) Effect of plant growth promoting rhizobia on seed germination, growth promotion and suppression of Fusarium wilt of fenugreek (Trigonella foenum-graecum L.). Crop Prot 30:1396–1403

    Google Scholar 

  172. Singh PK, Singh M, Vyas D (2010) Biocontrol of Fusarium wilt of chickpea using arbuscular mycorrhizal fungi and Rhizobium leguminosorum biovar. Caryologia 63:349–353

    Google Scholar 

  173. Volpiano CG, Lisboa BB, Granada CE, José JFBS, de Oliveira AMR, Beneduzi A, Perevalova Y, LMP P, Vargas LK (2019) Rhizobia for biological control of plant diseases. In: Kumar V, Prasad R, Kumar M, Choudhary DK (eds) Microbiome in plant health and disease: challenges and ppportunities. Springer, Singapore, pp 315–336

    Chapter  Google Scholar 

  174. Pappas ML, Steppuhn A, Broufas GD (2016) The role of phytophagy by predators in shaping plant interactions with their pests. Commun Integr Biol 9:1–4

    Article  Google Scholar 

  175. Pappas ML, Steppuhn A, Geuss D, Topalidou N, Zografou A, Sabelis MW, Broufas GD (2015) Beyond predation: the zoophytophagous predator Macrolophus pygmaeus induces tomato resistance against spider mites. PLoS One 10:e0127251

    Google Scholar 

  176. Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Flors V, Urbaneja A (2015) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88:543–554

    Google Scholar 

  177. Bouagga S, Urbaneja A, Rambla JL, Granell A, Pérez-Hedo M (2018) Orius laevigatus strengthens its role as a biological control agent by inducing plant defenses. J Pest Sci 91:55–64

    Google Scholar 

  178. Zhang NX, Messelink GJ, Alba JM, Schuurink RC, Kant MR, Janssen A (2018) Phytophagy of omnivorous predator Macrolophus pygmaeus affects performance of herbivores through induced plant defences. Oecologia 186:101–113

    Google Scholar 

  179. Pérez-Hedo M, Arias-Sanguino ÁM, Urbaneja A (2018) Induced tomato plant resistance against Tetranychus urticae triggered by the phytophagy of Nesidiocoris tenuis. Front Plant Sci 9:1419

    Google Scholar 

  180. Pérez-Hedo M, Bouagga S, Jaques JA, Flors V, Urbaneja A (2015) Tomato plant responses to feeding behavior of three zoophytophagous predators (Hemiptera: Miridae). Biol Control 86:46–51

    Article  Google Scholar 

  181. Zhang NX, van Wieringen D, Messelink GJ, Janssen A (2019) Herbivores avoid host plants previously exposed to their omnivorous predator Macrolophus pygmaeus. J Pest Sci 92:737–745

    Google Scholar 

  182. Pappas ML, Broekgaarden C, Broufas GD, Kant MR, Messelink GJ, Steppuhn A, Wäckers F, van Dam NM (2017) Induced plant defences in biological control of arthropod pests: a double-edged sword. Pest Manag Sci 73:1780–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Battaglia D, Bossi S, Cascone P, Digilio MC, Prieto JD, Fanti P, Guerrieri E, Iodice L, Lingua G, Lorito M, Maffei ME, Massa N, Ruocco M, Sasso R, Trotta V (2013) Tomato below ground-above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Mol Plant-Microbe Interact 26:1249–1256

    Google Scholar 

  184. Prieto JD, Castañé C, Calvet C, Camprubi A, Battaglia D, Trotta V, Fanti P (2017) Tomato belowground–aboveground interactions: Rhizophagus irregularis affects foraging behavior and life history traits of the predator Macrolophus pygmaeus (Hemiptera: Miridae). Arthropod Plant Interact 11:15–22

    Google Scholar 

  185. Eschweiler J, Holstein-Saj R, Marjolein Kruidhof H, Schouten A, Messelink GJ (2019) Tomato inoculation with a non-pathogenic strain of Fusarium oxysporum enhances pest control by changing the feeding preference of an omnivorous predator. Front Ecol Evol 7:213

    Google Scholar 

  186. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062–1071

    CAS  PubMed  Google Scholar 

  187. Conrath U, Chen Z, Ricigliano JR, Klessig DF (1995) Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid. inhibit catalase activity in tobacco. Proc Natl Acad Sci U S A 92:7143–7147

    CAS  PubMed  Google Scholar 

  188. Silverman FP, Petracek PD, Heiman DF, Fledderman CM, Warrior P (2005) Salicylate activity. 3. Structure relationship to systemic acquired resistance. J Agric Food Chem 53:9775–9780

    CAS  PubMed  Google Scholar 

  189. Zhou M, Wang W (2018) Recent advances in synthetic chemical inducers of plant immunity. Front Plant Sci 871

    Google Scholar 

  190. Zimmerli L, Jakab G, Métraux JP, Mauch-Mani B (2000) Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proc Natl Acad Sci U S A 97:12920–12925

    CAS  PubMed  PubMed Central  Google Scholar 

  191. Gamir J, Pastor V, Cerezo M, Flors V (2012) Identification of indole-3-carboxylic acid as mediator of priming against Plectosphaerella cucumerina. Plant Physiol Biochem 61:169–179

    Google Scholar 

  192. Cohen Y, Vaknin M, Mauch-Mani B (2016) BABA-induced resistance: milestones along a 55-year journey. Phytoparasitica 44:513–538

    CAS  Google Scholar 

  193. Hodge S, Ward JL, Galster AM, Beale MH, Powell G (2011) The effects of a plant defence priming compound, β-aminobutyric acid, on multitrophic interactions with an insect herbivore and a hymenopterous parasitoid. BioControl 56:699–711

    CAS  Google Scholar 

  194. Baccelli I, Mauch-Mani B (2017) When the story proceeds backward: the discovery of endogenous β-aminobutyric acid as the missing link for a potential new plant hormone. Commun Integr Biol 10:e1290019

    PubMed Central  Google Scholar 

  195. Schwarzenbacher RE, Luna E, Ton J (2014) The discovery of the BABA receptor: scientific implications and application potential. Front Plant Sci 5:304

    PubMed  PubMed Central  Google Scholar 

  196. Luna E, Van Hulten M, Zhang Y, Berkowitz O, López A, Pétriacq P, Sellwood MA, Chen B, Burrell M, Van De Meene A, Pieterse CMJ, Flors V, Ton J (2014) Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol 10:450–456

    CAS  PubMed  PubMed Central  Google Scholar 

  197. Thevenet D, Pastor V, Baccelli I, Balmer A, Vallat A, Neier R, Glauser G, Mauch-Mani B (2017) The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol 213:552–559

    Article  CAS  PubMed  Google Scholar 

  198. Hall CR, Waterman JM, Vandegeer RK, Hartley SE, Johnson SN (2019) The role of silicon in antiherbivore phytohormonal signalling. Front Plant Sci 10:1132

    Article  PubMed  PubMed Central  Google Scholar 

  199. Alhousari F, Greger M (2018) Silicon and mechanisms of plant resistance to insect pests. Plan Theory 7:33

    CAS  Google Scholar 

  200. Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291

    Article  PubMed  Google Scholar 

  201. Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Bélanger RR (2019) The controversies of silicon’s role in plant biology. New Phytol 221:67–85

    Article  PubMed  Google Scholar 

  202. Rahman A, Wallis CM, Uddin W (2015) Silicon-induced systemic defense responses in perennial ryegrass against infection by Magnaporthe oryzae. Phytopathology 105:748–757

    Google Scholar 

  203. Han Y, Li P, Gong S, Yang L, Wen L, Hou M (2016) Defense responses in rice induced by silicon amendment against infestation by the leaf folder Cnaphalocrocis medinalis. PLoS One 11:e0153918

    Google Scholar 

  204. Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  205. Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5:77

    Article  PubMed Central  CAS  Google Scholar 

  206. Wagner MR, Lundberg DS, del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Martins F, Pereira JA, Bota P, Bento A, Baptista P (2016) Fungal endophyte communities in above- and belowground olive tree organs and the effect of season and geographic location on their structures. Fungal Ecol 20:193–201

    Article  Google Scholar 

  208. Gomes T, Pereira JA, Benhadi J, Lino-Neto T, Baptista P (2018) Endophytic and epiphytic phyllosphere fungal communities are shaped by different environmental factors in a Mediterranean ecosystem. Microb Ecol 76:668–679

    Article  PubMed  Google Scholar 

  209. Gomes T, Pereira JA, Lino-Neto T, Bennett AE, Baptista P (2019) Bacterial disease induced changes in fungal communities of olive tree twigs depend on host genotype. Sci Rep 9:1–10

    Article  CAS  Google Scholar 

  210. Varanda CMR, Oliveira M, Materatski P, Landum M, Clara MIE, Félix MDR (2016) Fungal endophytic communities associated to the phyllosphere of grapevine cultivars under different types of management. Fungal Biol 120:1525–1536

    PubMed  Google Scholar 

  211. Latz MAC, Jensen B, Collinge DB, Jørgensen HJL (2018) Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression. Plant Ecol Divers 11:555–567

    Google Scholar 

  212. Gao FK, Dai CC, Liu XZ (2010) Mechanisms of fungal endophytes in plant protection against pathogens. Afr J Microbiol Res 4:1346–1351

    Google Scholar 

  213. Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 55:113–128

    Article  Google Scholar 

  214. Dutta D, Puzari KS, Gogoi R, Dutta P (2014) Endophytes: exploitation as a tool in plant protection. Braz Arch Biol Technol 57:621–629

    Article  Google Scholar 

  215. Alagarasan G, Aswathy KS, Madhaiyan M (2017) Shoot the message, not the messenger—combating pathogenic virulence in plants by inhibiting quorum sensing mediated signaling molecules. Front Plant Sci 8:2198

    Article  PubMed  PubMed Central  Google Scholar 

  216. Molitor A, Zajic D, Voll LM, Pons-Kühnemann J, Samans B, Kogel KH, Waller F (2011) Barley leaf transcriptome and metabolite analysis reveals new aspects of compatibility and Piriformospora indica-mediated systemic induced resistance to powdery mildew. Mol Plant-Microbe Interact 24:1427–1439

    Google Scholar 

  217. Nassimi Z, Taheri P (2017) Endophytic fungus Piriformospora indica induced systemic resistance against rice sheath blight via affecting hydrogen peroxide and antioxidants. Biocontrol Sci Tech 27:252–267

    Google Scholar 

  218. Bhattacharya A, Giri VP, Singh SP, Pandey S, Chauhan P, Soni SK, Srivastava S, Singh PC, Mishra A (2019) Intervention of bio-protective endophyte Bacillus tequilensis enhance physiological strength of tomato during Fusarium wilt infection. Biol Control 139

    Google Scholar 

  219. Chow YY, Rahman S, Ting ASY (2019) Evaluating the host defense responses in oil palm to complex biocontrol endophyte–pathogen–host plant interaction via Fluidigm® real-time polymerase chain reaction (RT-PCR). Biol Control 129:148–157

    CAS  Google Scholar 

  220. Chandrasekaran M, Belachew ST, Yoon E, Chun SC (2017) Expression of β-1,3-glucanase (GLU) and phenylalanine ammonia-lyase (PAL) genes and their enzymes in tomato plants induced after treatment with Bacillus subtilis CBR05 against Xanthomonas campestris pv. vesicatoria. J Gen Plant Pathol 83:7–13

    Google Scholar 

  221. Lanna-Filho R, Souza RM, Alves E (2017) Induced resistance in tomato plants promoted by two endophytic bacilli against bacterial speck. Trop Plant Pathol 42:96–108

    Google Scholar 

  222. Yang R, Fan X, Cai X, Hu F (2015) The inhibitory mechanisms by mixtures of two endophytic bacterial strains isolated from Ginkgo biloba against pepper phytophthora blight. Biol Control 85:59–67

    Google Scholar 

  223. Kloepper JW, Ryu CM (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: BJE S, CJC B, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 33–51

    Google Scholar 

  224. Singh S (2016) Role of Nonpathogenic fungi in inducing systemic resistance in crop plants against phytopathogens. In D. P. Singh, H. B. Singh, & R. Prabha (Eds.), Microbial Inoculants in Sustainable Agricultural Productivity: Vol. 2: Functional Applications (pp. 69-83). New Delhi: Springer India.

    Google Scholar 

  225. Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol 9:2732

    PubMed  PubMed Central  Google Scholar 

  226. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150

    CAS  PubMed  Google Scholar 

  227. Xu XH, Wang C, Li SX, Su ZZ, Zhou HN, Mao LJ, Feng XX, Liu PP, Chen X, Hugh Snyder J, Kubicek CP, Zhang CL, Lin FC (2015) Friend or foe: differential responses of rice to invasion by mutualistic or pathogenic fungi revealed by RNAseq and metabolite profiling. Sci Rep 5:13624

    PubMed  PubMed Central  Google Scholar 

  228. Beliën T, Van Campenhout S, Robben J, Volckaert G (2006) Microbial endoxylanases: effective weapons to breach the plant cell-wall barrier or, rather, triggers of plant defense systems? Mol Plant-Microbe Interact 19:1072–1081

    PubMed  Google Scholar 

  229. Bordiec S, Paquis S, Lacroix H, Dhondt S, Ait Barka E, Kauffmann S, Jeandet P, Mazeyrat-Gourbeyre F, Clément C, Baillieul F, Dorey S (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62:595–603

    Google Scholar 

  230. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759

    Google Scholar 

  231. Cord-Landwehr S, Melcher RLJ, Kolkenbrock S, Moerschbacher BM (2016) A chitin deacetylase from the endophytic fungus Pestalotiopsis sp. efficiently inactivates the elicitor activity of chitin oligomers in rice cells. Sci Rep 6:38018

    Google Scholar 

  232. Trdá L, Boutrot F, Ciaverie J, Brulé D, Dorey S, Poinssot B (2015) Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Front Plant Sci 6:219

    Article  PubMed  PubMed Central  Google Scholar 

  233. Zeidler D, Zähringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci U S A 101:15811–15816

    Google Scholar 

  234. Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K, Peng G (2014) Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene. and auxin biosynthesis. PLoS One 9:e94144

    Google Scholar 

  235. Waqas M, Khana AL, Hamayuna M, Shahzad R, Kang SM, Kim JG, Lee IJ (2015) Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of penicillium citrinum and aspergillus terreus. J Plant Interact 10:280–287

    Article  CAS  Google Scholar 

  236. Mishra A, Singh SP, Mahfooz S, Singh SP, Bhattacharya A, Mishra N, Nautiyal CS (2018) Endophyte-mediated modulation of defense-related genes and systemic resistance in Withania somnifera (L.) Dunal under Alternaria alternata stress. Appl Environ Microbiol 84:e02845–e02817

    Google Scholar 

  237. Constantin ME, de Lamo FJ, Vlieger BV, Rep M, Takken FLW (2019) Endophyte-mediated resistance in tomato to Fusarium oxysporum is independent of ET, JA. and SA. Front Plant Sci 10:979

    Google Scholar 

  238. Bidochka MJ, Kasperski JE, Wild GAM (1998) Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Can J Bot 76:1198–1204

    Google Scholar 

  239. Gange AC, Koricheva J, Currie AF, Jaber LR, Vidal S (2019) Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Phytol 223:2002–2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  240. Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82

    Article  Google Scholar 

  241. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles: Tansley review. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  242. Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357

    Article  CAS  PubMed  Google Scholar 

  243. Ownley BH, Pereira RM, Klingeman WE, Quigley NB, Leckie BM (2004) Beauveria bassiana, a dual purpose biocontrol organism, with activity against insect pests and plant pathogens. Emerg Concept Plant Health Manag:255–269

    Google Scholar 

  244. Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by Endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211

    Article  Google Scholar 

  245. Fuller-Schaefer C, Jung K, Jaronski S (2005) Colonization of sugar beet roots by entomopathogenic fungi. Proceedings of the 38th annual meeting of the society for invertebrate pathology, vol 49

    Google Scholar 

  246. Petrini O, Dreyfuss M (1981) Endophytische Pilze in Epiphytischen Araceae. Bromeliaceae und Orchidiaceae. Sydowia 34:135–148

    Google Scholar 

  247. Bills GF, Polishook JD (1991) Microfungi from Carpinus caroliniana. Can J Bot 69:1477–1482

    Google Scholar 

  248. Cao LX, You JL, Zhou SN (2002) Endophytic fungi from Musa acuminata leaves and roots in South China. World J Microbiol Biotechnol 18:169–171

    Google Scholar 

  249. Ananda K, Sridhar KR (2002) Diversity of endophytic fungi in the roots of mangrove species on the west coast of India. Can J Microbiol 48:871–878

    Article  CAS  PubMed  Google Scholar 

  250. An ZQ, Siegel MR, Hollin W, Tsai HF, Schmidt D, Schardl CL (1993) Relationships among non-Acremonium sp. fungal endophytes in five grass species. Appl Environ Microbiol 59:1540–1548

    Google Scholar 

  251. Cabanillas E, Barker KR, Daykin ME (1988) Histology of the interactions of Paecilomyces lilacinus with Meloidogyne incognita on tomato. J Nematol 20:362–365

    Google Scholar 

  252. Arthurs S, Dara SK (2019) Microbial biopesticides for invertebrate pests and their markets in the United States. J Invertebr Pathol 165:13–21

    Article  PubMed  Google Scholar 

  253. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433

    Article  CAS  PubMed  Google Scholar 

  254. Vidal S, Jaber LR (2015) Entomopathogenic fungi as endophytes: plant-endophyte-herbivore interactions and prospects for use in biological control. Curr Sci 109:46–54

    Google Scholar 

  255. Bamisile BS, Dash CK, Akutse KS, Keppanan R, Wang L (2018) Fungal endophytes: beyond herbivore management. Front Microbiol 9:544

    Article  PubMed  PubMed Central  Google Scholar 

  256. Branine M, Bazzicalupo A, Branco S (2019) Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathog 15:e1007831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Lopez DC, Sword GA (2015) The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control 89:53–60

    Google Scholar 

  258. Russo ML, Scorsetti AC, Vianna MF, Cabello M, Ferreri N, Pelizza S (2019) Endophytic effects of Beauveria bassiana on corn (Zea mays) and its herbivore, Rachiplusia nu (Lepidoptera: Noctuidae). Insects 10:110

    Google Scholar 

  259. Castillo Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA (2014) The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One 9:e103891

    Google Scholar 

  260. Akutse KS, Maniania NK, Fiaboe KKM, Van den Berg J, Ekesi S (2013) Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecol 6:293–301

    Google Scholar 

  261. Raad M, Glare TR, Brochero HL, Müller C, Rostás M (2019) Transcriptional reprogramming of Arabidopsis thaliana defence pathways by the entomopathogen Beauveria bassiana correlates with resistance against a fungal pathogen but not against insects. Front Microbiol 10:615

    Google Scholar 

  262. Griffin MR, Ownley B, Klingeman WE, Pereira R (2006) Evidence of induced systemic resistance with Beauveria bassiana against Xanthomonas in cotton. Phytopathology 96:S42

    Google Scholar 

  263. Jaber LR, Salem NM (2014) Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) for managing Zucchini yellow mosaic virus in cucurbits. Biocontrol Sci Tech 24:1096–1109

    Google Scholar 

  264. González-Mas N, Cuenca-Medina M, Gutiérrez-Sánchez F, Quesada-Moraga E (2019) Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. J Pest Sci 92:1271–1281

    Google Scholar 

  265. Bruce A, Srinivasan U, Staines HJ, Highley TL (1995) Chitinase and laminarinase production in liquid culture by Trichoderma spp. and their role in biocontrol of wood decay fungi. Int Biodeterior Biodegrad 35:337–353

    Google Scholar 

  266. Steyaert JM, Ridgway HJ, Elad Y, Stewart A (2003) Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma. N Z J Crop Hortic Sci 31:281–291

    Google Scholar 

  267. Calistru C, McLean M, Berjak P (1997) In vitro studies on the potential for biological control of Aspergillus flavus and Fusarium moniliforme by Trichoderma species: a study of the production of extracellular metabolites by Trichoderma species. Mycopathologia 137:115–124

    Google Scholar 

  268. Fenice M (2016) The psychrotolerant antarctic fungus Lecanicillium muscarium CCFEE 5003: a powerful producer of cold-tolerant chitinolytic enzymes. Molecules 21:447

    Google Scholar 

  269. Griffin MR (2007) Beauveria bassiana, a cotton endophyte with biocontrol activity against seedling disease. PhD diss., University of Tennessee, 2007.

    Google Scholar 

  270. Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45

    Article  Google Scholar 

  271. Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41

    Article  Google Scholar 

  272. Ríos-Moreno A, Garrido-Jurado I, Resquín-Romero G, Arroyo-Manzanares N, Arce L, Quesada-Moraga E (2016) Destruxin A production by Metarhizium brunneum strains during transient endophytic colonisation of Solanum tuberosum. Biocontrol Sci Tech 26:1574–1585

    Google Scholar 

  273. Leckie BM, Ownley BH, Pereira RM, Klingeman WE, Jones CJ, Gwinn KD (2008) Mycelia and spent fermentation broth of Beauveria bassiana incorporated into synthetic diets affect mortality, growth and development of larval Helicoverpa zea (Lepidoptera: Noctuidae). Biocontrol Sci Tech 18:697–710

    Google Scholar 

  274. Bernardini M, Carilli A, Pacioni G, Santurbano B (1975) Isolation of beauvericin from Paecilomyces fumoso-roseus. Phytochemistry 14:1865

    Google Scholar 

  275. Vining LC, Kelleher WJ, Schwarting AE (1962) Oosporein production by a strain of Beauveria bassiana originally identified as Amanita muscaria. Can J Microbiol 8:931–933

    Google Scholar 

  276. Strasser H, Abendstein D, Stuppner H, Butt TM (2000) Monitoring the distribution of secondary metabolites produced by the entomogenous fungus Beauveria brongniartii with particular reference to oosporein. Mycol Res 104:1227–1233

    Google Scholar 

  277. Suzuki A, Kanaoka M, Isogai A, Murakoshi S, Ichinoe M, Tamura S (1977) Bassianolide, a new insecticidal cyclodepsipeptide from Beauveria bassiana and Verticillium lecanii. Tetrahedron Lett 18:2167–2170

    Google Scholar 

  278. Wang Q, Xu L (2012) Beauvericin, a bioactive compound produced by fungi: a short review. Molecules 17:2367–2377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Zotti M, Dos Santos EA, Cagliari D, Christiaens O, Taning CNT, Smagghe G (2018) RNA interference technology in crop protection against arthropod pests. pathogens and nematodes. Pest Manag Sci 74:1239–1250

    Article  CAS  PubMed  Google Scholar 

  280. Jay F, Vitel M, Brioudes F, Louis M, Knobloch T, Voinnet O (2019) Chemical enhancers of posttranscriptional gene silencing in Arabidopsis. RNA 25:1078–1090

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  281. Collinge DB, Jørgensen HJL, Latz MAC, Manzotti A, Ntana F, Rojas Tayo EC, Jensen B (2019) Searching for novel fungal biological control agents for plant disease control among endophytes. In: Endophytes for a growing world

    Google Scholar 

  282. Vandenberg JD (1990) Safety of four entomopathogens for caged adult honey bees (Hymenoptera: Apidae). J Econ Entomol 83:755–759

    Article  Google Scholar 

  283. Al-Mazra’Awi MS, Kevan PG, Shipp L (2007) Development of Beauveria bassiana dry formulation for vectoring by honey bees Apis mellifera (Hymenoptera: Apidae) to the flowers of crops for pest control. Biocontrol Sci Tech 17:733–741

    Google Scholar 

  284. Cappa F, Petrocelli I, Dani FR, Dapporto L, Giovannini M, Silva-Castellari J, Turillazzi S, Cervo R (2019) Natural biocide disrupts nestmate recognition in honeybees. Sci Rep 9:3171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  285. United N (2015) Transforming our world: the 2030 Agenda for sustainable development

    Google Scholar 

  286. Stenberg JA (2017) A conceptual framework for integrated pest management. Trends Plant Sci 22:759–769

    Article  CAS  PubMed  Google Scholar 

  287. Westman SM, Kloth KJ, Hanson J, Ohlsson AB, Albrectsen BR (2019) Defence priming in Arabidopsis – a Meta-analysis. Sci Rep 9:1–13

    Article  CAS  Google Scholar 

  288. Pineda A, Kaplan I, Bezemer TM (2017) Steering soil microbiomes to suppress aboveground insect pests. Trends Plant Sci 22:770–778

    Article  CAS  PubMed  Google Scholar 

  289. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, DeWinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138

    Article  CAS  PubMed  Google Scholar 

  290. Reiner JE, Balijepalli A, Robertson JWF, Campbell J, Suehle J, Kasianowicz JJ (2012) Disease detection and management via single nanopore-based sensors. Chem Rev 112:6431–6451

    Article  CAS  PubMed  Google Scholar 

  291. Yu K, Liu Y, Tichelaar R, Savant N, Lagendijk E, van Kuijk SJL, Stringlis IA, van Dijken AJH, Pieterse CMJ, Bakker PAHM, Haney CH, Berendsen RL (2019) Rhizosphere-associated pseudomonas suppress local root immune responses by gluconic acid-mediated lowering of environmental pH. Curr Biol 29:3913–3920.e3914

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge funding from PRIMA programme, supported under Horizon 2020, the European Union’s Framework Programme for Research and Innovation (INTOMED project). AD and KP acknowledge funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement N. 793186 (RNASTIP). MP and GB gratefully acknowledge the support from the Onassis Foundation (R-ZJ 003-02) and the Hellenic Foundation for Research and Innovation (H.F.R.I.) under the “First Call for H.F.R.I. Research Projects to support Faculty members and Researchers and the procurement of high-cost research equipment grant” (Project Number: 50). MMG and WD acknowledge funding from Agence Nationale de la Promotion de la Recherche Scientifique (ANPR), Ministère de l’Enseignement Supérieur et de la Recherche Scientifique. PB and JP were supported by the Foundation for Science and Technology (FCT, Portugal) and FEDER under Programme PT2020 for financial support to CIMO (UID/AGR/00690/2019) within the project PRIMA/0002/2018. RM and SK acknowledge funding from Ministry of Higher Education, Scientific Research and Professional Training (MESRSFC, Morocco). VF, VP and PSB acknowledge funding from the Generalitat Valenciana GV/2018/115 in the hallmark of projects for Emergent Research Groups and the Spanish Ministry MINECO RTI2018-094350-B-C33.

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Authors and Affiliations

  1. School of Agricultural and Forestry Sciences Department of Agricultural Development, Democritus University of Thrace, Orestiada, Greece

    Maria L. Pappas & George D. Broufas

  2. Centro de Investigação de Montanha (CIMO), Instituto Politécnico de Bragança, Bragança, Portugal

    Paula Baptista & José Alberto Pereira

  3. Department of Biochemistry & Biotechnology, University of Thessaly, Larissa, Greece

    Athanasios Dalakouras & Kalliope Papadopoulou

  4. Institute of Plant Breeding and Genetic Resources ELGO-DEMETER, Thessaloniki, Greece

    Athanasios Dalakouras

  5. Laboratory of Biotechnology and Nuclear Technologies, LR16CNSTN01, National Centre of Nuclear Sciences and Technologies, Tunis, Tunisia

    Wafa Djobbi & Meriem Msaad Guerfali

  6. Metabolic Integration and Cell Signaling Laboratory, Plant Physiology Section, Unidad Asociada al Consejo Superior de Investigaciones Científicas (EEZ-CSIC)-Department of Ciencias Agrarias y del Medio Natural, Universitat Jaume I, Castellón, Spain

    Victor Flors, Victoria Pastor & Paloma Sánchez-Bel

  7. Biotechnology Research Unit, National Institute of Agricultural Research, Rabat, Morocco

    Slimane Khayi & Rachid Mentag

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  1. Maria L. Pappas
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Correspondence to Maria L. Pappas .

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  1. Faculty of Pharmaceutical Sciences, Université de Bordeaux, Bordeaux, France

    Jean-Michel Mérillon

  2. Department of Botany, Mohanlal Sukhadia University, Udaipur, India

    Kishan Gopal Ramawat

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Pappas, M.L. et al. (2020). Biological and Molecular Control Tools in Plant Defense. In: Mérillon, JM., Ramawat, K.G. (eds) Plant Defence: Biological Control. Progress in Biological Control, vol 22. Springer, Cham. https://doi.org/10.1007/978-3-030-51034-3_1

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