Pushing boundaries in above–belowground interactions

Abstract

James Hutton Institute, Dundee DD2 5DA, UKBelowground organisms, such as arbuscular mycorrhizal(AM) fungi, have long been credited with altering plant fit-ness. More recently, research on belowground organismshas revealed that AM fungi also influence a wide variety ofaboveground organisms via plants (reviewed in Van Dam H Bennett 2010). Schausberger et al. (2012) demon-strate that the presence of an AM fungus in the roots of ahost plant alters volatile emissions and host plant attractive-ness to parasitoids in the presence of herbivores. Thisextends previous studies that have focused on direct inter-actions of AM with plants (e.g. mycorrhizal fungal–plant–herbivore interactions; reviewed in Gehring & Bennett2009), but have not conclusively demonstrated how below-ground organisms, and AM fungi in particular, influencethird trophic level organisms such as parasitoids (Gange,Brown & Aplin 2003; Guerrieri et al. 2004; Hempel et al.2009; Leitner et al. 2010; Hoffmann, Vierheilig & Schaus-berger 2011a,b; Wooley & Paine 2011) via the release ofplant volatiles that attract parasitoids that attack herbivoreson host plants. Until recently, these studies failed to conclu-sively document the effects of AM fungi on both volatilerelease and attraction of parasitoids. For example, Wooley& Paine (2011) and Gange, Brown & Aplin (2003) haveshown variation in parasitoid attraction to plants hostingdifferent strains and species of Glomus as compared to non-mycorrhizal plants. Hoffmann, Vierheilig & Schausberger(2011a) also showed greater preference by parasitoids foreggs oviposited on plants associated with a single AMfungus. In addition, a single AM fungus in the roots of ahost plant has been shown to positively influence parasitoidlife-history characteristics (Hempel et al. 2009; Hoffmann,Vierheilig & Schausberger 2011b). However, none of thesestudies measured volatile profiles for host plants, so parasit-oid attraction could not be directly attributed to volatiles.A study on AM fungal influenced volatile release revealeddifferences but did not test whether changes in volatilesinfluenced parasitoids (Leitner et al. 2010). One study com-bined both parasitoid attractiveness and measurement ofvolatiles, but they primarily tested effects of attraction toplants in the absence of herbivory and never made compari-sons between mycorrhizal and non-mycorrhizal plantsexperiencing herbivory (Guerrieri et al. 2004). Unlike theseprevious experiments, Schausberger et al. measured bothchanges in volatile chemistry as well as parasitoid attractionin a fully factorial design.The results presented by Shausberger et al. open up multi-plefutureopportunitiesinabove–belowgroundresearch.Thefirst of these opportunities involves identifying the mecha-nisms by which AM fungi alter parasitoid attraction. Forexample,whatarethe biochemicalortranscriptionalchangesthat occur following AM fungal colonization that result inaltered volatile profiles? Are the mechanisms suggested forAM fungal alteration of direct chemical defences the samemechanisms that alter volatile profiles? Colonization by AMfungi has been shown to turn on the salicylic acid pathwaytemporarily,aprocessthatmayprimethejasmonicacidpath-way for herbivore attack (reviewed in Pozo & Azcon-Aguilar2007).Theinductionofvolatilesislinkedtothejasmonicacidpathway (reviewed in Heil 2008), and therefore, plants maybeprimedforafasterorgreaterreleaseofvolatileswhencolo-nizedbyAMfungi.However, there may be other mechanisms by which AMfungi influence volatile release. For example, given that AMfungi increase plant biomass and fitness in the PhaseolusvulgarissystemstudiedbyShausbergeret al.(aswellasmanyothersystems),itcouldsimplybethattheincreasedresourcesprovided by the mutualism allow plants to allocate moreresourcestoplantdefensivecharacteristics(e.g.directconstit-utiveandinduceddefencesaswellasindirectdefencesviavol-atile attraction; Bennett, Alers-Garcia & Bever 2006) or thatchanges in plant size or structure in association with AMfungi benefit or hinder parasitoid searching capabilities(Gange,Brown&Aplin2003).What characteristics of the volatile blends produced in thepresence of AM fungi are attractive for parasitoids? Shaus-bergeret al.showedtherewerefewerchemicalspresentinthevolatileblendsofAMfungalplantsbeforeherbivory(relativeto plants not hosting AM fungi), but this difference disap-peared after herbivory. However, different volatile chemicalswere released from plants experiencing herbivory and colo-nizedornotbyAMfungi(seealsoLeitneret al.2010).Shaus-berger et al. did not address whether increased attraction toplants hosting AM fungi is associated with a particular vola-