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Role of Jasmonates in Beneficial Microbe–Root Interactions

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Jasmonate in Plant Biology

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2085))

Abstract

The phytohormone jasmonate (JA) modulates various defense and developmental responses of plants, and is implied in the integration of multiple environmental signals. Given its centrality in regulating plant physiology according to external stimuli, JA influences the establishment of interactions between plant roots and beneficial bacteria or fungi. In many cases, moderate JA signaling promotes the onset of mutualism, while massive JA signaling inhibits it. The output also depends on the compatibility between microbe and host plant and on nutritional or environmental cues. Also, JA biosynthesis and perception participate in the systemic regulation of mutualistic interactions and in microbe-induced resistance to biotic and abiotic stress. Here, we review our current knowledge of the role of JA biosynthesis, signaling, and responses during mutualistic root–microbe interactions.

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References

  1. Lakshmanan V, Selvaraj G, Bais HP (2014) Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 166(2):689–700. https://doi.org/10.1104/pp.114.245811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Mercado-Blanco J, Abrantes I, Caracciolo AB, Bevivino A, Ciancio A, Grenni P et al (2018) Belowground microbiota and the health of tree crops. Front Microbiol 9(6):1006. https://doi.org/10.3389/fmicb.2018.01006

    Article  PubMed  PubMed Central  Google Scholar 

  3. Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66(8):2167–2175. https://doi.org/10.1093/jxb/erv157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML et al (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17(2):316–331. https://doi.org/10.1111/1462-2920.12439

    Article  PubMed  Google Scholar 

  5. Qin Y, Druzhinina IS, Pan X, Yuan Z (2016) Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol Adv 34(7):1245–1259. https://doi.org/10.1016/j.biotechadv.2016.08.005

    Article  CAS  PubMed  Google Scholar 

  6. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486. https://doi.org/10.1016/j.tplants.2012.04.001

    Article  CAS  PubMed  Google Scholar 

  7. Raaijmakers JM, Mazzola M (2016) Soil immune responses. Science 352(6292):1392–1393. https://doi.org/10.1126/science.aaf3252

    Article  CAS  PubMed  Google Scholar 

  8. Shikano I, Rosa C, Tan C-W, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55(1):313–331. https://doi.org/10.1146/annurev-phyto-080516-035319

    Article  CAS  PubMed  Google Scholar 

  9. Bakker PAHM, Pieterse CMJ, de Jonge R, Berendsen RL (2018) The soil-borne legacy. Cell 172(6):1178–1180. https://doi.org/10.1016/j.cell.2018.02.024

    Article  CAS  PubMed  Google Scholar 

  10. Gutjahr C, Parniske M (2013) Cell and developmental biology of Arbuscular Mycorrhiza Symbiosis. Annu Rev Cell Dev Biol 29(1):593–617. https://doi.org/10.1146/annurev-cellbio-101512-122413

    Article  CAS  PubMed  Google Scholar 

  11. Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-Rhizobial Symbiosis. Annu Rev Genet 45(1):119–144. https://doi.org/10.1146/annurev-genet-110410-132549

    Article  CAS  PubMed  Google Scholar 

  12. Gutjahr C (2014) Phytohormone signaling in arbuscular mycorhiza development. Curr Opin Plant Biol 20:26–34. https://doi.org/10.1016/j.pbi.2014.04.003

    Article  CAS  PubMed  Google Scholar 

  13. Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett DS (2016) Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol 14(12):760–773. https://doi.org/10.1038/nrmicro.2016.149

    Article  CAS  PubMed  Google Scholar 

  14. Pieterse CMJ, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316. https://doi.org/10.1038/nchembio.164

    Article  CAS  PubMed  Google Scholar 

  15. Nomura K, Melotto M, He S-Y (2005) Suppression of host defense in compatible plant–pseudomonas syringae interactions. Curr Opin Plant Biol 8(4):361–368. https://doi.org/10.1016/j.pbi.2005.05.005

    Article  CAS  PubMed  Google Scholar 

  16. El Oirdi M, El Rahman TA, Rigano L, El Hadrami A, Rodriguez MC, Daayf F et al (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23(6):2405–2421. https://doi.org/10.1105/tpc.111.083394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Marchetti M, Capela D, Glew M, Cruveiller S, Chane-Woon-Ming B, Gris C et al (2010) Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol 8(1):e1000280. https://doi.org/10.1371/journal.pbio.1000280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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(1):489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055

    Article  CAS  PubMed  Google Scholar 

  19. Kazan K, Manners JM (2011) The interplay between light and jasmonate signalling during defence and development. J Exp Bot 62(12):4087–4100. https://doi.org/10.1093/jxb/err142

    Article  CAS  PubMed  Google Scholar 

  20. Campos ML, Yoshida Y, Major IT, De Oliveira Ferreira D, Weraduwage SM, Froehlich JE et al (2016) Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570. https://doi.org/10.1038/ncomms12570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42(1):23–46. https://doi.org/10.1146/annurev-ecolsys-102710-145039

    Article  Google Scholar 

  22. Verhagen BWM, Glazebrook J, Zhu T, Chang H-S, van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant-Microbe Interact 17(8):895–908. https://doi.org/10.1094/MPMI.2004.17.8.895

    Article  CAS  PubMed  Google Scholar 

  23. Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E (2017) Nutrient exchange and regulation in Arbuscular Mycorrhizal Symbiosis. Mol Plant 10(9):1147–1158. https://doi.org/10.1016/j.molp.2017.07.012

    Article  CAS  PubMed  Google Scholar 

  24. Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6(1):1559. https://doi.org/10.3389/fmicb.2015.01559

    Article  PubMed  PubMed Central  Google Scholar 

  25. Nagata M, Yamamoto N, Miyamoto T, Shimomura A, Arima S, Hirsch AM, Suzuki A (2016) Enhanced hyphal growth of arbuscular mycorrhizae by root exudates derived from high R/FR treated Lotus japonicus. Plant Signal Behav 11(6):e1187356. https://doi.org/10.1080/15592324.2016.1187356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65(1):335–363. https://doi.org/10.1146/annurev-arplant-050213-040145

    Article  CAS  PubMed  Google Scholar 

  27. Siciliano V, Genre A, Balestrini R, Cappellazzo G, deWit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144(3):1455–1466. https://doi.org/10.1104/pp.107.097980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Blilou I, Ocampo JA, García-Garrido JM (1999) Resistance of pea roots to endomycorrhizal fungus or rhizobium correlates with enhanced levels of endogenous salicylic acid. J Exp Bot 50(340):1663–1668. https://doi.org/10.1093/jxb/50.340.1663

    Article  CAS  Google Scholar 

  29. Blilou I, Ocampo JA, García-Garrido JM, Garcia-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51(353):1969–1977. https://doi.org/10.1093/jexbot/51.353.1969

    Article  CAS  PubMed  Google Scholar 

  30. Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microbe Interact 22(7):763–772. https://doi.org/10.1094/MPMI-22-7-0763

    Article  CAS  PubMed  Google Scholar 

  31. Hause B, Maier W, Miersch O, Kramell R, Strach D (2002) Induction of Jasmonate biosynthesis in Arbuscular Mycorrhizal barley roots. Plant Physiol 130(3):1213–1220. https://doi.org/10.1104/pp.006007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Stumpe M, Carsjens J-G, Stenzel I, Göbel C, Lang I, Pawlowski K et al (2005) Lipid metabolism in arbuscular mycorrhizal roots of Medicago truncatula. Phytochemistry 66(7):781–791. https://doi.org/10.1016/j.phytochem.2005.01.020

    Article  CAS  PubMed  Google Scholar 

  33. Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222(4):709–715. https://doi.org/10.1007/s00425-005-0003-4

    Article  CAS  PubMed  Google Scholar 

  34. Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces Jasmonate levels and the degree of Mycorrhization with Glomus intraradices. Plant Physiol 139(3):1401–1410. https://doi.org/10.1104/pp.105.069054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. León-Morcillo RJ, Ángel J, Martín-Rodríguez, Vierheilig H, Ocampo JA, García-Garrido JM (2012) Late activation of the 9-oxylipin pathway during arbuscular mycorrhiza formation in tomato and its regulation by jasmonate signalling. J Exp Bot 63(10):3545–3558. https://doi.org/10.1093/jxb/ers010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tejeda-Sartorius M, Martínez De La Vega O, Délano-Frier JP (2008) Jasmonic acid influences mycorrhizal colonization in tomato plants by modifying the expression of genes involved in carbohydrate partitioning. Physiol Plant 133(2):339–353. https://doi.org/10.1111/j.1399-3054.2008.01081.x

    Article  CAS  PubMed  Google Scholar 

  37. Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68(1):101–110. https://doi.org/10.1016/j.phytochem.2006.09.025

    Article  CAS  PubMed  Google Scholar 

  38. Herrera-Medina MJ, Tamayo MI, Vierheilig H, Ocampo JA, García-Garrido JM (2008) The jasmonic acid signalling pathway restricts the development of the arbuscular mycorrhizal association in tomato. J Plant Growth Regul 27(3):221–230. https://doi.org/10.1007/s00344-008-9049-4

    Article  CAS  Google Scholar 

  39. Regvar M, Gogala N, Zalar P (1996) Effect of jasmonic acid on mycorrhizal Allium sativum. New Phytol 134(134):703–707. https://doi.org/10.1111/j.1469-8137.1996.tb04936.x

    Article  CAS  PubMed  Google Scholar 

  40. Kiers ET, Adler LS, Grman EL, van der Heijden MGA (2010) Manipulating the jasmonate response: how do methyl jasmonate additions mediate characteristics of aboveground and belowground mutualisms? Funct Ecol 24(2):434–443. https://doi.org/10.1111/j.1365-2435.2009.01625.x

    Article  Google Scholar 

  41. Landgraf R, Schaarschmidt S, Hause B (2012) Repeated leaf wounding alters the colonization of Medicago truncatula roots by beneficial and pathogenic microorganisms. Plant Cell Environ 35(7):1344–1357. https://doi.org/10.1111/j.1365-3040.2012.02495.x

    Article  CAS  PubMed  Google Scholar 

  42. Gutjahr C, Siegler H, Haga K, Iino M, Paszkowski U (2015) Full establishment of arbuscular mycorrhizal symbiosis in rice occurs independently of enzymatic jasmonate biosynthesis. PLoS One 10(4):e0123422. https://doi.org/10.1371/journal.pone.0123422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ludwig-Müller J, Bennett RN, García-Garrido JM, Piché Y, Vierheilig H (2002) Reduced arbuscular mycorrhizal root colonization in Tropaeolum majus and Carica papaya after jasmonic acid application can not be attributed to increased glucosinolate levels. J Plant Physiol 159(5):517–523. https://doi.org/10.1078/0176-1617-00731

    Article  Google Scholar 

  44. Riedel T, Groten K, Baldwin IT (2008) Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant Cell Environ 31(9):1203–1213. https://doi.org/10.1111/j.1365-3040.2008.01827.x

    Article  CAS  PubMed  Google Scholar 

  45. Fernández I, Merlos M, López-Ráez JA, Martínez-Medina A, Ferrol N, Azcón C et al (2014) Defense related Phytohormones regulation in Arbuscular Mycorrhizal symbioses depends on the partner genotypes. J Chem Ecol 40(7):791–803. https://doi.org/10.1007/s10886-014-0473-6

    Article  CAS  PubMed  Google Scholar 

  46. Yang Z-B, He C, Ma Y, Herde M, Ding Z (2017) Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol 173(2):1420–1433. https://doi.org/10.1104/pp.16.01756

    Article  CAS  PubMed  Google Scholar 

  47. Genre A, Bonfante P (1998) Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol 140(4):745–752. https://doi.org/10.1046/j.1469-8137.1998.00314.x

    Article  CAS  PubMed  Google Scholar 

  48. Blancaflor EB, Zhao L, Harrison MJ (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217(4):154–165. https://doi.org/10.1007/BF01283396

    Article  CAS  PubMed  Google Scholar 

  49. Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Pühler A, Perlick AM, Küster H (2004) Transcriptome profiling in root nodules and Arbuscular Mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root Endosymbioses. Mol Plant-Microbe Interact 17(10):1063–1077. https://doi.org/10.1094/MPMI.2004.17.10.1063

    Article  CAS  PubMed  Google Scholar 

  50. Koda Y (1997) Possible involvement of jasmonates in various morphogenic events. Physiol Plant 100(3):639–646. https://doi.org/10.1111/j.1399-3054.1997.tb03070.x

    Article  CAS  Google Scholar 

  51. Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ, Schueller M et al (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72. https://doi.org/10.1111/j.1469-8137.2005.01388.x

    Article  CAS  PubMed  Google Scholar 

  52. Gómez S, Ferrieri RA, Schueller M, Orians CM (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol 188(3):835–844. https://doi.org/10.1111/j.1469-8137.2010.03414.x

    Article  CAS  PubMed  Google Scholar 

  53. Hause B, Stenzel I, Miersch O, Maucher H, Kramell R, Ziegler J, Wasternack C (2000) Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J 24(1):113–126. https://doi.org/10.1046/j.1365-313X.2000.00861.x

    Article  CAS  PubMed  Google Scholar 

  54. Maucher H, Hause B, Feussner I, Ziegler J, Wasternack C (2001) Allene oxide synthases of barley (Hordeum vulgare cv. Salome): tissue specific regulation in seedling development. Plant J 21(2):199–213. https://doi.org/10.1046/j.1365-313x.2000.00669.x

    Article  Google Scholar 

  55. Sánchez-Bel P, Sanmartín N, Pastor V, Mateu D, Cerezo M, Vidal-Albalat A et al (2018) Mycorrhizal tomato plants fine tunes the growth-defence balance upon N depleted root environments. Plant Cell Environ 41(2):406–420. https://doi.org/10.1111/pce.13105

    Article  CAS  PubMed  Google Scholar 

  56. Schaarschmidt S, Roitsch T, Hause B (2006) Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J Exp Bot 57(15):4015–4023. https://doi.org/10.1093/jxb/erl172

    Article  CAS  PubMed  Google Scholar 

  57. Thoma I, Loeffler C, Sinha AK, Gupta M, Krischke M, Steffan B et al (2003) Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. Plant J 34(3):363–375. https://doi.org/10.1046/j.1365-313X.2003.01730.x

    Article  CAS  PubMed  Google Scholar 

  58. Daher Z, Recorbet G, Solymosi K, Wienkoop S, Mounier A, Morandi D et al (2017) Changes in plastid proteome and structure in arbuscular mycorrhizal roots display a nutrient starvation signature. Physiol Plant 159(1):13–29. https://doi.org/10.1111/ppl.12505

    Article  CAS  PubMed  Google Scholar 

  59. Harrison MJ, Dixon RA (1994) Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J 6(1):9–20. https://doi.org/10.1046/j.1365-313X.1994.6010009.x

    Article  CAS  Google Scholar 

  60. Vellosillo T, Martinez M, Lopez MA, Vicente J, Cascon T, Dolan L et al (2007) Oxylipins produced by the 9-Lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling Cascade. Plant Cell 19(3):831–846. https://doi.org/10.1105/tpc.106.046052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61(10):2589–2601. https://doi.org/10.1093/jxb/erq089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7(1):191–226. https://doi.org/10.1146/annurev.cb.07.110191.001203

    Article  CAS  PubMed  Google Scholar 

  63. Suzuki A, Suriyagoda L, Shigeyama T, Tominaga A, Sasaki M, Hiratsuka Y et al (2011) Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proc Natl Acad Sci 108(40):16837–16842. https://doi.org/10.1073/pnas.1105892108

    Article  PubMed  PubMed Central  Google Scholar 

  64. Nakagawa T, Kawaguchi M (2006) Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol 47(1):176–180. https://doi.org/10.1093/pcp/pci222

    Article  CAS  PubMed  Google Scholar 

  65. Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM (2006) Crosstalk between jasmonic acid, ethylene and nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 46(6):961–970. https://doi.org/10.1111/j.1365-313X.2006.02751.x

    Article  CAS  PubMed  Google Scholar 

  66. Seo HS, Li J, Lee S-Y, Yu J-W, Kim K-H, Lee S-H, Paek I-J, Paek NC (2007) The Hypernodulating nts mutation induces Jasmonate synthetic pathway in soybean leaves. Mol Cells 24(2):185–193

    CAS  PubMed  Google Scholar 

  67. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with Rhizobial infection in legumes. Annu Rev Plant Biol 59(1):519–546. https://doi.org/10.1146/annurev.arplant.59.032607.092839

    Article  CAS  PubMed  Google Scholar 

  68. Rosas S, Soria R, Correa N, Abdala G (1998) Jasmonic acid stimulates the expression of nod genes in rhizobium. Plant Mol Biol 38:1161–1168. https://doi.org/10.1023/A:1006064807870

    Article  CAS  PubMed  Google Scholar 

  69. Mabood F, Souleimanov A, Khan W, Smith DL (2006) Jasmonates induce nod factor production by Bradyrhizobium japonicum. Plant Physiol Biochem 44(11):759–765. https://doi.org/10.1016/j.plaphy.2006.10.025

    Article  CAS  PubMed  Google Scholar 

  70. Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res 41:1–62. https://doi.org/10.1016/S0065-2296(04)41001-5

    Article  CAS  Google Scholar 

  71. Zhang N, Venkateshwaran M, Boersma M, Harms A, Howes-Podoll M, Den Os D et al (2012) Metabolomic profiling reveals suppression of oxylipin biosynthesis during the early stages of legume-rhizobia symbiosis. FEBS Lett 586(19):3150–3158. https://doi.org/10.1016/j.febslet.2012.06.046

    Article  CAS  PubMed  Google Scholar 

  72. Kouchi H, Shimomura K, Hata S, Hirota A, Wu GJ, Kumagai H et al (2004) Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Res 11(4):263–274. https://doi.org/10.1093/dnares/11.4.263

    Article  CAS  PubMed  Google Scholar 

  73. Perlick AM, Albus U, Stavridis T, Frühling M, Küster H, Pühler A (1996) The Vicia faba Lipoxygenase gene VfLOX1 is expressed in the root nodule parenchyma. Mol Plant-Microbe Interact 9(9):860–863. https://doi.org/10.1094/MPMI-9-0860

    Article  CAS  PubMed  Google Scholar 

  74. Bueno P, Soto MJ, Rodríguez-Rosales MP, Sanjuan J, Olivares J, Donaire JP (2001) Time-course of lipoxygenase, antioxidant enzyme activities and H2O2 accumulation during the early stages of rhizobium–legume symbiosis. New Phytol 152(1):91–96. https://doi.org/10.1046/j.0028-646x.2001.00246.x

    Article  CAS  Google Scholar 

  75. Mohammadi M, Karr AL (2003) Induced lipoxygenases in soybean root nodules. Plant Sci 164(4):471–479. https://doi.org/10.1016/S0168-9452(02)00431-4

    Article  CAS  Google Scholar 

  76. Costanzo ME, Andrade A, Del Carmen Tordable M, Cassán F, Abdala G (2012) Production and function of jasmonates in nodulated roots of soybean plants inoculated with Bradyrhizobium japonicum. Arch Microbiol 194(10):837–845. https://doi.org/10.1007/s00203-012-0817-y

    Article  CAS  PubMed  Google Scholar 

  77. Demchenko K, Zdyb A, Feussner I, Pawlowski K (2012) Analysis of the subcellular localisation of lipoxygenase in legume and actinorhizal nodules. Plant Biol 14(1):56–63. https://doi.org/10.1111/j.1438-8677.2011.00480.x

    Article  CAS  PubMed  Google Scholar 

  78. Zdyb A, Salgado MG, Demchenko KN, Brenner WG, Płaszczyca M, Stumpe M et al (2018) Allene oxide synthase, allene oxide cyclase and jasmonic acid levels in Lotus japonicus nodules. PLoS One 13(1):1–16. https://doi.org/10.1371/journal.pone.0190884

    Article  CAS  Google Scholar 

  79. Zdyb A, Demchenko K, Heumann J, Mrosk C, Grzeganek P, Göbel C et al (2011) Jasmonate biosynthesis in legume and actinorhizal nodules. New Phytol 189(2):568–579. https://doi.org/10.1111/j.1469-8137.2010.03504.x

    Article  CAS  PubMed  Google Scholar 

  80. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial Interface in the Jasmonate signaling Cascade. Plant Cell 23(9):3089–3100. https://doi.org/10.1105/tpc.111.089300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Li Y, Xu M, Wang N, Li Y (2015) A JAZ protein in Astragalus sinicus interacts with a leghemoglobin through the TIFY domain and is involved in nodule development and nitrogen fixation. PLoS One 10(10):e0139964. https://doi.org/10.1371/journal.pone.0139964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Wittenberg JB, Bergersen FJ, Appleby CA, Turner GL (1974) The role of leghemoglobin in nitrogen fixation by bacteroids isolated from soybean root nodules. J Biol Chem 29(13):4057–4066. http://www.jbc.org/content/249/13/4057.abstract

    Google Scholar 

  83. Ott T, van Dongen JT, Günther C, Krusell L, Desbrosses G, Vigeolas H et al (2005) Symbiotic Leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15(6):531–535. https://doi.org/10.1016/j.cub.2005.01.042

    Article  CAS  PubMed  Google Scholar 

  84. Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108(5):789–795. https://doi.org/10.1093/aob/mcr205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K et al (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426. https://doi.org/10.1038/nature01207

    Article  CAS  PubMed  Google Scholar 

  86. Nishimura R, Hayashi M, Wu G-J, Kouchi H, Imaizumi-Anraku H, Murakami Y et al (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426. https://doi.org/10.1038/nature01231

    Article  CAS  PubMed  Google Scholar 

  87. Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299(5603):109–112. https://doi.org/10.1126/science.1077937

    Article  CAS  PubMed  Google Scholar 

  88. Schnabel E, Journet EP, De Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58(6):809–822. https://doi.org/10.1007/s11103-005-8102-y

    Article  CAS  PubMed  Google Scholar 

  89. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50(1):67–77. https://doi.org/10.1093/pcp/pcn194

    Article  CAS  PubMed  Google Scholar 

  90. Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’haeseleer K et al (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153(1):222–237. https://doi.org/10.1104/pp.110.153718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kinkema M, Gresshoff PM (2008) Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol Plant-Microbe Interact 21(10):1337–1348. https://doi.org/10.1094/MPMI-21-10-1337

    Article  CAS  PubMed  Google Scholar 

  92. Tsikou D, Yan Z, Holt DB, Abel NB, Reid DE, Madsen LH et al (2018) Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA. Science 6907(8):eaat6907. https://doi.org/10.1126/science.aat6907

    Article  CAS  Google Scholar 

  93. Magori S, Kawaguchi M (2010) Analysis of two potential long-distance signaling molecules, LjCLE-RS1/2 and jasmonic acid, in a hypernodulating mutant too much love. Plant Signal Behav 5(4):403–405. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2958591/

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19(7):2225–2245. https://doi.org/10.1105/tpc.106.048017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Caba JM, Centeno ML, Fernández B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211(1):98–104. https://doi.org/10.1007/s004250000265

    Article  CAS  PubMed  Google Scholar 

  96. Van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance Auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol 140(4):1494 LP–1491506. http://www.plantphysiol.org/content/140/4/1494.abstract

    Article  Google Scholar 

  97. Heath KD, Lau JA (2011) Herbivores alter the fitness benefits of a plant–rhizobium mutualism. Acta Oecol 37(2):87–92. https://doi.org/10.1016/j.actao.2010.12.002

    Article  Google Scholar 

  98. Perez-Moreno J, Read DJ (2000) Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytol 145(2):301–309. https://doi.org/10.1046/j.1469-8137.2000.00569.x

    Article  CAS  Google Scholar 

  99. Tibbett M, Sanders FE (2002) Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Ann Bot 89(6):783–789. http://www.jstor.org/stable/42771516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Luo Z-B, Janz D, Jiang X, Gobel C, Wildhagen H, Tan Y et al (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151(4):1902–1917. https://doi.org/10.1104/pp.109.143735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H et al (2013) Roots and associated fungi drive long-term carbon sequestration in boreal Forest. Science 339(6127):1615–1618. https://doi.org/10.1126/science.1231923

    Article  CAS  PubMed  Google Scholar 

  102. Lindahl BD, Tunlid A (2014) Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytol 205(4):1443–1447. https://doi.org/10.1111/nph.13201

    Article  CAS  PubMed  Google Scholar 

  103. Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can J Bot 82(8):1074–1088. https://doi.org/10.1139/b04-071

    Article  Google Scholar 

  104. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F et al (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410. https://doi.org/10.1038/ng.3223

    Article  CAS  PubMed  Google Scholar 

  105. Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A et al (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21(14):1197–1203. https://doi.org/10.1016/j.cub.2011.05.033

    Article  CAS  PubMed  Google Scholar 

  106. Plett JM, Daguerre Y, Wittulsky S, Vayssieres A, Deveau A, Melton SJ et al (2014) Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci 111(22):8299–8304. https://doi.org/10.1073/pnas.1322671111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Plett JM, Khachane A, Ouassou M, Sundberg B, Kohler A, Martin F (2014b) Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytol 202(1):270–286. https://doi.org/10.1111/nph.12655

    Article  CAS  PubMed  Google Scholar 

  108. Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23(1):25–41. https://doi.org/10.1016/j.tplants.2017.09.003

    Article  CAS  PubMed  Google Scholar 

  109. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206(4):1196–1206. https://doi.org/10.1111/nph.13312

    Article  PubMed  Google Scholar 

  110. Goh C-H, Veliz Vallejos DF, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39(7):826–839. https://doi.org/10.1007/s10886-013-0326-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52(1):347–375. https://doi.org/10.1146/annurev-phyto-082712-102340

    Article  CAS  PubMed  Google Scholar 

  112. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48(1):21–43. https://doi.org/10.1146/annurev-phyto-073009-114450

    Article  CAS  PubMed  Google Scholar 

  113. Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64(5):1263–1280. https://doi.org/10.1093/jxb/ert026

    Article  CAS  PubMed  Google Scholar 

  114. Haney CH, Samuel BS, Bush J, Ausubel FM, Hospital MG (2015) Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat Plants 1(6):1–22. https://doi.org/10.1038/nplants.2015.51

    Article  CAS  Google Scholar 

  115. Wintermans PCA, Bakker PAHM, Pieterse CMJ (2016) Natural genetic variation in Arabidopsis for responsiveness to plant growth-promoting rhizobacteria. Plant Mol Biol 90(6):623–634. https://doi.org/10.1007/s11103-016-0442-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Iavicoli A, Boutet E, Buchala A, Métraux J-P (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Microbe Interact 16(10):851–858. https://doi.org/10.1094/MPMI.2003.16.10.851

    Article  CAS  PubMed  Google Scholar 

  117. Pineda A, Soler R, Weldegergis BT, Shimwela MM, Van Loon JJA, Dicke M (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ 36(2):393–404. https://doi.org/10.1111/j.1365-3040.2012.02581.x

    Article  CAS  PubMed  Google Scholar 

  118. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40(1):309–348. https://doi.org/10.1146/annurev.phyto.40.030402.110010

    Article  CAS  PubMed  Google Scholar 

  119. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321(1):341–361. https://doi.org/10.1007/s11104-008-9568-6

    Article  CAS  Google Scholar 

  120. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker P, Raaijmakers J (2012) Deciphering the Rhizosphere microbiome. Science 1097(2011):1097–1100. https://doi.org/10.1126/science.1203980

    Article  CAS  Google Scholar 

  121. Carvalhais LC, Dennis PG, Badri DV, Tyson GW, Vivanco JM, Schenk PM (2013) Activation of the Jasmonic acid plant defence pathway alters the composition of Rhizosphere bacterial communities. PLoS One 8(2):e56457. https://doi.org/10.1371/journal.pone.0056457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Liu H, Carvalhais LC, Schenk PM, Dennis PG (2017) Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci Rep 7:41766. https://doi.org/10.1038/srep41766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. 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(9):1049–1058. https://doi.org/10.1094/MPMI-01-15-0016-R

    Article  CAS  PubMed  Google Scholar 

  124. Miché L, Battistoni F, Gemmer S, Belghazi M, Reinhold-Hurek B (2006) Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol Plant-Microbe Interact 19(5):502–511. https://doi.org/10.1094/MPMI-19-0502

    Article  CAS  PubMed  Google Scholar 

  125. Martínez-Medina A, Appels FVW, van Wees SCM (2017) Impact of salicylic acid- and jasmonic acid-regulated defences on root colonization by Trichoderma harzianum T-78. Plant Signal Behav 12(8):e1345404. https://doi.org/10.1080/15592324.2017.1345404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Varma A, Verma S, Sudha, Sahay N, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65(6):2741–2744

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci 102(38):13386–13391. https://doi.org/10.1073/pnas.0504423102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V et al (2011) Broad-Spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156(2):726–740. https://doi.org/10.1104/pp.111.176446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D et al (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7(10):e1002290. https://doi.org/10.1371/journal.ppat.1002290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Baker K, Cook RJ (1974) Biological control of plant pathogens. W.H. Freeman and Company, San Francisco

    Google Scholar 

  131. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F et al (2006) Priming: getting ready for Battle. Mol Plant-Microbe Interact 19(10):1062–1071. https://doi.org/10.1094/MPMI-19-1062

    Article  CAS  PubMed  Google Scholar 

  132. Van Wees SCM, Luijendijk M, Smoorenburg I, van Loon LC, Pieterse CMJ (1999) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol Biol 41(4):537–549. https://doi.org/10.1023/A:1006319216982

    Article  PubMed  Google Scholar 

  133. Pieterse CMJ, Van Wees SCM, Ton J, Van Pelt JA, Van Loon LC (2002) Signalling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol 4(5):535–544. https://doi.org/10.1055/s-2002-35441

    Article  CAS  Google Scholar 

  134. Pieterse CMJ, Van Pelt JA, Ton J, Parchmann S, Mueller MJ, Buchala AJ et al (2000) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol Mol Plant Pathol 57(3):123–134. https://doi.org/10.1006/pmpp.2000.0291

    Article  CAS  Google Scholar 

  135. Djonović S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A Proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145(3):875–889. https://doi.org/10.1104/pp.107.103689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Martínez-Medina A, Roldán A, Albacete A, Pascual JA (2011) The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72(2–3):223–229. https://doi.org/10.1016/j.phytochem.2010.11.008

    Article  CAS  PubMed  Google Scholar 

  137. Shavit R, Ofek-Lalzar M, Burdman S, Morin S (2013) Inoculation of tomato plants with rhizobacteria enhances the performance of the phloem-feeding insect Bemisia tabaci. Front Plant Sci 4(8):306. https://doi.org/10.3389/fpls.2013.00306

    Article  PubMed  PubMed Central  Google Scholar 

  138. Dean JM, Mescher MC, De Moraes CM (2014) Plant dependence on rhizobia for nitrogen influences induced plant defenses and herbivore performance. Int J Mol Sci 15(1):1466–1480. https://doi.org/10.3390/ijms15011466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11(4):443–448. https://doi.org/10.1016/j.pbi.2008.05.005

    Article  CAS  PubMed  Google Scholar 

  140. Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H et al (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10(9):1571–1580. https://doi.org/10.1105/tpc.10.9.1571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Knoester M, Pieterse CMJ, Bol JF, Van Loon LC (1999) Systemic resistance in Arabidopsis induced by Rhizobacteria requires ethylene-dependent signaling at the site of application. Mol Plant-Microbe Interact 12(8):720–727. https://doi.org/10.1094/MPMI.1999.12.8.720

    Article  CAS  PubMed  Google Scholar 

  142. Yan Z, Reddy MS, Ryu C-M, McInroy JA, Wilson M, Kloepper JW (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting Rhizobacteria. Phytopathology 92(12):1329–1333. https://doi.org/10.1094/PHYTO.2002.92.12.1329

    Article  CAS  PubMed  Google Scholar 

  143. Ryu C-M, Murphy JF, Mysore KS, Kloepper JW (2004) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39(3):381–392. https://doi.org/10.1111/j.1365-313X.2004.02142.x

    Article  CAS  PubMed  Google Scholar 

  144. Shoresh M, Yedidia I, Chet I (2005) Involvement of Jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95(1):76–84. https://doi.org/10.1094/PHYTO-95-0076

    Article  CAS  PubMed  Google Scholar 

  145. Ahn I-P, Lee S-W, Suh S-C (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, Jasmonic acid, and NPR1. Mol Plant-Microbe Interact 20(7):759–768. https://doi.org/10.1094/MPMI-20-7-0759

    Article  CAS  PubMed  Google Scholar 

  146. De Vleesschauwer D, Bakker PAHM, Djavaheri M, Hofte M (2008) Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol 148:1996–2012. https://doi.org/10.1104/pp.108.127878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Hase S, Takahashi S, Takenaka S, Nakaho K, Arie T, Seo S et al (2008) Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol 57(5):870–876. https://doi.org/10.1111/j.1365-3059.2008.01858.x

    Article  CAS  Google Scholar 

  148. Hossain MM, Sultana F, Kubota M, Hyakumachi M (2008) Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP16-2 and its cell free filtrate. Plant Soil 304(1):227–239. https://doi.org/10.1007/s11104-008-9542-3

    Article  CAS  Google Scholar 

  149. Korolev N, Rav David D, Elad Y (2008) The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biol Control 53(4):667–683. https://doi.org/10.1007/s10526-007-9103-3

    Article  CAS  Google Scholar 

  150. Stein E, Molitor A, Kogel K-H, Waller F (2008) Systemic resistance in Arabidopsis conferred by the Mycorrhizal fungus Piriformospora indica requires Jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49(11):1747–1751. https://doi.org/10.1093/pcp/pcn147

    Article  PubMed  Google Scholar 

  151. Weller DM, Mavrodi DV, Van Pelt JA, Pieterse CMJ, Van Loon LC, Bakker PA (2012) Induced systemic resistance in Arabidopsis thaliana against pseudomonas syringae pv. Tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102(4):403–412. https://doi.org/10.1094/PHYTO-08-11-0222

    Article  CAS  PubMed  Google Scholar 

  152. Pangesti N, Reichelt M, van de Mortel JE, Kapsomenou E, Gershenzon J, van Loon JJA et al (2016) Jasmonic acid and ethylene signaling pathways regulate Glucosinolate levels in plants during Rhizobacteria-induced systemic resistance against a leaf-chewing herbivore. J Chem Ecol 42(12):1212–1225. https://doi.org/10.1007/s10886-016-0787-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, Pel MJC et al (2008) MYB72 is required in early signaling steps of Rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146(3):1293–1304. https://doi.org/10.1104/pp.107.113829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Segarra G, Van Der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11(1):90–96. https://doi.org/10.1111/j.1438-8677.2008.00162.x

    Article  CAS  PubMed  Google Scholar 

  155. Audenaert K, Pattery T, Cornelis P, Höfte M (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant-Microbe Interact 15(11):1147–1156. https://doi.org/10.1094/MPMI.2002.15.11.1147

    Article  CAS  PubMed  Google Scholar 

  156. Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant-Microbe Interact 18(6):555–561. https://doi.org/10.1094/MPMI-18-0555

    Article  CAS  PubMed  Google Scholar 

  157. Van de Mortel JE, de Vos RCH, Dekkers E, Pineda A, Guillod L, Bouwmeester K et al (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the Rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160(4):2173–2188. https://doi.org/10.1104/pp.112.207324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Conn VM, Walker AR, Franco CMM (2008) Endophytic Actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant-Microbe Interact 21(2):208–218. https://doi.org/10.1094/MPMI-21-2-0208

    Article  CAS  PubMed  Google Scholar 

  159. Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera-Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal- and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungus Botrytis cinerea. Plant Signal Behav 6(10):1554–1563. https://doi.org/10.4161/psb.6.10.17443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Mathys J, De Cremer K, Timmermans P, Van Kerkhove S, Lievens B, Vanhaecke M et al (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci 3:108. https://doi.org/10.3389/fpls.2012.00108

    Article  PubMed  PubMed Central  Google Scholar 

  161. Martínez-Medina A, Fernández I, Sánchez-Guzmán MJ, Jung SC, Pascual JA, Pozo MJ (2013) Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front Plant Sci 4(6):206. https://doi.org/10.3389/fpls.2013.00206

    Article  PubMed  PubMed Central  Google Scholar 

  162. Alizadeh H, Behboudi K, Ahmadzadeh M, Javan-Nikkhah M, Zamioudis C, Pieterse CMJ, Bakker PAHM (2013) Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and pseudomonas sp. Ps14. Biol Control 65(1):14–23. https://doi.org/10.1016/j.biocontrol.2013.01.009

    Article  Google Scholar 

  163. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10(4):393–398. https://doi.org/10.1016/j.pbi.2007.05.004

    Article  CAS  PubMed  Google Scholar 

  164. Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 193–207. https://doi.org/10.1007/978-90-481-9489-6

    Chapter  Google Scholar 

  165. Jung SC, Martínez-Medina A, López-Ráez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38(6):651–664. https://doi.org/10.1007/s10886-012-0134-6

    Article  CAS  PubMed  Google Scholar 

  166. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82(8):1198–1227. https://doi.org/10.1139/b04-082

    Article  Google Scholar 

  167. Gernns H, Alten H, Poehling H-M (2001) Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen – is a compensation possible? Mycorrhiza 11(5):237–243. https://doi.org/10.1007/s005720100128

    Article  CAS  Google Scholar 

  168. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50(3):529–544. https://doi.org/10.1111/j.1365-313X.2007.03069.x

    Article  CAS  PubMed  Google Scholar 

  169. Fritz M, Jakobsen I, Lyngkjær MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16(6):413–419. https://doi.org/10.1007/s00572-006-0051-z

    Article  PubMed  Google Scholar 

  170. De La Noval B, Pérez E, Martínez B, León O, Martínez-Gallardo N, Délano-Frier J (2007) Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens. Mycorrhiza 17(5):449–460. https://doi.org/10.1007/s00572-007-0122-9

    Article  CAS  PubMed  Google Scholar 

  171. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54(1):323–342. https://doi.org/10.1146/annurev.ento.54.110807.090614

    Article  CAS  PubMed  Google Scholar 

  172. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53(368):525–534. https://doi.org/10.1093/jexbot/53.368.525

    Article  CAS  PubMed  Google Scholar 

  173. Gange AC (2007) Insect-mycorrhizal interactions: patterns, processes, and consequences. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 124–144. https://doi.org/10.1017/CBO9780511542701.007

    Chapter  Google Scholar 

  174. Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13(6):579–592. https://doi.org/10.1111/j.1364-3703.2011.00773.x

    Article  CAS  PubMed  Google Scholar 

  175. Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6(9):786. https://doi.org/10.3389/fpls.2015.00786

    Article  PubMed  PubMed Central  Google Scholar 

  176. Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol 17(3):625–631. https://doi.org/10.1111/plb.12277

    Article  CAS  PubMed  Google Scholar 

  177. Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an Arbuscular Mycorrhizal fungus. Mol Plant-Microbe Interact 11(10):1017–1028. https://doi.org/10.1094/MPMI.1998.11.10.1017

    Article  CAS  Google Scholar 

  178. Garmendia I, Goicoechea N, Aguirreolea J (2004) Effectiveness of three Glomus species in protecting pepper (Capsicum annuum L.) against verticillium wilt. Biol Control 31(3):296–305. https://doi.org/10.1016/j.biocontrol.2004.04.015

    Article  Google Scholar 

  179. Kobra N, Jalil K, Youbert G (2009) Effects of three Glomus species as biocontrol agents against verticillium-induced wilt in cotton. J Plant Protect Res 49(2):185–189. https://doi.org/10.2478/v10045-009-0027-z

    Article  Google Scholar 

  180. Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97(6):1274–1280. https://doi.org/10.1111/j.1365-2745.2009.01557.x

    Article  Google Scholar 

  181. Bernaola L, Cosme M, Schneider RW, Stout M (2018) Belowground inoculation with Arbuscular Mycorrhizal fungi increases local and systemic susceptibility of rice plants to different Pest organisms. Front Plant Sci 9(6):747. https://doi.org/10.3389/fpls.2018.00747

    Article  PubMed  PubMed Central  Google Scholar 

  182. Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by Arbuscular Mycorrhizal fungi. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas- functional processes and ecological impact. Springer, Berlin, Heidelberg, pp 123–135. https://doi.org/10.1007/978-90-481-9489-6_9

    Chapter  Google Scholar 

  183. Adolfsson L, Nziengui H, Abreu IN, Šimura J, Beebo A, Herdean A et al (2017) Enhanced secondary- and hormone metabolism in leaves of Arbuscular Mycorrhizal Medicago truncatula. Plant Physiol 175(9):392–411. https://doi.org/10.1104/pp.16.01509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Holland JN, Cheng W, Crossley DA (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107(1):87–94. https://doi.org/10.1007/BF00582238

    Article  PubMed  Google Scholar 

  185. Schultz JC, Appel HM, Ferrieri AP, Arnold TM (2013) Flexible resource allocation during plant defense responses. Front Plant Sci 4(8):324. https://doi.org/10.3389/fpls.2013.00324

    Article  PubMed  PubMed Central  Google Scholar 

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Basso, V., Veneault-Fourrey, C. (2020). Role of Jasmonates in Beneficial Microbe–Root Interactions. In: Champion, A., Laplaze, L. (eds) Jasmonate in Plant Biology. Methods in Molecular Biology, vol 2085. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-0142-6_4

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