Introduction
Arbuscular mycorrhizal fungi (AMF), shape ecosystem community assembly and function by altering plant survival and growth as well as their resistance to antagonists, Arbuscular mycorrhizae are fungal endosymbionts that provide plants with micro and macro nutrients and water in exchange for photosynthate. This can increase plant nutritional quality, growth, and fitness, as well as alter investment in plant defense, thus altering the outcome of their host plant’s competitive interactions (Allen and Allen 1984; Crowell et al. 1988; Shi et al. 2016) and their ability to defend themselves against herbivores (Mohr et al. 1998; Vannette and Hunter 2009; Gan et al. 2017).
Arbuscular mycorrhizal fungi have a wide range of effects on the defensive abilities of their plant partners. There is ample evidence in a wide range of systems of both arbuscular mycorrhizae-conferred resistance with mycorrhizae changing traits that affect herbivore performance or preference (Gange and Nice 1997; Gange 2001; Wooley and Paine 2007), and mycorrhizae-conferred susceptibility to herbivores and diseases (Gange et al. 1999, 2005; Babikova et al. 2013). Mycorrhizae can affect not only the constitutive defenses, those that exist regardless of herbivory (Hause et al. 2002; Bennett et al. 2009; Fontana et al. 2009) but also the induced defenses, the production of defensive compounds in response to herbivory (Mohr et al. 1998; Riedel, Groten, and Baldwin 2008). The two main mechanisms by which AMF affect plant resistance to herbivores are by 1) altering expression of hormonally regulated secondary metabolites, and 2) altering plant nutritional composition. Mycorrhizae change their host plant’s levels of resistance related hormones (Hause et al. 2002, 2007; Khaosaad et al. 2007) as well as defensive compounds such as β -1,3-glucanase and phenylalanine (Mohr et al. 1998), aucubin and catalpol (Bennett et al. 2009), and polyphenol oxidase (Minton et al. 2016). Mycorrhizae can alter plant nutritional quality(Gange and Nice 1997) and palatability to herbivores (Gange and West 1994a). While plants can reduce nutrient levels in specific tissue in response to an herbivore (Newingham et al. 2007; Gómez et al. 2010), it is not known whether this response is affected by mycorrhizae.
The few studies that have tested how arbuscular mycorrhizae-induced changes in both nutrients and chemical resistance traits find conflicting results. For example, Wurst et al. (2004) found that arbuscular mycorrhizae in plantago increased phosphorus and carbon in leaves as well as nitrogen in the roots but did not affect resistance compounds. This increase in foliar phosphorus caused accelerated development in Myzus persicae aphids. Gange and West (1994a) also found that arbuscular mycorrhizal fungi increased leaf C/N ratios and carbon and nitrogen based chemical defenses in their plant hosts, and subsequently reduced herbivory by the chewing lepidopteran Arctia caja . As most herbivores are nitrogen limited, a plant’s total nitrogen and C/N ratio can be an important determinants of herbivore preference and performance.
However, the fact that most plants grow in competitive environments further complicates the relationships between plants and herbivores and plants and mycorrhizae. The effects of competition on defense are traditionally viewed as a corollary of the growth defense trade-off hypothesis (Stamp 2003). Limited resources can either be allocated to growth or defense depending on the perceived levels of competition and herbivory. For instance, the ratio of red to far red light, a cue that a plant is being overshadowed by a competitor, leads to decreased sensitivity to jasmonate and thus a reduction of induced defenses and increased levels of herbivory (Moreno et al. 2009). Using predictions from the growth defense trade-off, one might assume that arbuscular mycorrhizae which bring nutrients to their hosts could create a ‘high nutrient environment’ and thus lead to lower defense levels. However, this is complicated by the fact that mycorrhizae are highly generalist, with single individuals often forming associations with multiple plant individuals and species in a common mycorrhizae network (CMN) (Smith and Read 2008). This often creates a complex and asymmetrical trading network with mycorrhizae distributing resources unequally among its connected hosts and can shift the outcome of plant-plant competitive interactions. Mycorrhizae also shifts the outcome of interspecific competition and thus community assembly (Watkinson and Freckleton 1997 and citations there in; Marler et al. 1999a; Danieli-Silva et al. 2010; Daisog et al. 2012), with mycorrhizal plants gaining a large competitive advantage over less mycorrhizal species (Hartnett et al. 1993). However, mycorrhizae have also been shown to reduce competition and competitive dominance to increase evenness and diversity (Wagg et al. 2011; Stanescu and Maherali 2017). In intraspecific competitive environments, mycorrhizae can preferentially allocate resources to the larger or older plants, (Moora and Zobel 1996, 1998; Weremijewicz and Janos 2013; Weremijewicz et al. 2016).
Previous work has highlighted the conditional nature of the interactions between plants and mycorrhizae. Competition is likely to alter the outcome of plant-mycorrhizae interactions by increasing stress. While competition is nearly ubiquitous in natural and agricultural systems, its role in mycorrhizae conferred resistance to herbivores has not yet been investigated. To address this gap, we employed tomato as a model plant system to investigate: 1) Do mycorrhizae confer resistance to herbivores in competitive environments? and 2) Are the effects of mycorrhizae and competition on plant resistance to herbivores due to constitutive or induced changes in nutritional quality or defensive secondary metabolites?