Abstract

This study sheds light on a poorly understood area in insect–plant–microbe interactions, focusing on aphid probing and feeding behavior on plants with varying levels of arbuscular mycorrhizal (AM) fungus root colonization. It investigates a commonly occurring interaction of three species: pea aphid Acyrthosiphon pisum, barrel medic Medicago truncatula, and the AM fungus Rhizophagus irregularis, examining whether aphid‐feeding behavior changes when insects feed on plants at different levels of AM fungus colonization (42% and 84% root length colonized). Aphid probing and feeding behavior was monitored throughout 8 h of recording using the electrical penetration graph (EPG) technique, also, foliar nutrient content and plant growth were measured. Summarizing, aphids took longer to reach their 1st sustained phloem ingestion on the 84% AM plants than on the 42% AM plants or on controls. Less aphids showed phloem ingestion on the 84% AM plants relative to the 42% AM plants. Shoots of the 84% AM plants had higher percent carbon (43.7%) relative to controls (40.5%), and the 84% AM plants had reduced percent nitrogen (5.3%) relative to the 42% AM plants (6%). In conclusion, EPG and foliar nutrient data support the hypothesis that modifications in plant anatomy (e.g., thicker leaves), and poor food quality (reduced nitrogen) in the 84% AM plants contribute to reduced aphid success in locating phloem and ultimately to differences in phloem sap ingestion. This work suggests that M. truncatula plants benefit from AM symbiosis not only because of increased nutrient uptake but also because of reduced susceptibility to aphids.

Highlights

  • Arbuscular mycorrhizal (AM) fungi are obligate biotrophs of the phylum Glomeromycota that form symbiosis with most vascular plants in a relationship dating back 450 million years (Remy et al, 1994)

  • Measurement of AM fungus colonization levels confirmed that inoculation with varying spore concentrations resulted in significant differences in root-length colonized (RLC) (Table 1), and treatments were thereafter designated as the resulting RLC levels, 42% AM fungus-colonized plants and 84% AM funguscolonized plants

  • We found that the number of times aphids were able to ingest phloem sap, and the waveform duration per insect (WDI) of the sustained phloem ingestion were reduced when aphids fed on the 84% AM fungus-colonized plants compared to those that fed on the 42% AM fungus-colonized plants (Fig. 3)

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Summary

Introduction

Arbuscular mycorrhizal (AM) fungi are obligate biotrophs of the phylum Glomeromycota that form symbiosis with most vascular plants in a relationship dating back 450 million years (Remy et al, 1994). An aspect of the symbiosis that has gained more attention in the last 15 years involves interactions between AM fungi, plants, and above- and below-ground herbivores (Rasmann et al, 2017). It has been proposed that mycorrhizal fungi could alter plant interactions with insects through multiple mechanisms involving changes in plant nutritional quantity and quality, defensive strategies and tolerance (Bennett et al, 2006). AM fungi alter plant tolerance to insect herbivores and chemical defenses simultaneously (Tao et al, 2016). Chemical defenses can increase or decrease based on plant growth, which can be influenced by the AM symbiosis (Tao et al, 2016). The phytohormone jasmonic acid (JA) has been proposed as a major player in modulating plant defenses that lead to mycorrhiza-induced resistance (MIR) (Jung et al, 2012), but there are still limited data supporting its role (Song et al, 2013)

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