Aphids alter host-plant nitrogen isotope fractionation

Abstract

Plant sap-feeding insects and blood-feeding parasites are frequently depleted in 15 N relative to their diet. Unfortunately, most fluid-feeder/host nitrogen stable-isotope studies simply report stable-isotope signatures, but few attempt to elucidate the mechanism of isotopic trophic depletion. Here we address this deficit by investigating the nitrogen stable-isotope dynamics of a fluidfeeding herbivore-host plant system: the green peach aphid, Myzus persicae, feeding on multiple brassicaceous host plants. M. persicae was consistently more than 6‰ depleted in 15 N relative to their hosts, although aphid colonized plants were 1.5‰ to 2.0‰ enriched in 15 N relative to uncolonized control plants. Isotopic depletion of aphids relative to hosts was strongly related to host nitrogen content. We tested whether the concomitant aphid 15 N depletion and host 15 N enrichment was coupled by isotopic mass balance and determined that aphid 15 N depletion and host 15 N enrichment are uncoupled processes. We hypothesized that colonized plants would have higher nitrate reductase activity than uncolonized plants because previous studies had demonstrated that high nitrate reductase activity under substrate-limiting conditions can result in increased plant δ 15 N values. Consistent with our hypothesis, nitrate reductase activity in colonized plants was twice that of uncolonized plants. This study offers two important insights that are likely applicable to understanding nitrogen dynamics in fluid-feeder/host systems. First, isotopic separation of aphid and host depends on nitrogen availability. Second, aphid colonization alters host nitrogen metabolism and subsequently host nitrogen stable-isotope signature. Notably, this work establishes a metabolic framework for future hypothesis-driven studies focused on aphid manipulation of host nitrogen metabolism.host-parasite interaction | nitrogen budget | plant-herbivore interaction | trophic enrichment N itrogen, required for the synthesis of nucleic and amino acids, is essential for development and growth. Found in the atmosphere, soil, and oceans in inorganic forms (1), animals depend on plants and microorganisms for nitrogen fixation and organic nitrogen supply in the form of proteins and amino acids. Universally, metabolic fractionation during nitrogen fixation, assimilation, respiration, and excretion results in differences in the ratio of nitrogen stable isotopes in different tissues within organisms (2) and at different levels within ecosystems (3). Typically, consumers are enriched in 15 N by ∼2‰ to 3‰ relative to their diet (2, 4, 5). However, important exceptions exist. Fluidfeeders, a group that includes blood-feeding parasites and hempiteran insects (2), frequently have been found to deviate from these typical patterns such that fluid-feeders are usually reported as showing no enrichment or even depletion in 15 N relative to their diet (2, 6-17). Although it is now commonly accepted that fluid-feeders deviate from typical patterns of enrichment, these observations have stimulat...

Transcriptional responses of tolerant and susceptible soybeans to soybean aphid (Aphis glycines Matsumura) herbivory

“…These authors suggest that possible signals present in the salivary secretions of the aphid trigger the increase in nitrate reductase activity in cabbage leaf. Data presented here are consistent with the Wilson et al (2011) Glyma05g26390 -5.35 0.01 AT1G48100 Pectin lyase-like superfamily protein…”

“…Transcripts for this gene were significantly (-2.3-fold) down-regulated in the tolerant plants and significantly up-regulated (3.2-fold) in the susceptible plants. Aphid feeding can lead to a 2-fold increase in nitrate reductase activity in cabbage seedlings infested with the green peach aphid (Myzus persicae) (Wilson et al 2011). These authors suggest that possible signals present in the salivary secretions of the aphid trigger the increase in nitrate reductase activity in cabbage leaf.…”

Tracing prey origins, proportions and feeding periods for predatory beetles from agricultural systems using carbon and nitrogen stable isotope analyses

“…However, this study documented that cotton aphids were only 0.5‰ enriched in 15 N relative to their hosts (cotton) and even maize aphids were more than 5‰ depleted in 15 N relative to their hosts (maize). The result was similar to the green peach aphid, Myzus persicae, which was more than 6‰ depleted in 15 N relative to their hosts (cabbage seedlings) (Wilson et al, 2011). Aphids are plant sap-feeding insects, which have been frequently reported as showing no enrichment or even depletion in 15 N relative to their diet (McCutchan et al, 2003;Sagers and Goggin, 2007;Schumacher and Platner, 2009;Scrimgeour et al, 1995).…”

Ethylene Contributes to maize insect resistance1-Mediated Maize Defense against the Phloem Sap-Sucking Corn Leaf Aphid

“…2011; Wilson et al, 2011;Nalam et al, 2012). We observed that the vascular sap obtained from Tx601 plants that were previously infested with aphids had less antibiotic factors, suggesting that CLA were able to suppress defenses in Tx601 plants.…”