Combined effects of mutualistic rhizobacteria counteract virus-induced suppression of indirect plant defences in soya bean

Abstract

It is increasingly clear that microbial plant symbionts can influence interactions between their plant hosts and other organisms. However, such effects remain poorly understood, particularly under ecologically realistic conditions where plants simultaneously interact with diverse mutualists and antagonists. Here, we examine how the effects of a plant virus on indirect plant defences against its insect vector are influenced by co-occurrence of other microbial plant symbionts. Using a multi-factorial design, we manipulated colonization of soya bean using three different microbes: a pathogenic plant virus (bean pod mottle virus (BPMV)), a nodule-forming beneficial rhizobacterium ( Bradyrhizobium japonicum ) and a plant growth-promoting rhizobacterium ( Delftia acidovorans ). We then assessed recruitment of parasitoids ( Pediobious foveolatus (Eulophidae)) and parasitism rates following feeding by the BPMV vector Epilachna varivestis (Coccinellidae). BPMV infection suppressed parasitoid recruitment, prolonged parasitoid foraging time and reduced parasitism rates in semi-natural foraging assays. However, simultaneous colonization of BPMV-infected hosts by both rhizobacteria restored parasitoid recruitment and rates of parasitism to levels similar to uninfected controls. Co-colonization by the two rhizobacteria also enhanced parasitoid recruitment in the absence of BPMV infection. These results illustrate the potential of plant-associated microbes to influence indirect plant defences, with implications for disease transmission and herbivory, but also highlight the potential complexity of such interactions.

Negative Effects of Rhizobacteria Association on Plant Recruitment of Generalist Predators

“…The observation that P. maculiventris soldier bugs avoid plants inoculated with P. simiae complements previous work showing that soil-borne microbes can influence the preferences of parasitoids [ 10 , 17 , 18 , 24 ] and predators [ 25 , 26 , 27 ]. Previous studies with P. simiae in Arabidopsis thaliana reported contrasting effects on indirect plant defenses.…”

“…Plant-associated rhizobacteria can alter plant traits in ways that influence their interactions with other organisms [ 3 , 4 , 10 ], yet few studies explore direct and indirect defenses when investigating the interactions with herbivores. The current findings show that plant-associated rhizobacteria can influence tritrophic interactions.…”

“…Behavioral responses of predatory bugs: To test whether inoculation with one of the rhizobacteria strains affects the behavioral responses of the predatory bug P. maculiventris to tomato plants, we conducted bioassays with a dynamic air-flow Y-tube olfactometer (each arm 15 cm, ø 2.5 cm) ( Figure 4 ) [ 10 , 45 ]. Adult P. maculiventris.…”

“…In addition to effects on plant nutrition, growth, and development, microbes can influence interactions among plants, and between plants and other organisms, with implications for plant fitness and the functioning of natural and agricultural ecosystems [ 5 , 6 , 7 ]. There is considerable interest in using microbes to steer such interactions to the benefit of the plant by strengthening plant resistance to pests while enhancing interactions with beneficial insects [ 5 , 8 , 9 , 10 ]. However, we currently have only a limited understanding of microbe-mediated effects on ecological interactions.…”

Rhizobium-Linked Nutritional and Phytochemical Changes Under Multitrophic Functional Contexts in Sustainable Food Systems

“…Organic carbon and nitrogen produced by the photosynthesis-nitrogen fixation machinery of legumes and rhizobia supports consumers at various trophic levels. Consumers are affected by compatible relationships between host plants and Rhizobium species (Dean et al, 2014;Naluyange et al, 2014Naluyange et al, , 2016Pulido et al, 2019;Karoney et al, 2020;Xu et al, 2020). Consumers are also affected by antagonisms arising from incompatible relationship between host plants and rhizobium species (Gourion et al, 2015;Clúa et al, 2018; Modi et al, 1985;Guerinot et al, 1990;Deshwal et al, 2003a Rhizobium Rioux et al, 1986;Dilworth et al, 1998;Deshwal et al, 2003a Benezech et al, 2020a).…”