Metabolism or behavior: explaining the performance of aphids on alkaloid-producing fungal endophytes in annual ryegrass (Lolium multiflorum)

Abstract

Plant-herbivore interactions are often mediated by plant microorganisms, and the "defensive mutualism" of epichloid fungal endophytes of grasses is an example. These endophytes synthesize bioactive alkaloids that generally have detrimental effects on the performance of insect herbivores, but the underlying mechanisms are not well understood. Our objective was to determine whether changes in the physiology and/or behavior of aphids explain the changes in performance of insects feeding on endophytic plants. We studied the interaction between the aphid Rhopalosiphum padi and the annual ryegrass Lolium multiflorum symbiotic (E+) or not symbiotic (E-) with the fungus Epichloë occultans that can synthesize loline alkaloids. We hypothesized that aphids feeding on E+ plants have higher energetic demands for detoxification of fungal alkaloids, thereby negatively impacting the individual performance, population growth, and structure. Aphids growing on E+ plants had lower values in morphometric and functional variables of individual performance, displayed lower birth rate, smaller population size, and dramatic structural changes. However, aphids exhibited lower values of standard metabolic rate (SMR) on E+ plants, which suggests no high costs of detoxification. Behavioral variables during the first 8 h of feeding showed that aphids did not change the phloem sap ingestion with the presence of fungal endophytes. We hypothesize that aphids may maintain phloem sap ingestion according to their fungal alkaloid tolerance capacity. In other words, when alkaloid concentrations overcome tolerance threshold, ingestion of phloem should decrease, which may explain the observed lower values of SMR in E+ feeding aphids.

Novel bioassay to assess antibiotic effects of fungal endophytes on aphids

“…<7 days) for both species, with very few nymphs reaching the adult stage on all endophyte treatments. The nymphal stage has been reported to be more susceptible to endophytes than the adult stage in other aphid species, such as R. padi [24]. This finding is of economic importance as early-acting insecticides that are most effective against nymphs will more successfully reduce aphid population growth, due to fewer aphids surviving to reproductive age.…”

“…Numerous studies have been carried out since the 1980s to determine what grass-endophyte association has the greatest negative effect on aphids but has minimal effect on vertebrates. In these studies, aphids' settling preferences, host acceptance, feeding, body size and life history parameters were assessed under a range of conditions [24][25][26][27][28]. A common trend across many studies has emerged that showed varying responses depending on the aphid-grassendophyte combination.…”

“…There is an additional factor that can influence aphid life history in response to grass endophyte symbiota, namely the methodology used to assess the insecticidal effect on aphids, which makes comparisons between studies difficult. This is not surprising as methods range from detached leaf bioassays to whole plant bioassays, density-dependent to density-independent bioassays, and different bioassay durations [19,24,28,30]. From a routine analytical perspective, it is important to develop a bioassay that is fast and easy to conduct with reproducible results.…”

Endophytes Potential Use in Crop Production

“…The Epichloë festucae symbiosis with ryegrass (Lolium perenne var. Lolii) enhances gene expression of jasmonic acid (JA) precursors [13], and the expression of the systemic defense genes HvPr17b and HvHsp70 in barley is associated with the presence of the endophyte Piriformospora indica [14]. Further, presence of endophytes may alter pathogenesis-related proteins (PR-proteins) concentration, as chitinase, peroxidase, glucanase and cellulase in cucumber inoculated with Trichoderma harzianum [15] The resistance induction is also related with the activity of defense enzymes, such as phenylalanine ammonia lyase, polyphenol oxidase, superoxide dismutase, peroxidase, ascorbate peroxidase, and guaiacol peroxidase.…”

High levels of arbuscular mycorrhizal fungus colonization on Medicago truncatula reduces plant suitability as a host for pea aphids (Acyrthosiphon pisum)

“…The EPG technique has been widely used to investigate different aspects of insect-plant interactions. For example, EPG was used to characterize host plant resistance to hemipterans (Vanhelden & Tjallingii, 1993;Alvarez et al, 2013) to understand the transmission mechanisms of plant pathogens by their insect vectors (Fereres & Moreno, 2009;Moreno et al, 2012), to understand the mode of action of pesticides (Harrewijn & Kayser, 1997;Garzo et al, 2016), and to examine the feeding behavior of aphids on plants colonized by fungal endophytes (Bastias et al, 2017). Surprisingly, few studies used the EPG technique to examine whether the feeding behavior of aphids changes during feeding on mycorrhizal plants.…”