Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant

Abstract

Legume-associated nitrogen-fixing bacteria play a key role for plant performance and productivity in natural and agricultural ecosystems. Although this plant-microbe mutualism has been known for decades, studies on effects of rhizobia colonisation on legume-herbivore interactions are scarce. We hypothesized that additional nitrogen provided by rhizobia may increase plant resistance by nitrogen-based defense mechanisms. We studied this below-aboveground interaction using a system consisting of lima bean (Phaseolus lunatus L.), rhizobia, and the Mexican bean beetle (Epilachna varivestis Muls.) as an insect herbivore. We showed that the rhizobial symbiosis not only promotes plant growth but also improves plant defense and resistance against herbivores. Results of our study lead to the suggestion that nitrogen provided by rhizobia is allocated to the production of nitrogen-containing cyanogenic defense compounds, and thereby crucially determines the outcome of plant-herbivore interactions. Our study supports the view that the fitness benefit of root symbioses includes defence mechanisms and thus extends beyond the promotion of plant growth. Since the associations between legumes and nitrogen-fixing rhizobia are ubiquitous in terrestrial ecosystems, improved knowledge on rhizobia-mediated effects on plant traits-and the resulting effects on higher trophic levels-is important for better understanding of the role of these microbes for ecosystem functioning.

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…However, this is not necessarily the case, as rhizobia have been shown to also affect plant defense responses directly (e.g., Thamer et al, 2011) and indirectly (Godschalx et al, 2015). The latter is illustrated by a study with potted plants placed in the field that reported positive effects of the addition of Rhizobium sp.…”

Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids

“…However, such studies of two-way interactions (e.g. between a plant and its herbivore or an insect herbivore and its symbionts) cannot always predict the responses of organisms in a community [7][8][9]. Here, we adopt a community approach and simultaneously examine the role of both plant -and insect -microbial interactions in modulating the plant -herbivore interaction.…”

Belowground Influence of Rhizobium Inoculant and Water Hyacinth Composts on Yellow Bean Infested by Aphis fabae and Colletotrichum lindemuthianum under Field Conditions

“…Belowground colonization of roots by Rhizobium has been found to interact with aphids and other aboveground herbivores (Kempel et al, 2009;Katayama et al, 2010Katayama et al, , 2011Martinuz et al, 2012). For example, root colonization by Rhizobium has been found to promote plant resistance to insect pests (Thamer et al, 2011). However, Rhizobium colonization of roots has also been related to an increase in aphid and fungal incidences on leguminous shoots, which has been attributed to improved nutritive suitability of the host plant due to nitrogen fixation (Dean et al, 2009(Dean et al, , 2014Naluyange et al, 2014).…”