Stem nematode counteracts plant resistance of aphids in alfalfa, Medicago sativa.

Ricardo A Ramirez,Lori R Spears

doi:10.1007/s10886-014-0504-3

Abstract

Plants are exploited by a diverse community of insect herbivores and phytopathogens that interact indirectly through plant-mediated interactions. Generally, plants are thought to respond to insects and pathogens through different defensive signaling pathways. As plants are selected for resistance to one phytophagous organism type (insect vs. pathogen) in managed systems, it is not clear how this selection may affect community interactions. This study examined the effect of nematode-resistant varieties on aphid (Acyrthosiphon pisum) suppression, and then determined how infection by the stem nematode, Ditylenchus dipsaci, mediated ecological effects on aphids and on plant defense proteins. Four alfalfa (Medicago sativa) varieties were selected with resistance to nematodes only (+,−), aphids only (−,+), nematodes and aphids (+,+), and susceptibility to nematodes and aphids (−,−). Field and greenhouse experiments were conducted to isolate the effect of nematode infection and aphid abundance on each variety. We found that varieties resistant to nematode, regardless of aphid resistance, had the lowest aphid counts, suggesting possible cross-resistance. Aphid abundance, however, increased when plants were exposed to nematodes. Resistant varieties were associated with elevated saponins but these compounds were not affected by insect or pathogen feeding. Concentrations of peroxidases and trypsin inhibitors, however, were increased in nematode resistant varieties when exposed to nematodes and aphids, respectively. The patterns of plant defense were variable, and a combination of resistance traits and changes in nutrient availability may drive positive interactions between nematodes and aphids aboveground.

Highlights

The recognition that plants host a diverse community of phytophagous organisms and mediate community interactions has led to a surge in studies investigating the interactions between herbivorous insects and plant parasitic nematodes (McCarville et al 2012, 2014; Wondafrash et al 2013)
In each of two years (2011–2012), we evaluated the presence of nematodes on aphid abundance and plant defense protein concentration for each of four alfalfa varieties varying in resistance to nematodes and aphids
When plants were exposed to stem nematodes we found an increase in aphid abundance (F1,55=8.234, P= 0.006)

Summary

Introduction

The recognition that plants host a diverse community of phytophagous organisms and mediate community interactions has led to a surge in studies investigating the interactions between herbivorous insects and plant parasitic nematodes (McCarville et al 2012, 2014; Wondafrash et al 2013). Nematodes appear to neutrally and negatively affect piercing-sucking arthropods (e.g., reducing aphid fecundity and plant attractiveness to aphids), while chewing arthropods (e.g., caterpillars) have neutral to positive interactions with nematode infected plants (Alston et al 1991; Carter-Wientjes et al 2004; Kaplan et al 2008, 2009; Olson et al 2008). The majority of plant parasitic nematodes feed belowground on roots, and understandably much of what we know comes from interactions between these root feeders and aboveground insects. Studies on the interactions between aboveground feeding stem nematodes and insects are lacking and would contribute to the growing

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