Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

Abstract

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant-associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant-growth promoting rhizobacteria (PGPR). This PGPR community modulates insect-induced defences of plants. Thus, PGPR and insects interact indirectly via plant-mediated interactions.3. Such plant-mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross-compartment plant-mediated interactions.4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant-mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop-protection strategies.

Reciprocal plant‐mediated antagonism between a legume plant virus and soil rhizobia

“…For example, early nodule formation in legumes can be inhibited by pathogens (López et al, 2017;Rao et al, 1987), although herbivory can promote abundance and greater size of nodules (Heath & Lau, 2011;Simonsen & Stinchcombe, 2014). Recent syntheses suggest while herbivores and pathogens alter benefits of microbes for plants, the plant-mediated mechanisms underlying these interactions need further investigation (Friman et al, 2020;Pangesti et al, 2013).…”

Plant Growth-Promoting Rhizobacteria Enhance Defense of Strawberry Plants Against Spider Mites

“…Beneficial below-ground microorganisms may influence the performance of herbivores via two major functional pathways, that is, enhancement of nutrition promoting plant growth and development, which in turn may favor the herbivores, or induced systemic resistance (ISR), which may disfavor the herbivores, or the combination thereof ( Kempel et al, 2009 ; Pineda et al, 2010 ; Gamalero and Glick, 2011 ; Friman et al, 2021b ). Many studies of above-belowground interactions showed that beneficial soil microorganisms such as free-living rhizobacteria can induce systemic resistance in above-ground plant parts and enhance the level of protection against herbivorous attackers ( Zehnder et al, 1997 ; Koricheva et al, 2009 ; Khoshfarman-Borji et al, 2020 ; Ruiu, 2020 ; Friman et al, 2021a ).…”

“…In terrestrial ecosystems, plants are the link between below- and above-ground communities, which may in consequence either indirectly, by altering plant traits, or directly, by moving up or down in the plant, interact with each other. During the last two decades, research on below-aboveground interactions has immensely intensified and many studies have focused on effects that cascade up and down between the communities of both subsystems ( Van der Putten et al, 2001 ; Pineda et al, 2010 ; Hoffmann et al, 2011a , b ; Friman et al, 2021b ). Plant-mediated below-aboveground interactions involving micro-organisms of the rhizosphere may occur between plant-associated and/or free-living microorganisms ( Bezemer and van Dam, 2005 ; Coskun et al, 2017 ; Dellagi et al, 2020 ), between micro-organisms and herbivores ( Hoffmann et al, 2009 ; Patiño-Ruiz and Schausberger, 2014 ; Disi et al, 2019 ; Friman et al, 2021a ) and, in turn, between micro-organisms and the herbivores’ natural enemies ( Hoffmann et al, 2011a , b ; Pineda et al, 2013 ; Gadhave et al, 2016 ).…”

“…The rhizosphere microbial community may consist of a huge diversity of pathogenic, neutral and/or mutualistic micro-organisms. Among the usually mutualistic symbionts, it is especially mycorrhizal fungi, rhizobia and plant growth-promoting rhizobacteria (PGPR) that may influence aboveground plant growth and defense against pathogens and herbivores ( Hoffmann et al, 2009 , 2011a , b ; Hoffmann and Schausberger, 2012 ; Khaitov et al, 2015 ; Pangesti et al, 2015 ; Nunes and Kotanen, 2017 ; Friman et al, 2021b ). Here, we studied plant-mediated interactions between free-living soil bacteria that are commonly considered PGPR and aboveground herbivorous spider mites on strawberry plants.…”

Tackling the Context-Dependency of Microbial-Induced Resistance

“…Several studies have reported effects of herbivory on mycorrhizal colonization, ranging from an increase to no effect to a decrease [88,89]. To date, these findings have not yet been tested in the context of ISR, even though they could potentially open up new insights into top-down effects on ISR when using a community approach [90]. Not much is known about the effects of natural enemies of insect herbivores on ISR.…”