Abstract
Symbiotic rhizobia induce many changes in legumes that could affect aboveground interactions with herbivores. We explored how changing the intensity of Bradyrhizobium japonicum, as modulated by soil nitrogen (N) levels, influenced the interaction between soybean (Glycine max) and herbivores of different feeding guilds. When we employed a range of fertilizer applications to manipulate soil N, plants primarily dependent on rhizobia for N exhibited increased root nodulation and higher levels of foliar ureides than plants given N fertilizer; yet all treatments maintained similar total N levels. Soybean podworm (Helicoverpa zea) larvae grew best on plants with the highest levels of rhizobia but, somewhat surprisingly, preferred to feed on high-N-fertilized plants when given a choice. Induction of the defense signaling compound jasmonic acid (JA) by H. zea feeding damage was highest in plants primarily dependent on rhizobia. Differences in rhizobial dependency on soybean did not appear to affect interactions with the phloem-feeding soybean aphid (Aphis glycines). Overall, our results suggest that rhizobia association can affect plant nutritional quality and the induction of defense signaling pathways and that these effects may influence herbivore feeding preferences and performance—though such effects may vary considerably for different classes of herbivores.
Highlights
Soil-dwelling microbial plant symbionts such as mycorrhizal fungi and nitrogen-fixing bacteria can have profound impacts on plant ecology via influences on soil fertility, plant growth, and interactions between plants and other organisms [1,2,3,4,5]
We examined the effects of variation in the intensity of the plant-rhizobia association by manipulating levels of available soil N, resulting in variation in nodulation intensity and soybean plants’ dependence on rhizobia-derived N
Plants fertilized with low amounts of nitrogen (Low-N) exhibited an intermediate level of rhizobial dependence and nodulation
Summary
Soil-dwelling microbial plant symbionts such as mycorrhizal fungi and nitrogen-fixing bacteria (rhizobia) can have profound impacts on plant ecology via influences on soil fertility, plant growth, and interactions between plants and other organisms [1,2,3,4,5]. The co-evolved relationship between legumes and rhizobia is characterized by the supply of fixed nitrogen from the microbial partner to the plant in exchange for plant-produced carbon resources and a protective root nodule within which the bacteria live [13]. Underlying changes in host plant signaling and nutritional quality due to this association with rhizobia are likely to influence herbivores. Legume plants exert a significant degree of control over their facultative mutualism with rhizobia, modulating the intensity of the association in response to several factors, soil nitrogen levels (as discussed below). Plant suppression of nodulation appears to be activated by signaling molecules from the shoots, likely including the phytohormones salicylic acid (SA) and jasmonic acid (JA), which have previously been implicated in induced plant defenses against herbivores [15,16,17,18,19]
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