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?