Skip to main content

Advertisement

SpringerLink
Log in

Mycorrhiza-Induced Resistance and Priming of Plant Defenses

  • Review Article
  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Symbioses between plants and beneficial soil microorganisms like arbuscular-mycorrhizal fungi (AMF) are known to promote plant growth and help plants to cope with biotic and abiotic stresses. Profound physiological changes take place in the host plant upon root colonization by AMF affecting the interactions with a wide range of organisms below- and above-ground. Protective effects of the symbiosis against pathogens, pests, and parasitic plants have been described for many plant species, including agriculturally important crop varieties. Besides mechanisms such as improved plant nutrition and competition, experimental evidence supports a major role of plant defenses in the observed protection. During mycorrhiza establishment, modulation of plant defense responses occurs thus achieving a functional symbiosis. As a consequence of this modulation, a mild, but effective activation of the plant immune responses seems to occur, not only locally but also systemically. This activation leads to a primed state of the plant that allows a more efficient activation of defense mechanisms in response to attack by potential enemies. Here, we give an overview of the impact on interactions between mycorrhizal plants and pathogens, herbivores, and parasitic plants, and we summarize the current knowledge of the underlying mechanisms. We focus on the priming of jasmonate-regulated plant defense mechanisms that play a central role in the induction of resistance by arbuscular mycorrhizas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akiyama, K., Matsuoka, H., and Hayashi, H. 2002. Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol. Plant-Microbe Interact. 15:334–340.

    Article  PubMed  CAS  Google Scholar 

  • Akiyama, K., Matsuzaki, K.-I., and Hayashi, H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827.

    Article  PubMed  CAS  Google Scholar 

  • Aloui, A., Recorbet, G., Robert, F., Schoefs, B., Bertrand, M., Henry, C., Gianinazzi-Pearson, V., Dumas-Gaudot, E., and Aschi-Smiti, S. 2011. Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biology 11:75.

    Article  PubMed  CAS  Google Scholar 

  • Artursson, V., Finlay, R. D., and Jansson, J. K. 2006. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 8:1–10.

    Article  PubMed  CAS  Google Scholar 

  • Ausubel, F. M. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6:973–979.

    Article  PubMed  CAS  Google Scholar 

  • Azaizeh, H. A., Marschner, H., Römheld, V., and Wittenmayer, L. 1995. Effects of a vesicular-arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil-grown maize plants. Mycorrhiza 5:321–327.

    Article  Google Scholar 

  • Azcón-Aguilar, C. and Barea, J. M. 1997. Arbuscular mycorrhizas and biological control of soil-borne plant pathogens - An overview of the mechanisms involved. Mycorrhiza 6:457–464.

    Article  Google Scholar 

  • Badri, D. V. and Vivanco, J. M. 2009. Regulation and function of root exudates. Plant Cell Environ. 32:666–681.

    Article  PubMed  CAS  Google Scholar 

  • Bansal, M. and Mukerji, K. G. 1994. Positive correlation between VAM-induced changes in root exudation and mycorrhizosphere mycoflora. Mycorrhiza 5:39–44.

    Article  Google Scholar 

  • Barea, J.-M., Pozo, M. J., Azcon, R., and Azcon-Aguilar, C. 2005. Microbial co-operation in the rhizosphere. J. Exp. Bot. 56:1761–1778.

    Article  PubMed  CAS  Google Scholar 

  • Batlle, A., Laviña, A., Sabaté, J., Camprubí, A., Estaún, V., and Calvet, C. 2011. Tolerance increase to Candidatus phytoplasma prunorum in mycorrhizal plums fruit trees. Bull. Insectology 64:125–126.

    Google Scholar 

  • Beckers, G. J. and Conrath, U. 2007. Priming for stress resistance: from the lab to the field. Curr. Opin. Plant Biol. 10:425–431.

    Article  PubMed  Google Scholar 

  • BECKERS, G. J. M., JASKIEWICZ, M., LIU, Y., UNDERWOOD, W. R., HE, S. Y., ZHANG, S., and CONRATH, U. 2009. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:425–431

  • Belimov, A. A., Serebrennikova, N. V., and Stepanok, V. V. 1999. Interaction of associative bacteria and an endomycorrhizal fungus with barley upon dual inoculation. Microbiology 68:104–108.

    CAS  Google Scholar 

  • Benhamou, N., Fortin, J. A., Hamel, C., St Arnaud, M., and Shatilla, A. 1994. Resistance responses of mycorrhizal Ri T-DNA-transformed carrot roots to infection by Fusarium oxysporum f. sp. chrysanthemi. Phytopathology 84:958–968.

    Article  CAS  Google Scholar 

  • Bennett, A. E. and Bever, J. D. 2007. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88:210–218.

    Article  PubMed  Google Scholar 

  • Berta, G., Fusconi, A., and Hooker, J. E. 2002. Arbuscular mycorrhizal modifications to plant root systems: scale, mechanisms and consequences, pp. 71–85, in S. Gianinazzi, H. Schüepp, J. M. Barea, and K. Haselwandter (eds.), Mycorrhizal Technology in Agriculture. From Genes to Bioproducts. Birkhaeuser, Basel.

    Chapter  Google Scholar 

  • Blilou, I., Ocampo, J. A., and García-Garrido, J. M. 1999. Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. J. Exp. Bot. 50:1663–1668.

    CAS  Google Scholar 

  • Boller, T. and He, S. Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744.

    Article  PubMed  CAS  Google Scholar 

  • Bouwmeester, H. J., Matusova, R., Zhongkui, S., and Beale, M. H. 2003. Secondary metabolite signaling in host–parasitic plant interactions. Curr. Opin. Plant Biol. 6:358–364.

    Article  PubMed  CAS  Google Scholar 

  • Bouwmeester, H. J., Roux, C., Lopez-Raez, J. A., and Bécard, G. 2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci. 12:224–230.

    Article  PubMed  CAS  Google Scholar 

  • Breuillin, F., Schramm, J., Hajirezaei, M., Ahkami, A., Favre, P., Druege, U., Hause, B., Bucher, M., Kretzschmar, T., Bossolini, E., Kuhlemeier, C., Martinoia, E., Franken, P., Scholz, U., and Reinhardt, D. 2010. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J. 64:1002–1017.

    Article  PubMed  CAS  Google Scholar 

  • Campos-Soriano, L., García-Garrido, J. M., and Segundo, B. S. 2010. Activation of basal defense mechanisms of rice plants by Glomus intraradices does not affect the arbuscular mycorrhizal symbiosis. New Phytol. 188:597–614.

    Article  PubMed  CAS  Google Scholar 

  • Campos-Soriano, L., García-Martínez, J., and Segundo, B. S. 2012. The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defense-related genes in rice leaves and confers resistance to pathogen infection. Mol. Plant Pathol. doi:. doi:10.1111/j.1364-3703.2011.00773.x.

  • CIPOLLINI, D., RIGSBY, C. M., and BARTO, E. K. 2012. Microbes as targets and mediators of allelopathy in plants. J. Chem. Ecol., this issue.

  • Conrath, U., Beckers, G. J. M., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., Newman, M. A., Pieterse, C. M. J., Poinssot, B., Pozo, M. J., Pugin, A., Schaffrath, U., Ton, J., Wendehenne, D., Zimmerli, L., and Mauch-Mani, B. 2006. Priming: Getting ready for battle. Mol. Plant-Microbe Interact. 19:1062–1071.

    Article  PubMed  CAS  Google Scholar 

  • Cordier, C., Pozo, M. J., Barea, J. M., Gianinazzi, S., and 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. 11:1017–1028.

    Article  CAS  Google Scholar 

  • Currie, A. F., Murray, P. J., and Gange, A. C. 2011. Is a specialist root-feeding insect affected by arbuscular mycorrhizal fungi? Appl. Soil Ecol. 47:77–83.

    Article  Google Scholar 

  • Chandanie, W., Kubota, M., and Hyakumachi, M. 2006. Interactions between plant growth promoting fungi and arbuscular mycorrhizal fungus Glomus mosseae and induction of systemic resistance to anthracnose disease in cucumber. Plant Soil 286:209–217.

    Article  CAS  Google Scholar 

  • Chandanie, W. A., Kubota, M., and Hyakumachi, M. 2005. Interaction between arbuscular mycorrhizal fungus Glomus mosseae and plant growth promoting fungus Phoma sp.on their root colonization and growth promotion of cucumber (Cucumis sativus L.). Mycoscience 46:201–204.

    Article  Google Scholar 

  • Chandanie, W. A., Kubota, M., and Hyakumachi, M. 2009. Interactions between the arbuscular mycorrhizal fungus Glomus mosseae and plant growth-promoting fungi and their significance for enhancing plant growth and suppressing damping-off of cucumber (Cucumis sativus L.). Appl. Soil Ecol 41:336–341.

    Article  Google Scholar 

  • D’AMELIO, R., BERTA, G., GAMALERO, E., MASSA, N., AVIDANO, L., CANTAMESSA, S., D’AGOSTINO, G., BOSCO, D., and MARZACHÌ, C. 2011. Increased plant tolerance against chrysanthemum yellows phytoplasma (Candidatus Phytoplasma asteris) following double inoculation with Glomus mosseae BEG12 and Pseudomonas putida S1Pf1Rif. Plant Pathol 60:1014–1022.

    Article  Google Scholar 

  • de la Noval, B., Pérez, E., Martínez, B., León, O., Martínez-Gallardo, N., and 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 17:449–460.

    Article  PubMed  CAS  Google Scholar 

  • de la Peña, E., Echeverría, S. R., van der Putten, W. H., Freitas, H., and Moens, M. 2006. Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol. 169:829–840.

    Article  PubMed  Google Scholar 

  • de Román, M., Fernández, I., Wyatt, T., Sahrawy, M., Heil, M., and Pozo, M. J. 2011. Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J. Ecol. 99:36–45.

    Article  CAS  Google Scholar 

  • Dicke, M., van Loon, J. J. A., and Soler, R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324.

    Article  PubMed  CAS  Google Scholar 

  • Dumas-Gaudot, E., Gollotte, A., Cordier, C., Gianinazzi, S., and Gianinazzi-Pearson, V. 2000. Modulation of host defence systems, pp. 173–200 in Y. Kapulnick, and D. D. Douds Jr (eds.), Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic Press, Dordrecht.

  • Dumas-Gaudot, E., Slezack, S., Dassi, B., Pozo, M., Gianinazzi-Pearson, V., and Gianinazzi, S. 1996. Plant hydrolytic enzymes (chitinases and β-1,3-glucanases) in root reactions to pathogenic and symbiotic microorganisms. Plant Soil 185:211–221.

    Article  CAS  Google Scholar 

  • EFFMERT U., KALDERAS J., WARNKE R., and PIECHULLA B. 2012. Volatile mediated interactions between bacteria and fungi in the soil. J. Chem. Ecol., this issue.

  • Elsen, A., Gervacio, D., Swennen, R., and de Waele, D. 2008. AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256.

    Article  PubMed  CAS  Google Scholar 

  • Ferrari, A. E. and Wall, L. G. 2008. Coinoculation of black locust with Rhizobium and Glomus on a desurfaced soil. Soil Sci. 173:195–202.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Fester, T. and Hause, G. 2005. Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15:373–379.

    Article  PubMed  CAS  Google Scholar 

  • Fester, T. and Sawers, R. 2011. Progress and challenges in agricultural applications of arbuscular mycorrhizal fungi. Crit. Rev. Plant Sci. 30:459–470.

    Article  Google Scholar 

  • Fiorilli, V., Catoni, M., Miozzi, L., Novero, M., Accotto, G. P., and Lanfranco, L. 2009. Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol. 184:975–987.

    Article  PubMed  CAS  Google Scholar 

  • FLOβ, D. S., HAUSE, B., LANGE, P. R., KÜSTER, H., STRACK, D., and WALTER, M. H. 2008. Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 56:86–100.

    Article  CAS  Google Scholar 

  • Fontana, A., Reichelt, M., Hempel, S., Gershenzon, J., and Unsicker, S. 2009. The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J. Chem. Ecol. 35:833–843.

    Article  PubMed  CAS  Google Scholar 

  • Fritz, M., Jakobsen, I., Lyngkjær, M. F., Thordal-Christensen, H., and Pons-Kühnemann, J. 2006. Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419.

    Article  PubMed  Google Scholar 

  • Gange, A. C. 1996. Reduction in vine weevil larval growth by mycorrhizal fungi. Mitt. Biol. Bund. Forst. 316:56–60.

    Google Scholar 

  • Gange, A. C. 2001. Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol. 150:611–618.

    Article  Google Scholar 

  • Gange, A. C. 2007. Insect–mycorrhizal interactions: patterns, processes, and consequences, pp. 124–144, in T. Ohgushi, T. P. Craig, and P. W. Price (eds.), Ecological Communities: Plant Mediation in Indirect Interaction Webs. Cambridge University Press, New York.

    Chapter  Google Scholar 

  • Gange, A. C., Bower, E., and Brown, V. K. 1999. Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120:123–131.

    Article  Google Scholar 

  • Gange, A. C. and Smith, A. K. 2005. Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecol. Entomol. 30:600–606.

    Article  Google Scholar 

  • Gange, A. C. and West, H. M. 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol. 128:79–87.

    Article  Google Scholar 

  • García-Garrido, J. M. and Ocampo, J. A. 2002. Regulation of the plant defense response in arbuscular mycorrhizal symbiosis. J. Exp. Bot. 53:1377–1386.

    Article  PubMed  Google Scholar 

  • Garmendia, I., Goicoechea, N., and Aguirreolea, J. 2004. Effectiveness of three Glomus species in protecting pepper (Capsicum annuum L.) against verticillium wilt. Biol. Contr. 31:296–305.

    Article  Google Scholar 

  • Gehring, C. and Bennett, A. 2009. Mycorrhizal fungal-plant-insect interactions: The importance of a community approach. Environ. Entomol. 38:93–102.

    Article  PubMed  Google Scholar 

  • Gernns, H., von Alten, H., and Poehling, H. M. 2001. Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen - Is a compensation possible? Mycorrhiza 11:237–243.

    Article  CAS  Google Scholar 

  • Goellner, K. and Conrath, U. 2008. Priming: It's all the world to induced disease resistance. Eur. J. Plant Pathol. 121:233–242.

    Article  Google Scholar 

  • Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–227.

    Google Scholar 

  • Goverde, M., van der Heijden, M. V. D. H., Wiemken, A., Sanders, I. S., and Erhardt, A. 2000. Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia 125:362–369.

    Article  Google Scholar 

  • Guerrieri, E., Lingua, G., Digilio, M. C., Massa, N., and Berta, G. 2004. Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol. Entomol. 29:753–756.

    Article  Google Scholar 

  • Güimil, S., Chang, H.-S., Zhu, T., Sesma, A., Osbourn, A., Roux, C., Ioannidis, V., Oakeley, E. J., Docquier, M., Descombes, P., Briggs, S. P., and Paszkowski, U. 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Nat. Acad. Sci. USA 102:8066–8070.

    Article  PubMed  CAS  Google Scholar 

  • Haggag, W. M. and Abd-El Latif, F. M. 2001. Interaction between vesicular arbuscular mycorrhizae and antagonistic biocontrol microorganisms on controlling root rot disease incidence of geranium plants. OnLine J. Biol. Sci. 1:1147–1153.

    Google Scholar 

  • Hao, Z., Fayolle, L., van Tuinen, D., Chatagnier, O., Li, X., Gianinazzi, S., and Gianinazzi-Pearson, V. 2012. Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defense gene responses in grapevine. J. Exp. Bot. doi:. doi:10.1093/jxb/ers046.

  • Harrier, L. A. and Watson, C. A. 2004. The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manag. Sci. 60:149–157.

    Article  PubMed  CAS  Google Scholar 

  • Harrison, M. J. 1999. Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:361–389.

    Article  PubMed  CAS  Google Scholar 

  • Hartley, S. E. and Gange, A. C. 2009. Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Annu. Rev. Entomol. 54:323–342.

    Article  PubMed  CAS  Google Scholar 

  • Hause, B. and Fester, T. 2005. Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221:184–196.

    Article  PubMed  CAS  Google Scholar 

  • Hause, B., Maier, W., Miersch, O., Kramell, R., and Strack, D. 2002. Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol. 130:1213–1220.

    Article  PubMed  CAS  Google Scholar 

  • Hause, B., Mrosk, C., Isayenkov, S., and Strack, D. 2007. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110.

    Article  PubMed  CAS  Google Scholar 

  • Hause, B. and Schaarschmidt, S. 2009. The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599.

    Article  PubMed  CAS  Google Scholar 

  • Heil, M. and Ton, J. 2008. Long-distance signaling in plant defense. Trends Plant Sci. 13:264–272.

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Medina, M. J., Gagnon, H., Piche, Y., Ocampo, J. A., García-Garrido, J. M., and Vierheilig, H. 2003. Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci. 164:993–998.

    Article  CAS  Google Scholar 

  • Hoffmann, D., Vierheilig, H., Peneder, S., and Schausberger, P. 2011. Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant. Ecol. Entomol. 36:574–581.

    Article  Google Scholar 

  • Howe, G. A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66.

    Google Scholar 

  • Jaiti, F., Meddich, A., and EL HADRAMI, I. 2007. Effectiveness of arbuscular mycorrhizal fungi in the protection of date palm (Phoenix dactylifera L.) against bayoud disease. Physiol. Mol Plant Pathol 71:166–173.

    Article  CAS  Google Scholar 

  • Jia, Y., Gray, V. M., and Straker, C. J. 2004. The influence of rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann. Bot. 94:251–258.

    Article  PubMed  CAS  Google Scholar 

  • Jones, J. D. G. and Dangl, J. L. 2006. The plant immune system. Nature 444:323–329.

    Article  PubMed  CAS  Google Scholar 

  • Kamińska, M., Klamkowski, K., Berniak, H., and Sowik, I. 2010a. Response of mycorrhizal periwinkle plants to aster yellows phytoplasma infection. Mycorrhiza 20:161–166.

    Article  PubMed  Google Scholar 

  • Kamińska, M., Klamkowski, K., Berniak, H., and Treder, W. 2010b. Effect of arbuscular mycorrhizal fungi inoculation on aster yellows phytoplasma-infected tobacco plants. Sci. Hortic. 125:500–503.

    Article  Google Scholar 

  • Kaschuk, G., Kuyper, T. W., Leffelaar, P. A., Hungria, M., and Giller, K. E. 2009. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem. 41:1233–1244.

    Article  CAS  Google Scholar 

  • Kessler, A., Halitschke, R., Diezel, C., and Baldwin, I. 2006. Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292.

    Article  PubMed  Google Scholar 

  • Khaosaad, T., García-Garrido, J. M., Steinkellner, S., and Vierheilig, H. 2007. Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol. Biochem. 39:727–734.

    Article  CAS  Google Scholar 

  • Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., Fellbaum, C. R., Kowalchuk, G. A., Hart, M. M., Bago, A., Palmer, T. M., West, S. A., Vandenkoornhuyse, P., Jansa, J., and Bücking, H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882.

    Article  PubMed  CAS  Google Scholar 

  • Kloppholz, S., Kuhn, H., and Requena, N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21:1204–1209.

    Article  PubMed  CAS  Google Scholar 

  • Kobra, N., Jalil, K., and Youbert, G. 2009. Effects of three Glomus species as biocontrol agents against verticillium-induced wilt in cotton. J. Plant Protect. Res. 49:4.

    Google Scholar 

  • Kohler, J., Caravaca, F., Carrasco, L., and Roldán, A. 2007. Interactions between a plant growth-promoting rhizobacterium, an AM fungus and a phosphate-solubilising fungus in the rhizosphere of Lactuca sativa. Appl. Soil Ecol. 35:480–487.

    Article  Google Scholar 

  • Koricheva, J., Gange, A. C., and Jones, T. 2009. Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097.

    Article  PubMed  Google Scholar 

  • Kravchuk, Z., Vicedo, B., Flors, V., Camañes, G., González-Bosch, C., and García-Agustín, P. 2011. Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea. Plant Physiol 168:359–366.

    Article  CAS  Google Scholar 

  • Kula, A. A. R., Hartnett, D. C., and Wilson, G. W. T. 2005. Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions. Ecol. Lett. 8:61–69.

    Article  Google Scholar 

  • Larimer, A., Bever, J., and Clay, K. 2010. The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148.

    Article  Google Scholar 

  • Lee, C. S., Lee, Y. J., and Jeun, Y. C. 2005. Observations of infection structures on the leaves of cucumber plants pre-treated with arbuscular mycorrhiza Glomus intraradices after challenge inoculation with Colletotrichum orbiculare. Plant Pathol. J. 21:237–243.

    Article  Google Scholar 

  • Leitner, M., Kaiser, R., Hause, B., Boland, W., and Mithöfer, A. 2010. Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101.

    Article  PubMed  Google Scholar 

  • Lendzemo, V. W., Kuyper, T. W., Matusova, R., Bouwmeester, H. J., and Ast, A. V. 2007. Colonization by arbuscular mycorrhizal fungi of Sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Sign. Behav. 2:58–62.

    Article  Google Scholar 

  • Li, H.-Y., Yang, G.-D., Shu, H.-R., Yang, Y.-T., Ye, B.-X., Nishida, I., and Zheng, C.-C. 2006. Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol 47:154–163.

    Article  PubMed  CAS  Google Scholar 

  • Linderman, R. G. 1994. Role of VAM fungi in biocontrol, pp. 1–26, in F. L. Pfleger and R. G. Linderman (eds.), Mycorrhizae and Plant Health. APS Press, St. Paul, MN.

    Google Scholar 

  • Lioussanne, L., Jolicoeur, M., and St-Arnaud, M. 2008. Mycorrhizal colonization with Glomus intraradices and development stage of transformed tomato roots significantly modify the chemotactic response of zoospores of the pathogen Phytophthora nicotianae. Soil Biol. Biochem. 40:2217–2224.

    Article  CAS  Google Scholar 

  • Liu, J., Blaylock, L. A., Endre, G., Cho, J., Town, C. D., Vandenbosch, K. A., and Harrison, M. J. 2003. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123.

    Article  PubMed  CAS  Google Scholar 

  • Liu, J., Maldonado-Mendoza, I., Lopez-Meyer, M., Cheung, F., Town, C. D., and Harrison, M. J. 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. 50:529–544.

    Article  PubMed  CAS  Google Scholar 

  • López-Ráez, J. A., Flors, V., García, J. M., and Pozo, M. J. 2010a. AM symbiosis alters phenolic acid content in tomato roots. Plant Sign Behav. 5:1138–1140.

    Article  CAS  Google Scholar 

  • López-Ráez, J. A., Verhage, A., Fernández, I., García, J. M., Azcón-Aguilar, C., Flors, V., and Pozo, M. J. 2010b. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J. Exp. Bot. 61:2589–2601.

    Article  PubMed  CAS  Google Scholar 

  • López-Ráez, J. A., Charnikhova, T., Fernández, I., Bouwmeester, H., and Pozo, M. J. 2011a. Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J. Plant Physiol. 168:294–297.

    Article  PubMed  CAS  Google Scholar 

  • López-Ráez, J. A., Pozo, M. J., and García-Garrido, J. M. 2011b. Strigolactones: a cry for help in the rhizosphere. Botany 89:513–522.

    Article  Google Scholar 

  • Ludwig-Müller, J. 2010. Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi, pp. 169–190, in H. Koltai and Y. Kapulnik (eds.), Arbuscular Mycorrhizas: Physiology and Function. Springer Netherlands, Dordrecht.

    Chapter  Google Scholar 

  • Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V., and Ton, J. 2012. Next-generation systemic acquired resistance. Plant Physiol. 158:844–853.

    Article  PubMed  CAS  Google Scholar 

  • Marschner, P., Crowley, D. E., and Higashi, R. M. 1997. Root exudation and physiological status of a root-colonizing fluorescent pseudomonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L.). Plant Soil 189:11–20.

    Article  CAS  Google Scholar 

  • Martínez-Medina, A., Pascual, J. A., Lloret, E., and Roldán, A. 2009. Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum and their effects on Fusarium wilt in melon plants grown in seedling nurseries. J. Sci. Food Agric. 89:1843–1850.

    Article  CAS  Google Scholar 

  • Martínez-Medina, A., Pascual, J. A., Pérez-Alfocea, F., Albacete, A., and Roldán, A. 2010. Trichoderma harzianum and Glomus intraradices modify the hormone disruption induced by Fusarium oxysporum infection in melon plants. Phytopathology 100:682–688.

    Article  PubMed  CAS  Google Scholar 

  • Meyer, J. R. and Linderman, R. G. 1986. Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungi and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol. Biochem. 18:185–190.

    Article  CAS  Google Scholar 

  • Miransari, M. 2010. Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol. 12:563–569.

    PubMed  CAS  Google Scholar 

  • Møller, K., Kristensen, K., Yohalem, D., and Larsen, J. 2009. Biological management of gray mold in pot roses by co-inoculation of the biocontrol agent Ulocladium atrum and the mycorrhizal fungus Glomus mosseae. Biol. Control 49:120–125.

    Article  Google Scholar 

  • Mukerji, K. and Ciancio, A. 2007. Mycorrhizae in the integrated pest and disease management, pp. 245–266, in A. Ciancio and K. G. Mukerji (eds.), General Concepts in Integrated Pest and Disease Management. Springer Netherlands, Dordrecht.

    Chapter  Google Scholar 

  • Newsham, K. K., Fitter, A. H., and Watkinson, A. R. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol. 10:407–411.

    Article  PubMed  CAS  Google Scholar 

  • Niranjan, R., Mohan, V., and Rao, V. M. 2007. Effect of indole acetic acid on the synergistic interactions of Bradyrhizobium and Glomus fasciculatum on growth, nodulation, and nitrogen fixation of Dalbergia sissoo Roxb. Arid Land Res. Manag. 21:329–342.

    Article  CAS  Google Scholar 

  • Norman, J. R. and Hooker, J. E. 2000. Sporulation of Phytophthora fragariae shows greater stimulation by exudates of non-mycorrhizal than by mycorrhizal strawberry roots. Mycol. Res. 104:1069–1073.

    Article  Google Scholar 

  • PASTOR, V., LUNA, E., MAUCH-MANI, B., TON, J., and FLORS, V. 2012. Primed plants do not forget. Environ. Exp. Bot., doi.: 10.1016/j.envexpbot.2012.02.013

  • Paszkowski, U. 2006. Mutualism and parasitism: the yin and yang of plant symbioses. Curr. Op. Plant Biol. 9:364–370.

    Article  Google Scholar 

  • PÉRET, B., SVISTOONOFF, S., and LAPLAZE, L. 2009. When plants socialize: Symbioses and root development. Annu. Plant Rev. 209–238

  • Pieterse, C. M. J., Koornneef, A., Leonreyes, H. A., Ritsema, T., Verhage, A., Joosten, R. G., Vos, M. D., Oosten, V. R. V., and Dicke, M. 2008. Cross-talk between signaling pathways leading to defense against pathogens and insects, pp. 1–9, in M. Lorito, S. L. Woo, and F. Scala (eds.), Biology of Plant-microbe Interactions. International Society for Molecular Plant-Microbe Interactions, St. Paul, MN.

    Google Scholar 

  • Pieterse, C. M. J., Leon-Reyes, A., van der Ent, S., and van Wees, S. C. M. 2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308–316.

    Article  PubMed  CAS  Google Scholar 

  • Pieterse, C. M. J., van Wees, S. C. M., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., and van Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580.

    PubMed  CAS  Google Scholar 

  • Pineda, A., Zheng, S.-J., van Loon, J. J. A., Pieterse, C. M. J., and Dicke, M. 2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15:507–514.

    Article  PubMed  CAS  Google Scholar 

  • Pinochet, J., Calvet, C., Camprubí, A., and Fernández, C. 1996. Interactions between migratory endoparasitic nematodes and arbuscular mycorrhizal fungi in perennial crops: A review. Plant Soil 185:183–190.

    Article  CAS  Google Scholar 

  • Pivato, B., Gamalero, E., Lemanceau, P., and Berta, G. 2008. Colonization of adventitious roots of Medicago truncatula by Pseudomonas fluorescens C7R12 as affected by arbuscular mycorrhiza. FEMS Microbiol. Lett. 289:173–180.

    Article  PubMed  CAS  Google Scholar 

  • Pozo, M. J. and Azcón-Aguilar, C. 2007. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10:393–398.

    Article  PubMed  CAS  Google Scholar 

  • Pozo, M. J., Azcón-Aguilar, C., Dumas-Gaudot, E., and Barea, J. M. 1998. Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophthora parasitica. J. Exp. Bot. 49:1729–1739.

    CAS  Google Scholar 

  • Pozo, M. J., Azcón-Aguilar, C., Dumas-Gaudot, E., and Barea, J. M. 1999. β-1,3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci. 141:149–157.

    Article  CAS  Google Scholar 

  • Pozo, M. J., Cordier, C., Dumas-Gaudot, E., Gianinazzi, S., Barea, J. M., and Azcón-Aguilar, C. 2002. Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J. Exp. Bot. 53:525–534.

    Article  PubMed  CAS  Google Scholar 

  • Pozo, M. J., Jung, S. C., López-Ráez, J. A., and Azcón-Aguilar, C. 2010. Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: The role of plant defence mechanisms, pp. 193–207, in H. Koltai and Y. Kapulnik (eds.), Arbuscular Mycorrhizas: Physiology and Function. Springer Netherlands, Dordrecht.

    Chapter  Google Scholar 

  • Pozo, M. J., van der Ent, S., van Loon, L. C., and Pieterse, C. M. J. 2008. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol. 180:511–523.

    Article  PubMed  CAS  Google Scholar 

  • Pozo, M. J., van Loon, L. C., and Pieterse, C. M. J. 2004. Jasmonates - Signals in plantmicrobe interactions. J. Plant Growth Reg. 23:211–222.

    Google Scholar 

  • Pozo, M. J., Verhage, A., García-Andrade, J., García, J. M., and Azcón-Aguilar, C. 2009. Priming plant defence against pathogens by arbuscular mycorrhizal fungi, pp. 123–135, in C. Azcón-Aguilar, J. M. Barea, S. Gianinazzi, and V. Gianinazzi-Pearson (eds.), Mycorrhizas - Functional Processes and Ecological Impact. Springer, Berlin Heidelberg.

    Chapter  Google Scholar 

  • Rabin, L. B. and Pacovsky, R. S. 1985. Reduced larva growth of two Lepidoptera (Noctuidae) on excised leaves of soybean infected with a mycorrhizal fungus. J. Econ. Entomol. 78:1358–1363.

    Google Scholar 

  • Rapparini, F., Llusià, J., and Peñuelas, J. 2008. Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol. 10:108–122.

    Article  PubMed  CAS  Google Scholar 

  • Rasmann, S., de Vos, M., Casteel, C. L., Tian, D., Halitschke, R., Sun, J. Y., Agrawal, A. A., Felton, G. W., and Jander, G. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 158:854–863.

    Article  PubMed  CAS  Google Scholar 

  • Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Kloepper, J. W., and Paré, P. W. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017–1026.

    Article  PubMed  CAS  Google Scholar 

  • Saldajeno, M. G. B. and Hyakumachi, M. 2011. The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae stimulate plant growth and reduce severity of anthracnose and damping-off diseases in cucumber (Cucumis sativus) seedlings. Ann. Appl. Biol. 159:28–40.

    Article  Google Scholar 

  • Schausberger, P., Peneder, S., Jürschik, S., and Hoffmann, D. 2011. Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct. Ecol. 26:441–449.

    Google Scholar 

  • Schliemann, W., Ammer, C., and Strack, D. 2008. Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69:112–146.

    Article  PubMed  CAS  Google Scholar 

  • SCHÜßLER, A., SCHWARZOTT, D., and WALKER, C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res 105:1413–1421.

    Article  Google Scholar 

  • Shoresh, M., Yedidia, I., and Chet, I. 2005. Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84.

    Article  PubMed  CAS  Google Scholar 

  • Sikes, B. A., Cottenie, K., and Klironomos, J. N. 2009. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J. Ecol. 97:1274–1280.

    Article  Google Scholar 

  • Slezack, S., Dumas-Gaudot, E., Paynot, M., and Gianinazzi, S. 2000. Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol. Plant-Microbe Interact. 13:238–241.

    Article  PubMed  CAS  Google Scholar 

  • Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., and Mauch-Mani, B. 2012. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158:835–843.

    Article  PubMed  CAS  Google Scholar 

  • Smith, S., Facelli, E., Pope, S., and ANDREW SMITH, F. 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 

  • Smith, S. E., Jakobsen, I., Grønlund, M., and Smith, F. A. 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156:1050–1057.

    Article  PubMed  CAS  Google Scholar 

  • Smith, S. E. and Read, D. J. 2008. Mycorrhizal Symbiosis. 3rd edition. Academic Press, New York.

  • Smith, S. E. and Smith, F. A. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62:227–250.

    Article  PubMed  CAS  Google Scholar 

  • Snoeren, T., van Poecke, R., and Dicke, M. 2009. Multidisciplinary approach to unravelling the relative contribution of different oxylipins in indirect defense of Arabidopsis thaliana. J. Chem. Ecol. 35:1021–1031.

    Article  PubMed  CAS  Google Scholar 

  • Song, Y. Y., Zeng, R. S., Xu, J. F., Li, J., Shen, X., and Yihdego, W. G. 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS ONE 5: doi:10.1371/journal.pone.0013324.s0013003

  • Sood, S. G. 2003. Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol. Ecol. 45:219–227.

    Article  CAS  Google Scholar 

  • Soto, M. J., Domínguez-Ferreras, A., Pérez-Mendoza, D., Sanjuán, J., and Olivares, J. 2009. Mutualism versus pathogenesis: the give-and-take in plant–bacteria interactions. Cell. Microbiol. 11:381–388.

    Article  PubMed  CAS  Google Scholar 

  • Stein, E., Molitor, A., Kogel, K. H., and 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. 49:1747–1751.

    Article  PubMed  CAS  Google Scholar 

  • Stepanova, A. N. and Alonso, J. M. 2009. Ethylene signaling and response: where different regulatory modules meet. Curr. Opin. Plant Biol. 12:548–555.

    Article  PubMed  CAS  Google Scholar 

  • Strack, D., Fester, T., Hause, B., Schliemann, W., and Walter, M. H. 2003. Arbuscular mycorrhiza: Biological, chemical, and molecular aspects. J. Chem. Ecol. 29:1955–1979.

    Article  PubMed  CAS  Google Scholar 

  • Strack, D. and Fester, T. 2006. Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol. 172:22–34.

    Article  PubMed  CAS  Google Scholar 

  • Thomma, B. P. H. J., Nürnberger, T., and Joosten, M. H. A. J. 2011. Of PAMPs and effectors: The blurred PTI-ETI dichotomy. Plant Cell 23:4–15.

    Article  PubMed  CAS  Google Scholar 

  • Ton, J., D'Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B., and Turlings, T. C. J. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49:16–26.

    Article  PubMed  CAS  Google Scholar 

  • Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M. N., Métraux, J. P., and Mauch-Mani, B. 2005. Dissecting the ß-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987–999.

    Article  PubMed  CAS  Google Scholar 

  • Toro, M., Azcón, R., and Herrera, R. 1996. Effects on yield and nutrition of mycorrhizal and nodulated Pueraria phaseoloides exerted by P-solubilizing rhizobacteria. Biol. Fertil. Soils 21:23–29.

    Article  Google Scholar 

  • Toussaint, J. P. 2007. Investigating physiological changes in the aerial parts of AM plants: What do we know and where should we be heading? Mycorrhiza 17:349–353.

    Article  PubMed  Google Scholar 

  • van der Ent, S., van Hulten, M., Pozo, M. J., Czechowski, T., Udvardi, M. K., Pieterse, C. M. J., and Ton, J. 2009a. Priming of plant innate immunity by rhizobacteria and β-aminobutyric acid: Differences and similarities in regulation. New Phytol. 183:419–431.

    Article  PubMed  CAS  Google Scholar 

  • van der Ent, S., van Wees, S. C. M., and Pieterse, C. M. J. 2009b. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588.

    Article  PubMed  CAS  Google Scholar 

  • van Hulten, M., Pelser, M., van Loon, L. C., Pieterse, C. M. J., and Ton, J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 103:5602–5607.

    Article  PubMed  CAS  Google Scholar 

  • van Wees, S. C. M., van der Ent, S., and Pieterse, C. M. J. 2008. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11:443–448.

    Article  PubMed  CAS  Google Scholar 

  • Verhagen, B. W. M., Glazebrook, J., Zhu, T., Chang, H. S., van Loon, L. C., and Pieterse, C. M. J. 2004. The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interact. 17:895–908.

    Article  PubMed  CAS  Google Scholar 

  • Vicari, M., Hatcher, P. E., and Ayres, P. G. 2002. Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology 83:2452–2464.

    Article  Google Scholar 

  • Vicedo, B., Flors, V., De La O Leyva, M., Finiti, I., Kravchuk, Z., Real, M. D., García-Agustín, P., and González-Bosch, C. 2009. Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol. Plant-Microbe Interact. 22:1455–1465.

    Article  PubMed  CAS  Google Scholar 

  • Vierheilig, H. 2004. Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. Plant Physiol. 161:339–341.

    Article  CAS  Google Scholar 

  • Vierheilig, H. and Piché, Y. 2002. Signalling in arbuscular mycorrhiza: Facts and hypotheses, pp. 23–39, in B. Buslig and J. Manthey (eds.), Flavonoids in Cell Functions. Kluwer Academic/Plenum Publishers, New York.

    Google Scholar 

  • Vierheilig, H., Steinkellner, S., Khaosaad, T., and Garcia-Garrido, J. M. 2008. The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of the AM symbiosis: One mechanism, two effects? pp. 307–320, in A. Varma (ed.), mycorrhiza. Springer, Berlin, Heidelberg.

    Chapter  Google Scholar 

  • VOS, C., CLAERHOUT, S., MK and AWIRE, R., PANIS, B., DE WAELE, D., and ELSEN, A. 2011. Arbuscular mycorrhizal fungi reduce root-knot nematode penetration through altered root exudation of their host. Plant Soil 354:335–345.

  • Walters, D. and Heil, M. 2007. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 71:3–17.

    Article  CAS  Google Scholar 

  • Walling, L. L. 2008. Avoiding effective defenses: Strategies employed by phloem-feeding insects. Plant Physiol. 146:859–866.

    Article  PubMed  CAS  Google Scholar 

  • Whipps, J. M. 2004. Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can. J. Bot. 82:1198–1227.

    Article  Google Scholar 

  • Wolfe, B. E., Husband, B. C., and Klironomos, J. N. 2005. Effects of a belowground mutualism on an aboveground mutualism. Ecol. Lett. 8:218–223.

    Article  Google Scholar 

  • Wright, D. P., Read, D. J., and Scholes, J. D. 1998a. Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ. 21:881–891.

    Article  Google Scholar 

  • Wright, D. P., Scholes, J. D., and Read, D. J. 1998b. Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ. 21:209–216.

    Article  Google Scholar 

  • Yan, Z., Reddy, M. S., Ryu, C. M., McInroy, J. A., Wilson, M., and Kloepper, J. W. 2002. Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92:1329–1333.

    Article  PubMed  CAS  Google Scholar 

  • Yao, M. K., Désilets, H., Charles, M. T., Boulanger, R., and Tweddell, R. J. 2003. Effect of mycorrhization on the accumulation of rishitin and solavetivone in potato plantlets challenged with Rhizoctonia solani. Mycorrhiza 13:333–336.

    Article  PubMed  CAS  Google Scholar 

  • Yi, H.-S., Heil, M., Adame-Álvarez, R. M., Ballhorn, D. J., and Ryu, C.-M. 2009. Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151:2152–2161.

    Article  PubMed  CAS  Google Scholar 

  • Zamioudis, C. and Pieterse, C. M. J. 2012. Modulation of host immunity by beneficial microbes. Mol. Plant-Microbe Interact. 25:139–150.

    Article  PubMed  CAS  Google Scholar 

  • Zeng, R.-S. 2006. Disease resistance in plants through mycorrhizal fungi induced allelochemicals, pp. 181–192, in Inderjit and and K. G. Mukerji (eds.), Allelochemicals: Biological Control of Plant Pathogens and Diseases. Springer Netherlands, Dordrecht.

    Chapter  Google Scholar 

  • Zhu, H. H. and Yao, Q. 2004. Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J. Phytopathol. 152:537–542.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Our research on MIR was financed by grant AGL2006-08029 and AGL2009- 07691 from the Spanish Ministry of Science and Technology. S.C.J. is supported by the JAE program of the Spanish National Research Council (CSIC).

Author information

Authors and Affiliations

  1. Department of Soil Microbiology and Symbiotic Systems, Estación Experimental del Zaidín (EEZ), CSIC, Prof. Albareda 1, 18008, Granada, Spain

    Sabine C. Jung, Ainhoa Martinez-Medina, Juan A. Lopez-Raez & Maria J. Pozo

Authors
  1. Sabine C. Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ainhoa Martinez-Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan A. Lopez-Raez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria J. Pozo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria J. Pozo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jung, S.C., Martinez-Medina, A., Lopez-Raez, J.A. et al. Mycorrhiza-Induced Resistance and Priming of Plant Defenses. J Chem Ecol 38, 651–664 (2012). https://doi.org/10.1007/s10886-012-0134-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0134-6

Keywords

Search

Navigation